Advances in Salmonella pathogenicity island 2 type III secretion system-A review
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    Abstract:

    Salmonella is a Gram-negative facultative intracellular pathogen that can infect vast array of hosts and cause a series of diseases, sometimes even life-threatening systemic diseases. As an indispensable virulence determinant associated with the systemic infections, Salmonella pathogenicity island 2 (SPI2) encodes type III secretion system 2 (T3SS2) which is induced after invasion, and the T3SS2 secreted effectors are essential for Salmonella to survive and replicate inside various cell types. In recent years, this issue remains the focus of pathogenic research. This review focuses on the aspects of gene characterization of SPI2, regulation of SPI2 gene expression, the structure and assembly of T3SS2, the T3SS2 effectors and some vaccine candidates associated with T3SS2 to present the current understanding of Salmonella T3SS2.

    Reference
    [1] Yan SS, Pendrak ML, Punderson JW, Fedorko DP, Foley SL. An overview of Salmonella typing:public health perspectives. Clinical and Applied Immunology Reviews, 2004, 4(3):189-204.
    [2] Lu CP. Veterinary microbiology. 3rd ed. Beijing:China Agricultural Press, 2001:223-231. (in Chinese) 陆承平. 兽医微生物学. 第3版. 北京:中国农业出版社, 2001:223-231.
    [3] Zhang JL, Wei LJ, Kelly P, Freeman M, Jaegerson K, Gong JS, Xu B, Pan ZM, Xu CL, Wang CM. Detection of Salmonella spp. using a generic and differential FRET-PCR. PLoS One, 2013, 8(10):e76053.
    [4] Fookes M, Schroeder GN, Langridge GC, Blondel CJ, Mammina C, Connor TR, Seth-Smith H, Vernikos GS, Robinson KS, Sanders M, Petty NK, Kingsley RA, Bäumler AJ, Nuccio S, Contreras I, Santiviago CA, Maskell D, Barrow P, Humphrey T, Nastasi A, Roberts M, Frankel G, Parkhill J, Dougan C, Thomson NR. Salmonella bongori provides insights into the evolution of the Salmonellae. PLoS Pathogens, 2011, 7(8):e1002191.
    [5] Hayward MR, Jansen VAA, Woodward MJ. Comparative genomics of Salmonella enterica serovars Derby and Mbandaka, two prevalent serovars associated with different livestock species in the UK. BMC Genomics, 2013, 14:356.
    [6] Moest TP, Méresse S. Salmonella T3SSs:successful mission of the secret(ion) agents. Current Opinion in Microbiology, 2013, 16(1):38-44.
    [7] Hensel M, Hinsley AP, Nikolaus T, Sawers G, Berks BC. The genetic basis of tetrathionate respiration in Salmonella typhimurium. Molecular Microbiology, 1999, 32(2):275-288.
    [8] Hensel M, Nikolaus T, Egelseer C. Molecular and functional analysis indicates a mosaic structure of Salmonella pathogenicity island 2. Molecular Microbiology, 1999, 31(2):489-498.
    [9] Wood MW, Jones MA, Watson PR, Hedges S, Wallis TS, Galyov EE. Identification of a pathogenicity island required for Salmonella enteropathogenicity. Molecular Microbiology, 1998, 29(3):883-891.
    [10] Hueck CJ. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiology and Molecular Biology Reviews, 1998, 62(2):379-433.
    [11] Fass E, Groisman EA. Control of Salmonella pathogenicity island-2 gene expression. Current Opinion in Microbiology, 2009, 12(2):199-204.
    [12] Hansen-Wester I, Hensel M. Salmonella pathogenicity islands encoding type III secretion systems. Microbes and Infection, 2001, 3(7):549-559.
    [13] Li J, Overall CC, Nakayasu ES, Kidwai AS, Jones MB, Johnson RC, Nguyen NT, McDermott JE, Ansong C, Heffron F, Cambronne ED, Adkins JN. Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σE-regulated SPI-2 gene expression. Frontiers in Microbiology, 2015, 6:27.
    [14] Choi J, Shin D, Yoon H, Kim J, Lee CR, Kim M, Seok YJ, Ryu S. Salmonella pathogenicity island 2 expression negatively controlled by EIIANtr-SsrB interaction is required for Salmonella virulence. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(47):20506-20511.
    [15] Choi E, Kim H, Lee H, Nam D, Choi J, Shin D. The iron-sensing fur regulator controls expression timing and levels of Salmonella pathogenicity island 2 genes in the course of environmental acidification. Infection and Immunity, 2014, 82(6):2203-2210.
    [16] Wang LC, Morgan LK, Godakumbura P, Kenney LJ, Anand GS. The inner membrane histidine kinase EnvZ senses osmolality via helix-coil transitions in the cytoplasm. The EMBO Journal, 2012, 31(11):2648-2659.
    [17] Chakraborty S, Mizusaki H, Kenney LJ. A FRET-based DNA biosensor tracks OmpR-dependent acidification of Salmonella during macrophage infection. PLoS Biology, 2015, 13(4):e1002116.
    [18] Bustamante VH, Martinez LC, Santana FJ, Knodler LA, Steele-Mortimer O, Puente JL. HilD-mediated transcriptional cross-talk between SPI-1 and SPI-2. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(38):14591-14596.
    [19] Martínez LC, Banda MM, Fernández-Mora M, Santana FJ, Bustamante VH. HilD induces expression of Salmonella pathogenicity island 2 genes by displacing the global negative regulator H-NS from ssrAB. Journal of Bacteriology, 2014, 196(21):3746-3755.
    [20] Bijlsma JJE, Groisman EA. The PhoP/PhoQ system controls the intramacrophage type three secretion system of Salmonella enterica. Molecular Microbiology, 2005, 57(1):85-96.
    [21] Steele-Mortimer O. The Salmonella-containing vacuole:moving with the times. Current Opinion in Microbiology, 2008, 11(1):38-45.
    [22] Ramos-Morales F. Impact of Salmonella enterica type III secretion system effectors on the eukaryotic host cell. ISRN Cell Biology, 2012, 2012:Article ID 787934.
    [23] Lefebre MD, Galán JE. The inner rod protein controls substrate switching and needle length in a Salmonella type III secretion system. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(2):817-82
    [24] Cooper CA, Zhang K, Andres SN, Fang Y, Kaniuk NA, Hannemann M, Brumell JH, Foster LJ, Junop MS, Coombes BK. Structural and biochemical characterization of SrcA, a multi-cargo type III secretion chaperone in Salmonella required for pathogenic association with a host. PLoS Pathogens, 2010, 6(2):e1000751.
    [25] Cooper CA, Mulder DT, Allison SE, Pilar AV, Coombes BK. The SseC translocon component in Salmonella enterica serovar Typhimurium is chaperoned by SscA. BMC Microbiology, 2013, 13:221.
    [26] Dai SP, Zhou DG. Secretion and function of Salmonella SPI-2 effector SseF require its chaperone, SscB. Journal of Bacteriology, 2004, 186(15):5078-5086.
    [27] Ruiz-Albert J, Mundy R, Yu XJ, Beuzón CR, Holden DW. SseA is a chaperone for the SseB and SseD translocon components of the Salmonella pathogenicity-island-2-encoded type III secretion system. Microbiology, 2003, 149(Pt5):1103-1111.
    [28] Yu XJ, McGourty K, Liu M, Unsworth KE, Holden DW. pH sensing by intracellular Salmonella induces effector translocation. Science, 2010, 328(5981):1040-1043.
    [29] Yoshida Y, Miki T, Ono S, Haneda T, Ito M, Okada N. Functional characterization of the type III secretion ATPase SsaN encoded by Salmonella pathogenicity island 2. PLoS One, 2014, 9(4):e94347.
    [30] Figueira R, Holden DW. Functions of the Salmonella pathogenicity island 2 (SPI-2) type III secretion system effectors. Microbiology, 2012, 158(Pt5):1147-1161.
    [31] Habyarimana F, Sabag-Daigle A, Ahmer BMM. The SdiA-regulated gene srgE encodes a type III secreted effector. Journal of Bacteriology, 2014, 196(12):2301-2312.
    [32] Langridge GC, Fookes M, Connor TR, Feltwell T, Feasey N, Parsons BN, Seth-Smith HMB, Barquist L, Stedman A, Humphrey T, Wigley P, Peters SE, Maskell DJ, Corander J, Chabalgoity JA, Barrow P, Parkhill J, Dougan G, Thomson NR. Patterns of genome evolution that have accompanied host adaptation in Salmonella. Proceedings of the National Academy of Sciences of the Unton TC, Goudet A, Sergeant R, Maillere B, Pollard AJ, Altmann DM, Boyton RJ. The serodominant secreted effector protein of Salmonella, SseB, is a strong CD4 antigen containing an immunodominant epitope presented by diverse HLA class II alleles. Immunology, 2014, 143(3):438-446.XA, Tang LH, Pan ZM, Yin YL. Construction and characterization of Salmonella typhimurium SL7207 SifA- mutant strain. Acta Microbiologica Sinica, 2005, 45(3):349-354. (in Chinese) 张晓明, 焦新安, 唐丽华, 潘志明, 殷月兰. 鼠伤寒沙门氏菌SL7207 SifA-突变株的构建和鉴定. 微生物学报, 2005, 45(3):349-354.
    [35] Yin JL, Xu LJ, Wang ZP, Lin ZJ, Li QC, Geng SZ, Jiao XA. Construction of a Salmonella pullorum S06004ΔsifA strain and study on its biological characteristics. Chinese Veterinary Science, 2015, 45(4):345-351. (in Chinese) 殷俊磊, 徐黎娟, 王志鹏, 蔺志杰, 李求春, 耿士忠, 焦新安. 鸡白痢沙门菌sifA基因缺失株的构建及其生物学特性的研究. 中国兽医科学, 2015, 45(4):345-351.
    [36] Uchiya KI, Barbieri MA, Funato K, Shah AH, Stahl PD, Groisman EA. A Salmonella virulence protein that inhibits cellular trafficking. The EMBO Journal, 1999, 18(14):3924-3933.
    [37] Geng SZ, Jiao X, Barrow P, Pan ZM, Chen X. Virulence determinants of Salmonella gallinarum biovar pullorum identified by PCR signature-tagged mutagenesis and the spiC mutant as a candidate live attenuated vaccine. Veterniary Microbiology, 2014, 168(2/4):388-394.
    [38] Kidwai AS, Mushamiri I, Niemann GS, Brown RN, Adkins JN, Heffron F. Diverse secreted effectors are required for Salmonella persistence in a mouse infection model. PLoS One, 2013, 8(8):e70753.
    [39] Tsolis RM, Adams LG, Ficht TA, Bäumler AJ. Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infection and Immunity, 1999, 67(9):4879-4885.
    [40] Matulova M, Havlickova H, Sisak F, Rychlik I. Vaccination of chickens with Salmonella pathogenicity island (SPI) 1 and SPI2 defective mutants of Salmonella enterica serovar Enteritidis. Vaccine, 2012, 30(12):2090-2097.
    [41] Khan SA, Stratford R, Wu T, McKelvie N, Bellaby T, Hindle Z, Sinha KA, Eltze S, Mastroeni P, Pickard D, Dougan G, Chatfield SN, Brennan FR. Salmonella typhi and S. typhimurium derivatives harbouring deletions in aromatic biosynthesis and Salmonella pathogenicity island-2 (SPI-2) genes as vaccines and vectors. Vaccine, 2003, 21(5/6):538-548.
    [42] Yin JL, Cheng Z, Wang XC, Xu LJ, Li QC, Geng SZ, Jiao X. Evaluation of Salmonella enterica serovar pullorum pathogenicity island 2 mutant as a candidate live attenuated oral vaccine. Clinical and Vaccine Immunology, 2015, 22(7):706-710.
    [43] Xiong GS, Husseiny MI, Song LP, Erdreich-Epstein A, Shackleford GM, Seeger RC, Jäckel D, Hensel M, Metelitsa LS. Novel cancer vaccine based on genes of Salmonella pathogenicity island 2. International Journal of Cancer, 2010, 126(11):2622-2634.
    [44] Xu X, Hegazy WAH, Guo LJ, Gao XH, Courtney AN, Kurbanov S, Liu DF, Tian GW, Manuel ER, Diamond DJ, Hensel M, Metelitsa LS. Effective cancer vaccine platform based on attenuated Salmonella and a type III secretion system. Cancer Research, 2014, 74(21):6260-6270.
    [45] Husseiny MI, Rawson J, Kaye A, Nair I, Todorov I, Hensel M, Kandeel F, Ferreri K. An oral vaccine for type 1 diabetes based on live attenuated Salmonella. Vaccine, 2014, 32(20):2300-2307.
    [46] Panthel K, Meinel KM, Domènech VES, Retzbach H, Igwe EI, Hardt WD, Rüssmann H. Salmonella pathogenicity island 2-mediated overexpression of chimeric SspH2 proteins for simultaneous induction of antigen-specific CD4 and CD8 T cells. Infection and Immunity, 2005, 73(1):334-341.
    [47] Hegazy WAH, Xu X, Metelitsa L, Hensel M. Evaluation of Salmonella enterica type III secretion system effector proteins as carriers for heterologous vaccine antigens. Infection and Immunity, 2012, 80(3):1193-1202.
    [48] Wisner AL, Desin TS, Lam PK, Berberov E, Mickael CS, Townsend HG, Potter AA, Köster W. Immunization of chickens with Salmonella enterica subspecies enterica serovar enteritidis pathogenicity island-2 proteins. Veterniary Microbiology, 2011, 153(3/4):274-284.
    [49] Reynolds CJ, Jones C, Blohmke CJ, Dar
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Junlei Yin, Qiuchun Li, Xin'an Jiao. Advances in Salmonella pathogenicity island 2 type III secretion system-A review. [J]. Acta Microbiologica Sinica, 2016, 56(4): 561-569

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History
  • Received:June 11,2015
  • Revised:August 21,2015
  • Online: March 30,2016
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