沙门菌Ⅲ型分泌系统研究进展
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摘要
沙门菌是一种重要的人兽共患肠道病原菌,在引起人类食物中毒的微生物中常列榜首。沙门菌的致病性与其Ⅲ型分泌系统(T3SS)密切相关。沙门菌能够利用T3SS选择性分泌效应蛋白至感染细胞的胞质中,在较短的时间内通过调节宿主细胞的功能,完成细菌的感染和胞内定殖过程,从而逃避机体的清除作用。沙门菌T3SS的作用机制研究对于沙门菌病的防治具有重要意义,论文主要对沙门菌T3SS的结构、组装及作用机理做一综述,以期为沙门菌病的防控提供参考。
Salmonellais a main pathogenic intestinal bacteria which can cause zoonosis.Among different food microbes,Salmonellais one of the most popular bacteria to cause food poison.The pathogenicity of Salmonellais closely associated with its typeⅢ secretion system(T3SS).After infection,Salmonellacan regulate the function of host cells through selective secretion of effector proteins into cytoplasm of cells by T3 SS and then complete the process of infection and intracellular colonization in a short time.Using this mechanism,Salmonellacan escape the killing of hosts.Therefore,the study of Salmonella T3 SS will benefit for the defense against salmonellosis.This paper focused on the review of the structure,assembly and action mechanism of T3 SS.The understanding of them will provide references for research in controlling salmonellosis.
Salmonellais a main pathogenic intestinal bacteria which can cause zoonosis.Among different food microbes,Salmonellais one of the most popular bacteria to cause food poison.The pathogenicity of Salmonellais closely associated with its typeⅢ secretion system(T3SS).After infection,Salmonellacan regulate the function of host cells through selective secretion of effector proteins into cytoplasm of cells by T3 SS and then complete the process of infection and intracellular colonization in a short time.Using this mechanism,Salmonellacan escape the killing of hosts.Therefore,the study of Salmonella T3 SS will benefit for the defense against salmonellosis.This paper focused on the review of the structure,assembly and action mechanism of T3 SS.The understanding of them will provide references for research in controlling salmonellosis.
引文
[1]Rosche K L,Aljasham A T,Kipfer J N,et al.Infection with Salmonella enteric serovar typhimurium leads to increased proportions of F4/80+red pulp macrophages and decreased proportions of B and T lymphocytes in the spleen[J].PLoS One,2015,10(6):eo130092.
[2]Portaliou A G,Tsolis K C,Loos M S,et al.TypeⅢsecretion:building and operating a remarkable nanomachine[J].Trends Biochem Sci,2015,S0968-0004(15)00182-00186.
[3]Hayward R,Jansen V,Woodward M J.Comparative genomics of Salmonella enterica serovars Derby and Mbandaka,two prevalent serovars associated with different livestock species in the UK[J].BMC Genomics,2013,14:365.
[4]Moest T P,Meresse S.Salmonella T3SSs:successful mission of the sectertion agents[J].Curr Opin Microbiol,2013,16:38-44.
[5]郭伟军,崔照琼,李华春.沙门氏菌毒力岛及其Ⅲ型分泌系统[J].上海畜牧兽医通讯,2006(5):49-51.
[6]Fass E,Groisman E A.Control of Salmonellapathogenicity island-2gene expression[J].Curr Opin Microbiol,2009,12(2):199-204.
[7]Diepold A,Wagner S.Assembly of the bacterial typeⅢsecretion machinery[J].FEMS Microbiol Rev,2014,38(4):802-822.
[8]Galán J E,Lara-Tejero M,Marlovits T C,et al.Bacterial typeⅢsecretion systems:specialized nanomachines for protein delivery into target cells[J].Annu Rev Microbiol,2014,68:415-438.
[9]Bergeron J R,Worrall L J,Sgourakis N G,et al.A refined model of the prototypical Salmonella SPI-1 T3SS basal body reveals the molecular basis for its assembly[J].PLoS Pathog,2013,9(4):e1003307.
[10]Wee D H,Hughes K T.Molecular ruler determines needle length for the Salmonella Spi-1injectisome[J].Proc Natl Acad Sci U S A,2015,112(13):4098-4103.
[11]Lefebre M D,Galán J E.The inner rod protein controls substrate switching and needle length in a Salmonella typeⅢsecretion system[J].Proc Natl Acad Sci U S A,2014,111(2):817-822.
[12]Kubori T,Sukhan A,Aizawa S I,et al.Molecular characterization and assembly of the needle complex of the Salmonella typhimuriumtypeⅢprotein secretion system[J].Proc Natl Acad Sci USA,2000,97(18):10225-10230.
[13]Rathinavelan T,Lara-Tejero M,Lefebre M,et al.NMR model of PrgI-SipD interaction and its implications in the needle-tip assembly of the SalmonellatypeⅢsecretion system[J].J Mol Biol,2014;426(16):2958-2969.
[14]Zhong D,Lefebre M,Kaur K,et al.The SalmonellatypeⅢsecretion system inner rod protein PrgJ is partially folded[J].J Biol Chem,2012,287(30):25303-25311.
[15]Rathinavelan T,Tang C,De Guzman R N.Characterization of the interaction between the SalmonellatypeⅢsecretion system tip protein SipD and the needle protein PrgI by paramagnetic relaxation enhancement[J].J Biol Chem,2011,286(6):4922-4930.
[16]Montagner C,Arquint C,Cornelis G R.Translocators YopB and YopD fromYersinia enterocoliticaform a multimeric integral membrane complex in eukaryotic cell membranes[J].J Bacteriol,2011,193(24):6923-6928.
[17]Chatterjee S,Zhong D,Nordhues B A,et al.The crystal structures of the SalmonellatypeⅢsecretion system tip protein SipD in complex with deoxycholate and chenodeoxycholate[J].Protein Sci,2011,20(1):75-86.
[18]Shen D K,Moriya N,Martinez-Argudo I,et al.Needle length control and the secretion substrate specificity switch are only loosely coupled in the typeⅢsecretion apparatus of Shigella[J].Microbiology,2012,158(7):1884-1896.
[19]Myeni S K,Wang L,Zhou D.SipB-SipC complex is essential for translocon formation[J].PLoS One,2013,8(3):e60499.
[20]Lara-Tejero M,Galán J E.Salmonella entericaserovar typhimuriumpathogenicity island 1-encoded typeⅢsecretion system translocases mediate intimate attachment to nonphagocytic cells[J].Infect Immun,2009,7(7):2635-2642.
[21]Hlzer S U,Hensel M.Functional dissection of translocon proteins of the Salmonella pathogenicity island 2-encoded typeⅢsecretion system[J].BMC Microbiol,2010,10:104.
[22]Schraidt O,Marlovits T C.Three-dimensional model of Salmonella’s needle complex at subnanometer resolution[J].Science,2011,331(6021):1192-1195.
[23]Bergeron J R,Worrall L J,De S,et al.The modular structure of the inner-membrane ring component PrgK facilitates assembly of the typeⅢsecretion system basal body[J].Structure,2015,23(1):161-172.
[24]Allison S E,Tuinema B R,Everson E S,et al.Identification of the docking site between a typeⅢsecretion system ATPase and a chaperone for effector cargo[J].J Biol Chem,2014,289(34):23734-23744.
[25]Romo-Castillo M,Andrade A,Espinosa N,et al.EscO,a functional and structural analog of the flagellar FliJ protein,is a positive regulator of EscN ATPase activity of the enteropathogenic Escherichia coli injectisome[J].J Bacteriol,2014,196(12):2227-2241.
[26]Biemans-Oldehinkel E,Sal-Man N,Deng W,et al.Quantitative proteomic analysis reveals formation of an EscL-EscQEscN typeⅢcomplex in enteropathogenic Escherichia coli[J].J Bacteriol,2011,193(19):5514-5519.
[27]Kim J S,Kim B H,Jang J I,et al.Functional insight from the tetratricopeptide repeat-like motifs of the typeⅢsecretion chaperone SicA in Salmonella enterica serovar typhimurium[J].FEMS Microbiol Lett,2014,350(2):146-153.
[28]Dehghani B,Rasooli I,Jalali-Nadoushan M,et al.Immunoprotectivity of Salmonella enterica serovar enteritidis virulence protein,InvH,against Salmonella typhi[J].Iran J Basic Med Sci,2014,17(8):560-565.
[29]Diepold A,Armitage J P.TypeⅢsecretion systems:the bacterial flagellum and the injectisome[J].Phil Trans R Soc B,2015,doi:10.1098/rstb.2015.0020.
[30]Monjarás Feria J,García-Gómez E,Espinosa N,et al.Role of EscP(Orf16)in injectisome biogenesis and regulation of typeⅢprotein secretion in enteropathogenic Escherichia coli[J].J Bacteriol,2012,194(22):6029-6045.
[31]Shibata S,Takahashi N,Chevance F F,et al.FliK regulates flagellar hook length as an internal ruler[J].Mol Microbiol,2007,64(5):1404-1415.
[32]Monjarás Feria J V,Lefebre M D,Stierhof Y D,et al.Role of autocleavage in the function of a typeⅢsecretion specificity switch protein in Salmonellaenterica serovar Typhimurium[J].MBio,2015,6(5):e01459-15.
[33]Marlovits T C,Kubori T,Lara-Tejero M,et al.Assembly of the inner rod determines needle length in the typeⅢsecretion injectisome[J].Nature,2006,441(7093):637-640.
[34]Poyraz O,Schmidt H,Seidel K,et al.Protein refolding is required for assembly of the type three secretion needle[J].Nat Struct Mol Biol,2010,17(7):788-792.
[35]Blocker A J,Deane J E,Veenendaal A K,et al.What's the point of the typeⅢsecretion system needle[J].Proc Nal Acad Sci USA,2008,105(18):6507-6513.
[36]Kubori T,Sukhan A,Aizawa SI,et al.Molecular characterization and assembly of the needle complex of the Salmonella typhimuriumtypeⅢprotein secretion system[J].Proc Natl Acad Sci USA,2000,97(18):10225-10230.
[37]Nguyen V S,Jobichen C,Tan K W,et al.Structure of AcrHAopB chaperone translocator complex reveals a role for membrane hairpins in typeⅢsecretion system translocon assembly[J].Structure,2015,23(11):2022-2031.
[38]Enninga J,Rosenshine I.Imaging the assembly,structure and activity of typeⅢsecretion systems[J].Cell Microbiol,2009,11(10):1462-1470.
[39]Abrusci P,Vergara-Irigaray M,Johnson S,et al.Architecture of the major component of the typeⅢsecretion system export apparatus[J].Nat Struct Mol Biol,2013,20(1):99-104.
[40]Figueira R,Holden D W.Functions of the Salmonella pathogenicity island 2(SPI-2)typeⅢsecretion system effectors[J].Microbiology,2012,158(Pt 5):1147-1161.
[41]Geng S,Jiao X,Barrow P,et al.Virulence determinants of Salmonella gallinarum biovar pullorum identified by PCR signature-tagged mutagenesis and the spiC mutant as a candidate live attenuated vaccine[J].Vet Microbiol,2014,168(2-4):388-394.
[2]Portaliou A G,Tsolis K C,Loos M S,et al.TypeⅢsecretion:building and operating a remarkable nanomachine[J].Trends Biochem Sci,2015,S0968-0004(15)00182-00186.
[3]Hayward R,Jansen V,Woodward M J.Comparative genomics of Salmonella enterica serovars Derby and Mbandaka,two prevalent serovars associated with different livestock species in the UK[J].BMC Genomics,2013,14:365.
[4]Moest T P,Meresse S.Salmonella T3SSs:successful mission of the sectertion agents[J].Curr Opin Microbiol,2013,16:38-44.
[5]郭伟军,崔照琼,李华春.沙门氏菌毒力岛及其Ⅲ型分泌系统[J].上海畜牧兽医通讯,2006(5):49-51.
[6]Fass E,Groisman E A.Control of Salmonellapathogenicity island-2gene expression[J].Curr Opin Microbiol,2009,12(2):199-204.
[7]Diepold A,Wagner S.Assembly of the bacterial typeⅢsecretion machinery[J].FEMS Microbiol Rev,2014,38(4):802-822.
[8]Galán J E,Lara-Tejero M,Marlovits T C,et al.Bacterial typeⅢsecretion systems:specialized nanomachines for protein delivery into target cells[J].Annu Rev Microbiol,2014,68:415-438.
[9]Bergeron J R,Worrall L J,Sgourakis N G,et al.A refined model of the prototypical Salmonella SPI-1 T3SS basal body reveals the molecular basis for its assembly[J].PLoS Pathog,2013,9(4):e1003307.
[10]Wee D H,Hughes K T.Molecular ruler determines needle length for the Salmonella Spi-1injectisome[J].Proc Natl Acad Sci U S A,2015,112(13):4098-4103.
[11]Lefebre M D,Galán J E.The inner rod protein controls substrate switching and needle length in a Salmonella typeⅢsecretion system[J].Proc Natl Acad Sci U S A,2014,111(2):817-822.
[12]Kubori T,Sukhan A,Aizawa S I,et al.Molecular characterization and assembly of the needle complex of the Salmonella typhimuriumtypeⅢprotein secretion system[J].Proc Natl Acad Sci USA,2000,97(18):10225-10230.
[13]Rathinavelan T,Lara-Tejero M,Lefebre M,et al.NMR model of PrgI-SipD interaction and its implications in the needle-tip assembly of the SalmonellatypeⅢsecretion system[J].J Mol Biol,2014;426(16):2958-2969.
[14]Zhong D,Lefebre M,Kaur K,et al.The SalmonellatypeⅢsecretion system inner rod protein PrgJ is partially folded[J].J Biol Chem,2012,287(30):25303-25311.
[15]Rathinavelan T,Tang C,De Guzman R N.Characterization of the interaction between the SalmonellatypeⅢsecretion system tip protein SipD and the needle protein PrgI by paramagnetic relaxation enhancement[J].J Biol Chem,2011,286(6):4922-4930.
[16]Montagner C,Arquint C,Cornelis G R.Translocators YopB and YopD fromYersinia enterocoliticaform a multimeric integral membrane complex in eukaryotic cell membranes[J].J Bacteriol,2011,193(24):6923-6928.
[17]Chatterjee S,Zhong D,Nordhues B A,et al.The crystal structures of the SalmonellatypeⅢsecretion system tip protein SipD in complex with deoxycholate and chenodeoxycholate[J].Protein Sci,2011,20(1):75-86.
[18]Shen D K,Moriya N,Martinez-Argudo I,et al.Needle length control and the secretion substrate specificity switch are only loosely coupled in the typeⅢsecretion apparatus of Shigella[J].Microbiology,2012,158(7):1884-1896.
[19]Myeni S K,Wang L,Zhou D.SipB-SipC complex is essential for translocon formation[J].PLoS One,2013,8(3):e60499.
[20]Lara-Tejero M,Galán J E.Salmonella entericaserovar typhimuriumpathogenicity island 1-encoded typeⅢsecretion system translocases mediate intimate attachment to nonphagocytic cells[J].Infect Immun,2009,7(7):2635-2642.
[21]Hlzer S U,Hensel M.Functional dissection of translocon proteins of the Salmonella pathogenicity island 2-encoded typeⅢsecretion system[J].BMC Microbiol,2010,10:104.
[22]Schraidt O,Marlovits T C.Three-dimensional model of Salmonella’s needle complex at subnanometer resolution[J].Science,2011,331(6021):1192-1195.
[23]Bergeron J R,Worrall L J,De S,et al.The modular structure of the inner-membrane ring component PrgK facilitates assembly of the typeⅢsecretion system basal body[J].Structure,2015,23(1):161-172.
[24]Allison S E,Tuinema B R,Everson E S,et al.Identification of the docking site between a typeⅢsecretion system ATPase and a chaperone for effector cargo[J].J Biol Chem,2014,289(34):23734-23744.
[25]Romo-Castillo M,Andrade A,Espinosa N,et al.EscO,a functional and structural analog of the flagellar FliJ protein,is a positive regulator of EscN ATPase activity of the enteropathogenic Escherichia coli injectisome[J].J Bacteriol,2014,196(12):2227-2241.
[26]Biemans-Oldehinkel E,Sal-Man N,Deng W,et al.Quantitative proteomic analysis reveals formation of an EscL-EscQEscN typeⅢcomplex in enteropathogenic Escherichia coli[J].J Bacteriol,2011,193(19):5514-5519.
[27]Kim J S,Kim B H,Jang J I,et al.Functional insight from the tetratricopeptide repeat-like motifs of the typeⅢsecretion chaperone SicA in Salmonella enterica serovar typhimurium[J].FEMS Microbiol Lett,2014,350(2):146-153.
[28]Dehghani B,Rasooli I,Jalali-Nadoushan M,et al.Immunoprotectivity of Salmonella enterica serovar enteritidis virulence protein,InvH,against Salmonella typhi[J].Iran J Basic Med Sci,2014,17(8):560-565.
[29]Diepold A,Armitage J P.TypeⅢsecretion systems:the bacterial flagellum and the injectisome[J].Phil Trans R Soc B,2015,doi:10.1098/rstb.2015.0020.
[30]Monjarás Feria J,García-Gómez E,Espinosa N,et al.Role of EscP(Orf16)in injectisome biogenesis and regulation of typeⅢprotein secretion in enteropathogenic Escherichia coli[J].J Bacteriol,2012,194(22):6029-6045.
[31]Shibata S,Takahashi N,Chevance F F,et al.FliK regulates flagellar hook length as an internal ruler[J].Mol Microbiol,2007,64(5):1404-1415.
[32]Monjarás Feria J V,Lefebre M D,Stierhof Y D,et al.Role of autocleavage in the function of a typeⅢsecretion specificity switch protein in Salmonellaenterica serovar Typhimurium[J].MBio,2015,6(5):e01459-15.
[33]Marlovits T C,Kubori T,Lara-Tejero M,et al.Assembly of the inner rod determines needle length in the typeⅢsecretion injectisome[J].Nature,2006,441(7093):637-640.
[34]Poyraz O,Schmidt H,Seidel K,et al.Protein refolding is required for assembly of the type three secretion needle[J].Nat Struct Mol Biol,2010,17(7):788-792.
[35]Blocker A J,Deane J E,Veenendaal A K,et al.What's the point of the typeⅢsecretion system needle[J].Proc Nal Acad Sci USA,2008,105(18):6507-6513.
[36]Kubori T,Sukhan A,Aizawa SI,et al.Molecular characterization and assembly of the needle complex of the Salmonella typhimuriumtypeⅢprotein secretion system[J].Proc Natl Acad Sci USA,2000,97(18):10225-10230.
[37]Nguyen V S,Jobichen C,Tan K W,et al.Structure of AcrHAopB chaperone translocator complex reveals a role for membrane hairpins in typeⅢsecretion system translocon assembly[J].Structure,2015,23(11):2022-2031.
[38]Enninga J,Rosenshine I.Imaging the assembly,structure and activity of typeⅢsecretion systems[J].Cell Microbiol,2009,11(10):1462-1470.
[39]Abrusci P,Vergara-Irigaray M,Johnson S,et al.Architecture of the major component of the typeⅢsecretion system export apparatus[J].Nat Struct Mol Biol,2013,20(1):99-104.
[40]Figueira R,Holden D W.Functions of the Salmonella pathogenicity island 2(SPI-2)typeⅢsecretion system effectors[J].Microbiology,2012,158(Pt 5):1147-1161.
[41]Geng S,Jiao X,Barrow P,et al.Virulence determinants of Salmonella gallinarum biovar pullorum identified by PCR signature-tagged mutagenesis and the spiC mutant as a candidate live attenuated vaccine[J].Vet Microbiol,2014,168(2-4):388-394.