1887

Abstract

is a Gram-negative enteric bacterium affecting both animals and humans. Recently, a type III secretion system (TTSS) was found in . Such systems are generally used by bacterial pathogens to deliver virulence factors into host cells to subvert normal cell functions. Genome-walking was performed from the and genes (homologues of and , respectively) identified in previous studies, to determine the sequences of the TTSS. Thirty-five ORFs were identified which encode the TTSS apparatus, chaperones, effectors and regulators. Mutants affected in genes representing each category were generated and found to have decreased survival and growth in fish phagocytes. LD values of the mutants were increased by at least 10-fold in comparison to those of the wild-type strain. The adherence and invasion rates of the and mutants were enhanced while those of the other mutants remained similar to the wild-type. The and mutants showed slight autoaggregation in Dulbecco's Modified Eagle Medium, whereas the rest of the mutants failed to autoaggregate. Regulation of the TTSS was found to involve the two-component regulatory system . This study showed that the TTSS is important for pathogenesis. An understanding of this system will provide greater insight into the virulence mechanisms of this bacterial pathogen.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28005-0
2005-07-01
2019-08-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/7/mic1512301.html?itemId=/content/journal/micro/10.1099/mic.0.28005-0&mimeType=html&fmt=ahah

References

  1. Alves de Brito, C. F., Carvalho, C. M. B., Santos, F. R., Gazzinelli, R. T., Oliveira, S. C., Azevedo, V. & Teixeira, S. M. R. ( 2004; ). Chromobacterium violaceum genome: molecular mechanisms associated with pathogenicity. Genet Mol Res 3, 148–161.
    [Google Scholar]
  2. Betts, H. J., Chaudhuri, R. R. & Pallen, M. J. ( 2004; ). An analysis of type-III secretion gene clusters in Chromobacterium violaceum. Trends Microbiol 12, 476–482.[CrossRef]
    [Google Scholar]
  3. Beuzon, C. R., Meresse, S., Unsworth, K. E., Ruiz-Albert, J., Garvis, S., Waterman, S. R., Ryder, T. A., Boucrot, E. & Holden, D. W. ( 2000; ). Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 19, 3235–3249. Erratum in EMBO J 19, 4191.
    [Google Scholar]
  4. Blum, H., Beier, H. & Gross, H. J. ( 1987; ). Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8, 93–99.[CrossRef]
    [Google Scholar]
  5. Brazilian National Genome Project Consortium ( 2003; ). The complete genome sequence of Chromobacterium violaceum reveals remarkable and exploitable bacterial adaptability. Proc Natl Acad Sci U S A 100, 11660–11665.[CrossRef]
    [Google Scholar]
  6. Brosius, J. & Holy, A. ( 1984; ). Regulation of ribosomal RNA promoters with a synthetic lac operator. Proc Natl Acad Sci U S A 81, 6929–6933.[CrossRef]
    [Google Scholar]
  7. Brumell, J. H., Kujat-Choy, S., Brown, N. F., Vallance, B. A., Knodler, L. A. & Finlay, B. B. ( 2003; ). SopD2 is a novel type III secreted effector of Salmonella typhimurium that targets late endocytic compartments upon delivery into host cells. Traffic 4, 36–48.[CrossRef]
    [Google Scholar]
  8. Chen, J. D., Lai, S. Y. & Huang, S. L. ( 1996; ). Molecular cloning, characterization, and sequencing of the hemolysin gene from Edwardsiella tarda. Arch Microbiol 165, 9–17.[CrossRef]
    [Google Scholar]
  9. Cirillo, D. M., Valdivia, R. H., Monack, D. M. & Falkow, S. ( 1998; ). Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol Microbiol 30, 175–188.[CrossRef]
    [Google Scholar]
  10. Cook, R. A. & Tappe, J. P. ( 1985; ). Chronic enteritis associated with Edwardsiella tarda infection in Rockhopper penguins. J Am Vet Med Assoc 187, 1219–1220.
    [Google Scholar]
  11. Creasey, E. A., Friedberg, D., Shaw, R. K., Umanski, T., Knutton, S., Rosenshine, I. & Frankel, G. ( 2003; ). CesAB is an enteropathogenic Escherichia coli chaperone for the type-III translocator proteins EspA and EspB. Microbiology 149, 3639–3647.[CrossRef]
    [Google Scholar]
  12. Datta, P., Goss, T. J., Omnaas, J. R. & Patil, R. V. ( 1987; ). Covalent structure of biodegradative threonine dehydratase of Escherichia coli: homology with other dehydratases. Proc Natl Acad Sci U S A 84, 393–397.[CrossRef]
    [Google Scholar]
  13. Deiwick, J., Nikolaus, T., Shea, J. E., Gleeson, C., Holden, D. & Hensel, M. ( 1998; ). Mutations in Salmonella pathogenicity island 2 (SPI2) genes affecting transcription of SPI1 genes and resistance to antimicrobial agents. J Bacteriol 180, 4775–4780.
    [Google Scholar]
  14. Deiwick, J., Nikolaus, T., Erdogan, S. & Hensel, M. ( 1999; ). Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol Microbiol 31, 1759–1773.[CrossRef]
    [Google Scholar]
  15. Deng, W., Puente, J. L., Gruenheid, S. & 12 other authors ( 2004; ). Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci U S A 101, 3597–3602.[CrossRef]
    [Google Scholar]
  16. Dobrindt, U., Blum-Oehler, G., Nagy, G., Schneider, G., Johann, A., Gottschalk, G. & Hacker, J. ( 2002; ). Genetic structure and distribution of four pathogenicity islands (PAI I(536) to PAI IV(536)) of uropathogenic Escherichia coli strain 536. Infect Immun 70, 6365–6372.[CrossRef]
    [Google Scholar]
  17. Edelman, S., Leskela, S., Ron, E., Apajalahti, J. & Korhonen, T. K. ( 2003; ). In vitro adhesion of an avian pathogenic Escherichia coli O78 strain to surfaces of the chicken intestinal tract and to ileal mucus. Vet Microbiol 91, 41–56.[CrossRef]
    [Google Scholar]
  18. Edwards, R. A., Keller, L. H. & Schifferli, D. M. ( 1998; ). Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene 207, 149–157.[CrossRef]
    [Google Scholar]
  19. Elliott, S. J., Wainwright, L. A., McDaniel, T. K., Jarvis, K. G., Deng, Y. K., Lai, L.-C., McNamara, B. P., Donnenberg, M. S. & Kaper, J. B. ( 1998; ). The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol Microbiol 28, 1–4.
    [Google Scholar]
  20. Elliott, S. J., Krejany, E. O., Mellies, J. L., Robins-Browne, R. M., Sasakawa, C. & Kaper, J. B. ( 2001; ). EspG, a novel type III system-secreted protein from enteropathogenic Escherichia coli with similarities to VirA of Shigella flexneri. Infect Immun 69, 4027–4033.[CrossRef]
    [Google Scholar]
  21. Elsinghorst, E. A. ( 1994; ). Measurement of invasion by gentamicin resistance. Methods Enzymol 236, 405–420.
    [Google Scholar]
  22. Farmer, J. J., III & McWhorter, A. C. ( 1984; ). Genus X. Edwardsiella Ewing and McWhorter 1965, 37AL. In Bergey's Manual of Systemic Bacteriology, vol. 1, pp. 486–491. Edited by N. R. Krieg. Baltimore: Williams & Wilkins.
  23. Galan, J. E. ( 1996; ). Molecular genetic bases of Salmonella entry into host cells. Mol Microbiol 20, 263–271.[CrossRef]
    [Google Scholar]
  24. Galan, J. E. & Curtiss, R., III ( 1989; ). Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci U S A 86, 6383–6387.[CrossRef]
    [Google Scholar]
  25. Gallegos, M.-T., Schleif, R., Bairoch, A., Hofmann, K. & Ramos, J. L. ( 1997; ). AraC/XylS family of transcriptional regulators. Microbiol Mol Biol Rev 61, 393–410.
    [Google Scholar]
  26. Ganduri, Y. L., Sadda, S. R., Datta, M. W., Jambukeswaran, R. K. & Datta, P. ( 1993; ). TdcA, a transcriptional activator of the tdcABC operon of Escherichia coli, is a member of the LysR family of proteins. Mol Gen Genet 240, 395–402.
    [Google Scholar]
  27. Garcia Vescovi, E., Soncini, F. C. & Groisman, E. A. ( 1996; ). Mg2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84, 165–174.[CrossRef]
    [Google Scholar]
  28. Goldstein, E. J. C., Agyare, E. O., Vagvolgi, A. E. & Halpern, M. ( 1981; ). Aerobic bacterial oral flora of garter snakes: development of normal flora and pathogenic potential for snakes and humans. J Clin Microbiol 13, 954–956.
    [Google Scholar]
  29. Goss, T. J., Schweizer, H. P. & Datta, P. ( 1988; ). Molecular characterization of the tdc operon of Escherichia coli K-12. J Bacteriol 170, 5352–5359.
    [Google Scholar]
  30. Hacker, J., Blum-Oehler, G., Mühldorfer, I. & Tschäpe, H. ( 1997; ). Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol 23, 1089–1097.[CrossRef]
    [Google Scholar]
  31. Hanahan, D. ( 1983; ). Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166, 557–580.[CrossRef]
    [Google Scholar]
  32. Hensel, M. ( 2000; ). Salmonella pathogenicity island 2. Mol Microbiol 36, 1015–1023.[CrossRef]
    [Google Scholar]
  33. Hensel, M., Shea, J. E., Baumler, A. J., Gleeson, C., Blattner, F. & Holden, D. W. ( 1997; ). Analysis of the boundaries of Salmonella pathogenicity island 2 and the corresponding chromosomal region of Escherichia coli K-12. J Bacteriol 179, 1105–1111.
    [Google Scholar]
  34. Hensel, M., Shea, J. E., Waterman, S. R. & 7 other authors ( 1998; ). Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol Microbiol 30, 163–174.[CrossRef]
    [Google Scholar]
  35. Hensel, M., Nikolaus, T. & Egelseer, C. ( 1999; ). Molecular and functional analysis indicates a mosaic structure of Salmonella pathogenicity island 2. Mol Microbiol 31, 489–498.[CrossRef]
    [Google Scholar]
  36. Hirono, I., Tange, N. & Aoki, T. ( 1997; ). Iron-regulated haemolysin gene from Edwardsiella tarda. Mol Microbiol 24, 851–856.[CrossRef]
    [Google Scholar]
  37. Hueck, C. J. ( 1998; ). Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62, 379–433.
    [Google Scholar]
  38. Janda, J. M. & Abbott, S. L. ( 1993a; ). Infections associated with the genus Edwardsiella: the role of Edwardsiella tarda in human disease. Clin Infect Dis 17, 742–748.[CrossRef]
    [Google Scholar]
  39. Janda, J. M. & Abbott, S. L. ( 1993b; ). Expression of an iron-regulated hemolysin from Edwardsiella tarda. FEMS Microbiol Lett 111, 275–280.[CrossRef]
    [Google Scholar]
  40. Janda, J. M., Abbott, S. L. & Oshiro, L. S. ( 1991; ). Penetration and replication of Edwardsiella spp. in HEp-2 cells. Infect Immun 59, 154–161.
    [Google Scholar]
  41. Jepson, M. A., Pellegrin, S., Peto, L., Banbury, D. N., Leard, A. D., Mellor, H. & Kenny, B. ( 2003; ). Synergistic roles for the Map and Tir effector molecules in mediating uptake of enteropathogenic Escherichia coli (EPEC) into non-phagocytic cells. Cell Microbiol 5, 773–783.[CrossRef]
    [Google Scholar]
  42. Kanack, K., Crawford, J. A., Karmali, M. A. & Kaper, J. B. ( 2004; ). SepZ, a novel enteropathogenic Escherichia coli type III system secreted and translocated protein mutation does not delay secretion of EspA/B or translocation of Tir. In American Society for Microbiology 104th General Meeting, May 23–27 2004, abstract B-085. Washington, DC: American Society for Microbiology.
  43. Knutton, S., Rosenshine, I., Pallen, M. J., Nisan, I., Neves, B. C., Bain, C., Wolff, C., Dougan, G. & Frankel, G. ( 1998; ). A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J 17, 2166–2176.[CrossRef]
    [Google Scholar]
  44. Kourany, M., Vasquez, M. & Saenz, R. ( 1977; ). Edwardsiellosis in man and animals in Panama: clinical and epidemiological characteristics. Am J Trop Med Hyg 26, 1183–1190.
    [Google Scholar]
  45. Kresse, A. U., Rohde, M. & Guzman, C. A. ( 1999; ). The EspD protein of enterohemorrhagic Escherichia coli is required for the formation of bacterial surface appendages and is incorporated in the cytoplasmic membranes of target cells. Infect Immun 67, 4834–4842.
    [Google Scholar]
  46. Leung, K. Y. & Stevenson, R. M. W. ( 1988; ). Characteristics and distribution of extracellular proteases from Aeromonas hydrophila. J Gen Microbiol 134, 151–160.
    [Google Scholar]
  47. Ling, S. H. M., Wang, X. H., Xie, L., Lim, T. M. & Leung, K. Y. ( 2000; ). Use of green fluorescent protein (GFP) to track the invasion pathways of Edwardsiella tarda in in vivo and in vitro fish models. Microbiology 146, 7–19.
    [Google Scholar]
  48. Maynes, J. T., Yuan, R. G. & Snyder, F. F. ( 2000; ). Identification, expression, and characterization of Escherichia coli guanine deaminase. J Bacteriol 182, 4658–4660.[CrossRef]
    [Google Scholar]
  49. Miller, V. L. & Mekalanos, J. J. ( 1988; ). A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170, 2575–2583.
    [Google Scholar]
  50. Neves, M. S., Nunes, M. P. & Milhomem, A. M. ( 1994; ). Aeromonas species exhibit aggregative adherence to HEp-2 cells. J Clin Microbiol 32, 1130–1131.
    [Google Scholar]
  51. Ng, V. H., Cox, J. S., Sousa, A. O., MacMicking, J. D. & Mckinney, J. D. ( 2004; ). Role of KatG catalase–peroxidase in mycobacterial pathogenesis: countering the phagocyte oxidative burst. Mol Microbiol 52, 1291–1302.[CrossRef]
    [Google Scholar]
  52. Nougayrede, J. P. & Donnenberg, M. S. ( 2004; ). Enteropathogenic Escherichia coli EspF is targeted to mitochondria and is required to initiate the mitochondrial death pathway. Cell Microbiol 6, 1097–1111.[CrossRef]
    [Google Scholar]
  53. Ochman, H., Soncini, F. C., Solomon, F. & Groisman, E. A. ( 1996; ). Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci U S A 93, 7800–7804.[CrossRef]
    [Google Scholar]
  54. O'Connell, C. B., Creasey, E. A., Knutton, S. & 7 other authors ( 2004; ). SepL, a protein required for enteropathogenic Escherichia coli type III translocation, interacts with secretion component SepD. Mol Microbiol 52, 1613–1625.[CrossRef]
    [Google Scholar]
  55. Pallen, M. J., Beatson, S. A. & Bailey, C. M. ( 2005; ). Bioinformatics analysis of the locus for enterocyte effacement provides novel insights into type III secretion. BMC Microbiol 5, 9. doi:10.1186/1471-2180-5-9.
    [Google Scholar]
  56. Phillips, A. D., Trabulsi, L. R., Dougan, G. & Frankel, G. ( 1998; ). Edwardsiella tarda induces plasma membrane ruffles on infection of HEp-2 cells. FEMS Microbiol Lett 161, 317–323.[CrossRef]
    [Google Scholar]
  57. Pratt, L. A. & Silhavy, T. J. ( 1995; ). Porin regulation of Escherichia coli. In Two-Component Signal Transduction, pp. 105–127. Edited by J. A. Hoch & T. J. Silhavy. Washington, DC: American Society for Microbiology.
  58. Pym, A. S., Saint-Joanis, B. & Cole, S. T. ( 2002; ). Effect of katG mutations on the virulence of Mycobacterium tuberculosis and the implication for transmission in humans. Infect Immun 70, 4955–4960.[CrossRef]
    [Google Scholar]
  59. Reed, L. J. & Muench, H. ( 1938; ). A simple method of estimating fifty percent end points. Am J Hyg 27, 493–497.
    [Google Scholar]
  60. Roine, E., Wei, W., Yuan, J., Nurmiaho-Lassila, E. L., Kalkkinen, N., Romantschuk, M. & He, S. Y. ( 1997; ). Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A 94, 3459–3464.[CrossRef]
    [Google Scholar]
  61. Rubires, X., Saigi, F., Pique, N., Climent, N., Merino, S., Alberti, S., Tomas, J. M. & Regue, M. ( 1997; ). A gene (wbbL) from Serratia marcescens N28b(O4) complements the rfb-50 mutation of Escherichia coli K-12 derivatives. J Bacteriol 179, 7581–7586.
    [Google Scholar]
  62. Ruiz-Albert, J., Mundy, R., Yu, X. J., Beuzon, C. R. & Holden, D. W. ( 2003; ). SseA is a chaperone for the SseB and SseD translocon components of the Salmonella pathogenicity-island-2-encoded type III secretion system. Microbiology 149, 1103–1111.[CrossRef]
    [Google Scholar]
  63. Sae-Oui, D., Muroga, K. & Nakai, T. ( 1984; ). A case of Edwardsiella tarda infection in cultured colored carp Cyprinus carpio. Fish Pathol 19, 197–199.[CrossRef]
    [Google Scholar]
  64. Sambrook, J. & Russell, D. W. ( 2000; ). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  65. Schellhorn, H. E. ( 1995; ). Regulation of hydroperoxidase (catalase) expression in Escherichia coli. FEMS Microbiol Lett 131, 113–119.[CrossRef]
    [Google Scholar]
  66. Schellhorn, H. E. & Hassan, H. M. ( 1988; ). Response of hydroperoxidase and superoxide dismutase deficient mutants of Escherichia coli K-12 to oxidative stress. Can J Microbiol 34, 1171–1176.[CrossRef]
    [Google Scholar]
  67. Secombs, C. J. ( 1990; ). Isolation of salmonid macrophages and analysis of their killing activity. In Techniques in Fish Immunology, pp. 137–154. Edited by J. S. Stolen, T. C. Fletcher, D. P. Anderson, B. S. Roberson & W. B. Van Muiswinkel. Fair Haven, NJ: SOS Publications.
  68. Shea, J. E., Hensel, M., Gleeson, C. & Holden, D. W. ( 1996; ). Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci U S A 93, 2593–2597.[CrossRef]
    [Google Scholar]
  69. Srinivasa Rao, P. S., Lim, T. M. & Leung, K. Y. ( 2001; ). Opsonized virulent Edwardsiella tarda strains are able to adhere to and survive and replicate within fish phagocytes but fail to stimulate reactive oxygen intermediates. Infect Immun 69, 5689–5697.[CrossRef]
    [Google Scholar]
  70. Srinivasa Rao, P. S., Lim, T. M. & Leung, K. Y. ( 2003a; ). Functional genomics approach to the identification of virulence genes involved in Edwardsiella tarda pathogenesis. Infect Immun 71, 1343–1351.[CrossRef]
    [Google Scholar]
  71. Srinivasa Rao, P. S., Yamada, Y. & Leung, K. Y. ( 2003b; ). A major catalase (KatB) that is required for resistance to H2O2 and phagocyte-mediated killing in Edwardsiella tarda. Microbiology 149, 2635–2644.[CrossRef]
    [Google Scholar]
  72. Srinivasa Rao, P. S., Yamada, Y., Tan, Y. P. & Leung, K. Y. ( 2004; ). Use of proteomics to identify novel virulence determinants that are required for Edwardsiella tarda pathogenesis. Mol Microbiol 53, 573–586.[CrossRef]
    [Google Scholar]
  73. Strauss, E. J., Ghori, N. & Falkow, S. ( 1997; ). An Edwardsiella tarda strain containing a mutation in a gene with homology to shlB and hpmB is defective for entry into epithelial cells in culture. Infect Immun 65, 3924–3932.
    [Google Scholar]
  74. Sumantran, V. N., Schweizer, H. P. & Datta, P. ( 1990; ). A novel membrane-associated threonine permease encoded by the tdcC gene of Escherichia coli. J Bacteriol 172, 4288–4294.
    [Google Scholar]
  75. Tan, Y. P., Lin, Q., Wang, X. H., Joshi, S., Hew, C. L. & Leung, K. Y. ( 2002; ). Comparative proteomic analysis of extracellular proteins of Edwardsiella tarda. Infect Immun 70, 6475–6480.[CrossRef]
    [Google Scholar]
  76. Tardy, F., Homble, F., Neyt, C., Wattiez, R., Cornelis, G. R., Ruysschaert, J. M. & Cabiaux, V. ( 1999; ). Yersinia enterocolitica type III secretion-translocation system: channel formation by secreted Yops. EMBO J 18, 6793–6799.[CrossRef]
    [Google Scholar]
  77. Ti, T. Y., Tan, W. C., Chong, A. P. & Lee, E. H. ( 1993; ). Nonfatal and fatal infections caused by Chromobacterium violaceum. Clin Infect Dis 17, 505–507.[CrossRef]
    [Google Scholar]
  78. Tu, X., Nisan, I., Yona, C., Hanski, E. & Rosenshine, I. ( 2003; ). EspH, a new cytoskeleton-modulating effector of enterohaemorrhagic and enteropathogenic Escherichia coli. Mol Microbiol 47, 595–606.[CrossRef]
    [Google Scholar]
  79. Uchiya, K., Barbieri, M. A., Funato, K., Shah, A. H., Stahl, P. D. & Groisman, E. A. ( 1999; ). A Salmonella virulence protein that inhibits cellular trafficking. EMBO J 18, 3924–3933.[CrossRef]
    [Google Scholar]
  80. Wachter, C., Beinke, C., Mattes, M. & Schmidt, M. A. ( 1999; ). Insertion of EspD into epithelial target cell membranes by infecting enteropathogenic Escherichia coli. Mol Microbiol 31, 1695–1707.[CrossRef]
    [Google Scholar]
  81. Wainwright, L. A. & Kaper, J. B. ( 1998; ). EspB and EspD require a specific chaperone for proper secretion from enteropathogenic E. coli. Mol Microbiol 27, 1247–1260.[CrossRef]
    [Google Scholar]
  82. Wang, X. H., Oon, H. L., Ho, G. W. P., Wong, W. S. F., Lim, T. M. & Leung, K. Y. ( 1998; ). Internalisation and cytotoxicity are important virulence mechanisms in Vibrio–fish epithelial cell interactions. Microbiology 144, 2987–3002.[CrossRef]
    [Google Scholar]
  83. Wattiau, P. & Cornelis, G. R. ( 1994; ). Identification of DNA sequences recognized by VirF, the transcriptional activator of the Yersinia yop regulon. J Bacteriol 176, 3878–3884.
    [Google Scholar]
  84. Wolf, K. & Mann, J. A. ( 1980; ). Poikilotherm vertebrate cell lines and viruses, a current listing for fishes. In Vitro 16, 168–179.[CrossRef]
    [Google Scholar]
  85. Zheng, J., Tung, S. L. & Leung, K. Y. ( 2005; ). Regulation of a type III and a putative secretion system (EVP) in Edwardsiella tarda by EsrC is under the control of a two-component system EsrA-EsrB. Infect Immun 73 (in press)
    [Google Scholar]
  86. Zurawski, D. V. & Stein, M. A. ( 2003; ). SseA acts as the chaperone for the SseB component of the Salmonella Pathogenicity Island 2 translocon. Mol Microbiol 47, 1341–1351.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28005-0
Loading
/content/journal/micro/10.1099/mic.0.28005-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error