肠出血性大肠杆菌（EHEC O157：H7）VT2毒素致病机理研究
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摘要
肠出血性大肠杆菌(EHEC)是产VT毒素大肠杆菌(VTEC)的一个亚群。O157:H7血清型是EHEC中典型的致病菌株,是大规模O157感染爆发的主要病原菌。O157:H7是一种食源性致病菌,牛是其首要的天然寄主,主要是食物被牛粪污染,导致感染爆发。EHEC感染会引起轻度腹泻到出血性肠炎、严重者会引起出血性尿毒综合症,甚至死亡。EHEC最关键的两个致病因子是由噬菌体编码的VT毒素和介导粘附作用的LEE毒力岛(肠道上皮细胞损伤位点)。LEE毒力岛编码的蛋白负责形成粘附抹平损伤,其典型特征是通过病原菌和寄主肠道表面的紧密粘附,在寄主细胞表面细菌粘附位点肌动蛋白富集,形成杯状基座和细胞表面边缘刷状微绒毛损伤。LEE毒力岛由LEE1到LEE5主要5个操纵子组成,编码的Ⅲ型分泌系统涉及到移位因子的分泌、效应蛋白和外膜表面紧密粘附素Intinmin与其受体蛋白Tir(由细菌编码转运到宿主细胞上的粘附素受体)。粘附素Intinmin除了和其主要受体蛋白Tir结合之外,还会和寄主细胞表面的粘附素受体(HIR)结合,如Intinmin与肠道细胞表面的β1整合素(β1-integrin)和核仁素(nucleolin)结合。有研究认为在形成稳定的intimin-Tir结构之前,粘附素intimin首先和寄主细胞的粘附素受体HIRs结合,使得细菌和寄主细胞足够接近从而完成Tir和其他效应因子从细菌到寄主上皮细胞表面的注射转运过程。
EHEC O157:H7产生的VT毒素是其重要的致病因素之一,本研究关注肠出血性大肠杆菌EHEC86-24感染猪空肠细胞系(IPEC-J2)、人结肠细胞系(CaCo-2)和人喉癌细胞系(HEp-2)过程中,产生的VT毒素对其粘附定植过程的影响,以及在细菌感染IPEC-J2细胞过程中,VT毒素对其相关致病因子的基因表达水平影响,包括对致病粘附因子β1整合素(β1-integrin)和核仁素( nucleolin)的基因表达影响,对VT毒素受体Gb3合成表达的影响,从而深入分析VT毒素在EHEC致病过程中的作用机理。试验利用λ-Red同源重组技术构建了vt2基因敲除突变菌株86-24-vt2S,同时产生了编码VT2毒素的噬菌体缺失突变菌株86-24△933W、以及突变菌株的vt2基因补充菌株86-24-vt2S(pVT2)和86-24-933W(pVT2)。将野生型菌株EHEC 86-24和不同vt2基因突变菌株与真核细胞系进行粘附试验,并对感染过程真核细胞IPEC-J2的相关粘附因子基因进行实时定量PCR检测。试验结果显示:与其亲本野生型EHEC菌株和vt2基因补充菌株比较,vt2基因敲除突变株对3株真核细胞系的粘附能力均显著降低;野生型EHEC菌株在感染IPEC-J2细胞系过程中,伴随宿主细胞相关粘附因子β1-integrin、nucleolin和Gb3合成基因的表达增加;IPEC-J2细胞系与野生型EHEC O157:H7或vt2基因补充突变株相互作用时,β1整合素的表达水平高于IPEC-J2与vt2基因敲除突变菌株或无细菌粘附时的表达水平;IPEC-J2与vt2基因敲除突变菌株粘附感染时,核仁素的表达水平降低,但是其基因补充菌株没有修复核仁素的表达到野生型水平。试验数据揭示VT2毒素在EHEC O157:H7致病菌对肠道上皮细胞的粘附过程中有促进作用,这种促进作用从基因水平上是通过提高宿主细胞表面受体因子β1-integrin和nucleolin的表达水平,从而提高了细菌的粘附功能。
核仁素(Nucleolin)是一种可以表达在多种类型真核细胞表面的多功能核蛋白,作为一些病毒和粘附素的受体。核仁素是与广泛的细胞和细胞之间相互作用相关的一个受体大家族。肠致病性大肠杆菌杆(EPEC)的粘附素与β1整合素特异结合。在猪和牛的组织感染试验中,免疫染色发现β1整合素聚集在细菌粘附位点,说明整合素在EHEC字O157:H7感染过程中是一个潜在的受体蛋白。VT毒素是一种典型的AB_5结构蛋白,能抑制真核细胞蛋白合成。VT毒素在EHEC感染过程中导致出血性肠炎(HC)、溶血性尿毒综合症(HUS)等严重的临床症状。VT毒素的B亚基和目标细胞表面的糖脂类受体(Gb3)结合,通过受体介导毒素内化。最近研究报道VT2毒素通过刺激真核细胞表达核仁素,从而促进EHEC在肠道上的定植过程。然而,关于VT毒素促进细菌粘附定植的理论依然具有争议。
本实验室前期研究工作中构建了萘啶酮酸抗性EHEC菌株的vt2基因插入突变菌株,实验结果显示vt2基因突变导致EHEC 86-24对IPEC-J2和HEp-2的粘附能力降低。本研究中重新在萘啶酮酸敏感的野生型EHEC 86-24菌株基础上,产生了vt2基因敲除突变菌株和编码VT2噬菌体缺失突变菌株,评估了两株EHEC O157:H7突变菌株对IPEC-J2细胞系的粘附特征,并和细胞系HEp-2和CaCo-2进行了比较。实验室前期用小猪做了动物肠道感染体内实验,在此基础上本研究建立新的猪结肠IPEC-J2细胞体外感染模型,研究了EHEC O157:H7 86-24及其等位基因vt2-突变菌株对IPEC-J2细胞的粘附受体nucleolin、β1-intergrin和Gb3合成的表达影响,为进一步准确分析EHEC O157:H7的感染机理提供理论依据。
Enterohemorrhagic E. coli (EHEC) is a subgroup of verotoxin-producing E. coli (VTEC), also referred to as Shiga-toxin-producing E. coli (STEC). Serotype O157:H7 is the prototypic EHEC, associated with large outbreaks of disease in North America due to the ingestion of food contaminated with feces from cattle, which are the primary reservoir for EHEC O157:H7. The disease syndromes caused by EHEC infection include mild diarrhea to hemorrhagic colitis (HC) and, in the most severe cases, the hemolytic uremic syndrome (HUS). The key virulence factors for EHEC are a phage-encoded verotoxin (VT) and adherence mediated by the LEE (locus for enterocyte effacement) pathogenicity island (PAI). The LEE encodes proteins responsible for the attaching and effacing lesion (AE), which is characterized by intimate adhesion of the pathogen to the enterocyte surface, formation of an actin-rich pedestal on the host cell surface beneath the bacterium, and destruction of brush border microvilli. The LEE PAI consists of five major operons (LEE1, LEE2, LEE3, tir/LEE5 and LEE4) that encode a typeⅢsecretion system involved in secretion of translocon and effector proteins and the outer membrane surface adhesin intimin and its receptor Tir (translocated intimin receptor). In addition to binding to its primary receptor Tir, intimin also interacts with host cell intimin receptors (HIR), such asβ1-integrin and nucleolin, on the surface of enterocytes. It is hypothesized that prior to the formation of a stable intimin-Tir interaction, intimin binds to HIRs and brings the bacteria close enough for injection of Tir and other effectors into the host epithelial cells.
Verotoxin (VT) has been implicated in promotion of adherence to and colonization of intestinal epithelial cells by enterohemorrhagic Escherichia coli (EHEC) O157:H7. The present study investigated the effect of VT2 on adherence of EHEC O157:H7 strain 86-24 to porcine jejunal (IPEC-J2), human colon (CaCo-2) and human laryngeal carcinoma (HEp-2) cell lines and on expression in IPEC-J2 cells of synthases forβ1-integrin and nucleolin, which are both implicated in bacterial adherence. The effect on expression of Gb3 synthase, the receptor for VT, was also examined. Data were obtained by adherence assays and quantitative reverse transcriptase PCR, using EHEC O157 strain 86-24, a vt2 deletion mutant, a vt2-phage negative strain, and complemented mutants in which the vt2 gene was restored. Compared with the parent and complemented mutant strains, the vt2-negative strains adhered significantly less to all three types of cells. Adherence of the wild type EHEC strain to IPEC-J2 cells was accompanied by increased expression ofβ1-integrin, nucleolin, and Gb3 synthase. IPEC-J2 cells in association with the wild type EHEC O157 or the complemented mutants expressed higher levels ofβ1-integrin than did cells associating with the vt2-negative strains or with no bacteria. Expression of nucleolin was decreased by association with the vt2-negative mutant but complementation failed to restore wild type expression. The data indicate that VT2 plays a role in adherence of EHEC O157:H7 to intestinal epithelial cells, possibly by increasing the expression of the host receptorβ1-integrin.
Nucleolin is a multifunctional nuclear protein that can be expressed at the surface of many cell types and serves as a receptor for some viruses and intimin. Integrins are a large family of heterodimeric receptors that are associated with a wide range of cell to cell interactions. Intimin of enteropathogenic E. coli (EPEC) specifically binds toβ1 integrin. Immunostainedβ1 integrin clusters at the sites of bacterial adherence to porcine and bovine tissues, suggesting thatβ1 integrin potentially serves as a receptor for intimin during EHEC O157:H7 infection. VT, an AB_5 toxin that inhibits protein synthesis in eukaryotic cells, is responsible for the severe clinical manifestations of EHEC infection, such as HC and HUS. The toxins are internalized by receptor-mediated endocytosis after binding of the B pentamer to the target cell glycolipid receptor globotriaosylceramide (Gb3). Recent studies have indicated that VT2 also promotes EHEC colonization of the intestine by stimulating expression of nucleolin. However, this role is still controversial.
In a previous study, we showed that a Nal~R vt2-insertion mutant caused a reduction in adherence of EHEC O157:H7 strain 86-24 to IPEC-J2 and HEp-2 cells. In the present study, new vt2-deletion and VT2-phage cured mutants were generated in a Nal-sensitive strain 86-24 and the effect of the mutants on adherence of EHEC O157:H7 to IPEC-J2 cells was assessed and compared to effects on adherence to HEp-2 and CaCo-2 cells. To further characterize the new in-vitro model of porcine jejunal IPEC-J2 cells for use in combination with pig gut-loops for the study of EHEC O157:H7 pathogenesis, we analyzed the effect of EHEC O157:H7 strain 86-24 and its isogenic vt2~- mutant on expression of nucleolin,β1-intergrin, and Gb3 synthase in IPEC-J2 cells.
EHEC O157:H7产生的VT毒素是其重要的致病因素之一,本研究关注肠出血性大肠杆菌EHEC86-24感染猪空肠细胞系(IPEC-J2)、人结肠细胞系(CaCo-2)和人喉癌细胞系(HEp-2)过程中,产生的VT毒素对其粘附定植过程的影响,以及在细菌感染IPEC-J2细胞过程中,VT毒素对其相关致病因子的基因表达水平影响,包括对致病粘附因子β1整合素(β1-integrin)和核仁素( nucleolin)的基因表达影响,对VT毒素受体Gb3合成表达的影响,从而深入分析VT毒素在EHEC致病过程中的作用机理。试验利用λ-Red同源重组技术构建了vt2基因敲除突变菌株86-24-vt2S,同时产生了编码VT2毒素的噬菌体缺失突变菌株86-24△933W、以及突变菌株的vt2基因补充菌株86-24-vt2S(pVT2)和86-24-933W(pVT2)。将野生型菌株EHEC 86-24和不同vt2基因突变菌株与真核细胞系进行粘附试验,并对感染过程真核细胞IPEC-J2的相关粘附因子基因进行实时定量PCR检测。试验结果显示:与其亲本野生型EHEC菌株和vt2基因补充菌株比较,vt2基因敲除突变株对3株真核细胞系的粘附能力均显著降低;野生型EHEC菌株在感染IPEC-J2细胞系过程中,伴随宿主细胞相关粘附因子β1-integrin、nucleolin和Gb3合成基因的表达增加;IPEC-J2细胞系与野生型EHEC O157:H7或vt2基因补充突变株相互作用时,β1整合素的表达水平高于IPEC-J2与vt2基因敲除突变菌株或无细菌粘附时的表达水平;IPEC-J2与vt2基因敲除突变菌株粘附感染时,核仁素的表达水平降低,但是其基因补充菌株没有修复核仁素的表达到野生型水平。试验数据揭示VT2毒素在EHEC O157:H7致病菌对肠道上皮细胞的粘附过程中有促进作用,这种促进作用从基因水平上是通过提高宿主细胞表面受体因子β1-integrin和nucleolin的表达水平,从而提高了细菌的粘附功能。
核仁素(Nucleolin)是一种可以表达在多种类型真核细胞表面的多功能核蛋白,作为一些病毒和粘附素的受体。核仁素是与广泛的细胞和细胞之间相互作用相关的一个受体大家族。肠致病性大肠杆菌杆(EPEC)的粘附素与β1整合素特异结合。在猪和牛的组织感染试验中,免疫染色发现β1整合素聚集在细菌粘附位点,说明整合素在EHEC字O157:H7感染过程中是一个潜在的受体蛋白。VT毒素是一种典型的AB_5结构蛋白,能抑制真核细胞蛋白合成。VT毒素在EHEC感染过程中导致出血性肠炎(HC)、溶血性尿毒综合症(HUS)等严重的临床症状。VT毒素的B亚基和目标细胞表面的糖脂类受体(Gb3)结合,通过受体介导毒素内化。最近研究报道VT2毒素通过刺激真核细胞表达核仁素,从而促进EHEC在肠道上的定植过程。然而,关于VT毒素促进细菌粘附定植的理论依然具有争议。
本实验室前期研究工作中构建了萘啶酮酸抗性EHEC菌株的vt2基因插入突变菌株,实验结果显示vt2基因突变导致EHEC 86-24对IPEC-J2和HEp-2的粘附能力降低。本研究中重新在萘啶酮酸敏感的野生型EHEC 86-24菌株基础上,产生了vt2基因敲除突变菌株和编码VT2噬菌体缺失突变菌株,评估了两株EHEC O157:H7突变菌株对IPEC-J2细胞系的粘附特征,并和细胞系HEp-2和CaCo-2进行了比较。实验室前期用小猪做了动物肠道感染体内实验,在此基础上本研究建立新的猪结肠IPEC-J2细胞体外感染模型,研究了EHEC O157:H7 86-24及其等位基因vt2-突变菌株对IPEC-J2细胞的粘附受体nucleolin、β1-intergrin和Gb3合成的表达影响,为进一步准确分析EHEC O157:H7的感染机理提供理论依据。
Enterohemorrhagic E. coli (EHEC) is a subgroup of verotoxin-producing E. coli (VTEC), also referred to as Shiga-toxin-producing E. coli (STEC). Serotype O157:H7 is the prototypic EHEC, associated with large outbreaks of disease in North America due to the ingestion of food contaminated with feces from cattle, which are the primary reservoir for EHEC O157:H7. The disease syndromes caused by EHEC infection include mild diarrhea to hemorrhagic colitis (HC) and, in the most severe cases, the hemolytic uremic syndrome (HUS). The key virulence factors for EHEC are a phage-encoded verotoxin (VT) and adherence mediated by the LEE (locus for enterocyte effacement) pathogenicity island (PAI). The LEE encodes proteins responsible for the attaching and effacing lesion (AE), which is characterized by intimate adhesion of the pathogen to the enterocyte surface, formation of an actin-rich pedestal on the host cell surface beneath the bacterium, and destruction of brush border microvilli. The LEE PAI consists of five major operons (LEE1, LEE2, LEE3, tir/LEE5 and LEE4) that encode a typeⅢsecretion system involved in secretion of translocon and effector proteins and the outer membrane surface adhesin intimin and its receptor Tir (translocated intimin receptor). In addition to binding to its primary receptor Tir, intimin also interacts with host cell intimin receptors (HIR), such asβ1-integrin and nucleolin, on the surface of enterocytes. It is hypothesized that prior to the formation of a stable intimin-Tir interaction, intimin binds to HIRs and brings the bacteria close enough for injection of Tir and other effectors into the host epithelial cells.
Verotoxin (VT) has been implicated in promotion of adherence to and colonization of intestinal epithelial cells by enterohemorrhagic Escherichia coli (EHEC) O157:H7. The present study investigated the effect of VT2 on adherence of EHEC O157:H7 strain 86-24 to porcine jejunal (IPEC-J2), human colon (CaCo-2) and human laryngeal carcinoma (HEp-2) cell lines and on expression in IPEC-J2 cells of synthases forβ1-integrin and nucleolin, which are both implicated in bacterial adherence. The effect on expression of Gb3 synthase, the receptor for VT, was also examined. Data were obtained by adherence assays and quantitative reverse transcriptase PCR, using EHEC O157 strain 86-24, a vt2 deletion mutant, a vt2-phage negative strain, and complemented mutants in which the vt2 gene was restored. Compared with the parent and complemented mutant strains, the vt2-negative strains adhered significantly less to all three types of cells. Adherence of the wild type EHEC strain to IPEC-J2 cells was accompanied by increased expression ofβ1-integrin, nucleolin, and Gb3 synthase. IPEC-J2 cells in association with the wild type EHEC O157 or the complemented mutants expressed higher levels ofβ1-integrin than did cells associating with the vt2-negative strains or with no bacteria. Expression of nucleolin was decreased by association with the vt2-negative mutant but complementation failed to restore wild type expression. The data indicate that VT2 plays a role in adherence of EHEC O157:H7 to intestinal epithelial cells, possibly by increasing the expression of the host receptorβ1-integrin.
Nucleolin is a multifunctional nuclear protein that can be expressed at the surface of many cell types and serves as a receptor for some viruses and intimin. Integrins are a large family of heterodimeric receptors that are associated with a wide range of cell to cell interactions. Intimin of enteropathogenic E. coli (EPEC) specifically binds toβ1 integrin. Immunostainedβ1 integrin clusters at the sites of bacterial adherence to porcine and bovine tissues, suggesting thatβ1 integrin potentially serves as a receptor for intimin during EHEC O157:H7 infection. VT, an AB_5 toxin that inhibits protein synthesis in eukaryotic cells, is responsible for the severe clinical manifestations of EHEC infection, such as HC and HUS. The toxins are internalized by receptor-mediated endocytosis after binding of the B pentamer to the target cell glycolipid receptor globotriaosylceramide (Gb3). Recent studies have indicated that VT2 also promotes EHEC colonization of the intestine by stimulating expression of nucleolin. However, this role is still controversial.
In a previous study, we showed that a Nal~R vt2-insertion mutant caused a reduction in adherence of EHEC O157:H7 strain 86-24 to IPEC-J2 and HEp-2 cells. In the present study, new vt2-deletion and VT2-phage cured mutants were generated in a Nal-sensitive strain 86-24 and the effect of the mutants on adherence of EHEC O157:H7 to IPEC-J2 cells was assessed and compared to effects on adherence to HEp-2 and CaCo-2 cells. To further characterize the new in-vitro model of porcine jejunal IPEC-J2 cells for use in combination with pig gut-loops for the study of EHEC O157:H7 pathogenesis, we analyzed the effect of EHEC O157:H7 strain 86-24 and its isogenic vt2~- mutant on expression of nucleolin,β1-intergrin, and Gb3 synthase in IPEC-J2 cells.
引文
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