介导NO信号转导的人可溶性鸟苷酸环化酶的表达纯化及其结构与性质研究
|
摘要
一氧化氮(NO)于1992年被美国Science杂志评选为明星分子。1998年,美国的三位科学家(Furchgott RF, Ignarro LJ和Murad F)因发现“NO是心血管系统中一种重要的信号转导分子”而荣获了诺贝尔生理和医学奖。至此以后,NO信号转导越发受到人们的密切关注。可溶性鸟苷酸环化酶(sGC)是介导NO信号转导通路中的一个核心金属蛋白,扮演着NO受体这一重要角色。NO结合到sGC后将激活sGC催化其底物GTP转化为cGMP。cGMP是我们所熟知的一个重要的二级信使分子,通过对其效应蛋白的调节进而在多种生理过程中起着重要的作用,例如促进血管和平滑肌舒张；抑制血小板凝聚、血管重塑、细胞凋亡和炎症发生以及参与神经传递等等。一旦NO信号转导通路异常,将会导致多种疾病的发生,如多种心血管疾病(如肺动脉高血压、心力衰竭、动脉粥样硬化和再狭窄等)及神经退行性疾病等。
真核生物sGC是一个含b型血红素,由α和β亚基组成的异源二聚体蛋白,每个亚基分别有两种异构体形式(α1/α2和β1/β2),其中以α1β1这种异源二聚体形式最为广泛,研究也最多。按照同源序列和结构功能的分析,α和β亚基都可以大致分为三大结构域,分别是N-端血红素结构域(属于H-NOX家族)、中间结构域(也有将其细分为Per/Arnt/Sim (PAS)-like结构域和螺旋卷曲(CC)结构域)和C-端催化结构域。其中血红素结构域是sGC研究的核心,因为它正是信号分子NO/CO等的调节结构域,信号小分子的调节机理研究对NO信号转导异常所引发的疾病诊断治疗及新药开发具有重要的指导意义,也是近年来化学生物学研究领域的热点。
sGC的研究已历经三十多年,目前已有近5000篇文献报道。但是许多关键问题尚未彻底解决,一直存在争议。例如,血红素是sGC活性调节的一个重要的辅基,但是它的结合区域及方式备受争议；NO激活及失活机理也是众说纷纭,仍无定论；α和β亚基异源二聚关键作用部位及其作用机理也尚待解决；sGC的晶体结构更是鲜有报道。所有问题的一大源头就是能否获取足量的蛋白。这么多年来sGC蛋白多数都是通过组织提取或者昆虫细胞表达而得,但是这些方法蛋白的产量都不高,而且耗费高,可以满足对其活性的测定研究,但是在很大程度上它限制了sGC的深入研究,尤其是在分子水平上详细研究其结构-性质-反应关系。大肠杆菌一直都以高效率、低成本、高产量著称,因此能否在大肠杆菌中成功的表达纯化我们所需的sGC蛋白是该课题研究之初最大的挑战。
本论文的核心内容是集中在对sGC血红素结构域的研究。首先我们对人sGC (hsGC)β1亚基的N-端血红素结构域片段和全长蛋白(hsGCβ195,hsGCβ384和hsGC(3619)进行了质粒构建及其在大肠杆菌中的表达与纯化研究,成功建立了一套hsGC蛋白的高效表达与纯化体系(产量约20mg/L培养液),解决了sGC研究中的第一大瓶颈问题,为之后的结构-性质-反应研究奠定了很好的基础。这一体系我们已经申请了专利。通过同源结构模拟及能量优化我们得到了hsGCβ195蛋白的结构模型。在血红素重组基础上,我们对含血红素的hsGC蛋白进行了紫外可见光谱、EPR谱、圆二色光谱、荧光光谱的性质研究,研究发现血红素结构域(hsGCβ195)可以作为一个很好的工具用以进行sGC血红素相关的性质研究。变温圆二色光谱结果表明hsGCβ195蛋白脱辅基和含血红素形式的转变中点温度分别是56±1℃和54±3℃,说明两种形式都具有较好的热稳定性。pH滴定实验结果显示酸滴定和碱滴定的滴定中点(pKa)值分别为5.7±0.2和9.3±0.1,说明hsGCβ195蛋白具有较好的碱稳定性,但是在酸性条件下血红素容易脱出,蛋白容易沉淀。hsGCβ195蛋白中只含有一个色氨酸(Trp22),通过监测Trp22内源荧光光谱可以用来研究蛋白的构象变化。Trp22荧光结果显示：脱辅基hsGCβ195中Trp22处于比较疏水的环境,血红素重组后荧光最大发射波长(λmax)红移,荧光信号强度大幅度下降,说明蛋白的构象发生了较大的变化,尤其是还原态和NO结合态,荧光信号几乎完全淬灭。我们推测是血红素结合后引发第一个α螺旋(aA)构象变化,使得Glu10(位于aA螺旋上)与Trp22相对位置改变并淬灭荧光。1-苯胺基萘-8-磺酸(ANS)是一个常用的疏水荧光探针,ANS外源荧光光谱结果显示ANS可能会与血红素部分竞争结合sGC疏水腔。
为了探讨血红素的结合区域及作用方式,我们成功构建并表达纯化了α1亚基血红素结构域(hsGCa259)蛋白,并首次探索了其在血红素结合、NO/CO结合上的性质特征。同源结构模拟及能量优化得到的hsGCa259同源结构显示该蛋白存在一个大的空腔,血红素重组结果显示血红素可以稳定结合到hsGCa259上,因此我们推测该空腔主要作用是用于血红素的结合。EPR谱进而证实α1和β1两个亚基在结合血红素的微环境上最大的区别在于β1亚基有一个近端轴向配体(His105)配位而α1亚基缺乏强的轴向配体。血红素转移及ANS外源荧光实验表明hsGCa259可能是通过强的疏水相互作用稳定结合血红素的。我们认为：在异源二聚sGC蛋白中,α1和β1亚基的N-端血红素结构域共同参与了血红素的结合,其中β1亚基提供一个轴向配体(His105)与血红素铁配位,而α1主要是以疏水相互作用稳定血红素的结合。我们进而研究了hsGCa259和hsGCβ195的CO和NO结合过程。在CO结合过程的稳态平衡滴定和动力学结果的基础上我们提出了一个可能的CO结合模型。NO解离过程的研究表明NO解离是一个复杂的过程,需要用二级反应进行拟合,可能是由于NO结合态具有"open"和‘'closed"两种构象,这两种构象在电子吸收光谱上没有区别,但是在活性调节上有所区分。曾经有报道推测hsGCa259蛋白的空腔是用于sGC激活剂(如YC-1)的结合,YC-1的结合会增加sGC对CO的亲和力。但是我们CO滴定的结果显示YC-1对CO结合没有影响,等温滴定量热(ITC)测定结果也表明YC-1与hsGCα259并没有强的相互作用。
为了详细研究轴向配位(Fe-H105)的作用,我们构建了hsGCβ195H105G突变体蛋白并进行详细的性质表征。EPR谱证明该蛋白的确没有了强的轴向配位。Trp22内源荧光结果也显示：Hisl05突变前后脱辅基蛋白的构象变化不大,但是血红素重组后的蛋白构象有明显的改变。血红素转移和血红素还原实验表明轴向配体(H105)对提高血红素亲和力的作用不大,但是它可以减缓血红素氧化丢失进而对蛋白起到一定的保护作用,这在生理过程中具有重要意义。基于氧化态及脱辅基sGC的药物设计(sGC激活剂,sGC activator)是心血管疾病治疗的另一思路。
为了研究异源二聚对血红素结构域的结构-性质-反应的影响,我们通过添加linker的方式将α1和β1两个亚基血红素结构域连接起来,构建出了一个新的蛋白质(hsGCβ195-α259)并对其进行了详细的表征。圆二色光谱及Trp22内源荧光光谱结果都表明该蛋白与单个亚基相比发生了很大的构象变化,并具有很好的稳定性。血红素重组及EPR谱结果显示：hsGCp195-α259能够稳定结合血红素,但是其结合方式与α1亚基相似,其序列中的His105并没有与血红素轴向配位。我们推测hsGCp195-α259中血红素构象存在两种可能性：一是血红素主要还是结合在β195的疏水腔里,添加linker及α1259后β195与α259相互作用使得蛋白构象发生一定的变化,血红素远离H105,从而无法配位；另一种方式是linker的添加使得血红素进入β195的入口受阻,血红素主要结合在a259的疏水空腔,血红素与H105距离较远而无法配位,但是血红素具体的结合方式还有待于进一步的实验验证或者晶体结构的解析。对CO结合和NO解离过程的研究表明：hsGCβ195-α259蛋白与单个亚基相比,CO亲和力增加了近一倍,NO解离速率加快了约一倍。除此之外,我们还将p195和a259同时构建到pETDuet-1载体中以实现两个亚基的共表达。Amylose和Ni-NTA pull-down实验结果表明这两个亚基在体内的确存在相互作用。而分别表达纯化的β195和a259在体外混合后却不能发生相互作用形成异源二聚蛋白。这一结果一方面说明sGC的血红素结构域对异源二聚具有一定的贡献,同时也反映出sGC异源二聚可能是由体内信号调节完成的。
最后,我们还对sGC血红素结构域在晶体学方面进行了初步研究。经过大量的结晶条件筛选及多次尝试,最终我们成功培养出了hsGCβ195-α259和hsGCβ195H105G-α259突变体的脱辅基及含血红素形式蛋白的多种晶体,并已经获得晶体衍射数据,结构的解析工作正在进行中。晶体结构的解析将为理解sGC的血红素结合方式、NO调节机理提供重要的结构基础。
The Nobel Prize in physiology and medicine in1998was awarded to R. F. Furchgott, L. J. Ignarro, and F. Murad for their discovery of "the nitric oxide (NO) as a signaling molecule in the cardiovascular system". This stimulated intense interests of scientists in the study on soluble guanylate cyclase (sGC) mediated NO-signaling system. sGC, as a nitric oxide sensor, is a critical heme-containing enzyme in NO-signaling pathway of eukaryotes. Upon NO binding, sGC catalyzes the conversion of guanosine5'-triphosphate (GTP) to3',5'-cyclic guanosine monophosphate (cGMP). cGMP, as an important second messenger, regulates several effector proteins and plays an important role in many physiological processes, for example, vasodilatation, smooth muscle relaxation, platelet aggregation, and neuronal transmission. Dysfunction of NO signaling results in many pathological disorders, ranging from several cardiovascular diseases, such as arterial hypertension, pulmonary hypertension, heart failure, atherosclerosis and restenosis, to neurodegenerative diseases.
sGC in eukaryote is a heterodimeric hemoprotein, composed of a and β subunit. For human sGC, there are two isoforms for each subunit in vivo:α1/α2and (β1/β2, while the α1β1heterodimer is the more abundant. The prosthetic heme moiety, crucial for NO sensing, is located in the heme binding domain with His105of β1subunit as the axial ligand. Both α and β subunit can be divided into three domains:the N-terminal heme domain (H-NOX family), central domain (containing Per/Armt/Sim (PAS)-like region and Coiled-coil region) and the C-terminal catalytic domain. The heme domain, responsible for heme binding and NO/CO binding, is one of the most important and popular regions in sGC study.
In the past decades, there were nearly5,000papers published in this area. However, several crucial problems are still unclear and controversial. For example, the exact heme binding region and environment is to be determined; the exact mechanism of NO activation and deactivation is unknown although several models have been proposed; the region for the heterodimerization regulation and related mechanism is ambiguous; all the above problems are largely due to the limited structural information for sGC structure. Limited availability of large quantities of highly pure sGC and its large size has impeded analysis of the crystal structure. Originally, sGC was isolated from a number of mammalian tissues, mainly bovine and rat lungs. In the case of human isoforms, direct isolation from native sources becomes virtually impossible. Although the functional expression of recombinant human sGC was achieved in the baculovirus/sf9cells, the yield of human sGC was relatively limited. To this end, the E. coli expression system is the most desired method to overexpress sGC. However, the overexpression and purification of eukaryotic sGC is one of the bottle neck for sGC study and hardly reported.
This thesis is focused on the heme domain of human sGC (hsGC). We report, for the first time, the recombinant hsGC in full-length (hsGCβ619) and its truncated N-terminal fragments with195and384residues (hsGCβ195and hsGCβ384), which were overexpressed in E. coli and purified successfully with a yield of20mg/L cell culture. This highly efficient E. coli expression system of hsGC proteins is critical to the study of the structure, function and catalytic mechanism of human sGC and we have submitted the application of patent. As for sGC heme domain, there are only two published crystal structures of H-NOX domain from bacteria, Tt H-NOX and Ns H-NOX. Based on the crystal structure of Ns H-NOX domain (pdb entry:2O09), the homology model of hsGCβ195was constructed through energy optimization by NAMD program. After heme reconstitution, the three proteins in different forms (ferric, ferrous, NO-bound and CO-bound) were characterized via UV-vis, EPR, CD and fluorescence spectroscopy. The characterization results suggested that hsGCβ195, as an excellent tool, can be used to further study the sGC heme pocket and NO activation/deactivation mechanism. The midpoint temperature (Tm) of conformation transition for the apo-hsGCβ195and heme-hsGCβ195is56±1℃and54±3℃, respectively, indicating the similar and good stability for temperature. The pH titration results showed that the midpoint pH (pKa) for the acid and alkaline transition process is5.7±0.2and9.3±0.1, respectively. hsGCβ195exhibites desirable stability in alkaline condition, while hsGCβ195easily precipitates along with heme dissociation in acidic condition. Trp22, the only tryptophan residue in hsGCβ195, can be used to study the conformation change with the intrinsic fluorescence spectra measurement. The Trp22fluorescence spectra revealed that Trp22was at a relative hydrophobic environment with the maximum emission wavelength (λmax) at327nm for the apo-hsGCβ195protein. Heme reconstitution resulted in the λmax red-shifting and a largely concomitant decrease in the fluorescence intensity, revealing the large conformation change occurred, especially for the ferrous and NO-bound forms. We conferred that the heme binding induced the movement of the first a-helix (aA), leading to the change of relative position between Glu10(located at aA) and Trp22and further quench the Trp22fluorescence. ANS fluorescence is commonly to investigate the hydrophobic properties of proteins. We found that ANS could bind to some part of sGC hydrophobic pocket and complete with heme binding.
To further explore the heme binding region and heme pocket microenvironment, the heme domain of hsGC al subunit (hsGCa259) was constructed, expressed and purified. The homology model of hsGCa259displayed a large hydrophobic pocket and the heme could be located at hsGCa259stably via heme reconstitution, which resulted in the speculation that the role of the pocket is heme binding. The EPR spectra of ferric hsGC identified that the heme of hsGCβ195is5-coordinate high spin with His105as the axial ligand, while both the axial ligands of the heme in hsGCa259are weak, probably H2O. We guessed that heme binds to hsGCa259probably with strong hydrophobic interaction according to heme transfer and ANS fluorescence measurements. This is the first direct evidence that both the heme domain of al and β1subunit contribute to the heme binding. The CO and NO binding equilibrium and kinetics of hsGCa259and hsGCβ195were carried out by UV-vis and stopped-flow measurement. One possible CO binding model is proposed. NO dissociation results suggested that NO dissociation is a more complex process and possibly two different but UV-vis spectroscopy indistinguishable NO-bound heme existed. Recently, the pocket of hsGCα1subunit was inferred to YC-1binding, which will lead to CO affinity increase. However, we found that YC-1had little effect on CO affinity, the isothermal titration calorimetry (ITC) also indicated no obvious interaction between YC-1and hsGCa259.
In order to investigate the exact role of the heme axial ligand (His105), hsGCβ195H105G was constructed and fully characterized. EPR spectra proved that the axial ligand was removed in hsGCβ195H105G. The Trp22fluorescence indicated that the H105G mutation had little effect on the apo-hsGCβ195conformation, while exhibited large influence on the heme-hsGCβ195conformation. The heme transfer and reduction experiments suggested that H105mainly increase the heme reduced potential and protect the protein from heme oxidation and loss, which is critical for several physiological processes.
On the purpose of studying the effect of heterodimerization on the heme binding properties, hsGCβ195-a259, the hybrid protein of hsGCβ195and hsGCa259linked with GSGSGG peptide, was constructed and detailed characterized. The CD and Trp22fluorescence spectra demonstrated that hsGCβ195-α259displayed tremendous conformation change compared to hsGCβ195or hsGCα259with excellent stability. The heme reconstitution and EPR spectra identified that hsGCβ195-α259could bind heme via the similar fashion with that of hsGCα259, in which His105did not bond to heme. We conferred that there are two possible modes of heme location in hsGCβ195-α259. The first possibility is that heme mainly resides at the hydrophobic pocket of β195. The addition of linker and α259induces a large conformation change through interaction with β195, resulting that H105is not close enough to bond with heme. The other situation is that the entrance of heme to β195is blocked by the addition of linker and α259, which leads to the impossible bonding between H105and heme. The exact heme binding pattern awaits further experiments, particularly the resolution of crystal structure. The CO and NO binding results showed that hsGCβ195-α259exhibited higher CO affinity (almost twice) and larger NO dissociation rates (approximate twice) compared with hsGCβ195or hsGCα259. Besides, we co-expressed hsGCβ195and hsGCα259by inserting β195and α259into the two multi-cloning sites (MCS) of pETDuet-1vector, respectively and demonstrated that hsGCβ195definitely interacted with hsGCα259in vivo through Amylose pull-down and Ni-NTA pull-down methods. In contrast, no observable heterodimer was detected by mixing purified hsGCβ195or hsGCα259in vitro. The above observations revealed that the heme domain of sGC indeed contributed to the sGC heterodimerization to a certain extent, which may be regulated by in vivo signaling.
In addition, we devoted much effort to study the crystal structure of α1/β1heme domain. Recently and fortunately, we cultured several hsGCβ195-α259and hsGCβ195H105G-α259crystals, containing apo, heme-containing, CO-bound and NO-bound forms. The diffraction data have collected and the structure determination is undergoing. We believe that the related crystal structure will broaden our knowledge of the structure-property-reactivity relationships of sGC and be beneficial for understanding the overall structure of the heme binding site of hsGC and the NO/CO signaling mechanism.
真核生物sGC是一个含b型血红素,由α和β亚基组成的异源二聚体蛋白,每个亚基分别有两种异构体形式(α1/α2和β1/β2),其中以α1β1这种异源二聚体形式最为广泛,研究也最多。按照同源序列和结构功能的分析,α和β亚基都可以大致分为三大结构域,分别是N-端血红素结构域(属于H-NOX家族)、中间结构域(也有将其细分为Per/Arnt/Sim (PAS)-like结构域和螺旋卷曲(CC)结构域)和C-端催化结构域。其中血红素结构域是sGC研究的核心,因为它正是信号分子NO/CO等的调节结构域,信号小分子的调节机理研究对NO信号转导异常所引发的疾病诊断治疗及新药开发具有重要的指导意义,也是近年来化学生物学研究领域的热点。
sGC的研究已历经三十多年,目前已有近5000篇文献报道。但是许多关键问题尚未彻底解决,一直存在争议。例如,血红素是sGC活性调节的一个重要的辅基,但是它的结合区域及方式备受争议；NO激活及失活机理也是众说纷纭,仍无定论；α和β亚基异源二聚关键作用部位及其作用机理也尚待解决；sGC的晶体结构更是鲜有报道。所有问题的一大源头就是能否获取足量的蛋白。这么多年来sGC蛋白多数都是通过组织提取或者昆虫细胞表达而得,但是这些方法蛋白的产量都不高,而且耗费高,可以满足对其活性的测定研究,但是在很大程度上它限制了sGC的深入研究,尤其是在分子水平上详细研究其结构-性质-反应关系。大肠杆菌一直都以高效率、低成本、高产量著称,因此能否在大肠杆菌中成功的表达纯化我们所需的sGC蛋白是该课题研究之初最大的挑战。
本论文的核心内容是集中在对sGC血红素结构域的研究。首先我们对人sGC (hsGC)β1亚基的N-端血红素结构域片段和全长蛋白(hsGCβ195,hsGCβ384和hsGC(3619)进行了质粒构建及其在大肠杆菌中的表达与纯化研究,成功建立了一套hsGC蛋白的高效表达与纯化体系(产量约20mg/L培养液),解决了sGC研究中的第一大瓶颈问题,为之后的结构-性质-反应研究奠定了很好的基础。这一体系我们已经申请了专利。通过同源结构模拟及能量优化我们得到了hsGCβ195蛋白的结构模型。在血红素重组基础上,我们对含血红素的hsGC蛋白进行了紫外可见光谱、EPR谱、圆二色光谱、荧光光谱的性质研究,研究发现血红素结构域(hsGCβ195)可以作为一个很好的工具用以进行sGC血红素相关的性质研究。变温圆二色光谱结果表明hsGCβ195蛋白脱辅基和含血红素形式的转变中点温度分别是56±1℃和54±3℃,说明两种形式都具有较好的热稳定性。pH滴定实验结果显示酸滴定和碱滴定的滴定中点(pKa)值分别为5.7±0.2和9.3±0.1,说明hsGCβ195蛋白具有较好的碱稳定性,但是在酸性条件下血红素容易脱出,蛋白容易沉淀。hsGCβ195蛋白中只含有一个色氨酸(Trp22),通过监测Trp22内源荧光光谱可以用来研究蛋白的构象变化。Trp22荧光结果显示：脱辅基hsGCβ195中Trp22处于比较疏水的环境,血红素重组后荧光最大发射波长(λmax)红移,荧光信号强度大幅度下降,说明蛋白的构象发生了较大的变化,尤其是还原态和NO结合态,荧光信号几乎完全淬灭。我们推测是血红素结合后引发第一个α螺旋(aA)构象变化,使得Glu10(位于aA螺旋上)与Trp22相对位置改变并淬灭荧光。1-苯胺基萘-8-磺酸(ANS)是一个常用的疏水荧光探针,ANS外源荧光光谱结果显示ANS可能会与血红素部分竞争结合sGC疏水腔。
为了探讨血红素的结合区域及作用方式,我们成功构建并表达纯化了α1亚基血红素结构域(hsGCa259)蛋白,并首次探索了其在血红素结合、NO/CO结合上的性质特征。同源结构模拟及能量优化得到的hsGCa259同源结构显示该蛋白存在一个大的空腔,血红素重组结果显示血红素可以稳定结合到hsGCa259上,因此我们推测该空腔主要作用是用于血红素的结合。EPR谱进而证实α1和β1两个亚基在结合血红素的微环境上最大的区别在于β1亚基有一个近端轴向配体(His105)配位而α1亚基缺乏强的轴向配体。血红素转移及ANS外源荧光实验表明hsGCa259可能是通过强的疏水相互作用稳定结合血红素的。我们认为：在异源二聚sGC蛋白中,α1和β1亚基的N-端血红素结构域共同参与了血红素的结合,其中β1亚基提供一个轴向配体(His105)与血红素铁配位,而α1主要是以疏水相互作用稳定血红素的结合。我们进而研究了hsGCa259和hsGCβ195的CO和NO结合过程。在CO结合过程的稳态平衡滴定和动力学结果的基础上我们提出了一个可能的CO结合模型。NO解离过程的研究表明NO解离是一个复杂的过程,需要用二级反应进行拟合,可能是由于NO结合态具有"open"和‘'closed"两种构象,这两种构象在电子吸收光谱上没有区别,但是在活性调节上有所区分。曾经有报道推测hsGCa259蛋白的空腔是用于sGC激活剂(如YC-1)的结合,YC-1的结合会增加sGC对CO的亲和力。但是我们CO滴定的结果显示YC-1对CO结合没有影响,等温滴定量热(ITC)测定结果也表明YC-1与hsGCα259并没有强的相互作用。
为了详细研究轴向配位(Fe-H105)的作用,我们构建了hsGCβ195H105G突变体蛋白并进行详细的性质表征。EPR谱证明该蛋白的确没有了强的轴向配位。Trp22内源荧光结果也显示：Hisl05突变前后脱辅基蛋白的构象变化不大,但是血红素重组后的蛋白构象有明显的改变。血红素转移和血红素还原实验表明轴向配体(H105)对提高血红素亲和力的作用不大,但是它可以减缓血红素氧化丢失进而对蛋白起到一定的保护作用,这在生理过程中具有重要意义。基于氧化态及脱辅基sGC的药物设计(sGC激活剂,sGC activator)是心血管疾病治疗的另一思路。
为了研究异源二聚对血红素结构域的结构-性质-反应的影响,我们通过添加linker的方式将α1和β1两个亚基血红素结构域连接起来,构建出了一个新的蛋白质(hsGCβ195-α259)并对其进行了详细的表征。圆二色光谱及Trp22内源荧光光谱结果都表明该蛋白与单个亚基相比发生了很大的构象变化,并具有很好的稳定性。血红素重组及EPR谱结果显示：hsGCp195-α259能够稳定结合血红素,但是其结合方式与α1亚基相似,其序列中的His105并没有与血红素轴向配位。我们推测hsGCp195-α259中血红素构象存在两种可能性：一是血红素主要还是结合在β195的疏水腔里,添加linker及α1259后β195与α259相互作用使得蛋白构象发生一定的变化,血红素远离H105,从而无法配位；另一种方式是linker的添加使得血红素进入β195的入口受阻,血红素主要结合在a259的疏水空腔,血红素与H105距离较远而无法配位,但是血红素具体的结合方式还有待于进一步的实验验证或者晶体结构的解析。对CO结合和NO解离过程的研究表明：hsGCβ195-α259蛋白与单个亚基相比,CO亲和力增加了近一倍,NO解离速率加快了约一倍。除此之外,我们还将p195和a259同时构建到pETDuet-1载体中以实现两个亚基的共表达。Amylose和Ni-NTA pull-down实验结果表明这两个亚基在体内的确存在相互作用。而分别表达纯化的β195和a259在体外混合后却不能发生相互作用形成异源二聚蛋白。这一结果一方面说明sGC的血红素结构域对异源二聚具有一定的贡献,同时也反映出sGC异源二聚可能是由体内信号调节完成的。
最后,我们还对sGC血红素结构域在晶体学方面进行了初步研究。经过大量的结晶条件筛选及多次尝试,最终我们成功培养出了hsGCβ195-α259和hsGCβ195H105G-α259突变体的脱辅基及含血红素形式蛋白的多种晶体,并已经获得晶体衍射数据,结构的解析工作正在进行中。晶体结构的解析将为理解sGC的血红素结合方式、NO调节机理提供重要的结构基础。
The Nobel Prize in physiology and medicine in1998was awarded to R. F. Furchgott, L. J. Ignarro, and F. Murad for their discovery of "the nitric oxide (NO) as a signaling molecule in the cardiovascular system". This stimulated intense interests of scientists in the study on soluble guanylate cyclase (sGC) mediated NO-signaling system. sGC, as a nitric oxide sensor, is a critical heme-containing enzyme in NO-signaling pathway of eukaryotes. Upon NO binding, sGC catalyzes the conversion of guanosine5'-triphosphate (GTP) to3',5'-cyclic guanosine monophosphate (cGMP). cGMP, as an important second messenger, regulates several effector proteins and plays an important role in many physiological processes, for example, vasodilatation, smooth muscle relaxation, platelet aggregation, and neuronal transmission. Dysfunction of NO signaling results in many pathological disorders, ranging from several cardiovascular diseases, such as arterial hypertension, pulmonary hypertension, heart failure, atherosclerosis and restenosis, to neurodegenerative diseases.
sGC in eukaryote is a heterodimeric hemoprotein, composed of a and β subunit. For human sGC, there are two isoforms for each subunit in vivo:α1/α2and (β1/β2, while the α1β1heterodimer is the more abundant. The prosthetic heme moiety, crucial for NO sensing, is located in the heme binding domain with His105of β1subunit as the axial ligand. Both α and β subunit can be divided into three domains:the N-terminal heme domain (H-NOX family), central domain (containing Per/Armt/Sim (PAS)-like region and Coiled-coil region) and the C-terminal catalytic domain. The heme domain, responsible for heme binding and NO/CO binding, is one of the most important and popular regions in sGC study.
In the past decades, there were nearly5,000papers published in this area. However, several crucial problems are still unclear and controversial. For example, the exact heme binding region and environment is to be determined; the exact mechanism of NO activation and deactivation is unknown although several models have been proposed; the region for the heterodimerization regulation and related mechanism is ambiguous; all the above problems are largely due to the limited structural information for sGC structure. Limited availability of large quantities of highly pure sGC and its large size has impeded analysis of the crystal structure. Originally, sGC was isolated from a number of mammalian tissues, mainly bovine and rat lungs. In the case of human isoforms, direct isolation from native sources becomes virtually impossible. Although the functional expression of recombinant human sGC was achieved in the baculovirus/sf9cells, the yield of human sGC was relatively limited. To this end, the E. coli expression system is the most desired method to overexpress sGC. However, the overexpression and purification of eukaryotic sGC is one of the bottle neck for sGC study and hardly reported.
This thesis is focused on the heme domain of human sGC (hsGC). We report, for the first time, the recombinant hsGC in full-length (hsGCβ619) and its truncated N-terminal fragments with195and384residues (hsGCβ195and hsGCβ384), which were overexpressed in E. coli and purified successfully with a yield of20mg/L cell culture. This highly efficient E. coli expression system of hsGC proteins is critical to the study of the structure, function and catalytic mechanism of human sGC and we have submitted the application of patent. As for sGC heme domain, there are only two published crystal structures of H-NOX domain from bacteria, Tt H-NOX and Ns H-NOX. Based on the crystal structure of Ns H-NOX domain (pdb entry:2O09), the homology model of hsGCβ195was constructed through energy optimization by NAMD program. After heme reconstitution, the three proteins in different forms (ferric, ferrous, NO-bound and CO-bound) were characterized via UV-vis, EPR, CD and fluorescence spectroscopy. The characterization results suggested that hsGCβ195, as an excellent tool, can be used to further study the sGC heme pocket and NO activation/deactivation mechanism. The midpoint temperature (Tm) of conformation transition for the apo-hsGCβ195and heme-hsGCβ195is56±1℃and54±3℃, respectively, indicating the similar and good stability for temperature. The pH titration results showed that the midpoint pH (pKa) for the acid and alkaline transition process is5.7±0.2and9.3±0.1, respectively. hsGCβ195exhibites desirable stability in alkaline condition, while hsGCβ195easily precipitates along with heme dissociation in acidic condition. Trp22, the only tryptophan residue in hsGCβ195, can be used to study the conformation change with the intrinsic fluorescence spectra measurement. The Trp22fluorescence spectra revealed that Trp22was at a relative hydrophobic environment with the maximum emission wavelength (λmax) at327nm for the apo-hsGCβ195protein. Heme reconstitution resulted in the λmax red-shifting and a largely concomitant decrease in the fluorescence intensity, revealing the large conformation change occurred, especially for the ferrous and NO-bound forms. We conferred that the heme binding induced the movement of the first a-helix (aA), leading to the change of relative position between Glu10(located at aA) and Trp22and further quench the Trp22fluorescence. ANS fluorescence is commonly to investigate the hydrophobic properties of proteins. We found that ANS could bind to some part of sGC hydrophobic pocket and complete with heme binding.
To further explore the heme binding region and heme pocket microenvironment, the heme domain of hsGC al subunit (hsGCa259) was constructed, expressed and purified. The homology model of hsGCa259displayed a large hydrophobic pocket and the heme could be located at hsGCa259stably via heme reconstitution, which resulted in the speculation that the role of the pocket is heme binding. The EPR spectra of ferric hsGC identified that the heme of hsGCβ195is5-coordinate high spin with His105as the axial ligand, while both the axial ligands of the heme in hsGCa259are weak, probably H2O. We guessed that heme binds to hsGCa259probably with strong hydrophobic interaction according to heme transfer and ANS fluorescence measurements. This is the first direct evidence that both the heme domain of al and β1subunit contribute to the heme binding. The CO and NO binding equilibrium and kinetics of hsGCa259and hsGCβ195were carried out by UV-vis and stopped-flow measurement. One possible CO binding model is proposed. NO dissociation results suggested that NO dissociation is a more complex process and possibly two different but UV-vis spectroscopy indistinguishable NO-bound heme existed. Recently, the pocket of hsGCα1subunit was inferred to YC-1binding, which will lead to CO affinity increase. However, we found that YC-1had little effect on CO affinity, the isothermal titration calorimetry (ITC) also indicated no obvious interaction between YC-1and hsGCa259.
In order to investigate the exact role of the heme axial ligand (His105), hsGCβ195H105G was constructed and fully characterized. EPR spectra proved that the axial ligand was removed in hsGCβ195H105G. The Trp22fluorescence indicated that the H105G mutation had little effect on the apo-hsGCβ195conformation, while exhibited large influence on the heme-hsGCβ195conformation. The heme transfer and reduction experiments suggested that H105mainly increase the heme reduced potential and protect the protein from heme oxidation and loss, which is critical for several physiological processes.
On the purpose of studying the effect of heterodimerization on the heme binding properties, hsGCβ195-a259, the hybrid protein of hsGCβ195and hsGCa259linked with GSGSGG peptide, was constructed and detailed characterized. The CD and Trp22fluorescence spectra demonstrated that hsGCβ195-α259displayed tremendous conformation change compared to hsGCβ195or hsGCα259with excellent stability. The heme reconstitution and EPR spectra identified that hsGCβ195-α259could bind heme via the similar fashion with that of hsGCα259, in which His105did not bond to heme. We conferred that there are two possible modes of heme location in hsGCβ195-α259. The first possibility is that heme mainly resides at the hydrophobic pocket of β195. The addition of linker and α259induces a large conformation change through interaction with β195, resulting that H105is not close enough to bond with heme. The other situation is that the entrance of heme to β195is blocked by the addition of linker and α259, which leads to the impossible bonding between H105and heme. The exact heme binding pattern awaits further experiments, particularly the resolution of crystal structure. The CO and NO binding results showed that hsGCβ195-α259exhibited higher CO affinity (almost twice) and larger NO dissociation rates (approximate twice) compared with hsGCβ195or hsGCα259. Besides, we co-expressed hsGCβ195and hsGCα259by inserting β195and α259into the two multi-cloning sites (MCS) of pETDuet-1vector, respectively and demonstrated that hsGCβ195definitely interacted with hsGCα259in vivo through Amylose pull-down and Ni-NTA pull-down methods. In contrast, no observable heterodimer was detected by mixing purified hsGCβ195or hsGCα259in vitro. The above observations revealed that the heme domain of sGC indeed contributed to the sGC heterodimerization to a certain extent, which may be regulated by in vivo signaling.
In addition, we devoted much effort to study the crystal structure of α1/β1heme domain. Recently and fortunately, we cultured several hsGCβ195-α259and hsGCβ195H105G-α259crystals, containing apo, heme-containing, CO-bound and NO-bound forms. The diffraction data have collected and the structure determination is undergoing. We believe that the related crystal structure will broaden our knowledge of the structure-property-reactivity relationships of sGC and be beneficial for understanding the overall structure of the heme binding site of hsGC and the NO/CO signaling mechanism.
引文
[1]de Mel A, Murad F, Seifalian AM, Nitric oxide:a guardian for vascular grafts? [J]. Chemical Reviews,2011,111(9):5742-67.
[2]Moller JK, Skibsted LH, Nitric oxide and myoglobins [J]. Chemical Reviews, 2002,102(4):1167-78.
[3]Peluffo G, Radi R, Biochemistry of protein tyrosine nitration in cardiovascular pathology [J]. Cardiovasc Res,2007,75(2):291-302.
[4]Shi W, Wang X, Shih DM, Laubach VE, Navab M, Lusis AJ, Paradoxical reduction of fatty streak formation in mice lacking endothelial nitric oxide synthase [J]. Circulation,2002,105(17):2078-82.
[5]Reiter TA, Pang B, Dedon P, Demple B, Resistance to nitric oxide-induced necrosis in heme oxygenase-1 overexpressing pulmonary epithelial cells associated with decreased lipid peroxidation [J]. J Biol Chem,2006,281(48): 36603-12.
[6]Virag L, Szabo E, Gergely P, Szabo C, Peroxynitrite-induced cytotoxicity: mechanism and opportunities for intervention [J].0378-4274,2003,140-141: 113-24.
[7]Goldstein S, Lind J, Merenyi G, Chemistry of peroxynitrites as compared to peroxynitrates [J]. Chemical Reviews,2005,105(6):2457-70.
[8]Hill BG, Dranka BP, Bailey SM, Lancaster JR, Jr., Darley-Usmar VM, What part of NO don't you understand? Some answers to the cardinal questions in nitric oxide biology [J]. J Biol Chem,2010,285(26):19699-704.
[9]Hall CN, Garthwaite J, What is the real physiological NO concentration in vivo? [J]. Nitric Oxide,2009,21 (2):92-103.
[10]Coulter JA, McCarthy HO, Xiang J, Roedl W, Wagner E, Robson T, Hirst DG, Nitric oxide--a novel therapeutic for cancer [J]. Nitric Oxide,2008,19(2):192-8.
[11]Chen KJ, Pittman RN, Popel AS, Nitric oxide in the vasculature:Where does it come from and where does it go? A quantitative perspective [J]. Antioxidants & Redox Signaling,2008,10(7):1185-1198.
[12]Pacher P, Beckman JS, Liaudet L, Nitric oxide and peroxynitrite in health and disease [J]. Physiol Rev,2007,87(1):315-424.
[13]Thippeswamy T, McKay JS, Quinn JP, Morris R, Nitric oxide, a biological double-faced janus-is this good or bad? [J]. Histol Histopathol,2006,21(4): 445-58.
[14]Denninger JW, Marletta MA, Guanylate cyclase and the.NO/cGMP signaling pathway [J]. Biochim Biophys Acta,1999,1411(2-3):334-50.
[15]Evgenov OV, Pacher P, Schmidt PM, Hasko G, Schmidt HH, Stasch JP, NO-independent stimulators and activators of soluble guanylate cyclase: discovery and therapeutic potential [J]. Nat Rev Drug Discov,2006,5(9): 755-68.
[16]Wang-Rosenke Y, Neumayer HH, Peters H, NO signaling through cGMP in renal tissue fibrosis and beyond:key pathway and novel therapeutic target [J]. Curr Med Chem,2008,15(14):1396-406.
[17]Stasch JP, Pacher P, Evgenov OV, Soluble guanylate cyclase as an emerging therapeutic target in cardiopulmonary disease [J]. Circulation,2011,123(20): 2263-73.
[18]Potter LR, Guanylyl cyclase structure, function and regulation [J]. Cell Signal, 2011.
[19]Pellicena P, Karow DS, Boon EM, Marietta MA, Kuriyan J, Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases [J]. Proc Natl Acad Sci U S A,2004,101(35):12854-12859.
[20]Schmidt PM, Schramm M, Schroder H, Wunder F, Stasch JP, Identification of residues crucially involved in the binding of the heme moiety of soluble guanylate cyclase [J]. J Biol Chem,2004,279(4):3025-32.
[21]Zhong F, Wang H, Ying T, Huang ZX, Tan X, Efficient expression of human soluble guanylate cyclase in Escherichia coli and its signaling-related interaction with nitric oxide [J]. Amino Acids,2010,39:399-408.
[22]Haase N, Haase T, Kraehling JR, Behrends S, Direct fusion of subunits of heterodimeric nitric oxide sensitive guanylyl cyclase leads to functional enzymes with preserved biochemical properties:evidence for isoform specific activation by ciguates [J]. Biochemical Pharmacology,2010,80(11):1676-83.
[23]Buechler WA, Nakane M, Murad F, Expression of soluble guanylate cyclase activity requires both enzyme subunits [J]. Biochemical and Biophysical Research Communications,1991,174(1):351-7.
[24]Nakane M, Arai K, Saheki S, Kuno T, Buechler W, Murad F, Molecular-cloning and expression of cDNAs coding for soluble guanylate-cyclase from rat lung [J]. Journal of Biological Chemistry,1990,265(28):16841-16845.
[25]Harteneck C, Wedel B, Koesling D, Malkewitz J, Bohme E, Schultz G, Molecular cloning and expression of a new alpha-subunit of soluble guanylyl cyclase. Interchangeability of the alpha-subunits of the enzyme [J]. FEBS Letters, 1991,292(1-2):217-22.
[26]Yuen PS, Potter LR, Garbers DL, A new form of guanylyl cyclase is preferentially expressed in rat kidney [J]. Biochemistry (Mosc),1990,29(49): 10872-8.
[27]Mergia E, Russwurm M, Zoidl G, Koesling D, Major occurrence of the new alpha2betal isoform of NO-sensitive guanylyl cyclase in brain [J]. Cell Signal, 2003,15(2):189-95.
[28]Russwurm M, Behrends S, Harteneck C, Koesling D, Functional properties of a naturally occurring isoform of soluble guanylyl cyclase [J]. Biochemical Journal, 1998,335 (Pt 1):125-30.
[29]Zabel U, Hausler C, Weeger M, Schmidt HH, Homodimerization of soluble guanylyl cyclase subunits. Dimerization analysis using a glutathione s-transferase affinity tag [J]. J Biol Chem,1999,274(26):18149-52.
[30]Hsieh CL, Cai C, Giwa A, Bivins A, Chen SY, Sabry D, Govardhan K, Shemshedini L, Expression of a hyperactive androgen receptor leads to androgen-independent growth of prostate cancer cells [J]. J Mol Endocrinol, 2008,41(1):13-23.
[31]Cai C, Chen SY, Zheng Z, Omwancha J, Lin MF, Balk SP, Shemshedini L, Androgen regulation of soluble guanylyl cyclasealphal mediates prostate cancer cell proliferation [J]. Oncogene,2007,26(11):1606-15.
[32]Pifarre P, Baltrons MA, Foldi I, Garcia A, NO-sensitive guanylyl cyclase betal subunit is peripherally associated to chromosomes during mitosis. Novel role in chromatin condensation and cell cycle progression [J]. Int J Biochem Cell Biol., 2009,41(8-9):1719-30.
[33]Ignarro LJ, Degnan JN, Baricos WH, Kadowitz PJ, Wolin MS, Activation of purified guanylate cyclase by nitric oxide requires heme-comparison of heme-deficient, heme-reconstituted and heme-containing forms of soluble enzyme from bovine lung [J]. Biochimica Et Biophysica Acta,1982,718(1): 49-59.
[34]Makino R, Obayashi E, Homma N, Shiro Y, Hori H, YC-1 facilitates release of the proximal His residue in the NO and CO complexes of soluble guanylate cyclase [J]. J Biol Chem,2003,278(13):11130-7.
[35]Mathis KJ, Emmons TL, Curran DF, Day JE, Tomasselli AG, High yield purification of soluble guanylate cyclase from bovine lung [J]. Protein Expr Purif, 2008,60(1):58-63.
[36]Ohlstein EH, Wood KS, Ignarro LJ, Purification and properties of heme-deficient hepatic soluble guanylate cyclase:effects of heme and other factors on enzyme activation by NO, NO-heme, and protoporphyrin Ⅸ [J]. Arch Biochem Biophys, 1982,218(1):187-98.
[37]Stone JR. Marietta MA, Spectral and kinetic studies on the activation of soluble guanylate cyclase by nitric oxide [J]. Biochemistry (Mosc),1996,35(4):1093-9.
[38]Stone JR, Sands RH, Dunham WR, Marietta MA, Electron paramagnetic resonance spectral evidence for the formation of a pentacoordinate nitrosyl-heme complex on soluble guanylate cyclase [J]. Biochem Biophys Res Commun,1995, 207(2):572-7.
[39]Wolin MS, Wood KS, Ignarro LJ, Guanylate cyclase from bovine lung. A kinetic analysis of the regulation of the purified soluble enzyme by protoporphyrin IX, heme, and nitrosyl-heme [J]. J Biol Chem,1982,257(22):13312-20.
[40]Zabel U, Weeger M, La M, Schmidt HH, Human soluble guanylate cyclase: functional expression and revised isoenzyme family [J]. Biochem J,1998,335 (Pt 1):51-7.
[41]Hoenicka M, Becker EM, Apeler H, Sirichoke T, Schroder H, Gerzer R, Stasch JP, Purified soluble guanylyl cyclase expressed in a baculovirus/Sf9 system: stimulation by YC-1, nitric oxide, and carbon monoxide [J]. J Mol Med,1999, 77(1):14-23.
[42]Lee YC, Martin E, Murad F, Human recombinant soluble guanylyl cyclase: Expression, purification, and regulation [J]. Proc Natl Acad Sci U S A,2000, 97(20):10763-10768.
[43]Haase T, Haase N, Kraehling JR, Behrends S, Fluorescent fusion proteins of soluble guanylyl cyclase indicate proximity of the heme nitric oxide domain and catalytic domain [J]. PLoS One,2010,5(7):e11617.
[44]Zhao Y, Marietta MA, Localization of the heme binding region in soluble guanylate cyclase [J]. Biochemistry (Mosc),1997,36(50):15959-64.
[45]Karow DS, Pan DH, Davis JH, Behrends S, Mathies RA, Marietta MA, Characterization of functional heme domains from soluble guanylate cyclase [J]. Biochemistry (Mosc),2005,44(49):16266-16274.
[46]Winger JA, Marietta MA, Expression and characterization of the catalytic domains of soluble guanylate cyclase:Interaction with the heme domain [J]. Biochemistry (Mosc),2005,44(10):4083-4090.
[47]Furchgott RF, Zawadzki JV, The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine [J]. Nature,1980, 288(5789):373-6.
[48]Lewicki JA, Brandwein HJ, Waldman SA, Murad F, Purified guanylate cyclase: characterization, iodination and preparation of monoclonal antibodies [J]. J Cyclic Nucleotide Res,1980,6(4):283-96.
[49]Ignarro LJ, Byrns RE, Buga GM, Wood KS, Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties identical to those of nitric oxide radical [J]. Circ Res,1987,61(6): 866-79.
[50]Ignarro LJ, Wood KS, Wolin MS, Activation of purified soluble guanylate cyclase by photopophyrin-IX [J]. Proceedings of the National Academy of Sciences of the United States of America-Biological Sciences,1982,79(9): 2870-2873.
[51]Stone JR, Marietta MA, Soluble guanylate cyclase from bovine lung:activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states [J]. Biochemistry (Mosc),1994,33(18):5636-40.
[52]Wedel B, Humbert P, Harteneck C, Foerster J, Malkewitz J, Bohme E, Schultz G, Koesling D, Mutation of His-105 in the beta 1 subunit yields a nitric oxide-insensitive form of soluble guanylyl cyclase [J]. Proc Natl Acad Sci U S A, 1994,91(7):2592-6.
[53]Zhao Y, Brandish PE, Ballou DP, Marietta MA, A molecular basis for nitric oxide sensing by soluble guanylate cyclase [J]. Proc Natl Acad Sci U S A,1999, 96(26):14753-8.
[54]Bellamy TC, Wood J, Garthwaite J, On the activation of soluble guanylyl cyclase by nitric oxide [J]. Proc Nat1 Acad Sci U S A,2002,99(1):507-10.
[55]Ballou DP, Zhao Y, Brandish PE, Marietta MA, Revisiting the kinetics of nitric oxide (NO) binding to soluble guanylate cyclase:the simple NO-binding model is incorrect [J]. Proc Natl Acad Sci U S A,2002,99(19):12097-101.
[56]Cary SPL, Winger JA, Marietta MA, Tonic and acute nitric oxide signaling through soluble guanylate cyclase is mediated by nonheme nitric oxide, ATP, and GTP [J]. Proc Natl Acad Sci U S A,2005,102(37):13064-13069.
[57]Russwurm M, Koesling D, NO activation of guanylyl cyclase [J]. EMBO Journal, 2004,23(22):4443-50.
[58]Lawson DM, Stevenson CE, Andrew CR, Eady RR, Unprecedented proximal binding of nitric oxide to heme:implications for guanylate cyclase [J]. EMBO Journal,2000,19(21):5661-71.
[59]Derbyshire ER, Marietta MA, Butyl isocyanide as a probe of the activation mechanism of soluble guanylate cyclase [J]. J Biol Chem,2007,282(49): 35741-35748.
[60]Margulis A, Sitaramayya A, Rate of deactivation of nitric oxide-stimulated soluble guanylate cyclase:influence of nitric oxide scavengers and calcium [J]. Biochemistry (Mosc),2000,39(5):1034-9.
[61]Kharitonov VG, Russwurm M, Magde D, Sharma VS, Koesling D, Dissociation of nitric oxide from soluble guanylate cyclase [J]. Biochem Biophys Res Commun,1997,239(1):284-6.
[62]Brandish PE, Buechler W, Marletta MA, Regeneration of the ferrous heme of soluble guanylate cyclase from the nitric oxide complex:acceleration by thiols and oxyhemoglobin [J]. Biochemistry (Mosc),1998,37(48):16898-907.
[63]Makino R, Matsuda H, Obayashi E, Shiro Y, Iizuka T, Hori H, EPR characterization of axial bond in metal center of native and cobalt-substituted guanylate cyclase [J]. J Biol Chem,1999,274(12):7714-23.
[64]Bellamy TC, Wood J, Goodwin DA, Garthwaite J, Rapid desensitization of the nitric oxide receptor, soluble guanylyl cyclase, underlies diversity of cellular cGMP responses [J]. Proc Natl Acad Sci U S A,2000,97(6):2928-33.
[65]Bellamy TC, Garthwaite J, Sub-second kinetics of the nitric oxide receptor, soluble guanylyl cyclase, in intact cerebellar cells [J]. J Biol Chem,2001,276(6): 4287-92.
[66]Winger JA, Derbyshire ER, Marietta MA, Dissociation of nitric oxide from soluble guanylate cyclase and heme-nitric oxide/oxygen binding domain constructs [J]. J Biol Chem,2007,282(2):897-907.
[67]Aono S, Metal-containing sensor proteins sensing diatomic gas molecules [J]. Dalton Trans,2008, (24):3137-46.
[68]Chen L, Lyubimov AY, Brammer L, Vrielink A, Sampson NS, The binding and release of oxygen and hydrogen peroxide are directed by a hydrophobic tunnel in cholesterol oxidase [J]. Biochemistry (Mosc),2008,47(19):5368-77.
[69]Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS, Protein S-nitrosylation:purview and parameters [J]. Nat Rev Mol Cell Biol,2005,6(2): 150-66.
[70]Sayed N, Baskaran P, Ma X, van den Akker F, Beuve A, Desensitization of soluble guanylyl cyclase, the NO receptor, by S-nitrosylation [J]. Proc Natl Acad Sci USA,2007,104(30):12312-7.
[71]Iyer AK, Azad N, Wang L, Rojanasakul Y, Role of S-nitrosylation in apoptosis resistance and carcinogenesis [J]. Nitric Oxide,2008,19(2):146-51.
[72]Sayed N, Kim DD, Fioramonti X, Iwahashi T, Duran WN, Beuve A, Nitroglycerin-induced S-nitrosylation and desensitization of soluble guanylyl cyclase contribute to nitrate tolerance [J]. Circ Res,2008,103(6):606-14.
[73]Lima B, Forrester MT, Hess DT, Stamler JS, S-nitrosylation in cardiovascular signaling [J]. Circ Res,2010,106(4):633-46.
[74]Martinez-Ruiz A, Cadenas S, Lamas S, Nitric oxide signaling:classical, less classical, and nonclassical mechanisms [J]. Free Radical Biology and Medicine, 2011,51(1):17-29.
[75]Brandwein HJ, Lewicki JA, Murad F, Reversible inactivation of guanylate cyclase by mixed disulfide formation [J]. J Biol Chem,1981,256(6):2958-62.
[76]DeMaster EG, Quast BJ, Redfern B, Nagasawa HT, Reaction of nitric oxide with the free sulfhydryl group of human serum albumin yields a sulfenic acid and nitrous oxide [J]. Biochemistry (Mosc),1995,34(36):11494-9.
[77]Artz JD, Schmidt B, McCracken JL, Marietta MA, Effects of nitroglycerin on soluble guanylate cyclase:implications for nitrate tolerance [J]. J Biol Chem, 2002,277(21):18253-6.
[78]Gonrren AC, Russwurm M, Kollau A, Koesling D, Schmidt K, Mayer B, Effects of nitroglycerin/L-cysteine on soluble guanylate cyclase:evidence for an activation/inactivation equilibrium controlled by nitric oxide binding and haem oxidation [J]. Biochemical Journal,2005,390(Pt 2):625-31.
[79]Fernhoff NB, Derbyshire ER, Marletta MA, A nitric oxide/cysteine interaction mediates the activation of soluble guanylate cyclase [J]. Proc Natl Acad Sci U S A,2009,106(51):21602-7.
[80]Mayer B, Kleschyov AL, Stessel H, Russwurm M, Munzel T, Koesling D, Schmidt K, Inactivation of soluble guanylate cyclase by stoichiometric S-nitrosation [J]. Molecular Pharmacology,2009,75(4):886-91.
[81]Miller TW, Cherney MM, Lee AJ, Francoleon NE, Farmer PJ, King SB, Hobbs AJ, Miranda KM, Burstyn JN, Fukuto JM, The effects of nitroxyl (HNO) on soluble guanylate cyclase activity:interactions at ferrous heme and cysteine thiols [J]. J Biol Chem,2009,284(33):21788-96.
[82]Riego JA, Broniowska KA, Kettenhofen NJ, Hogg N, Activation and inhibition of soluble guanylyl cyclase by S-nitrosocysteine:involvement of amino acid transport system L [J]. Free Radical Biology and Medicine,2009,47(3):269-74.
[83]Murthy KS, Modulation of soluble guanylate cyclase activity by phosphorylation [J]. Neurochem Int,2004,45(6):845-51.
[84]Meurer S, Pioch S, Gross S, Muller-Esterl W, Reactive oxygen species induce tyrosine phosphorylation of and Src kinase recruitment to NO-sensitive guanylyl cyclase [J]. J Biol Chem,2005,280(39):33149-56.
[85]Murad F, Shattuck Lecture. Nitric oxide and cyclic GMP in cell signaling and drug development [J]. N Engl J Med,2006,355(19):2003-11.
[86]Lubos E, Handy DE, Loscalzo J, Role of oxidative stress and nitric oxide in atherothrombosis [J]. Front Biosci,2008,13:5323-44.
[87]Tsai EJ, Kass DA, Cyclic GMP signaling in cardiovascular pathophysiology and therapeutics [J]. Pharmacol Ther,2009,122(3):216-38.
[88]McLaughlin VV, Archer SL, Badesch DB, Barst RJ, Farber HW, Lindner JR, Mathier MA, McGoon MD, Park MH, Rosenson RS, Rubin LJ, Tapson VF, Varga J, Harrington RA, Anderson JL, Bates ER, Bridges CR, Eisenberg MJ, Ferrari VA, Grines CL, Hlatky MA, Jacobs AK, Kaul S, Lichtenberg RC, Moliterno DJ, Mukherjee D, Pohost GM, Schofield RS, Shubrooks SJ, Stein JH, Tracy CM, Weitz HH, Wesley DJ, ACCF/AHA 2009 expert consensus document on pulmonary hypertension:a report of the American College of Cardiology Foundation Task Force on Expert Consensus Documents and the American Heart Association:developed in collaboration with the American College of Chest Physicians, American Thoracic Society, Inc., and the Pulmonary Hypertension Association [J]. Circulation,2009,119(16):2250-94.
[89]Chirkov YY, Horowitz JD, Impaired tissue responsiveness to organic nitrates and nitric oxide:a new therapeutic frontier? [J]. Pharmacol Ther,2007,116(2): 287-305.
[90]Szabo C, Ischiropoulos H, Radi R, Peroxynitrite:biochemistry, pathophysiology and development of therapeutics [J]. Nat Rev Drug Discov,2007,6(8):662-80.
[91]Ko FN, Wu CC, Kuo SC, Lee FY, Teng CM, YC-1, a novel activator of platelet guanylate cyclase [J]. Blood,1994,84(12):4226-33.
[92]Stasch JP, Becker EM, Alonso-Alija C, Apeler H, Dembowsky K, Feurer A, Gerzer R, Minuth T, Perzborn E, Pleiss U, Schroder H, Schroeder W, Stahl E, Steinke W, Straub A, Schramm M, NO-independent regulatory site on soluble guanylate cyclase [J]. Nature,2001,410(6825):212-215.
[93]Stasch JP, Alonso-Alija C, Apeler H, Dembowsky K, Feurer A, Minuth T, Perzborn E, Schramm M, Straub A, Pharmacological actions of a novel NO-independent guanylyl cyclase stimulator, BAY 41-8543:in vitro studies [J]. Br J Pharmacol,2002,135(2):333-43.
[94]Schmidt P, Schramm M, Schroder H, Stasch JP, Mechanisms of nitric oxide independent activation of soluble guanylyl cyclase [J]. Eur J Pharmacol,2003, 468(3):167-74.
[95]Bischoff E, Stasch JP, Effects of the sGC stimulator BAY 41-2272 are not mediated by phosphodiesterase 5 inhibition [J]. Circulation,2004,110(12): e320-1; author reply e320-1.
[96]Mittendorf J, Weigand S, Alonso-Alija C, Bischoff E, Feurer A, Gerisch M, Kern A, Knorr A, Lang D, Muenter K, Radtke M, Schirok H, Schlemmer KH, Stahl E, Straub A, Wunder F, Stasch JP, Discovery of riociguat (BAY 63-2521):a potent, oral stimulator of soluble guanylate cyclase for the treatment of pulmonary hypertension [J]. ChemMedChem,2009,4(5):853-65.
[97]Ghofrani HA, Hoeper MM, Halank M, Meyer FJ, Staehler G, Behr J, Ewert R, Weimann G, Grimminger F, Riociguat for chronic thromboembolic pulmonary hypertension and pulmonary arterial hypertension:a phase Ⅱ study [J]. Eur Respir J,2010,36(4):792-9.
[98]Gladwin MT, Deconstructing endothelial dysfunction:soluble guanylyl cyclase oxidation and the NO resistance syndrome [J]. J Clin Invest,2006,116(9): 2330-2.
[99]Stasch JP, Schmidt PM, Nedvetsky PI, Nedvetskaya TY, H SA, Meurer S, Deile M, Taye A, Knorr A, Lapp H, Muller H, Turgay Y, Rothkegel C, Tersteegen A, Kemp-Harper B, Muller-Esterl W, Schmidt HH, Targeting the heme-oxidized nitric oxide receptor for selective vasodilatation of diseased blood vessels [J]. J Clin Invest,2006,116(9):2552-61.
[100]Schindler U, Strobel H, Schonafinger K, Linz W, Lohn M, Martorana PA, Rutten H, Schindler PW, Busch AE, Sohn M, Topfer A, Pistorius A, Jannek C, Mulsch A, Biochemistry and pharmacology of novel anthranilic acid derivatives activating heme-oxidized soluble guanylyl cyclase [J]. Molecular Pharmacology, 2006,69(4):1260-8.
[101]Pankey EA, Bhartiya M, Badejo AM, Jr., Haider U, Stasch JP, Murthy SN, Nossaman BD, Kadowitz PJ, Pulmonary and systemic vasodilator responses to the soluble guanylyl cyclase activator, BAY 60-2770, are not dependent on endogenous nitric oxide or reduced heme [J]. Am J Physiol Heart Circ Physiol, 2011,300(3):H792-802.
[102]Gavin AC, Superti-Furga G, Protein complexes and proteome organization from yeast to man [J]. Curr Opin Chem Biol,2003,7(1):21-7.
[103]Alberts B, The cell as a collection of protein machines:preparing the next generation of molecular biologists [J]. Cell,1998,92(3):291-4.
[104]Gavin AC, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon AM, Cruciat CM, Remor M, Hofert C, Schelder M, Brajenovic M, Ruffner H, Merino A, Klein K, Hudak M, Dickson D, Rudi T, Gnau V, Bauch A, Bastuck S, Huhse B, Leutwein C, Heurtier MA, Copley RR, Edelmann A, Querfurth E, Rybin V, Drewes G, Raida M, Bouwmeester T, Bork P, Seraphin B, Kuster B, Neubauer G, Superti-Furga G, Functional organization of the yeast proteome by systematic analysis of protein complexes [J]. Nature,2002, 415(6868):141-7.
[105]Rodriguez P, Braun H, Kolodziej KE, de Boer E, Campbell J, Bonte E, Grosveld F, Philipsen S, Strouboulis J, Isolation of transcription factor complexes by in vivo biotinylation tagging and direct binding to streptavidin beads [J]. Methods Mol Biol,2006,338:305-23.
[106]Li C, Schwabe JW, Banayo E, Evans RM, Coexpression of nuclear receptor partners increases their solubility and biological activities [J]. Proc Natl Acad Sci U S A,1997,94(6):2278-83.
[107]Fribourg S, Romier C, Werten S, Gangloff YG, Poterszman A, Moras D, Dissecting the interaction network of multiprotein complexes by pairwise coexpression of subunits in E. coli [J]. J Mol Biol,2001,306(2):363-73.
[108]Copeland WC, Expression, purification, and characterization of the two human primase subunits and truncated complexes from Escherichia coli [J]. Protein Expr Purif,1997,9(1):1-9.
[109]Johnston K, Clements A, Venkataramani RN, Trievel RC, Marmorstein R, Coexpression of proteins in bacteria using T7-based expression plasmids: expression of heteromeric cell-cycle and transcriptional regulatory complexes [J]. Protein Expr Purif,2000,20(3):435-43.
[110]Fribourg S, Romier C, Werten S, Gangloff YG, Poterszman A, Moras D, Dissecting the interaction network of multiprotein complexes by pairwise coexpression of subunits in E. coli [J]. Journal of Molecular Biology,2001, 306(2):363-73.
[111]Tan S, Kern RC, Selleck W, The pST44 polycistronic expression system for producing protein complexes in Escherichia coli [J]. Protein Expr Purif,2005, 40(2):385-95.
[112]Romier C, Ben Jelloul M, Albeck S, Buchwald G, Busso D, Celie PH, Christodoulou E, De Marco V, van Gerwen S, Knipscheer P, Lebbink JH, Notenboom V, Poterszman A, Rochel N, Cohen SX, Unger T, Sussman JL, Moras D, Sixma TK, Perrakis A, Co-expression of protein complexes in prokaryotic and eukaryotic hosts:experimental procedures, database tracking and case studies [J]. Acta Crystallogr D Biol Crystallogr,2006,62(Pt 10): 1232-42.
[113]Neumann D, Woods A, Carling D, Wallimann T, Schlattner U, Mammalian AMP-activated protein kinase:functional, heterotrimeric complexes by co-expression of subunits in Escherichia coli [J]. Protein Expr Purif,2003,30(2): 230-7.
[114]Kim KJ, Kim HE, Lee KH, Han W, Yi MJ, Jeong J, Oh BH, Two-promoter vector is highly efficient for overproduction of protein complexes [J]. Protein Science,2004,13(6):1698-703.
[115]Alexandrov A, Vignali M, LaCount DJ, Quartley E, de Vries C, De Rosa D, Babulski J, Mitchell SF, Schoenfeld LW, Fields S, Hol WG, Dumont ME, Phizicky EM, Grayhack EJ, A facile method for high-throughput co-expression of protein pairs [J]. Mol Cell Proteomics,2004,3(9):934-8.
[116]Garbers DL, Purification of soluble guanylate cyclase from rat lung [J]. J Biol Chem,1979,254(1):240-3.
[117]Wilson EM, Chinkers M, Identification of sequences mediating guanylyl cyclase dimerization [J]. Biochemistry (Mosc),1995,34(14):4696-701.
[118]Zhou Z, Gross S, Roussos C, Meurer S, Muller-Esterl W, Papapetropoulos A, Structural and functional characterization of the dimerization region of soluble guanylyl cyclase [J]. J Biol Chem,2004,279(24):24935-43.
[119]Wagner C, Russwurm M, Jager R, Friebe A, Koesling D, Dimerization of nitric oxide-sensitive guanylyl cyclase requires the alpha 1 N terminus [J]. J Biol Chem,2005,280(18):17687-93.
[120]Shiga T, Suzuki N, Amphipathic alpha-helix mediates the heterodimerization of soluble guanylyl cyclase [J].0289-0003,2005,22(7):735-42.
[121]Ma X, Sayed N, Baskaran P, Beuve A, van den Akker F, PAS-mediated dimerization of soluble guanylyl cyclase revealed by signal transduction histidine kinase domain crystal structure [J]. J Biol Chem,2008,283(2): 1167-78.
[122]Harteneck C, Koesling D, Soling A, Schultz G, Bohme E, Expression of soluble guanylyl cyclase. Catalytic activity requires two enzyme subunits [J]. FEBS Lett, 1990,272(1-2):221-3.
[123]Haase N, Haase T, Seeanner M, Behrends S, Nitric oxide sensitive guanylyl cyclase activity decreases during cerebral postnatal development because of a reduction in heterodimerization [J]. Journal of Neurochemistry,2010,112(2): 542-51.
[124]Nioche P, Berka V, Vipond J, Minton N, Tsai AL, Raman CS, Femtomolar sensitivity of a NO sensor from Clostridium botulinum [J]. Science,2004, 306(5701):1550-3.
[125]Weinert EE, Phillips-Piro CM, Tran R, Mathies RA, Marletta MA, Controlling Conformational Flexibility of an O(2)-Binding H-NOX Domain [J]. Biochemistry (Mosc),2011,50(32):6832-40.
[126]Tran R, Weinert EE, Boon EM, Mathies RA, Marletta MA, Determinants of the Heme-CO Vibrational Modes in the H-NOX Family [J]. Biochemistry (Mosc), 2011,50(30):6519-30.
[127]Menyhard DK, Conformational selection mechanism governs oxygen ligation to H-NOX proteins [J]. Bioorganic and Medicinal Chemistry Letters,2011,21(12): 3523-6.
[128]Olea C, Jr., Kuriyan J, Marietta MA, Modulating heme redox potential through protein-induced porphyrin distortion [J]. J Am Chem Soc,2010,132(37): 12794-5.
[129]Olea C, Jr., Herzik MA, Jr., Kuriyan J, Marietta MA, Structural insights into the molecular mechanism of H-NOX activation [J]. Protein Science,2010,19(4): 881-7.
[130]Dai Z, Boon EM, Engineering of the heme pocket of an H-NOX domain for direct cyanide detection and quantification [J]. J Am Chem Soc,2010,132(33): 11496-503.
[131]Olea C, Boon EM, Pellicena P, Kuriyan J, Marietta MA, Probing the function of heme distortion in the H-NOX family [J]. ACS Chem Biol,2008,3(11):703-10.
[132]Boon EM, Marietta MA, Ligand discrimination in soluble guanylate cyclase and the H-NOX family of heme sensor proteins [J]. Curr Opin Chem Biol,2005, 9(5):441-6.
[133]Ma X, Sayed N, Beuve A, van den Akker F, NO and CO differentially activate soluble guanylyl cyclase via a heme pivot-bend mechanism [J]. EMBO Journal, 2007,26(2):578-88.
[134]Martin F, Baskaran P, Ma X, Dunten PW, Schaefer M, Stasch JP, Beuve A, van den Akker F, Structure of cinaciguat (BAY 58-2667) bound to Nostoc H-NOX domain reveals insights into heme-mimetic activation of the soluble guanylyl cyclase [J]. J Biol Chem,2010,285(29):22651-7.
[135]Winger JA, Derbyshire ER, Lamers MH, Marietta MA, Kuriyan J, The crystal structure of the catalytic domain of a eukaryotic guanylate cyclase [J]. BMC Struct Biol,2008,8:42.
[136]Ma X, Beuve A, van den Akker F, Crystal structure of the signaling helix coiled-coil domain of the betal subunit of the soluble guanylyl cyclase [J]. BMC Struct Biol,2010,10:2.
[1]Ma X, Sayed N, Beuve A, van den Akker F, NO and CO differentially activate soluble guanylyl cyclase via a heme pivot-bend mechanism [J]. EMBO Journal, 2007,26(2):578-88.
[2]Nioche P, Berka V, Vipond J, Minton N, Tsai AL, Raman CS, Femtomolar sensitivity of a NO sensor from Clostridium botulinum [J]. Science,2004, 306(5701):1550-3.
[3]Hu X, Murata LB, Weichsel A, Brailey JL, Roberts SA, Nighorn A, Montfort WR, Allostery in recombinant soluble guanylyl cyclase from Manduca sexta [J]. J Biol Chem,2008,283(30):20968-77.
[4]Winger JA, Marietta MA, Expression and characterization of the catalytic domains of soluble guanylate cyclase:Interaction with the heme domain [J]. Biochemistry (Mosc),2005,44(10):4083-4090.
[5]Karow DS, Pan DH, Davis JH, Behrends S, Mathies RA, Marietta MA, Characterization of functional heme domains from soluble guanylate cyclase [J]. Biochemistry (Mosc),2005,44(49):16266-16274.
[6]Zhao Y, Marietta MA, Localization of the heme binding region in soluble guanylate cyclase [J]. Biochemistry (Mosc),1997,36(50):15959-64.
[7]Zhong F, Wang H, Ying T, Huang ZX, Tan X, Efficient expression of human soluble guanylate cyclase in Escherichia coli and its signaling-related interaction with nitric oxide [J].Amino Acids,2010,39:399-408.
[8]Derbyshire ER, Winter MB, Ibrahim M, Deng S, Spiro TG, Marietta MA, Probing domain interactions in soluble guanylate cyclase [J]. Biochemistry (Mosc),2011,50(20):4281-90.
[9]Autenrieth F, Tajkhorshid E, Baudry J, Luthey-Schulten Z, Classical force field parameters for the heme prosthetic group of cytochrome c [J]. J Comput Chem, 2004,25(13):1613-22.
[10]Laidig KE, Daggett V, Molecular dynamics simulations of apocytochrome b562--the highly ordered limit of molten globules [J]. Folding and Design,1996, 1(5):335-46.
[11]Mackerell AD, Jr., Feig M, Brooks CL,3rd, Extending the treatment of backbone energetics in protein force fields:limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations [J]. J Comput Chem,2004,25(11):1400-15.
[12]Berry EA, Trumpower BL, Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra [J]. Anal Biochem,1987,161(1):1-15.
[13]Mukherjee P, Halder M, Hargrove MS, Petrich JW, Characterization of the interactions of fluorescent probes with proteins:coumarin 153 and 1,8-ANS in complex with holo-and apomyoglobin [J]. Photochem Photobiol,2006,82(6): 1586-90.
[14]Pellicena P, Karow DS, Boon EM, Marletta MA, Kuriyan J, Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases [J]. Proc Natl Acad Sci U S A,2004,101(35):12854-12859.
[15]Capece L, Estrin DA, Marti MA, Dynamical characterization of the heme NO oxygen binding (HNOX) domain. Insight into soluble guanylate cyclase allosteric transition [J]. Biochemistry (Mosc),2008,47(36):9416-27.
[16]Burstyn JN, Yu AE, Dierks EA, Hawkins BK, Dawson JH, Studies of the heme coordination and ligand binding properties of soluble guanylyl cyclase (sGC): characterization of Fe(II)sGC and Fe(II)sGC(CO) by electronic absorption and magnetic circular dichroism spectroscopies and failure of CO to activate the enzyme [J]. Biochemistry (Mosc),1995,34(17):5896-903.
[17]Lee YC, Martin E, Murad F, Human recombinant soluble guanylyl cyclase: Expression, purification, and regulation [J]. Proc Natl Acad Sci U S A,2000, 97(20):10763-10768.
[18]Stone JR, Marletta MA, Soluble guanylate cyclase from bovine lung:activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states [J]. Biochemistry (Mosc),1994,33(18):5636-40.
[19]Deinum G, Stone JR, Babcock GT, Marletta MA, Binding of nitric oxide and carbon monoxide to soluble guanylate cyclase as observed with resonance Raman spectroscopy [J]. Biochemistry (Mosc),1996,35(5):1540-1547.
[20]Fan B, Gupta G, Danziger RS, Friedman JM, Rousseau DL, Resonance Raman characterization of soluble guanylate cyclase expressed from baculovirus [J]. Biochemistry (Mosc),1998,37(5):1178-84.
[21]Li Z, Pal B, Takenaka S, Tsuyama S, Kitagawa T, Resonance Raman evidence for the presence of two heme pocket conformations with varied activities in CO-bound bovine soluble guanylate cyclase and their conversion [J]. Biochemistry (Mosc),2005,44(3):939-46.
[22]Tomita T, Ogura T, Tsuyama S, Imai Y, Kitagawa T, Effects of GTP on bound nitric oxide of soluble guanylate cyclase probed by resonance Raman spectroscopy [J]. Biochemistry (Mosc),1997,36(33):10155-60.
[23]Vogel KM, Hu S, Spiro TG, Dierks EA, Yu AE, Burstyn JN, Variable forms of soluble guanylyl cyclase:protein-ligand interactions and the issue of activation by carbon monoxide [J]. J Biol Inorg Chem,1999,4(6):804-13.
[24]Yu AE, Hu SZ, Spiro TG, Burstyn JN, Resonance raman-spectroscopy of soluble guanylyl cyclase reveal displacement of distal and proximal heme ligands by NO [J]. J Am Chem Soc,1994,116(9):4117-4118.
[25]Antonini E, Brunori M, in Frontiers of Biology. North-Holland Publishing Co: Amsterdam,1971.
[26]Yamanaka T, in The Biochemistry of Bacterial Cytochromes. Japan Scientific Societies Press:Tokyo,1992.
[27]Gerzer R, Bohme E, Hofmann F, Schultz G, Soluble guanylate cyclase purified from bovine lung contains heme and copper [J]. FEBS Lett,1981,132(1):71-4.
[28]Ignarro LJ, Adams JB, Horwitz PM, Wood KS, Activation of soluble guanylate cyclase by NO-hemoproteins involves NO-heme exchange. Comparison of heme-containing and heme-deficient enzyme forms [J]. J Biol Chem,1986, 261(11):4997-5002.
[29]Makino R, Matsuda H, Obayashi E, Shiro Y, Iizuka T, Hori H, EPR characterization of axial bond in metal center of native and cobalt-substituted guanylate cyclase [J]. J Biol Chem,1999,274(12):7714-23.
[30]Yazawa S, Tsuchiya H, Hori H, Makino R, Functional characterization of two nucleotide-binding sites in soluble guanylate cyclase [J]. J Biol Chem,2006, 281(31):21763-70.
[31]Tsaprailis G, Chan DW, English AM, Conformational states in denaturants of cytochrome c and horseradish peroxidases examined by fluorescence and circular dichroism [J]. Biochemistry (Mosc),1998,37(7):2004-16.
[32]Jang DJ, el-Sayed MA, Tryptophan fluorescence quenching as a monitor for the protein conformation changes occurring during the photocycle of bacteriorhodopsin under different perturbations [J]. Proc Natl Acad Sci U S A, 1989,86(15):5815-9.
[33]Kamatari YO, Konno T, Kataoka M, Akasaka K, The methanol-induced globular and expanded denatured states of cytochrome c:a study by CD fluorescence, NMR and small-angle X-ray scattering [J]. Journal of Molecular Biology,1996, 259(3):512-23.
[34]Latypov RF, Cheng H, Roder NA, Zhang J, Roder H, Structural characterization of an equilibrium unfolding intermediate in cytochrome c [J]. Journal of Molecular Biology,2006,357(3):1009-25.
[35]Chen Y, Barkley MD, Toward understanding tryptophan fluorescence in proteins [J]. Biochemistry (Mosc),1998,37(28):9976-82.
[36]Weinert EE, Phillips-Piro CM, Tran R, Mathies RA, Marletta MA, Controlling Conformational Flexibility of an O(2)-Binding H-NOX Domain [J]. Biochemistry (Mosc),2011,50(32):6832-40.
[37]Olea C, Jr., Kuriyan J, Marletta MA, Modulating heme redox potential through protein-induced porphyrin distortion [J]. J Am Chem Soc,2010,132(37): 12794-5.
[38]Fritz BG, Hu X, Brailey JL, Berry RE, Walker FA, Montfort WR, Oxidation and loss of heme in soluble guanylyl cyclase from Manduca sexta [J]. Biochemistry (Mosc),2011,50(26):5813-5.
[39]Ali V, Prakash K, Kulkarni S, Ahmad A, Madhusudan KP, Bhakuni V, 8-anilino-l-naphthalene sulfonic acid (ANS) induces folding of acid unfolded cytochrome c to molten globule state as a result of electrostatic interactions [J]. Biochemistry (Mosc),1999,38(41):13635-42.
[1]Evgenov OV, Pacher P, Schmidt PM, Hasko G, Schmidt HH, Stasch JP, NO-independent stimulators and activators of soluble guanylate cyclase: discovery and therapeutic potential [J]. Nat Rev Drug Discov,2006,5(9): 755-68.
[2]Pellicena P, Karow DS, Boon EM, Marietta MA, Kuriyan J, Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases [J]. Proc Natl Acad Sci U S A,2004,101(35):12854-12859.
[3]Schmidt PM, Schramm M, Schroder H, Wunder F, Stasch JP, Identification of residues crucially involved in the binding of the heme moiety of soluble guanylate cyclase [J]. J Biol Chem,2004,279(4):3025-32.
[4]Foerster J, Harteneck C, Malkewitz J, Schultz G, Koesling D, A functional heme-binding site of soluble guanylyl cyclase requires intact N-termini of alpha 1 and beta 1 subunits [J]. Eur J Biochem,1996,240(2):380-6.
[5]Stone JR, Marietta MA, Soluble guanylate cyclase from bovine lung:activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states [J]. Biochemistry (Mosc),1994,33(18):5636-40.
[6]Stone JR, Marietta MA, Heme stoichiometry of heterodimeric soluble guanylate cyclase [J]. Biochemistry (Mosc),1995,34(45):14668-74.
[7]Tomita T, Tsuyama S, Imai Y, Kitagawa T, Purification of bovine soluble guanylate cyclase and ADP-ribosylation on its small subunit by bacterial toxins [J]. J Biochem,1997,122(3):531-6.
[8]Hu X, Murata LB, Weichsel A, Brailey JL, Roberts SA, Nighorn A, Montfort WR, Allostery in recombinant soluble guanylyl cyclase from Manduca sexta [J]. J Biol Chem,2008,283(30):20968-77.
[9]Pal B, Kitagawa T, Binding of YC-1/BAY 41-2272 to soluble guanylate cyclase: A new perspective to the mechanism of activation [J]. Biochem Biophys Res Commun,2010,397(3):375-9.
[10]Chivian D, Kim DE, Malmstrom L, Bradley P, Robertson T, Murphy P, Strauss CE, Bonneau R, Rohl CA, Baker D, Automated prediction of CASP-5 structures using the Robetta server [J]. Proteins,2003,53 Suppl 6:524-33.
[11]Zhao Y, Marietta MA, Localization of the heme binding region in soluble guanylate cyclase [J]. Biochemistry (Mosc),1997,36(50):15959-64.
[12]Karow DS, Pan DH, Davis JH, Behrends S, Mathies RA, Marietta MA, Characterization of functional heme domains from soluble guanylate cyclase [J]. Biochemistry (Mosc),2005,44(49):16266-16274.
[13]Winger JA, Marietta MA, Expression and characterization of the catalytic domains of soluble guanylate cyclase:Interaction with the heme domain [J]. Biochemistry (Mosc),2005.44(10):4083-4090.
[14]Zhong F, Pan J, Liu X, Wang H, Ying T, Su J, Huang ZX, Tan X, A novel insight into the heme and NO/CO binding mechanism of the alpha subunit of human soluble guanylate cyclase [J]. J Biol Inorg Chem,2011, DOI 10.1007/s00775-011-0811-x.
[15]Hargrove MS, Barrick D, Olson JS, The association rate constant for heme binding to globin is independent of protein structure [J]. Biochemistry (Mosc), 1996,35(35):11293-9.
[16]Guryev OL, Gilep AA, Usanov SA, Estabrook RW, Interaction of apo-cytochrome b5 with cytochromes P4503A4 and P45017A:relevance of heme transfer reactions [J]. Biochemistry (Mosc),2001,40(16):5018-31.
[17]Hargrove MS, Singleton EW, Quillin ML, Ortiz LA, Phillips GN, Jr., Olson JS, Mathews AJ, His64(E7)-->Tyr apomyoglobin as a reagent for measuring rates of hemin dissociation [J]. J Biol Chem,1994,269(6):4207-14.
[18]Winger JA, Derbyshire ER, Marletta MA, Dissociation of nitric oxide from soluble guanylate cyclase and heme-nitric oxide/oxygen binding domain constructs [J]. J Biol Chem,2007,282(2):897-907.
[19]Emmons TL, Mathis KJ, Shuck ME, Reitz BA, Curran DF, Walker MC, Leone JW, Day JE, Bienkowski MJ, Fischer HD, Tomasselli AG, Purification and characterization of recombinant human soluble guanylate cyclase produced from baculovirus-infected insect cells [J]. Protein Expr Purif,2009.
[20]Garbers DL, Purification of soluble guanylate cyclase from rat lung [J]. J Biol Chem,1979,254(1):240-3.
[21]Gupta G, Kim J, Yang L, Sturley SL, Danziger RS, Expression and purification of soluble, active heterodimeric guanylyl cyclase from baculovirus [J]. Protein Expr Purif,1997,10(3):325-30.
[22]Kamisaki Y, Saheki S, Nakane M, Palmieri JA, Kuno T, Chang BY, Waldman SA, Murad F, Soluble guanylate cyclase from rat lung exists as a heterodimer [J]. J Biol Chem,1986,261(16):7236-41.
[23]Koglin M, Behrends S, Native human nitric oxide sensitive guanylyl cyclase: purification and characterization [J]. Biochemical Pharmacology,2004,67(8): 1579-85.
[24]Lee YC, Martin E, Murad F, Human recombinant soluble guanylyl cyclase: Expression, purification, and regulation [J]. Proc Natl Acad Sci U S A,2000, 97(20):10763-10768.
[25]Mathis KJ, Emmons TL, Curran DF, Day JE, Tomasselli AG, High yield purification of soluble guanylate cyclase from bovine lung [J]. Protein Expr Purif, 2008,60(1):58-63.
[26]Zhong F, Wang H, Ying T, Huang ZX, Tan X, Efficient expression of human soluble guanylate cyclase in Escherichia coli and its signaling-related interaction with nitric oxide [J]. Amino Acids,2010,39:399-408.
[27]Walker FA, Pulsed EPR and NMR spectroscopy of paramagnetic iron porphyrinates and related iron macrocycles:how to understand patterns of spin delocalization and recognize macrocycle radicals [J]. Inorg Chem,2003,42(15): 4526-44.
[28]Iyer LM, Anantharaman V, Aravind L, Ancient conserved domains shared by animal soluble guanylyl cyclases and bacterial signaling proteins [J].1471-2164, 2003,4(1):5.
[29]Ballou DP, Zhao Y, Brandish PE, Marletta MA, Revisiting the kinetics of nitric oxide (NO) binding to soluble guanylate cyclase:the simple NO-binding model is incorrect [J]. Proc Natl Acad Sci U S A,2002,99(19):12097-101.
[30]Olea C, Jr., Herzik MA, Jr., Kuriyan J, Marietta MA, Structural insights into the molecular mechanism of H-NOX activation [J]. Protein Science,2010,19(4): 881-7.
[31]Vogel KM, Hu S, Spiro TG, Dierks EA, Yu AE, Burstyn JN, Variable forms of soluble guanylyl cyclase:protein-ligand interactions and the issue of activation by carbon monoxide [J]. J Biol Inorg Chem,1999,4(6):804-13.
[32]Zhao Y, Brandish PE, Ballou DP, Marietta MA, A molecular basis for nitric oxide sensing by soluble guanylate cyclase [J]. Proc Natl Acad Sci U S A,1999,96(26): 14753-8.
[33]Zhao YD, Hoganson C, Babcock GT, Marietta MA, Structural changes in the heme proximal pocket induced by nitric oxide binding to soluble guanylate cyclase [J]. Biochemistry (Mosc),1998,37(36):12458-12464.
[34]Deinum G, Stone JR., Babcock GT, Marietta MA, Binding of nitric oxide and carbon monoxide to soluble guanylate cyclase as observed with resonance Raman spectroscopy [J]. Biochemistry (Mosc),1996,35(5):1540-1547.
[35]Denninger JW, Schelvis JPM, Brandish PE, Zhao Y, Babcock GT, Marietta MA, Interaction of soluble guanylate cyclase with YC-1:Kinetic and resonance Raman studies [J]. Biochemistry (Mosc),2000,39(14):4191-4198.
[36]Fan B, Gupta G, Danziger RS, Friedman JM, Rousseau DL, Resonance Raman characterization of soluble guanylate cyclase expressed from baculovirus [J]. Biochemistry (Mosc),1998,37(5):1178-84.
[37]Ibrahim M, Derbyshire ER, Soldatova AV, Marietta MA, Spiro TG, Soluble guanylate cyclase is activated differently by excess NO and by YC-1:resonance Raman spectroscopic evidence [J]. Biochemistry (Mosc),2010,49(23):4864-71.
[38]Li Z, Pal B, Takenaka S, Tsuyama S, Kitagawa T, Resonance Raman evidence for the presence of two heme pocket conformations with varied activities in CO-bound bovine soluble guanylate cyclase and their conversion [J]. Biochemistry (Mosc),2005,44(3):939-46.
[39]Martin E, Czarnecki K, Jayaraman V, Murad F, Kincaid J, Resonance Raman and infrared spectroscopic studies of high-output forms of human soluble guanylyl cyclase [J]. J Am Chem Soc,2005,127(13):4625-31.
[40]Schelvis JP, Zhao Y, Marletta MA, Babcock GT, Resonance raman characterization of the heme domain of soluble guanylate cyclase [J]. Biochemistry (Mosc),1998,37(46):16289-97.
[41]Yu AE, Hu SZ, Spiro TG, Burstyn JN, Resonance raman-spectroscopy of soluble guanylyl cyclase reveal displacement of distal and proximal heme ligands by NO [J]. J Am Chem Soc,1994,116(9):4117-4118.
[42]Stone JR, Marietta MA, The ferrous heme of soluble guanylate cyclase: formation of hexacoordinate complexes with carbon monoxide and nitrosomethane [J]. Biochemistry (Mosc),1995,34(50):16397-403.
[43]Stone JR, Marietta MA, Synergistic activation of soluble guanylate cyclase by YC-1 and carbon monoxide:implications for the role of cleavage of the iron-histidine bond during activation by nitric oxide [J]. Chem Biol,1998,5(5): 255-61.
[44]Tsai AL, Berka V, Martin F, Ma X, van den Akker F, Fabian M, Olson JS, Is Nostoc H-NOX a NO sensor or redox switch? [J]. Biochemistry (Mosc),2010, 49(31):6587-99.
[45]Stone JR, Sands RH, Dunham WR, Marietta MA, Electron paramagnetic resonance spectral evidence for the formation of a pentacoordinate nitrosyl-heme complex on soluble guanylate cyclase [J]. Biochem Biophys Res Commun,1995, 207(2):572-7.
[46]Boon EM, Davis JH, Tran R, Karow DS, Huang SH, Pan DH, Miazgowicz MM, Mathies RA, Marlletta MA, Nitric oxide binding to prokaryotic homologs of the soluble guanylate cyclase beta 1 H-NOX domain [J]. J Biol Chem,2006,281(31): 21892-21902.
[47]Cary SPL, Winger JA, Marletta MA, Tonic and acute nitric oxide signaling through soluble guanylate cyclase is mediated by nonheme nitric oxide, ATP, and GTP[J].Proc Natl Acad Sci U S A,2005,102(37):13064-13069.
[48]Kharitonov VQ Russwurm M, Magde D, Sharma VS, Koesling D, Dissociation of nitric oxide from soluble guanylate cyclase [J]. Biochem Biophys Res Commun,1997,239(1):284-6.
[49]Kharitonov VG, Sharma VS, Magde D, Koesling D, Kinetics of nitric oxide dissociation from five-and six-coordinate nitrosyl hemes and heme proteins, including soluble guanylate cyclase [J]. Biochemistry (Mosc),1997,36(22): 6814-8.
[50]Margulis A, Sitaramayya A, Rate of deactivation of nitric oxide-stimulated soluble guanylate cyclase:influence of nitric oxide scavengers and calcium [J]. Biochemistry (Mosc),2000,39(5):1034-9.
[51]Derbyshire ER, Fernhoff NB, Deng S, Marletta MA, Nucleotide regulation of soluble guanylate cyclase substrate specificity [J]. Biochemistry (Mosc),2009, 48(31):7519-24.
[52]Friebe A, Koesling D, Mechanism of YC-1-induced activation of soluble guanylyl cyclase [J]. Molecular Pharmacology,1998,53(1):123-7.
[53]Friebe A, Russwurm M, Mergia E, Koesling D, A point-mutated guanylyl cyclase with features of the YC-1-stimulated enzyme:implications for the YC-1 binding site? [J]. Biochemistry (Mosc),1999,38(46):15253-7.
[54]Hu X, Feng C, Hazzard JT, Tollin G,Montfort WR, Binding of YC-1 or BAY 41-2272 to soluble guanylyl cyclase induces a geminate phase in CO photolysis [J]. J Am Chem Soc,2008,130(47):15748-9.
[55]Ibrahim M, Derbyshire ER, Marletta MA, Spiro TG, Probing soluble guanylate cyclase activation by CO and YC-1 using resonance Raman spectroscopy [J]. Biochemistry (Mosc),2010,49(18):3815-23.
[56]Lamothe M, Chang FJ, Balashova N, Shirokov R, Beuve A, Functional characterization of nitric oxide and YC-1 activation of soluble guanylyl cyclase: structural implication for the YC-1 binding site? [J]. Biochemistry (Mosc),2004, 43(11):3039-48.
[57]Makino R, Obayashi E, Homma N, Shiro Y, Hori H, YC-1 facilitates release of the proximal His residue in the NO and CO complexes of soluble guanylate cyclase [J]. J Biol Chem,2003,278(13):11130-7.
[58]Martin E, Lee YC, Murad F, YC-1 activation of human soluble guanylyl cyclase has both heme-dependent and heme-independent components [J]. Proc Natl Acad Sci USA,2001,98(23):12938-42.
[59]Sharma VS, Magde D, Kharitonov VG, Koesling D, Soluble guanylate cyclase: effect of YC-1 on ligation kinetics with carbon monoxide [J]. Biochemical and Biophysical Research Communications,1999,254(1):188-91.
[60]Tsaprailis G, Chan DW, English AM, Conformational states in denaturants of cytochrome c and horseradish peroxidases examined by fluorescence and circular dichroism [J]. Biochemistry (Mosc),1998,37(7):2004-16.
[61]Light WR, Rohlfs RJ, Palmer G, Olson JS, Functional effects of heme orientational disorder in sperm whale myoglobin [J]. J Biol Chem,1987,262(1): 46-52.
[62]Fritz BG, Hu X, Brailey JL, Berry RE, Walker FA, Montfort WR, Oxidation and loss of heme in soluble guanylyl cyclase from Manduca sexta [J]. Biochemistry (Mosc),2011,50(26):5813-5.
[63]Meurer S, Pioch S, Pabst T, Opitz N, Schmidt PM, Beckhaus T, Wagner K, Matt S, Gegenbauer K, Geschka S, Karas M, Stasch JP, Schmidt HH, Muller-Esterl W, Nitric oxide-independent vasodilator rescues heme-oxidized soluble guanylate cyclase from proteasomal degradation [J]. Circ Res,2009,105(1):33-41.
[64]Maron BA, Zhang YY, Handy DE, Beuve A, Tang SS, Loscalzo J, Leopold JA, Aldosterone increases oxidant stress to impair guanylyl cyclase activity by cysteinyl thiol oxidation in vascular smooth muscle cells [J]. J Biol Chem,2009, 284(12):7665-72.
[65]Stasch JP, Schmidt PM, Nedvetsky PI, Nedvetskaya TY, H SA, Meurer S, Deile M, Taye A, Knorr A, Lapp H, Muller H, Turgay Y, Rothkegel C, Tersteegen A, Kemp-Harper B, Muller-Esterl W, Schmidt HH, Targeting the heme-oxidized nitric oxide receptor for selective vasodilatation of diseased blood vessels [J]. J Clin Invest,2006,116(9):2552-61.
[66]Gladwin MT, Deconstructing endothelial dysfunction:soluble guanylyl cyclase oxidation and the NO resistance syndrome [J]. J Clin Invest,2006,116(9): 2330-2.
[67]Stasch JP, Pacher P, Evgenov OV, Soluble guanylate cyclase as an emerging therapeutic target in cardiopulmonary disease [J]. Circulation,2011,123(20): 2263-73.
[68]Weinert EE, Phillips-Piro CM, Tran R, Mathies RA, Marietta MA, Controlling Conformational Flexibility of an O(2)-Binding H-NOX Domain [J]. Biochemistry (Mosc),2011,50(32):6832-40.
[69]Olea C, Jr., Kuriyan J, Marietta MA, Modulating heme redox potential through protein-induced porphyrin distortion [J]. J Am Chem Soc,2010,132(37): 12794-5.
[1]Haase T, Haase N, Kraehling JR, Behrends S, Fluorescent fusion proteins of soluble guanylyl cyclase indicate proximity of the heme nitric oxide domain and catalytic domain [J]. PLoS One,2010,5(7):e11617.
[2]Haase N, Haase T, Kraehling JR, Behrends S, Direct fusion of subunits of heterodimeric nitric oxide sensitive guanylyl cyclase leads to functional enzymes with preserved biochemical properties:evidence for isoform specific activation by ciguates [J]. Biochemical Pharmacology,2010,80(11):1676-83.
[3]Lee YC, Martin E, Murad F, Human recombinant soluble guanylyl cyclase: Expression, purification, and regulation [J]. Proc Natl Acad Sci U S A,2000, 97(20):10763-10768.
[4]Zabel U, Hausler C, Weeger M, Schmidt HH, Homodimerization of soluble guanylyl cyclase subunits. Dimerization analysis using a glutathione s-transferase affinity tag [J]. J Biol Chem,1999,274(26):18149-52.
[5]Wedel B, Harteneck C, Foerster J, Friebe A, Schultz G, Koesling D, Functional domains of soluble guanylyl cyclase [J]. J Biol Chem,1995,270(42):24871-5.
[6]Zhong F, Pan J, Liu X, Wang H, Ying T, Su J, Huang ZX, Tan X, A novel insight into the heme and NO/CO binding mechanism of the alpha subunit of human soluble guanylate cyclase [J]. J Biol Inorg Chem,2011, DOI 10.1007/s00775-011-0811-x.
[7]Hu X, Murata LB, Weichsel A, Brailey JL, Roberts SA, Nighorn A,--Montfort WR, Allostery in recombinant soluble guanylyl cyclase from Manduca sexta [J]. J Biol Chem,2008,283(30):20968-77.
[8]Haase N, Haase T, Seeanner M, Behrends S, Nitric oxide sensitive guanylyl cyclase activity decreases during cerebral postnatal development because of a reduction in heterodimerization [J]. Journal of Neurochemistry,2010,112(2): 542-51.
[9]Baskaran P, Heckler EJ, van den Akker F, Beuve A, Aspartate 102 in the heme domain of soluble guanylyl cyclase has a key role in NO activation [J]. Biochemistry (Mosc),2011,50(20):4291-7.
[10]Zhong F, Wang H, Ying T, Huang ZX, Tan X, Efficient expression of human soluble guanylate cyclase in Escherichia coli and its signaling-related interaction with nitric oxide [J]. Amino Acids,2010,39:399-408.
[11]Weinert EE, Phillips-Piro CM, Tran R, Mathies RA, Marletta MA, Controlling Conformational Flexibility of an O(2)-Binding H-NOX Domain [J]. Biochemistry (Mosc),2011,50(32):6832-40.
[12]Olea C, Jr., Kuriyan J, Marletta MA, Modulating heme redox potential through protein-induced porphyrin distortion [J]. J Am Chem Soc,2010,132(37): 12794-5.
[13]Hargrove MS, Singleton EW, Quillin ML, Ortiz LA, Phillips GN, Jr., Olson JS, Mathews AJ, His64(E7)-->Tyr apomyoglobin as a reagent for measuring rates of hemin dissociation [J]. J Biol Chem,1994,269(6):4207-14.
[14]Foerster J, Harteneck C, Malkewitz J, Schultz G, Koesling D, A functional heme-binding site of soluble guanylyl cyclase requires intact N-termini of alpha 1 and beta 1 subunits [J]. Eur J Biochem,1996,240(2):380-6.
[15]Karow DS, Pan DH, Davis JH, Behrends S, Mathies RA, Marietta MA, Characterization of functional heme domains from soluble guanylate cyclase [J]. Biochemistry (Mosc),2005,44(49):16266-16274.
[16]Walker FA, Pulsed EPR and NMR spectroscopy of paramagnetic iron porphyrinates and related iron macrocycles:how to understand patterns of spin delocalization and recognize macrocycle radicals [J]. Inorg Chem,2003,42(15): 4526-44.
[17]Ballou DP, Zhao Y, Brandish PE, Marietta MA, Revisiting the kinetics of nitric oxide (NO) binding to soluble guanylate cyclase:the simple NO-binding model is incorrect [J]. Proc Natl Acad Sci U S A,2002,99(19):12097-101.
[18]Olea C, Jr., Herzik MA, Jr., Kuriyan J, Marietta MA, Structural insights into the molecular mechanism of H-NOX activation [J]. Protein Science,2010,19(4): 881-7.
[19]Vogel KM, Hu S, Spiro TG, Dierks EA, Yu AE, Burstyn JN, Variable forms of soluble guanylyl cyclase:protein-ligand interactions and the issue of activation by carbon monoxide [J]. J Biol Inorg Chem,1999,4(6):804-13.
[20]Winger JA, Derbyshire ER, Marletta MA, Dissociation of nitric oxide from soluble guanylate cyclase and heme-nitric oxide/oxygen binding domain constructs [J]. J Biol Chem,2007,282(2):897-907.
[21]Zhao Y, Brandish PE, Ballou DP, Marletta MA, A molecular basis for nitric oxide sensing by soluble guanylate cyclase [J]. Proc Natl Acad Sci U S A,1999,96(26): 14753-8.
[22]Zhao YD, Hoganson C, Babcock GT, Marletta MA, Structural changes in the heme proximal pocket induced by nitric oxide binding to soluble guanylate cyclase [J]. Biochemistry (Mosc),1998,37(36):12458-12464.
[23]Ali V, Prakash K, Kulkarni S, Ahmad A, Madhusudan KP, Bhakuni V, 8-anilino-l-naphthalene sulfonic acid (ANS) induces folding of acid unfolded cytochrome c to molten globule state as a result of electrostatic interactions [J]. Biochemistry (Mosc),1999,38(41):13635-42.
[24]Martin F, Baskaran P, Ma X, Dunten PW, Schaefer M, Stasch JP, Beuve A, van den Akker F, Structure of cinaciguat (BAY 58-2667) bound to Nostoc H-NOX domain reveals insights into heme-mimetic activation of the soluble guanylyl cyclase [J]. J Biol Chem,2010,285(29):22651-7.
[25]Garbers DL, Purification of soluble guanylate cyclase from rat lung [J]. J Biol Chem,1979,254(1):240-3.
[26]Ma X, Sayed N, Baskaran P, Beuve A, van den Akker F, PAS-mediated dimerization of soluble guanylyl cyclase revealed by signal transduction histidine kinase domain crystal structure [J]. J Biol Chem,2008,283(2): 1167-78.
[27]Shiga T, Suzuki N, Amphipathic alpha-helix mediates the heterodimerization of soluble guanylyl cyclase [J].0289-0003,2005,22(7):735-42.
[28]Wagner C, Russwurm M, Jager R, Friebe A, Koesling D, Dimerization of nitric oxide-sensitive guanylyl cyclase requires the alpha 1 N terminus [J]. J Biol Chem,2005,280(18):17687-93.
[29]Wilson EM, Chinkers M, Identification of sequences mediating guanylyl cyclase dimerization [J]. Biochemistry (Mosc),1995,34(14):4696-701.
[30]Winger JA, Marletta MA, Expression and characterization of the catalytic domains of soluble guanylate cyclase:Interaction with the heme domain [J]. Biochemistry (Mosc),2005,44(10):4083-4090.
[31]Zhao Y, Marietta MA, Localization of the heme binding region in soluble guanylate cyclase [J]. Biochemistry (Mosc),1997,36(50):15959-64.
[32]Zhou Z, Gross S, Roussos C, Meurer S, Muller-Esterl W, Papapetropoulos A, Structural and functional characterization of the dimerization region of soluble guanylyl cyclase [J]. J Biol Chem,2004,279(24):24935-43.
[1]Nioche P, Berka V, Vipond J, Minton N, Tsai AL, Raman CS, Femtomolar sensitivity of a NO sensor from Clostridium botulinum [J]. Science,2004, 306(5701):1550-3.
[2]Weinert EE, Phillips-Piro CM, Tran R, Mathies RA, Marietta MA, Controlling Conformational Flexibility of an O(2)-Binding H-NOX Domain [J]. Biochemistry (Mosc),2011,50(32):6832-40.
[3]Tran R, Weinert EE, Boon EM, Mathies RA, Marietta MA, Determinants of the Heme-CO Vibrational Modes in the H-NOX Family [J]. Biochemistry (Mosc), 2011,50(30):6519-30.
[4]Menyhard DK, Conformational selection mechanism governs oxygen ligation to H-NOX proteins [J]. Bioorganic and Medicinal Chemistry Letters,2011,21(12): 3523-6.
[5]Olea C, Jr., Kuriyan J, Marietta MA, Modulating heme redox potential through protein-induced porphyrin distortion [J]. J Am Chem Soc,2010,132(37): 12794-5.
[6]Olea C, Jr., Herzik MA, Jr., Kuriyan J, Marietta MA, Structural insights into the molecular mechanism of H-NOX activation [J]. Protein Science,2010,19(4): 881-7.
[7]Dai Z, Boon EM, Engineering of the heme pocket of an H-NOX domain for direct cyanide detection and quantification [J]. J Am Chem Soc,2010,132(33): 11496-503.
[8]Olea C, Boon EM, Pellicena P, Kuriyan J, Marietta MA, Probing the function of heme distortion in the H-NOX family [J]. ACS Chem Biol,2008,3(11):703-10.
[9]Boon EM, Marietta MA, Ligand discrimination in soluble guanylate cyclase and the H-NOX family of heme sensor proteins [J]. Curr Opin Chem Biol,2005,9(5): 441-6.
[10]Pellicena P, Karow DS, Boon EM, Marietta MA, Kuriyan J, Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases [J]. Proc Natl Acad Sci U S A,2004,101(35):12854-12859.
[11]Ma X, Sayed N, Beuve A, van den Akker F, NO and CO differentially activate soluble guanylyl cyclase via a heme pivot-bend mechanism [J]. EMBO Journal, 2007,26(2):578-88.
[12]Zhong F, Wang H, Ying T, Huang ZX, Tan X, Efficient expression of human soluble guanylate cyclase in Escherichia coli and its signaling-related interaction with nitric oxide [J]. Amino Acids,2010,39:399-408.
[13]Zhong F, Pan J, Liu X, Wang H, Ying T, Su J, Huang ZX, Tan X, A novel insight into the heme and NO/CO binding mechanism of the alpha subunit of human soluble guanylate cyclase [J]. J Biol Inorg Chem,2011, DOI 10.1007/s00775-011-0811-x.
[14]Martin F, Baskaran P, Ma X, Dunten PW, Schaefer M, Stasch JP, Beuve A, van den Akker F, Structure of cinaciguat (BAY 58-2667) bound to Nostoc H-NOX domain reveals insights into heme-mimetic activation of the soluble guanylyl cyclase [J]. J Biol Chem,2010,285(29):22651-7.
[15]Winger JA, Derbyshire ER, Lamers MH, Marietta MA, Kuriyan J, The crystal structure of the catalytic domain of a eukaryotic guanylate cyclase [J]. BMC Struct Biol,2008,8:42.
[16]Ma X, Beuve A, van den Akker F, Crystal structure of the signaling helix coiled-coil domain of the beta1 subunit of the soluble guanylyl cyclase [J]. BMC Struct Biol,2010,10:2.
[2]Moller JK, Skibsted LH, Nitric oxide and myoglobins [J]. Chemical Reviews, 2002,102(4):1167-78.
[3]Peluffo G, Radi R, Biochemistry of protein tyrosine nitration in cardiovascular pathology [J]. Cardiovasc Res,2007,75(2):291-302.
[4]Shi W, Wang X, Shih DM, Laubach VE, Navab M, Lusis AJ, Paradoxical reduction of fatty streak formation in mice lacking endothelial nitric oxide synthase [J]. Circulation,2002,105(17):2078-82.
[5]Reiter TA, Pang B, Dedon P, Demple B, Resistance to nitric oxide-induced necrosis in heme oxygenase-1 overexpressing pulmonary epithelial cells associated with decreased lipid peroxidation [J]. J Biol Chem,2006,281(48): 36603-12.
[6]Virag L, Szabo E, Gergely P, Szabo C, Peroxynitrite-induced cytotoxicity: mechanism and opportunities for intervention [J].0378-4274,2003,140-141: 113-24.
[7]Goldstein S, Lind J, Merenyi G, Chemistry of peroxynitrites as compared to peroxynitrates [J]. Chemical Reviews,2005,105(6):2457-70.
[8]Hill BG, Dranka BP, Bailey SM, Lancaster JR, Jr., Darley-Usmar VM, What part of NO don't you understand? Some answers to the cardinal questions in nitric oxide biology [J]. J Biol Chem,2010,285(26):19699-704.
[9]Hall CN, Garthwaite J, What is the real physiological NO concentration in vivo? [J]. Nitric Oxide,2009,21 (2):92-103.
[10]Coulter JA, McCarthy HO, Xiang J, Roedl W, Wagner E, Robson T, Hirst DG, Nitric oxide--a novel therapeutic for cancer [J]. Nitric Oxide,2008,19(2):192-8.
[11]Chen KJ, Pittman RN, Popel AS, Nitric oxide in the vasculature:Where does it come from and where does it go? A quantitative perspective [J]. Antioxidants & Redox Signaling,2008,10(7):1185-1198.
[12]Pacher P, Beckman JS, Liaudet L, Nitric oxide and peroxynitrite in health and disease [J]. Physiol Rev,2007,87(1):315-424.
[13]Thippeswamy T, McKay JS, Quinn JP, Morris R, Nitric oxide, a biological double-faced janus-is this good or bad? [J]. Histol Histopathol,2006,21(4): 445-58.
[14]Denninger JW, Marletta MA, Guanylate cyclase and the.NO/cGMP signaling pathway [J]. Biochim Biophys Acta,1999,1411(2-3):334-50.
[15]Evgenov OV, Pacher P, Schmidt PM, Hasko G, Schmidt HH, Stasch JP, NO-independent stimulators and activators of soluble guanylate cyclase: discovery and therapeutic potential [J]. Nat Rev Drug Discov,2006,5(9): 755-68.
[16]Wang-Rosenke Y, Neumayer HH, Peters H, NO signaling through cGMP in renal tissue fibrosis and beyond:key pathway and novel therapeutic target [J]. Curr Med Chem,2008,15(14):1396-406.
[17]Stasch JP, Pacher P, Evgenov OV, Soluble guanylate cyclase as an emerging therapeutic target in cardiopulmonary disease [J]. Circulation,2011,123(20): 2263-73.
[18]Potter LR, Guanylyl cyclase structure, function and regulation [J]. Cell Signal, 2011.
[19]Pellicena P, Karow DS, Boon EM, Marietta MA, Kuriyan J, Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases [J]. Proc Natl Acad Sci U S A,2004,101(35):12854-12859.
[20]Schmidt PM, Schramm M, Schroder H, Wunder F, Stasch JP, Identification of residues crucially involved in the binding of the heme moiety of soluble guanylate cyclase [J]. J Biol Chem,2004,279(4):3025-32.
[21]Zhong F, Wang H, Ying T, Huang ZX, Tan X, Efficient expression of human soluble guanylate cyclase in Escherichia coli and its signaling-related interaction with nitric oxide [J]. Amino Acids,2010,39:399-408.
[22]Haase N, Haase T, Kraehling JR, Behrends S, Direct fusion of subunits of heterodimeric nitric oxide sensitive guanylyl cyclase leads to functional enzymes with preserved biochemical properties:evidence for isoform specific activation by ciguates [J]. Biochemical Pharmacology,2010,80(11):1676-83.
[23]Buechler WA, Nakane M, Murad F, Expression of soluble guanylate cyclase activity requires both enzyme subunits [J]. Biochemical and Biophysical Research Communications,1991,174(1):351-7.
[24]Nakane M, Arai K, Saheki S, Kuno T, Buechler W, Murad F, Molecular-cloning and expression of cDNAs coding for soluble guanylate-cyclase from rat lung [J]. Journal of Biological Chemistry,1990,265(28):16841-16845.
[25]Harteneck C, Wedel B, Koesling D, Malkewitz J, Bohme E, Schultz G, Molecular cloning and expression of a new alpha-subunit of soluble guanylyl cyclase. Interchangeability of the alpha-subunits of the enzyme [J]. FEBS Letters, 1991,292(1-2):217-22.
[26]Yuen PS, Potter LR, Garbers DL, A new form of guanylyl cyclase is preferentially expressed in rat kidney [J]. Biochemistry (Mosc),1990,29(49): 10872-8.
[27]Mergia E, Russwurm M, Zoidl G, Koesling D, Major occurrence of the new alpha2betal isoform of NO-sensitive guanylyl cyclase in brain [J]. Cell Signal, 2003,15(2):189-95.
[28]Russwurm M, Behrends S, Harteneck C, Koesling D, Functional properties of a naturally occurring isoform of soluble guanylyl cyclase [J]. Biochemical Journal, 1998,335 (Pt 1):125-30.
[29]Zabel U, Hausler C, Weeger M, Schmidt HH, Homodimerization of soluble guanylyl cyclase subunits. Dimerization analysis using a glutathione s-transferase affinity tag [J]. J Biol Chem,1999,274(26):18149-52.
[30]Hsieh CL, Cai C, Giwa A, Bivins A, Chen SY, Sabry D, Govardhan K, Shemshedini L, Expression of a hyperactive androgen receptor leads to androgen-independent growth of prostate cancer cells [J]. J Mol Endocrinol, 2008,41(1):13-23.
[31]Cai C, Chen SY, Zheng Z, Omwancha J, Lin MF, Balk SP, Shemshedini L, Androgen regulation of soluble guanylyl cyclasealphal mediates prostate cancer cell proliferation [J]. Oncogene,2007,26(11):1606-15.
[32]Pifarre P, Baltrons MA, Foldi I, Garcia A, NO-sensitive guanylyl cyclase betal subunit is peripherally associated to chromosomes during mitosis. Novel role in chromatin condensation and cell cycle progression [J]. Int J Biochem Cell Biol., 2009,41(8-9):1719-30.
[33]Ignarro LJ, Degnan JN, Baricos WH, Kadowitz PJ, Wolin MS, Activation of purified guanylate cyclase by nitric oxide requires heme-comparison of heme-deficient, heme-reconstituted and heme-containing forms of soluble enzyme from bovine lung [J]. Biochimica Et Biophysica Acta,1982,718(1): 49-59.
[34]Makino R, Obayashi E, Homma N, Shiro Y, Hori H, YC-1 facilitates release of the proximal His residue in the NO and CO complexes of soluble guanylate cyclase [J]. J Biol Chem,2003,278(13):11130-7.
[35]Mathis KJ, Emmons TL, Curran DF, Day JE, Tomasselli AG, High yield purification of soluble guanylate cyclase from bovine lung [J]. Protein Expr Purif, 2008,60(1):58-63.
[36]Ohlstein EH, Wood KS, Ignarro LJ, Purification and properties of heme-deficient hepatic soluble guanylate cyclase:effects of heme and other factors on enzyme activation by NO, NO-heme, and protoporphyrin Ⅸ [J]. Arch Biochem Biophys, 1982,218(1):187-98.
[37]Stone JR. Marietta MA, Spectral and kinetic studies on the activation of soluble guanylate cyclase by nitric oxide [J]. Biochemistry (Mosc),1996,35(4):1093-9.
[38]Stone JR, Sands RH, Dunham WR, Marietta MA, Electron paramagnetic resonance spectral evidence for the formation of a pentacoordinate nitrosyl-heme complex on soluble guanylate cyclase [J]. Biochem Biophys Res Commun,1995, 207(2):572-7.
[39]Wolin MS, Wood KS, Ignarro LJ, Guanylate cyclase from bovine lung. A kinetic analysis of the regulation of the purified soluble enzyme by protoporphyrin IX, heme, and nitrosyl-heme [J]. J Biol Chem,1982,257(22):13312-20.
[40]Zabel U, Weeger M, La M, Schmidt HH, Human soluble guanylate cyclase: functional expression and revised isoenzyme family [J]. Biochem J,1998,335 (Pt 1):51-7.
[41]Hoenicka M, Becker EM, Apeler H, Sirichoke T, Schroder H, Gerzer R, Stasch JP, Purified soluble guanylyl cyclase expressed in a baculovirus/Sf9 system: stimulation by YC-1, nitric oxide, and carbon monoxide [J]. J Mol Med,1999, 77(1):14-23.
[42]Lee YC, Martin E, Murad F, Human recombinant soluble guanylyl cyclase: Expression, purification, and regulation [J]. Proc Natl Acad Sci U S A,2000, 97(20):10763-10768.
[43]Haase T, Haase N, Kraehling JR, Behrends S, Fluorescent fusion proteins of soluble guanylyl cyclase indicate proximity of the heme nitric oxide domain and catalytic domain [J]. PLoS One,2010,5(7):e11617.
[44]Zhao Y, Marietta MA, Localization of the heme binding region in soluble guanylate cyclase [J]. Biochemistry (Mosc),1997,36(50):15959-64.
[45]Karow DS, Pan DH, Davis JH, Behrends S, Mathies RA, Marietta MA, Characterization of functional heme domains from soluble guanylate cyclase [J]. Biochemistry (Mosc),2005,44(49):16266-16274.
[46]Winger JA, Marietta MA, Expression and characterization of the catalytic domains of soluble guanylate cyclase:Interaction with the heme domain [J]. Biochemistry (Mosc),2005,44(10):4083-4090.
[47]Furchgott RF, Zawadzki JV, The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine [J]. Nature,1980, 288(5789):373-6.
[48]Lewicki JA, Brandwein HJ, Waldman SA, Murad F, Purified guanylate cyclase: characterization, iodination and preparation of monoclonal antibodies [J]. J Cyclic Nucleotide Res,1980,6(4):283-96.
[49]Ignarro LJ, Byrns RE, Buga GM, Wood KS, Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties identical to those of nitric oxide radical [J]. Circ Res,1987,61(6): 866-79.
[50]Ignarro LJ, Wood KS, Wolin MS, Activation of purified soluble guanylate cyclase by photopophyrin-IX [J]. Proceedings of the National Academy of Sciences of the United States of America-Biological Sciences,1982,79(9): 2870-2873.
[51]Stone JR, Marietta MA, Soluble guanylate cyclase from bovine lung:activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states [J]. Biochemistry (Mosc),1994,33(18):5636-40.
[52]Wedel B, Humbert P, Harteneck C, Foerster J, Malkewitz J, Bohme E, Schultz G, Koesling D, Mutation of His-105 in the beta 1 subunit yields a nitric oxide-insensitive form of soluble guanylyl cyclase [J]. Proc Natl Acad Sci U S A, 1994,91(7):2592-6.
[53]Zhao Y, Brandish PE, Ballou DP, Marietta MA, A molecular basis for nitric oxide sensing by soluble guanylate cyclase [J]. Proc Natl Acad Sci U S A,1999, 96(26):14753-8.
[54]Bellamy TC, Wood J, Garthwaite J, On the activation of soluble guanylyl cyclase by nitric oxide [J]. Proc Nat1 Acad Sci U S A,2002,99(1):507-10.
[55]Ballou DP, Zhao Y, Brandish PE, Marietta MA, Revisiting the kinetics of nitric oxide (NO) binding to soluble guanylate cyclase:the simple NO-binding model is incorrect [J]. Proc Natl Acad Sci U S A,2002,99(19):12097-101.
[56]Cary SPL, Winger JA, Marietta MA, Tonic and acute nitric oxide signaling through soluble guanylate cyclase is mediated by nonheme nitric oxide, ATP, and GTP [J]. Proc Natl Acad Sci U S A,2005,102(37):13064-13069.
[57]Russwurm M, Koesling D, NO activation of guanylyl cyclase [J]. EMBO Journal, 2004,23(22):4443-50.
[58]Lawson DM, Stevenson CE, Andrew CR, Eady RR, Unprecedented proximal binding of nitric oxide to heme:implications for guanylate cyclase [J]. EMBO Journal,2000,19(21):5661-71.
[59]Derbyshire ER, Marietta MA, Butyl isocyanide as a probe of the activation mechanism of soluble guanylate cyclase [J]. J Biol Chem,2007,282(49): 35741-35748.
[60]Margulis A, Sitaramayya A, Rate of deactivation of nitric oxide-stimulated soluble guanylate cyclase:influence of nitric oxide scavengers and calcium [J]. Biochemistry (Mosc),2000,39(5):1034-9.
[61]Kharitonov VG, Russwurm M, Magde D, Sharma VS, Koesling D, Dissociation of nitric oxide from soluble guanylate cyclase [J]. Biochem Biophys Res Commun,1997,239(1):284-6.
[62]Brandish PE, Buechler W, Marletta MA, Regeneration of the ferrous heme of soluble guanylate cyclase from the nitric oxide complex:acceleration by thiols and oxyhemoglobin [J]. Biochemistry (Mosc),1998,37(48):16898-907.
[63]Makino R, Matsuda H, Obayashi E, Shiro Y, Iizuka T, Hori H, EPR characterization of axial bond in metal center of native and cobalt-substituted guanylate cyclase [J]. J Biol Chem,1999,274(12):7714-23.
[64]Bellamy TC, Wood J, Goodwin DA, Garthwaite J, Rapid desensitization of the nitric oxide receptor, soluble guanylyl cyclase, underlies diversity of cellular cGMP responses [J]. Proc Natl Acad Sci U S A,2000,97(6):2928-33.
[65]Bellamy TC, Garthwaite J, Sub-second kinetics of the nitric oxide receptor, soluble guanylyl cyclase, in intact cerebellar cells [J]. J Biol Chem,2001,276(6): 4287-92.
[66]Winger JA, Derbyshire ER, Marietta MA, Dissociation of nitric oxide from soluble guanylate cyclase and heme-nitric oxide/oxygen binding domain constructs [J]. J Biol Chem,2007,282(2):897-907.
[67]Aono S, Metal-containing sensor proteins sensing diatomic gas molecules [J]. Dalton Trans,2008, (24):3137-46.
[68]Chen L, Lyubimov AY, Brammer L, Vrielink A, Sampson NS, The binding and release of oxygen and hydrogen peroxide are directed by a hydrophobic tunnel in cholesterol oxidase [J]. Biochemistry (Mosc),2008,47(19):5368-77.
[69]Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS, Protein S-nitrosylation:purview and parameters [J]. Nat Rev Mol Cell Biol,2005,6(2): 150-66.
[70]Sayed N, Baskaran P, Ma X, van den Akker F, Beuve A, Desensitization of soluble guanylyl cyclase, the NO receptor, by S-nitrosylation [J]. Proc Natl Acad Sci USA,2007,104(30):12312-7.
[71]Iyer AK, Azad N, Wang L, Rojanasakul Y, Role of S-nitrosylation in apoptosis resistance and carcinogenesis [J]. Nitric Oxide,2008,19(2):146-51.
[72]Sayed N, Kim DD, Fioramonti X, Iwahashi T, Duran WN, Beuve A, Nitroglycerin-induced S-nitrosylation and desensitization of soluble guanylyl cyclase contribute to nitrate tolerance [J]. Circ Res,2008,103(6):606-14.
[73]Lima B, Forrester MT, Hess DT, Stamler JS, S-nitrosylation in cardiovascular signaling [J]. Circ Res,2010,106(4):633-46.
[74]Martinez-Ruiz A, Cadenas S, Lamas S, Nitric oxide signaling:classical, less classical, and nonclassical mechanisms [J]. Free Radical Biology and Medicine, 2011,51(1):17-29.
[75]Brandwein HJ, Lewicki JA, Murad F, Reversible inactivation of guanylate cyclase by mixed disulfide formation [J]. J Biol Chem,1981,256(6):2958-62.
[76]DeMaster EG, Quast BJ, Redfern B, Nagasawa HT, Reaction of nitric oxide with the free sulfhydryl group of human serum albumin yields a sulfenic acid and nitrous oxide [J]. Biochemistry (Mosc),1995,34(36):11494-9.
[77]Artz JD, Schmidt B, McCracken JL, Marietta MA, Effects of nitroglycerin on soluble guanylate cyclase:implications for nitrate tolerance [J]. J Biol Chem, 2002,277(21):18253-6.
[78]Gonrren AC, Russwurm M, Kollau A, Koesling D, Schmidt K, Mayer B, Effects of nitroglycerin/L-cysteine on soluble guanylate cyclase:evidence for an activation/inactivation equilibrium controlled by nitric oxide binding and haem oxidation [J]. Biochemical Journal,2005,390(Pt 2):625-31.
[79]Fernhoff NB, Derbyshire ER, Marletta MA, A nitric oxide/cysteine interaction mediates the activation of soluble guanylate cyclase [J]. Proc Natl Acad Sci U S A,2009,106(51):21602-7.
[80]Mayer B, Kleschyov AL, Stessel H, Russwurm M, Munzel T, Koesling D, Schmidt K, Inactivation of soluble guanylate cyclase by stoichiometric S-nitrosation [J]. Molecular Pharmacology,2009,75(4):886-91.
[81]Miller TW, Cherney MM, Lee AJ, Francoleon NE, Farmer PJ, King SB, Hobbs AJ, Miranda KM, Burstyn JN, Fukuto JM, The effects of nitroxyl (HNO) on soluble guanylate cyclase activity:interactions at ferrous heme and cysteine thiols [J]. J Biol Chem,2009,284(33):21788-96.
[82]Riego JA, Broniowska KA, Kettenhofen NJ, Hogg N, Activation and inhibition of soluble guanylyl cyclase by S-nitrosocysteine:involvement of amino acid transport system L [J]. Free Radical Biology and Medicine,2009,47(3):269-74.
[83]Murthy KS, Modulation of soluble guanylate cyclase activity by phosphorylation [J]. Neurochem Int,2004,45(6):845-51.
[84]Meurer S, Pioch S, Gross S, Muller-Esterl W, Reactive oxygen species induce tyrosine phosphorylation of and Src kinase recruitment to NO-sensitive guanylyl cyclase [J]. J Biol Chem,2005,280(39):33149-56.
[85]Murad F, Shattuck Lecture. Nitric oxide and cyclic GMP in cell signaling and drug development [J]. N Engl J Med,2006,355(19):2003-11.
[86]Lubos E, Handy DE, Loscalzo J, Role of oxidative stress and nitric oxide in atherothrombosis [J]. Front Biosci,2008,13:5323-44.
[87]Tsai EJ, Kass DA, Cyclic GMP signaling in cardiovascular pathophysiology and therapeutics [J]. Pharmacol Ther,2009,122(3):216-38.
[88]McLaughlin VV, Archer SL, Badesch DB, Barst RJ, Farber HW, Lindner JR, Mathier MA, McGoon MD, Park MH, Rosenson RS, Rubin LJ, Tapson VF, Varga J, Harrington RA, Anderson JL, Bates ER, Bridges CR, Eisenberg MJ, Ferrari VA, Grines CL, Hlatky MA, Jacobs AK, Kaul S, Lichtenberg RC, Moliterno DJ, Mukherjee D, Pohost GM, Schofield RS, Shubrooks SJ, Stein JH, Tracy CM, Weitz HH, Wesley DJ, ACCF/AHA 2009 expert consensus document on pulmonary hypertension:a report of the American College of Cardiology Foundation Task Force on Expert Consensus Documents and the American Heart Association:developed in collaboration with the American College of Chest Physicians, American Thoracic Society, Inc., and the Pulmonary Hypertension Association [J]. Circulation,2009,119(16):2250-94.
[89]Chirkov YY, Horowitz JD, Impaired tissue responsiveness to organic nitrates and nitric oxide:a new therapeutic frontier? [J]. Pharmacol Ther,2007,116(2): 287-305.
[90]Szabo C, Ischiropoulos H, Radi R, Peroxynitrite:biochemistry, pathophysiology and development of therapeutics [J]. Nat Rev Drug Discov,2007,6(8):662-80.
[91]Ko FN, Wu CC, Kuo SC, Lee FY, Teng CM, YC-1, a novel activator of platelet guanylate cyclase [J]. Blood,1994,84(12):4226-33.
[92]Stasch JP, Becker EM, Alonso-Alija C, Apeler H, Dembowsky K, Feurer A, Gerzer R, Minuth T, Perzborn E, Pleiss U, Schroder H, Schroeder W, Stahl E, Steinke W, Straub A, Schramm M, NO-independent regulatory site on soluble guanylate cyclase [J]. Nature,2001,410(6825):212-215.
[93]Stasch JP, Alonso-Alija C, Apeler H, Dembowsky K, Feurer A, Minuth T, Perzborn E, Schramm M, Straub A, Pharmacological actions of a novel NO-independent guanylyl cyclase stimulator, BAY 41-8543:in vitro studies [J]. Br J Pharmacol,2002,135(2):333-43.
[94]Schmidt P, Schramm M, Schroder H, Stasch JP, Mechanisms of nitric oxide independent activation of soluble guanylyl cyclase [J]. Eur J Pharmacol,2003, 468(3):167-74.
[95]Bischoff E, Stasch JP, Effects of the sGC stimulator BAY 41-2272 are not mediated by phosphodiesterase 5 inhibition [J]. Circulation,2004,110(12): e320-1; author reply e320-1.
[96]Mittendorf J, Weigand S, Alonso-Alija C, Bischoff E, Feurer A, Gerisch M, Kern A, Knorr A, Lang D, Muenter K, Radtke M, Schirok H, Schlemmer KH, Stahl E, Straub A, Wunder F, Stasch JP, Discovery of riociguat (BAY 63-2521):a potent, oral stimulator of soluble guanylate cyclase for the treatment of pulmonary hypertension [J]. ChemMedChem,2009,4(5):853-65.
[97]Ghofrani HA, Hoeper MM, Halank M, Meyer FJ, Staehler G, Behr J, Ewert R, Weimann G, Grimminger F, Riociguat for chronic thromboembolic pulmonary hypertension and pulmonary arterial hypertension:a phase Ⅱ study [J]. Eur Respir J,2010,36(4):792-9.
[98]Gladwin MT, Deconstructing endothelial dysfunction:soluble guanylyl cyclase oxidation and the NO resistance syndrome [J]. J Clin Invest,2006,116(9): 2330-2.
[99]Stasch JP, Schmidt PM, Nedvetsky PI, Nedvetskaya TY, H SA, Meurer S, Deile M, Taye A, Knorr A, Lapp H, Muller H, Turgay Y, Rothkegel C, Tersteegen A, Kemp-Harper B, Muller-Esterl W, Schmidt HH, Targeting the heme-oxidized nitric oxide receptor for selective vasodilatation of diseased blood vessels [J]. J Clin Invest,2006,116(9):2552-61.
[100]Schindler U, Strobel H, Schonafinger K, Linz W, Lohn M, Martorana PA, Rutten H, Schindler PW, Busch AE, Sohn M, Topfer A, Pistorius A, Jannek C, Mulsch A, Biochemistry and pharmacology of novel anthranilic acid derivatives activating heme-oxidized soluble guanylyl cyclase [J]. Molecular Pharmacology, 2006,69(4):1260-8.
[101]Pankey EA, Bhartiya M, Badejo AM, Jr., Haider U, Stasch JP, Murthy SN, Nossaman BD, Kadowitz PJ, Pulmonary and systemic vasodilator responses to the soluble guanylyl cyclase activator, BAY 60-2770, are not dependent on endogenous nitric oxide or reduced heme [J]. Am J Physiol Heart Circ Physiol, 2011,300(3):H792-802.
[102]Gavin AC, Superti-Furga G, Protein complexes and proteome organization from yeast to man [J]. Curr Opin Chem Biol,2003,7(1):21-7.
[103]Alberts B, The cell as a collection of protein machines:preparing the next generation of molecular biologists [J]. Cell,1998,92(3):291-4.
[104]Gavin AC, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon AM, Cruciat CM, Remor M, Hofert C, Schelder M, Brajenovic M, Ruffner H, Merino A, Klein K, Hudak M, Dickson D, Rudi T, Gnau V, Bauch A, Bastuck S, Huhse B, Leutwein C, Heurtier MA, Copley RR, Edelmann A, Querfurth E, Rybin V, Drewes G, Raida M, Bouwmeester T, Bork P, Seraphin B, Kuster B, Neubauer G, Superti-Furga G, Functional organization of the yeast proteome by systematic analysis of protein complexes [J]. Nature,2002, 415(6868):141-7.
[105]Rodriguez P, Braun H, Kolodziej KE, de Boer E, Campbell J, Bonte E, Grosveld F, Philipsen S, Strouboulis J, Isolation of transcription factor complexes by in vivo biotinylation tagging and direct binding to streptavidin beads [J]. Methods Mol Biol,2006,338:305-23.
[106]Li C, Schwabe JW, Banayo E, Evans RM, Coexpression of nuclear receptor partners increases their solubility and biological activities [J]. Proc Natl Acad Sci U S A,1997,94(6):2278-83.
[107]Fribourg S, Romier C, Werten S, Gangloff YG, Poterszman A, Moras D, Dissecting the interaction network of multiprotein complexes by pairwise coexpression of subunits in E. coli [J]. J Mol Biol,2001,306(2):363-73.
[108]Copeland WC, Expression, purification, and characterization of the two human primase subunits and truncated complexes from Escherichia coli [J]. Protein Expr Purif,1997,9(1):1-9.
[109]Johnston K, Clements A, Venkataramani RN, Trievel RC, Marmorstein R, Coexpression of proteins in bacteria using T7-based expression plasmids: expression of heteromeric cell-cycle and transcriptional regulatory complexes [J]. Protein Expr Purif,2000,20(3):435-43.
[110]Fribourg S, Romier C, Werten S, Gangloff YG, Poterszman A, Moras D, Dissecting the interaction network of multiprotein complexes by pairwise coexpression of subunits in E. coli [J]. Journal of Molecular Biology,2001, 306(2):363-73.
[111]Tan S, Kern RC, Selleck W, The pST44 polycistronic expression system for producing protein complexes in Escherichia coli [J]. Protein Expr Purif,2005, 40(2):385-95.
[112]Romier C, Ben Jelloul M, Albeck S, Buchwald G, Busso D, Celie PH, Christodoulou E, De Marco V, van Gerwen S, Knipscheer P, Lebbink JH, Notenboom V, Poterszman A, Rochel N, Cohen SX, Unger T, Sussman JL, Moras D, Sixma TK, Perrakis A, Co-expression of protein complexes in prokaryotic and eukaryotic hosts:experimental procedures, database tracking and case studies [J]. Acta Crystallogr D Biol Crystallogr,2006,62(Pt 10): 1232-42.
[113]Neumann D, Woods A, Carling D, Wallimann T, Schlattner U, Mammalian AMP-activated protein kinase:functional, heterotrimeric complexes by co-expression of subunits in Escherichia coli [J]. Protein Expr Purif,2003,30(2): 230-7.
[114]Kim KJ, Kim HE, Lee KH, Han W, Yi MJ, Jeong J, Oh BH, Two-promoter vector is highly efficient for overproduction of protein complexes [J]. Protein Science,2004,13(6):1698-703.
[115]Alexandrov A, Vignali M, LaCount DJ, Quartley E, de Vries C, De Rosa D, Babulski J, Mitchell SF, Schoenfeld LW, Fields S, Hol WG, Dumont ME, Phizicky EM, Grayhack EJ, A facile method for high-throughput co-expression of protein pairs [J]. Mol Cell Proteomics,2004,3(9):934-8.
[116]Garbers DL, Purification of soluble guanylate cyclase from rat lung [J]. J Biol Chem,1979,254(1):240-3.
[117]Wilson EM, Chinkers M, Identification of sequences mediating guanylyl cyclase dimerization [J]. Biochemistry (Mosc),1995,34(14):4696-701.
[118]Zhou Z, Gross S, Roussos C, Meurer S, Muller-Esterl W, Papapetropoulos A, Structural and functional characterization of the dimerization region of soluble guanylyl cyclase [J]. J Biol Chem,2004,279(24):24935-43.
[119]Wagner C, Russwurm M, Jager R, Friebe A, Koesling D, Dimerization of nitric oxide-sensitive guanylyl cyclase requires the alpha 1 N terminus [J]. J Biol Chem,2005,280(18):17687-93.
[120]Shiga T, Suzuki N, Amphipathic alpha-helix mediates the heterodimerization of soluble guanylyl cyclase [J].0289-0003,2005,22(7):735-42.
[121]Ma X, Sayed N, Baskaran P, Beuve A, van den Akker F, PAS-mediated dimerization of soluble guanylyl cyclase revealed by signal transduction histidine kinase domain crystal structure [J]. J Biol Chem,2008,283(2): 1167-78.
[122]Harteneck C, Koesling D, Soling A, Schultz G, Bohme E, Expression of soluble guanylyl cyclase. Catalytic activity requires two enzyme subunits [J]. FEBS Lett, 1990,272(1-2):221-3.
[123]Haase N, Haase T, Seeanner M, Behrends S, Nitric oxide sensitive guanylyl cyclase activity decreases during cerebral postnatal development because of a reduction in heterodimerization [J]. Journal of Neurochemistry,2010,112(2): 542-51.
[124]Nioche P, Berka V, Vipond J, Minton N, Tsai AL, Raman CS, Femtomolar sensitivity of a NO sensor from Clostridium botulinum [J]. Science,2004, 306(5701):1550-3.
[125]Weinert EE, Phillips-Piro CM, Tran R, Mathies RA, Marletta MA, Controlling Conformational Flexibility of an O(2)-Binding H-NOX Domain [J]. Biochemistry (Mosc),2011,50(32):6832-40.
[126]Tran R, Weinert EE, Boon EM, Mathies RA, Marletta MA, Determinants of the Heme-CO Vibrational Modes in the H-NOX Family [J]. Biochemistry (Mosc), 2011,50(30):6519-30.
[127]Menyhard DK, Conformational selection mechanism governs oxygen ligation to H-NOX proteins [J]. Bioorganic and Medicinal Chemistry Letters,2011,21(12): 3523-6.
[128]Olea C, Jr., Kuriyan J, Marietta MA, Modulating heme redox potential through protein-induced porphyrin distortion [J]. J Am Chem Soc,2010,132(37): 12794-5.
[129]Olea C, Jr., Herzik MA, Jr., Kuriyan J, Marietta MA, Structural insights into the molecular mechanism of H-NOX activation [J]. Protein Science,2010,19(4): 881-7.
[130]Dai Z, Boon EM, Engineering of the heme pocket of an H-NOX domain for direct cyanide detection and quantification [J]. J Am Chem Soc,2010,132(33): 11496-503.
[131]Olea C, Boon EM, Pellicena P, Kuriyan J, Marietta MA, Probing the function of heme distortion in the H-NOX family [J]. ACS Chem Biol,2008,3(11):703-10.
[132]Boon EM, Marietta MA, Ligand discrimination in soluble guanylate cyclase and the H-NOX family of heme sensor proteins [J]. Curr Opin Chem Biol,2005, 9(5):441-6.
[133]Ma X, Sayed N, Beuve A, van den Akker F, NO and CO differentially activate soluble guanylyl cyclase via a heme pivot-bend mechanism [J]. EMBO Journal, 2007,26(2):578-88.
[134]Martin F, Baskaran P, Ma X, Dunten PW, Schaefer M, Stasch JP, Beuve A, van den Akker F, Structure of cinaciguat (BAY 58-2667) bound to Nostoc H-NOX domain reveals insights into heme-mimetic activation of the soluble guanylyl cyclase [J]. J Biol Chem,2010,285(29):22651-7.
[135]Winger JA, Derbyshire ER, Lamers MH, Marietta MA, Kuriyan J, The crystal structure of the catalytic domain of a eukaryotic guanylate cyclase [J]. BMC Struct Biol,2008,8:42.
[136]Ma X, Beuve A, van den Akker F, Crystal structure of the signaling helix coiled-coil domain of the betal subunit of the soluble guanylyl cyclase [J]. BMC Struct Biol,2010,10:2.
[1]Ma X, Sayed N, Beuve A, van den Akker F, NO and CO differentially activate soluble guanylyl cyclase via a heme pivot-bend mechanism [J]. EMBO Journal, 2007,26(2):578-88.
[2]Nioche P, Berka V, Vipond J, Minton N, Tsai AL, Raman CS, Femtomolar sensitivity of a NO sensor from Clostridium botulinum [J]. Science,2004, 306(5701):1550-3.
[3]Hu X, Murata LB, Weichsel A, Brailey JL, Roberts SA, Nighorn A, Montfort WR, Allostery in recombinant soluble guanylyl cyclase from Manduca sexta [J]. J Biol Chem,2008,283(30):20968-77.
[4]Winger JA, Marietta MA, Expression and characterization of the catalytic domains of soluble guanylate cyclase:Interaction with the heme domain [J]. Biochemistry (Mosc),2005,44(10):4083-4090.
[5]Karow DS, Pan DH, Davis JH, Behrends S, Mathies RA, Marietta MA, Characterization of functional heme domains from soluble guanylate cyclase [J]. Biochemistry (Mosc),2005,44(49):16266-16274.
[6]Zhao Y, Marietta MA, Localization of the heme binding region in soluble guanylate cyclase [J]. Biochemistry (Mosc),1997,36(50):15959-64.
[7]Zhong F, Wang H, Ying T, Huang ZX, Tan X, Efficient expression of human soluble guanylate cyclase in Escherichia coli and its signaling-related interaction with nitric oxide [J].Amino Acids,2010,39:399-408.
[8]Derbyshire ER, Winter MB, Ibrahim M, Deng S, Spiro TG, Marietta MA, Probing domain interactions in soluble guanylate cyclase [J]. Biochemistry (Mosc),2011,50(20):4281-90.
[9]Autenrieth F, Tajkhorshid E, Baudry J, Luthey-Schulten Z, Classical force field parameters for the heme prosthetic group of cytochrome c [J]. J Comput Chem, 2004,25(13):1613-22.
[10]Laidig KE, Daggett V, Molecular dynamics simulations of apocytochrome b562--the highly ordered limit of molten globules [J]. Folding and Design,1996, 1(5):335-46.
[11]Mackerell AD, Jr., Feig M, Brooks CL,3rd, Extending the treatment of backbone energetics in protein force fields:limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations [J]. J Comput Chem,2004,25(11):1400-15.
[12]Berry EA, Trumpower BL, Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra [J]. Anal Biochem,1987,161(1):1-15.
[13]Mukherjee P, Halder M, Hargrove MS, Petrich JW, Characterization of the interactions of fluorescent probes with proteins:coumarin 153 and 1,8-ANS in complex with holo-and apomyoglobin [J]. Photochem Photobiol,2006,82(6): 1586-90.
[14]Pellicena P, Karow DS, Boon EM, Marletta MA, Kuriyan J, Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases [J]. Proc Natl Acad Sci U S A,2004,101(35):12854-12859.
[15]Capece L, Estrin DA, Marti MA, Dynamical characterization of the heme NO oxygen binding (HNOX) domain. Insight into soluble guanylate cyclase allosteric transition [J]. Biochemistry (Mosc),2008,47(36):9416-27.
[16]Burstyn JN, Yu AE, Dierks EA, Hawkins BK, Dawson JH, Studies of the heme coordination and ligand binding properties of soluble guanylyl cyclase (sGC): characterization of Fe(II)sGC and Fe(II)sGC(CO) by electronic absorption and magnetic circular dichroism spectroscopies and failure of CO to activate the enzyme [J]. Biochemistry (Mosc),1995,34(17):5896-903.
[17]Lee YC, Martin E, Murad F, Human recombinant soluble guanylyl cyclase: Expression, purification, and regulation [J]. Proc Natl Acad Sci U S A,2000, 97(20):10763-10768.
[18]Stone JR, Marletta MA, Soluble guanylate cyclase from bovine lung:activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states [J]. Biochemistry (Mosc),1994,33(18):5636-40.
[19]Deinum G, Stone JR, Babcock GT, Marletta MA, Binding of nitric oxide and carbon monoxide to soluble guanylate cyclase as observed with resonance Raman spectroscopy [J]. Biochemistry (Mosc),1996,35(5):1540-1547.
[20]Fan B, Gupta G, Danziger RS, Friedman JM, Rousseau DL, Resonance Raman characterization of soluble guanylate cyclase expressed from baculovirus [J]. Biochemistry (Mosc),1998,37(5):1178-84.
[21]Li Z, Pal B, Takenaka S, Tsuyama S, Kitagawa T, Resonance Raman evidence for the presence of two heme pocket conformations with varied activities in CO-bound bovine soluble guanylate cyclase and their conversion [J]. Biochemistry (Mosc),2005,44(3):939-46.
[22]Tomita T, Ogura T, Tsuyama S, Imai Y, Kitagawa T, Effects of GTP on bound nitric oxide of soluble guanylate cyclase probed by resonance Raman spectroscopy [J]. Biochemistry (Mosc),1997,36(33):10155-60.
[23]Vogel KM, Hu S, Spiro TG, Dierks EA, Yu AE, Burstyn JN, Variable forms of soluble guanylyl cyclase:protein-ligand interactions and the issue of activation by carbon monoxide [J]. J Biol Inorg Chem,1999,4(6):804-13.
[24]Yu AE, Hu SZ, Spiro TG, Burstyn JN, Resonance raman-spectroscopy of soluble guanylyl cyclase reveal displacement of distal and proximal heme ligands by NO [J]. J Am Chem Soc,1994,116(9):4117-4118.
[25]Antonini E, Brunori M, in Frontiers of Biology. North-Holland Publishing Co: Amsterdam,1971.
[26]Yamanaka T, in The Biochemistry of Bacterial Cytochromes. Japan Scientific Societies Press:Tokyo,1992.
[27]Gerzer R, Bohme E, Hofmann F, Schultz G, Soluble guanylate cyclase purified from bovine lung contains heme and copper [J]. FEBS Lett,1981,132(1):71-4.
[28]Ignarro LJ, Adams JB, Horwitz PM, Wood KS, Activation of soluble guanylate cyclase by NO-hemoproteins involves NO-heme exchange. Comparison of heme-containing and heme-deficient enzyme forms [J]. J Biol Chem,1986, 261(11):4997-5002.
[29]Makino R, Matsuda H, Obayashi E, Shiro Y, Iizuka T, Hori H, EPR characterization of axial bond in metal center of native and cobalt-substituted guanylate cyclase [J]. J Biol Chem,1999,274(12):7714-23.
[30]Yazawa S, Tsuchiya H, Hori H, Makino R, Functional characterization of two nucleotide-binding sites in soluble guanylate cyclase [J]. J Biol Chem,2006, 281(31):21763-70.
[31]Tsaprailis G, Chan DW, English AM, Conformational states in denaturants of cytochrome c and horseradish peroxidases examined by fluorescence and circular dichroism [J]. Biochemistry (Mosc),1998,37(7):2004-16.
[32]Jang DJ, el-Sayed MA, Tryptophan fluorescence quenching as a monitor for the protein conformation changes occurring during the photocycle of bacteriorhodopsin under different perturbations [J]. Proc Natl Acad Sci U S A, 1989,86(15):5815-9.
[33]Kamatari YO, Konno T, Kataoka M, Akasaka K, The methanol-induced globular and expanded denatured states of cytochrome c:a study by CD fluorescence, NMR and small-angle X-ray scattering [J]. Journal of Molecular Biology,1996, 259(3):512-23.
[34]Latypov RF, Cheng H, Roder NA, Zhang J, Roder H, Structural characterization of an equilibrium unfolding intermediate in cytochrome c [J]. Journal of Molecular Biology,2006,357(3):1009-25.
[35]Chen Y, Barkley MD, Toward understanding tryptophan fluorescence in proteins [J]. Biochemistry (Mosc),1998,37(28):9976-82.
[36]Weinert EE, Phillips-Piro CM, Tran R, Mathies RA, Marletta MA, Controlling Conformational Flexibility of an O(2)-Binding H-NOX Domain [J]. Biochemistry (Mosc),2011,50(32):6832-40.
[37]Olea C, Jr., Kuriyan J, Marletta MA, Modulating heme redox potential through protein-induced porphyrin distortion [J]. J Am Chem Soc,2010,132(37): 12794-5.
[38]Fritz BG, Hu X, Brailey JL, Berry RE, Walker FA, Montfort WR, Oxidation and loss of heme in soluble guanylyl cyclase from Manduca sexta [J]. Biochemistry (Mosc),2011,50(26):5813-5.
[39]Ali V, Prakash K, Kulkarni S, Ahmad A, Madhusudan KP, Bhakuni V, 8-anilino-l-naphthalene sulfonic acid (ANS) induces folding of acid unfolded cytochrome c to molten globule state as a result of electrostatic interactions [J]. Biochemistry (Mosc),1999,38(41):13635-42.
[1]Evgenov OV, Pacher P, Schmidt PM, Hasko G, Schmidt HH, Stasch JP, NO-independent stimulators and activators of soluble guanylate cyclase: discovery and therapeutic potential [J]. Nat Rev Drug Discov,2006,5(9): 755-68.
[2]Pellicena P, Karow DS, Boon EM, Marietta MA, Kuriyan J, Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases [J]. Proc Natl Acad Sci U S A,2004,101(35):12854-12859.
[3]Schmidt PM, Schramm M, Schroder H, Wunder F, Stasch JP, Identification of residues crucially involved in the binding of the heme moiety of soluble guanylate cyclase [J]. J Biol Chem,2004,279(4):3025-32.
[4]Foerster J, Harteneck C, Malkewitz J, Schultz G, Koesling D, A functional heme-binding site of soluble guanylyl cyclase requires intact N-termini of alpha 1 and beta 1 subunits [J]. Eur J Biochem,1996,240(2):380-6.
[5]Stone JR, Marietta MA, Soluble guanylate cyclase from bovine lung:activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states [J]. Biochemistry (Mosc),1994,33(18):5636-40.
[6]Stone JR, Marietta MA, Heme stoichiometry of heterodimeric soluble guanylate cyclase [J]. Biochemistry (Mosc),1995,34(45):14668-74.
[7]Tomita T, Tsuyama S, Imai Y, Kitagawa T, Purification of bovine soluble guanylate cyclase and ADP-ribosylation on its small subunit by bacterial toxins [J]. J Biochem,1997,122(3):531-6.
[8]Hu X, Murata LB, Weichsel A, Brailey JL, Roberts SA, Nighorn A, Montfort WR, Allostery in recombinant soluble guanylyl cyclase from Manduca sexta [J]. J Biol Chem,2008,283(30):20968-77.
[9]Pal B, Kitagawa T, Binding of YC-1/BAY 41-2272 to soluble guanylate cyclase: A new perspective to the mechanism of activation [J]. Biochem Biophys Res Commun,2010,397(3):375-9.
[10]Chivian D, Kim DE, Malmstrom L, Bradley P, Robertson T, Murphy P, Strauss CE, Bonneau R, Rohl CA, Baker D, Automated prediction of CASP-5 structures using the Robetta server [J]. Proteins,2003,53 Suppl 6:524-33.
[11]Zhao Y, Marietta MA, Localization of the heme binding region in soluble guanylate cyclase [J]. Biochemistry (Mosc),1997,36(50):15959-64.
[12]Karow DS, Pan DH, Davis JH, Behrends S, Mathies RA, Marietta MA, Characterization of functional heme domains from soluble guanylate cyclase [J]. Biochemistry (Mosc),2005,44(49):16266-16274.
[13]Winger JA, Marietta MA, Expression and characterization of the catalytic domains of soluble guanylate cyclase:Interaction with the heme domain [J]. Biochemistry (Mosc),2005.44(10):4083-4090.
[14]Zhong F, Pan J, Liu X, Wang H, Ying T, Su J, Huang ZX, Tan X, A novel insight into the heme and NO/CO binding mechanism of the alpha subunit of human soluble guanylate cyclase [J]. J Biol Inorg Chem,2011, DOI 10.1007/s00775-011-0811-x.
[15]Hargrove MS, Barrick D, Olson JS, The association rate constant for heme binding to globin is independent of protein structure [J]. Biochemistry (Mosc), 1996,35(35):11293-9.
[16]Guryev OL, Gilep AA, Usanov SA, Estabrook RW, Interaction of apo-cytochrome b5 with cytochromes P4503A4 and P45017A:relevance of heme transfer reactions [J]. Biochemistry (Mosc),2001,40(16):5018-31.
[17]Hargrove MS, Singleton EW, Quillin ML, Ortiz LA, Phillips GN, Jr., Olson JS, Mathews AJ, His64(E7)-->Tyr apomyoglobin as a reagent for measuring rates of hemin dissociation [J]. J Biol Chem,1994,269(6):4207-14.
[18]Winger JA, Derbyshire ER, Marletta MA, Dissociation of nitric oxide from soluble guanylate cyclase and heme-nitric oxide/oxygen binding domain constructs [J]. J Biol Chem,2007,282(2):897-907.
[19]Emmons TL, Mathis KJ, Shuck ME, Reitz BA, Curran DF, Walker MC, Leone JW, Day JE, Bienkowski MJ, Fischer HD, Tomasselli AG, Purification and characterization of recombinant human soluble guanylate cyclase produced from baculovirus-infected insect cells [J]. Protein Expr Purif,2009.
[20]Garbers DL, Purification of soluble guanylate cyclase from rat lung [J]. J Biol Chem,1979,254(1):240-3.
[21]Gupta G, Kim J, Yang L, Sturley SL, Danziger RS, Expression and purification of soluble, active heterodimeric guanylyl cyclase from baculovirus [J]. Protein Expr Purif,1997,10(3):325-30.
[22]Kamisaki Y, Saheki S, Nakane M, Palmieri JA, Kuno T, Chang BY, Waldman SA, Murad F, Soluble guanylate cyclase from rat lung exists as a heterodimer [J]. J Biol Chem,1986,261(16):7236-41.
[23]Koglin M, Behrends S, Native human nitric oxide sensitive guanylyl cyclase: purification and characterization [J]. Biochemical Pharmacology,2004,67(8): 1579-85.
[24]Lee YC, Martin E, Murad F, Human recombinant soluble guanylyl cyclase: Expression, purification, and regulation [J]. Proc Natl Acad Sci U S A,2000, 97(20):10763-10768.
[25]Mathis KJ, Emmons TL, Curran DF, Day JE, Tomasselli AG, High yield purification of soluble guanylate cyclase from bovine lung [J]. Protein Expr Purif, 2008,60(1):58-63.
[26]Zhong F, Wang H, Ying T, Huang ZX, Tan X, Efficient expression of human soluble guanylate cyclase in Escherichia coli and its signaling-related interaction with nitric oxide [J]. Amino Acids,2010,39:399-408.
[27]Walker FA, Pulsed EPR and NMR spectroscopy of paramagnetic iron porphyrinates and related iron macrocycles:how to understand patterns of spin delocalization and recognize macrocycle radicals [J]. Inorg Chem,2003,42(15): 4526-44.
[28]Iyer LM, Anantharaman V, Aravind L, Ancient conserved domains shared by animal soluble guanylyl cyclases and bacterial signaling proteins [J].1471-2164, 2003,4(1):5.
[29]Ballou DP, Zhao Y, Brandish PE, Marletta MA, Revisiting the kinetics of nitric oxide (NO) binding to soluble guanylate cyclase:the simple NO-binding model is incorrect [J]. Proc Natl Acad Sci U S A,2002,99(19):12097-101.
[30]Olea C, Jr., Herzik MA, Jr., Kuriyan J, Marietta MA, Structural insights into the molecular mechanism of H-NOX activation [J]. Protein Science,2010,19(4): 881-7.
[31]Vogel KM, Hu S, Spiro TG, Dierks EA, Yu AE, Burstyn JN, Variable forms of soluble guanylyl cyclase:protein-ligand interactions and the issue of activation by carbon monoxide [J]. J Biol Inorg Chem,1999,4(6):804-13.
[32]Zhao Y, Brandish PE, Ballou DP, Marietta MA, A molecular basis for nitric oxide sensing by soluble guanylate cyclase [J]. Proc Natl Acad Sci U S A,1999,96(26): 14753-8.
[33]Zhao YD, Hoganson C, Babcock GT, Marietta MA, Structural changes in the heme proximal pocket induced by nitric oxide binding to soluble guanylate cyclase [J]. Biochemistry (Mosc),1998,37(36):12458-12464.
[34]Deinum G, Stone JR., Babcock GT, Marietta MA, Binding of nitric oxide and carbon monoxide to soluble guanylate cyclase as observed with resonance Raman spectroscopy [J]. Biochemistry (Mosc),1996,35(5):1540-1547.
[35]Denninger JW, Schelvis JPM, Brandish PE, Zhao Y, Babcock GT, Marietta MA, Interaction of soluble guanylate cyclase with YC-1:Kinetic and resonance Raman studies [J]. Biochemistry (Mosc),2000,39(14):4191-4198.
[36]Fan B, Gupta G, Danziger RS, Friedman JM, Rousseau DL, Resonance Raman characterization of soluble guanylate cyclase expressed from baculovirus [J]. Biochemistry (Mosc),1998,37(5):1178-84.
[37]Ibrahim M, Derbyshire ER, Soldatova AV, Marietta MA, Spiro TG, Soluble guanylate cyclase is activated differently by excess NO and by YC-1:resonance Raman spectroscopic evidence [J]. Biochemistry (Mosc),2010,49(23):4864-71.
[38]Li Z, Pal B, Takenaka S, Tsuyama S, Kitagawa T, Resonance Raman evidence for the presence of two heme pocket conformations with varied activities in CO-bound bovine soluble guanylate cyclase and their conversion [J]. Biochemistry (Mosc),2005,44(3):939-46.
[39]Martin E, Czarnecki K, Jayaraman V, Murad F, Kincaid J, Resonance Raman and infrared spectroscopic studies of high-output forms of human soluble guanylyl cyclase [J]. J Am Chem Soc,2005,127(13):4625-31.
[40]Schelvis JP, Zhao Y, Marletta MA, Babcock GT, Resonance raman characterization of the heme domain of soluble guanylate cyclase [J]. Biochemistry (Mosc),1998,37(46):16289-97.
[41]Yu AE, Hu SZ, Spiro TG, Burstyn JN, Resonance raman-spectroscopy of soluble guanylyl cyclase reveal displacement of distal and proximal heme ligands by NO [J]. J Am Chem Soc,1994,116(9):4117-4118.
[42]Stone JR, Marietta MA, The ferrous heme of soluble guanylate cyclase: formation of hexacoordinate complexes with carbon monoxide and nitrosomethane [J]. Biochemistry (Mosc),1995,34(50):16397-403.
[43]Stone JR, Marietta MA, Synergistic activation of soluble guanylate cyclase by YC-1 and carbon monoxide:implications for the role of cleavage of the iron-histidine bond during activation by nitric oxide [J]. Chem Biol,1998,5(5): 255-61.
[44]Tsai AL, Berka V, Martin F, Ma X, van den Akker F, Fabian M, Olson JS, Is Nostoc H-NOX a NO sensor or redox switch? [J]. Biochemistry (Mosc),2010, 49(31):6587-99.
[45]Stone JR, Sands RH, Dunham WR, Marietta MA, Electron paramagnetic resonance spectral evidence for the formation of a pentacoordinate nitrosyl-heme complex on soluble guanylate cyclase [J]. Biochem Biophys Res Commun,1995, 207(2):572-7.
[46]Boon EM, Davis JH, Tran R, Karow DS, Huang SH, Pan DH, Miazgowicz MM, Mathies RA, Marlletta MA, Nitric oxide binding to prokaryotic homologs of the soluble guanylate cyclase beta 1 H-NOX domain [J]. J Biol Chem,2006,281(31): 21892-21902.
[47]Cary SPL, Winger JA, Marletta MA, Tonic and acute nitric oxide signaling through soluble guanylate cyclase is mediated by nonheme nitric oxide, ATP, and GTP[J].Proc Natl Acad Sci U S A,2005,102(37):13064-13069.
[48]Kharitonov VQ Russwurm M, Magde D, Sharma VS, Koesling D, Dissociation of nitric oxide from soluble guanylate cyclase [J]. Biochem Biophys Res Commun,1997,239(1):284-6.
[49]Kharitonov VG, Sharma VS, Magde D, Koesling D, Kinetics of nitric oxide dissociation from five-and six-coordinate nitrosyl hemes and heme proteins, including soluble guanylate cyclase [J]. Biochemistry (Mosc),1997,36(22): 6814-8.
[50]Margulis A, Sitaramayya A, Rate of deactivation of nitric oxide-stimulated soluble guanylate cyclase:influence of nitric oxide scavengers and calcium [J]. Biochemistry (Mosc),2000,39(5):1034-9.
[51]Derbyshire ER, Fernhoff NB, Deng S, Marletta MA, Nucleotide regulation of soluble guanylate cyclase substrate specificity [J]. Biochemistry (Mosc),2009, 48(31):7519-24.
[52]Friebe A, Koesling D, Mechanism of YC-1-induced activation of soluble guanylyl cyclase [J]. Molecular Pharmacology,1998,53(1):123-7.
[53]Friebe A, Russwurm M, Mergia E, Koesling D, A point-mutated guanylyl cyclase with features of the YC-1-stimulated enzyme:implications for the YC-1 binding site? [J]. Biochemistry (Mosc),1999,38(46):15253-7.
[54]Hu X, Feng C, Hazzard JT, Tollin G,Montfort WR, Binding of YC-1 or BAY 41-2272 to soluble guanylyl cyclase induces a geminate phase in CO photolysis [J]. J Am Chem Soc,2008,130(47):15748-9.
[55]Ibrahim M, Derbyshire ER, Marletta MA, Spiro TG, Probing soluble guanylate cyclase activation by CO and YC-1 using resonance Raman spectroscopy [J]. Biochemistry (Mosc),2010,49(18):3815-23.
[56]Lamothe M, Chang FJ, Balashova N, Shirokov R, Beuve A, Functional characterization of nitric oxide and YC-1 activation of soluble guanylyl cyclase: structural implication for the YC-1 binding site? [J]. Biochemistry (Mosc),2004, 43(11):3039-48.
[57]Makino R, Obayashi E, Homma N, Shiro Y, Hori H, YC-1 facilitates release of the proximal His residue in the NO and CO complexes of soluble guanylate cyclase [J]. J Biol Chem,2003,278(13):11130-7.
[58]Martin E, Lee YC, Murad F, YC-1 activation of human soluble guanylyl cyclase has both heme-dependent and heme-independent components [J]. Proc Natl Acad Sci USA,2001,98(23):12938-42.
[59]Sharma VS, Magde D, Kharitonov VG, Koesling D, Soluble guanylate cyclase: effect of YC-1 on ligation kinetics with carbon monoxide [J]. Biochemical and Biophysical Research Communications,1999,254(1):188-91.
[60]Tsaprailis G, Chan DW, English AM, Conformational states in denaturants of cytochrome c and horseradish peroxidases examined by fluorescence and circular dichroism [J]. Biochemistry (Mosc),1998,37(7):2004-16.
[61]Light WR, Rohlfs RJ, Palmer G, Olson JS, Functional effects of heme orientational disorder in sperm whale myoglobin [J]. J Biol Chem,1987,262(1): 46-52.
[62]Fritz BG, Hu X, Brailey JL, Berry RE, Walker FA, Montfort WR, Oxidation and loss of heme in soluble guanylyl cyclase from Manduca sexta [J]. Biochemistry (Mosc),2011,50(26):5813-5.
[63]Meurer S, Pioch S, Pabst T, Opitz N, Schmidt PM, Beckhaus T, Wagner K, Matt S, Gegenbauer K, Geschka S, Karas M, Stasch JP, Schmidt HH, Muller-Esterl W, Nitric oxide-independent vasodilator rescues heme-oxidized soluble guanylate cyclase from proteasomal degradation [J]. Circ Res,2009,105(1):33-41.
[64]Maron BA, Zhang YY, Handy DE, Beuve A, Tang SS, Loscalzo J, Leopold JA, Aldosterone increases oxidant stress to impair guanylyl cyclase activity by cysteinyl thiol oxidation in vascular smooth muscle cells [J]. J Biol Chem,2009, 284(12):7665-72.
[65]Stasch JP, Schmidt PM, Nedvetsky PI, Nedvetskaya TY, H SA, Meurer S, Deile M, Taye A, Knorr A, Lapp H, Muller H, Turgay Y, Rothkegel C, Tersteegen A, Kemp-Harper B, Muller-Esterl W, Schmidt HH, Targeting the heme-oxidized nitric oxide receptor for selective vasodilatation of diseased blood vessels [J]. J Clin Invest,2006,116(9):2552-61.
[66]Gladwin MT, Deconstructing endothelial dysfunction:soluble guanylyl cyclase oxidation and the NO resistance syndrome [J]. J Clin Invest,2006,116(9): 2330-2.
[67]Stasch JP, Pacher P, Evgenov OV, Soluble guanylate cyclase as an emerging therapeutic target in cardiopulmonary disease [J]. Circulation,2011,123(20): 2263-73.
[68]Weinert EE, Phillips-Piro CM, Tran R, Mathies RA, Marietta MA, Controlling Conformational Flexibility of an O(2)-Binding H-NOX Domain [J]. Biochemistry (Mosc),2011,50(32):6832-40.
[69]Olea C, Jr., Kuriyan J, Marietta MA, Modulating heme redox potential through protein-induced porphyrin distortion [J]. J Am Chem Soc,2010,132(37): 12794-5.
[1]Haase T, Haase N, Kraehling JR, Behrends S, Fluorescent fusion proteins of soluble guanylyl cyclase indicate proximity of the heme nitric oxide domain and catalytic domain [J]. PLoS One,2010,5(7):e11617.
[2]Haase N, Haase T, Kraehling JR, Behrends S, Direct fusion of subunits of heterodimeric nitric oxide sensitive guanylyl cyclase leads to functional enzymes with preserved biochemical properties:evidence for isoform specific activation by ciguates [J]. Biochemical Pharmacology,2010,80(11):1676-83.
[3]Lee YC, Martin E, Murad F, Human recombinant soluble guanylyl cyclase: Expression, purification, and regulation [J]. Proc Natl Acad Sci U S A,2000, 97(20):10763-10768.
[4]Zabel U, Hausler C, Weeger M, Schmidt HH, Homodimerization of soluble guanylyl cyclase subunits. Dimerization analysis using a glutathione s-transferase affinity tag [J]. J Biol Chem,1999,274(26):18149-52.
[5]Wedel B, Harteneck C, Foerster J, Friebe A, Schultz G, Koesling D, Functional domains of soluble guanylyl cyclase [J]. J Biol Chem,1995,270(42):24871-5.
[6]Zhong F, Pan J, Liu X, Wang H, Ying T, Su J, Huang ZX, Tan X, A novel insight into the heme and NO/CO binding mechanism of the alpha subunit of human soluble guanylate cyclase [J]. J Biol Inorg Chem,2011, DOI 10.1007/s00775-011-0811-x.
[7]Hu X, Murata LB, Weichsel A, Brailey JL, Roberts SA, Nighorn A,--Montfort WR, Allostery in recombinant soluble guanylyl cyclase from Manduca sexta [J]. J Biol Chem,2008,283(30):20968-77.
[8]Haase N, Haase T, Seeanner M, Behrends S, Nitric oxide sensitive guanylyl cyclase activity decreases during cerebral postnatal development because of a reduction in heterodimerization [J]. Journal of Neurochemistry,2010,112(2): 542-51.
[9]Baskaran P, Heckler EJ, van den Akker F, Beuve A, Aspartate 102 in the heme domain of soluble guanylyl cyclase has a key role in NO activation [J]. Biochemistry (Mosc),2011,50(20):4291-7.
[10]Zhong F, Wang H, Ying T, Huang ZX, Tan X, Efficient expression of human soluble guanylate cyclase in Escherichia coli and its signaling-related interaction with nitric oxide [J]. Amino Acids,2010,39:399-408.
[11]Weinert EE, Phillips-Piro CM, Tran R, Mathies RA, Marletta MA, Controlling Conformational Flexibility of an O(2)-Binding H-NOX Domain [J]. Biochemistry (Mosc),2011,50(32):6832-40.
[12]Olea C, Jr., Kuriyan J, Marletta MA, Modulating heme redox potential through protein-induced porphyrin distortion [J]. J Am Chem Soc,2010,132(37): 12794-5.
[13]Hargrove MS, Singleton EW, Quillin ML, Ortiz LA, Phillips GN, Jr., Olson JS, Mathews AJ, His64(E7)-->Tyr apomyoglobin as a reagent for measuring rates of hemin dissociation [J]. J Biol Chem,1994,269(6):4207-14.
[14]Foerster J, Harteneck C, Malkewitz J, Schultz G, Koesling D, A functional heme-binding site of soluble guanylyl cyclase requires intact N-termini of alpha 1 and beta 1 subunits [J]. Eur J Biochem,1996,240(2):380-6.
[15]Karow DS, Pan DH, Davis JH, Behrends S, Mathies RA, Marietta MA, Characterization of functional heme domains from soluble guanylate cyclase [J]. Biochemistry (Mosc),2005,44(49):16266-16274.
[16]Walker FA, Pulsed EPR and NMR spectroscopy of paramagnetic iron porphyrinates and related iron macrocycles:how to understand patterns of spin delocalization and recognize macrocycle radicals [J]. Inorg Chem,2003,42(15): 4526-44.
[17]Ballou DP, Zhao Y, Brandish PE, Marietta MA, Revisiting the kinetics of nitric oxide (NO) binding to soluble guanylate cyclase:the simple NO-binding model is incorrect [J]. Proc Natl Acad Sci U S A,2002,99(19):12097-101.
[18]Olea C, Jr., Herzik MA, Jr., Kuriyan J, Marietta MA, Structural insights into the molecular mechanism of H-NOX activation [J]. Protein Science,2010,19(4): 881-7.
[19]Vogel KM, Hu S, Spiro TG, Dierks EA, Yu AE, Burstyn JN, Variable forms of soluble guanylyl cyclase:protein-ligand interactions and the issue of activation by carbon monoxide [J]. J Biol Inorg Chem,1999,4(6):804-13.
[20]Winger JA, Derbyshire ER, Marletta MA, Dissociation of nitric oxide from soluble guanylate cyclase and heme-nitric oxide/oxygen binding domain constructs [J]. J Biol Chem,2007,282(2):897-907.
[21]Zhao Y, Brandish PE, Ballou DP, Marletta MA, A molecular basis for nitric oxide sensing by soluble guanylate cyclase [J]. Proc Natl Acad Sci U S A,1999,96(26): 14753-8.
[22]Zhao YD, Hoganson C, Babcock GT, Marletta MA, Structural changes in the heme proximal pocket induced by nitric oxide binding to soluble guanylate cyclase [J]. Biochemistry (Mosc),1998,37(36):12458-12464.
[23]Ali V, Prakash K, Kulkarni S, Ahmad A, Madhusudan KP, Bhakuni V, 8-anilino-l-naphthalene sulfonic acid (ANS) induces folding of acid unfolded cytochrome c to molten globule state as a result of electrostatic interactions [J]. Biochemistry (Mosc),1999,38(41):13635-42.
[24]Martin F, Baskaran P, Ma X, Dunten PW, Schaefer M, Stasch JP, Beuve A, van den Akker F, Structure of cinaciguat (BAY 58-2667) bound to Nostoc H-NOX domain reveals insights into heme-mimetic activation of the soluble guanylyl cyclase [J]. J Biol Chem,2010,285(29):22651-7.
[25]Garbers DL, Purification of soluble guanylate cyclase from rat lung [J]. J Biol Chem,1979,254(1):240-3.
[26]Ma X, Sayed N, Baskaran P, Beuve A, van den Akker F, PAS-mediated dimerization of soluble guanylyl cyclase revealed by signal transduction histidine kinase domain crystal structure [J]. J Biol Chem,2008,283(2): 1167-78.
[27]Shiga T, Suzuki N, Amphipathic alpha-helix mediates the heterodimerization of soluble guanylyl cyclase [J].0289-0003,2005,22(7):735-42.
[28]Wagner C, Russwurm M, Jager R, Friebe A, Koesling D, Dimerization of nitric oxide-sensitive guanylyl cyclase requires the alpha 1 N terminus [J]. J Biol Chem,2005,280(18):17687-93.
[29]Wilson EM, Chinkers M, Identification of sequences mediating guanylyl cyclase dimerization [J]. Biochemistry (Mosc),1995,34(14):4696-701.
[30]Winger JA, Marletta MA, Expression and characterization of the catalytic domains of soluble guanylate cyclase:Interaction with the heme domain [J]. Biochemistry (Mosc),2005,44(10):4083-4090.
[31]Zhao Y, Marietta MA, Localization of the heme binding region in soluble guanylate cyclase [J]. Biochemistry (Mosc),1997,36(50):15959-64.
[32]Zhou Z, Gross S, Roussos C, Meurer S, Muller-Esterl W, Papapetropoulos A, Structural and functional characterization of the dimerization region of soluble guanylyl cyclase [J]. J Biol Chem,2004,279(24):24935-43.
[1]Nioche P, Berka V, Vipond J, Minton N, Tsai AL, Raman CS, Femtomolar sensitivity of a NO sensor from Clostridium botulinum [J]. Science,2004, 306(5701):1550-3.
[2]Weinert EE, Phillips-Piro CM, Tran R, Mathies RA, Marietta MA, Controlling Conformational Flexibility of an O(2)-Binding H-NOX Domain [J]. Biochemistry (Mosc),2011,50(32):6832-40.
[3]Tran R, Weinert EE, Boon EM, Mathies RA, Marietta MA, Determinants of the Heme-CO Vibrational Modes in the H-NOX Family [J]. Biochemistry (Mosc), 2011,50(30):6519-30.
[4]Menyhard DK, Conformational selection mechanism governs oxygen ligation to H-NOX proteins [J]. Bioorganic and Medicinal Chemistry Letters,2011,21(12): 3523-6.
[5]Olea C, Jr., Kuriyan J, Marietta MA, Modulating heme redox potential through protein-induced porphyrin distortion [J]. J Am Chem Soc,2010,132(37): 12794-5.
[6]Olea C, Jr., Herzik MA, Jr., Kuriyan J, Marietta MA, Structural insights into the molecular mechanism of H-NOX activation [J]. Protein Science,2010,19(4): 881-7.
[7]Dai Z, Boon EM, Engineering of the heme pocket of an H-NOX domain for direct cyanide detection and quantification [J]. J Am Chem Soc,2010,132(33): 11496-503.
[8]Olea C, Boon EM, Pellicena P, Kuriyan J, Marietta MA, Probing the function of heme distortion in the H-NOX family [J]. ACS Chem Biol,2008,3(11):703-10.
[9]Boon EM, Marietta MA, Ligand discrimination in soluble guanylate cyclase and the H-NOX family of heme sensor proteins [J]. Curr Opin Chem Biol,2005,9(5): 441-6.
[10]Pellicena P, Karow DS, Boon EM, Marietta MA, Kuriyan J, Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases [J]. Proc Natl Acad Sci U S A,2004,101(35):12854-12859.
[11]Ma X, Sayed N, Beuve A, van den Akker F, NO and CO differentially activate soluble guanylyl cyclase via a heme pivot-bend mechanism [J]. EMBO Journal, 2007,26(2):578-88.
[12]Zhong F, Wang H, Ying T, Huang ZX, Tan X, Efficient expression of human soluble guanylate cyclase in Escherichia coli and its signaling-related interaction with nitric oxide [J]. Amino Acids,2010,39:399-408.
[13]Zhong F, Pan J, Liu X, Wang H, Ying T, Su J, Huang ZX, Tan X, A novel insight into the heme and NO/CO binding mechanism of the alpha subunit of human soluble guanylate cyclase [J]. J Biol Inorg Chem,2011, DOI 10.1007/s00775-011-0811-x.
[14]Martin F, Baskaran P, Ma X, Dunten PW, Schaefer M, Stasch JP, Beuve A, van den Akker F, Structure of cinaciguat (BAY 58-2667) bound to Nostoc H-NOX domain reveals insights into heme-mimetic activation of the soluble guanylyl cyclase [J]. J Biol Chem,2010,285(29):22651-7.
[15]Winger JA, Derbyshire ER, Lamers MH, Marietta MA, Kuriyan J, The crystal structure of the catalytic domain of a eukaryotic guanylate cyclase [J]. BMC Struct Biol,2008,8:42.
[16]Ma X, Beuve A, van den Akker F, Crystal structure of the signaling helix coiled-coil domain of the beta1 subunit of the soluble guanylyl cyclase [J]. BMC Struct Biol,2010,10:2.
© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号 地址：北京市海淀区学院路29号 邮编：100083 电话：办公室：(+86 10)66554848；文献借阅、咨询服务、科技查新：66554700 |