吡咯喹啉醌对甲基汞引起PC12细胞毒性的保护作用及其机理研究
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摘要
汞是一种全球范围的环境污染物。甲基汞是汞的有机形式,极易透过血脑屏障和胎盘屏障,从而对成年和发育中的大脑造成中枢神经系统损伤。一般人群对于甲基汞的暴露主要是通过饮食途径,尤其是食用了被甲基汞污染的鱼类引起临床或亚临床中毒症状。虽然对于甲基汞神经毒性作用的具体机制尚不完全清楚,但诱导各种细胞发生凋亡性死亡和造成广泛的氧化损伤被认为是其毒性作用的重要原因。另外,各种抗氧化性物质能够保护神经元免受甲基汞的毒性也侧面证实了上述推断。
吡咯喹啉醌(PQQ)是由某些革兰氏阴性菌产生的小分子氧醌型化合物,以非共价键形式与细菌中某些脱氢酶的活性中心连接。目前,PQQ被认为是继烟酰胺腺嘌呤二核苷酸(NAD~+)或烟酰胺腺嘌呤二核苷酸磷酸(NADP~+),和黄素腺嘌呤二核苷酸(FAD)或黄素单核苷酸(FMN)之后,在自然界中发现的一个新有机辅基。PQQ以痕量水平广泛存在于各种微生物、植物和动物组织中。由于动物和人体不能自行合成PQQ,因此其体内的PQQ主要是来源于饮食。虽然对于PQQ生物学功效的探索尚处于发展阶段,但其在营养学和药理学上的作用,尤其是神经营养和保护方面的表现,已经引起了各国科学家的注意。
本研究采用PC12细胞为体外神经元模型,通过MTT、LDH试验检测了甲基汞和PQQ的细胞毒性及其相互作用关系。结果显示,甲基汞能够降低细胞存活率,破坏细胞膜完整性,且存在剂量-效应关系和时间-效应关系。甲基汞暴露前预加纳摩尔浓度的PQQ能够明显提高细胞存活率,保护细胞膜完整性。但随着PQQ处理方式不同和处理浓度的增加,其表现则有所差异。
采用Hoechst33258荧光染色、PI单染检测细胞周期分布、AV/PI双染和TUNEL检测细胞凋亡等方法,表明甲基汞以浓度依赖性方式诱导PC12细胞凋亡,干扰DNA正常合成,造成细胞周期阻滞于S期。明确了甲基汞通过破坏线粒体膜电位,降低Bcl-2/Bax蛋白比率,增加ROS含量,并激活caspase级联反应,最终导致细胞经由线粒体途径凋亡。PQQ能够保护细胞免受甲基汞诱导的凋亡,缓解细胞周期阻滞现象,其作用机制是通过保持线粒体膜电位,增加Bcl-2蛋白水平,进而抑制了caspase级联反应。另外,抑制ROS过量生成可能是其发挥保护作用的重要原因。
对胞内氧自由基含量、脂质过氧化程度、抗氧化酶活力和GSH水平检测发现,甲基汞暴露导致PC12细胞内O_2·~-、·OH和H_2O_2含量均显著提高,MDA水平升高也反映出细胞脂质过氧化程度增加,而抗氧化酶如SOD、CAT和GSH-Px活力明显降低,胞内GSH水平急剧减少。PQQ能够降低O_2·~-、·OH和H_2O_2等氧自由基的含量,降低MDA水平,显著提高SOD、CAT和GSH-Px活力,并能够维持胞内GSH水平。说明PQQ不仅能够直接清除氧自由基,抑制脂质过氧化损伤,同时也可以通过提高胞内抗氧化酶活力、维持硫醇水平等方式间接发挥保护作用。
总之,本研究首次报道了PQQ能够缓解甲基汞对PC12细胞引起的神经毒性作用,初步阐明了其拮抗机制与抑制细胞凋亡,减少氧化损伤有关。这对于更好地了解甲基汞的毒性作用机理,为甲基汞神经毒害的防治提供了理论依据,同时也为广泛而深入地探索PQQ的生物学功能开辟了新的方向。
Mercury is a worldwide environmental contaminant. Methylmercury (MeHg) is an organic form of mercury that can cause central nervous system (CNS) damage in both the adult and developing brain. The general population is exposed to MeHg primarily through excessive ingestion from a diet that can lead to a dangerous toxicant burden with clinical or subclinical implications. Though the mechanisms of action for MeHg are not well understood, extensive research has been conducted to elucidate the cellular events associated with MeHg-induced neurotoxicity. Investigators have presented work on induction of apoptosis by MeHg in multiple cell types. On the other hand, previous studies on the mechanism of MeHg neurotoxicity have implicated the oxidative injury. Moreover, the fact that a variety of antioxidants can protect cells against MeHg-induced toxicity has also confirmed the above inference.
Pyrroloquinoline quinone (PQQ) is a low molecular weight compound that synthesized by some Gram-negative bacteria. This ortho-quinone compound serves as a noncovalent cofactor for bacterial dehydrogenases. In present, PQQ has been evaluated as the third coenzyme following nicotinamide adenine dinucleotide (NAD~+) or nicotinamide adenine dinucleotide phosphate (NADP~+) , and flavin adenine dinucleotide (FAD) or flavin mononucleotide (FMN) in biological oxidoreduction. Rather soon after the discovery of PQQ, it has been identified in various microorganisms, plants and animal tissues. Because animals or humans do not appear to synthesize PQQ, the diet is assumed to be the major source. Due to its inherent antioxidative properties and redox regulative functions, PQQ has been drawing attention from both the nutritional and the pharmacological viewpoint.
In this study, we investigated the protective effects of PQQ on MeHg-induced neurotoxicity in PC12 cells model by MTT and LDH assay. The results showed that MeHg decreased the PC12 cell viability in a dose-dependent and time- dependent manner. After pretreatment of PC12 cells with PQQ (3～300 nM) prior to MeHg exposure, the MeHg-induced cytotoxicity was significantly attenuated. Further, PQQ can also maintain the plasma membrane integrity. But with the change in treatment method and increase in treatment concentrations, the effect of PQQ on MeHg-induced cytotoxicity is different.
MeHg exposure results in apoptotic cell death, increased the proportion of cells in S-phase, decreased the mitochondrial membrane potential and the level of Bcl-2 protein, and then increased the activity of caspase-3. Further, the overproduction of ROS was also oberved in PC12 cells exposed to MeHg. The addition of PQQ evidently reduced the number of apoptotic cells, ameliorated S-phase arrest, recovered the mitochondrial membrane potential, regulated the level of Bcl-2 , and then inhibited the activation of caspase-3. Moreover, PQQ also decreased the production in PC12 cells exposed to MeHg. Thus, these results indicate that PQQ can protect PC12 cells against MeHg-induced apoptosis via ameliorating the mitochondrial dysfunction.
Exposure to MeHg increased the production of superoxide anion (O_2·~-), hydrogen peroxide (H_2O_2) and hydroxyl free radical (·OH), and further resulted in lipid peroxidation in PC12 cells. Pretreatment with PQQ significantly suppressed these ROS production and attenuated lipid peroxidation in a dose-dependent manner. Moreover, PQQ increased the activity of superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GSH-Px) in PC12 cells exposed to MeHg.
In conclusion, altogether our fidings demonstrated that PQQ could protect PC12 cells from MeHg-induced apoptosis by ameliorating the mitochondrial dysfunction. Moreover, the underlying mechanism of the protective effects of PQQ may be associated with reducing the MeHg-caused oxidative injury and modulating the antioxidative defense system. To our knowledge, this is the first report describing the in vitro protective effect of PQQ on MeHg-induced neurotoxicity. Data from this study provided not only a useful strategy for the treatment of neuronal toxicity induced by mercury toxins, but a novel insight into the physiological functions and mechanisms of PQQ.
吡咯喹啉醌(PQQ)是由某些革兰氏阴性菌产生的小分子氧醌型化合物,以非共价键形式与细菌中某些脱氢酶的活性中心连接。目前,PQQ被认为是继烟酰胺腺嘌呤二核苷酸(NAD~+)或烟酰胺腺嘌呤二核苷酸磷酸(NADP~+),和黄素腺嘌呤二核苷酸(FAD)或黄素单核苷酸(FMN)之后,在自然界中发现的一个新有机辅基。PQQ以痕量水平广泛存在于各种微生物、植物和动物组织中。由于动物和人体不能自行合成PQQ,因此其体内的PQQ主要是来源于饮食。虽然对于PQQ生物学功效的探索尚处于发展阶段,但其在营养学和药理学上的作用,尤其是神经营养和保护方面的表现,已经引起了各国科学家的注意。
本研究采用PC12细胞为体外神经元模型,通过MTT、LDH试验检测了甲基汞和PQQ的细胞毒性及其相互作用关系。结果显示,甲基汞能够降低细胞存活率,破坏细胞膜完整性,且存在剂量-效应关系和时间-效应关系。甲基汞暴露前预加纳摩尔浓度的PQQ能够明显提高细胞存活率,保护细胞膜完整性。但随着PQQ处理方式不同和处理浓度的增加,其表现则有所差异。
采用Hoechst33258荧光染色、PI单染检测细胞周期分布、AV/PI双染和TUNEL检测细胞凋亡等方法,表明甲基汞以浓度依赖性方式诱导PC12细胞凋亡,干扰DNA正常合成,造成细胞周期阻滞于S期。明确了甲基汞通过破坏线粒体膜电位,降低Bcl-2/Bax蛋白比率,增加ROS含量,并激活caspase级联反应,最终导致细胞经由线粒体途径凋亡。PQQ能够保护细胞免受甲基汞诱导的凋亡,缓解细胞周期阻滞现象,其作用机制是通过保持线粒体膜电位,增加Bcl-2蛋白水平,进而抑制了caspase级联反应。另外,抑制ROS过量生成可能是其发挥保护作用的重要原因。
对胞内氧自由基含量、脂质过氧化程度、抗氧化酶活力和GSH水平检测发现,甲基汞暴露导致PC12细胞内O_2·~-、·OH和H_2O_2含量均显著提高,MDA水平升高也反映出细胞脂质过氧化程度增加,而抗氧化酶如SOD、CAT和GSH-Px活力明显降低,胞内GSH水平急剧减少。PQQ能够降低O_2·~-、·OH和H_2O_2等氧自由基的含量,降低MDA水平,显著提高SOD、CAT和GSH-Px活力,并能够维持胞内GSH水平。说明PQQ不仅能够直接清除氧自由基,抑制脂质过氧化损伤,同时也可以通过提高胞内抗氧化酶活力、维持硫醇水平等方式间接发挥保护作用。
总之,本研究首次报道了PQQ能够缓解甲基汞对PC12细胞引起的神经毒性作用,初步阐明了其拮抗机制与抑制细胞凋亡,减少氧化损伤有关。这对于更好地了解甲基汞的毒性作用机理,为甲基汞神经毒害的防治提供了理论依据,同时也为广泛而深入地探索PQQ的生物学功能开辟了新的方向。
Mercury is a worldwide environmental contaminant. Methylmercury (MeHg) is an organic form of mercury that can cause central nervous system (CNS) damage in both the adult and developing brain. The general population is exposed to MeHg primarily through excessive ingestion from a diet that can lead to a dangerous toxicant burden with clinical or subclinical implications. Though the mechanisms of action for MeHg are not well understood, extensive research has been conducted to elucidate the cellular events associated with MeHg-induced neurotoxicity. Investigators have presented work on induction of apoptosis by MeHg in multiple cell types. On the other hand, previous studies on the mechanism of MeHg neurotoxicity have implicated the oxidative injury. Moreover, the fact that a variety of antioxidants can protect cells against MeHg-induced toxicity has also confirmed the above inference.
Pyrroloquinoline quinone (PQQ) is a low molecular weight compound that synthesized by some Gram-negative bacteria. This ortho-quinone compound serves as a noncovalent cofactor for bacterial dehydrogenases. In present, PQQ has been evaluated as the third coenzyme following nicotinamide adenine dinucleotide (NAD~+) or nicotinamide adenine dinucleotide phosphate (NADP~+) , and flavin adenine dinucleotide (FAD) or flavin mononucleotide (FMN) in biological oxidoreduction. Rather soon after the discovery of PQQ, it has been identified in various microorganisms, plants and animal tissues. Because animals or humans do not appear to synthesize PQQ, the diet is assumed to be the major source. Due to its inherent antioxidative properties and redox regulative functions, PQQ has been drawing attention from both the nutritional and the pharmacological viewpoint.
In this study, we investigated the protective effects of PQQ on MeHg-induced neurotoxicity in PC12 cells model by MTT and LDH assay. The results showed that MeHg decreased the PC12 cell viability in a dose-dependent and time- dependent manner. After pretreatment of PC12 cells with PQQ (3～300 nM) prior to MeHg exposure, the MeHg-induced cytotoxicity was significantly attenuated. Further, PQQ can also maintain the plasma membrane integrity. But with the change in treatment method and increase in treatment concentrations, the effect of PQQ on MeHg-induced cytotoxicity is different.
MeHg exposure results in apoptotic cell death, increased the proportion of cells in S-phase, decreased the mitochondrial membrane potential and the level of Bcl-2 protein, and then increased the activity of caspase-3. Further, the overproduction of ROS was also oberved in PC12 cells exposed to MeHg. The addition of PQQ evidently reduced the number of apoptotic cells, ameliorated S-phase arrest, recovered the mitochondrial membrane potential, regulated the level of Bcl-2 , and then inhibited the activation of caspase-3. Moreover, PQQ also decreased the production in PC12 cells exposed to MeHg. Thus, these results indicate that PQQ can protect PC12 cells against MeHg-induced apoptosis via ameliorating the mitochondrial dysfunction.
Exposure to MeHg increased the production of superoxide anion (O_2·~-), hydrogen peroxide (H_2O_2) and hydroxyl free radical (·OH), and further resulted in lipid peroxidation in PC12 cells. Pretreatment with PQQ significantly suppressed these ROS production and attenuated lipid peroxidation in a dose-dependent manner. Moreover, PQQ increased the activity of superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GSH-Px) in PC12 cells exposed to MeHg.
In conclusion, altogether our fidings demonstrated that PQQ could protect PC12 cells from MeHg-induced apoptosis by ameliorating the mitochondrial dysfunction. Moreover, the underlying mechanism of the protective effects of PQQ may be associated with reducing the MeHg-caused oxidative injury and modulating the antioxidative defense system. To our knowledge, this is the first report describing the in vitro protective effect of PQQ on MeHg-induced neurotoxicity. Data from this study provided not only a useful strategy for the treatment of neuronal toxicity induced by mercury toxins, but a novel insight into the physiological functions and mechanisms of PQQ.
引文
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