1887

Abstract

pathogenicity island (SPI)-1 is essential for invasion of non-phagocytic cells, whereas SPI-2 is required for intracellular survival and proliferation in phagocytes. Some SPI-1 effectors, however, are induced upon invasion of both phagocytic and non-phagocytic cells, suggesting that they may also be required post-invasion. In the present work, the presence was analysed of SipA, SopA, SopB, SopD and SopE2 effector proteins of serovar Typhimurium and during murine salmonellosis. Tagged (3×FLAG) strains of serovar Typhimurium were inoculated intraperitoneally or intragastrically to BALB/c mice and recovered from the spleen and mesenteric lymph nodes of moribund mice. Tagged proteins were detected by SDS-PAGE and immunoblotting with anti-FLAG antibodies. experiments showed that SPI-1 effector proteins SipA, SopA, SopB, SopD and SopE2 were secreted under SPI-1 conditions. Interestingly, it was found that serovar Typhimurium continued to synthesize SipA, SopB, SopD and SopE2 in colonized organs for several days, regardless of the route of inoculation. Together, these results indicate that SPI-1 effector proteins may participate in the late stages of infection in mice.

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2007-04-01
2024-03-28
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References

  1. Bajaj V., Lucas R. L., Hwang C., Lee C. A. 1996; Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol Microbiol 22:703–714 [CrossRef]
    [Google Scholar]
  2. Ben-Barak Z., Streckel W., Yaron S., Cohen S., Prager R., Tschape H. 2006; The expression of the virulence-associated effector protein gene avrA is dependent on a Salmonella enterica -specific regulatory function. Int J Med Microbiol 296:25–38
    [Google Scholar]
  3. Brown N. F., Vallance B. A., Coombes B. K., Valdez Y., Coburn B. A., Finlay B. B. 2005; Salmonella pathogenicity island 2 is expressed prior to penetrating the intestine. PLoS Pathog 1:252–258
    [Google Scholar]
  4. 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]
  5. Buchwald G., Friebel A., Galan J. E., Hardt W. D., Wittinghofer A., Scheffzek K. 2002; Structural basis for the reversible activation of a Rho protein by the bacterial toxin SopE. EMBO J 21:3286–3295 [CrossRef]
    [Google Scholar]
  6. Cherayil B. J., McCormick B. A., Bosley J. 2000; Salmonella enterica serovar Typhimurium-dependent regulation of iNOS expression in macrophages by invasins SipB, SipC, and SipD, and effector SopE2. Infect Immun 68:5567–5574 [CrossRef]
    [Google Scholar]
  7. Clark M. A., Jepson M. A., Simmons N. L., Hirst B. H. 1994; Preferential interaction of Salmonella typhimurium with mouse Peyer's patch M cells. Res Microbiol 145:543–552 [CrossRef]
    [Google Scholar]
  8. Coburn B., Li Y., Owen D., Vallance B. A., Finlay B. B. 2005; Salmonella enterica serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis. Infect Immun 73:3219–3227 [CrossRef]
    [Google Scholar]
  9. Collier-Hyams L. S., Zeng H., Sun J., Tomlinson A. D., Bao Z. Q., Chen H., Madara J. L., Orth K., Neish A. S. 2002; Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappa B pathway. J Immunol 169:2846–2850 [CrossRef]
    [Google Scholar]
  10. Dominguez-Bernal G., Pucciarelli M. G., Ramos-Morales F., Garcia-Quintanilla M., Cano D. A., Casadesus J., Garcia-del Portillo F. 2004; Repression of the RcsC-YojN-RcsB phosphorelay by the IgaA protein is a requisite for Salmonella virulence. Mol Microbiol 53:1437–1449 [CrossRef]
    [Google Scholar]
  11. Drecktrah D., Knodler L. A., Galbraith K., Steele-Mortimer O. 2005; The Salmonella SPI1 effector SopB stimulates nitric oxide production long after invasion. Cell Microbiol 7:105–113
    [Google Scholar]
  12. Galan J. E. 2001; Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol 17:53–86 [CrossRef]
    [Google Scholar]
  13. Galan J. E., Curtiss R. III 1989; Cloning and molecular characterization of genes whose products allowed Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci U S A 86:6383–6387 [CrossRef]
    [Google Scholar]
  14. Huang F.-C., Werne A., Li Q., Galyov E. E., Walker W. A., Cherayil B. J. 2004; Cooperative interactions between flagellin and SopE2 in the epithelial interleukin-8 response to Salmonella enterica . Infect Immun 72:5052–5062 [CrossRef]
    [Google Scholar]
  15. Jiang X., Rossanese O. W., Brown N. F., Kujat-Choy S., Galan J. E., Finlay B. B., Brumell J. H. 2004; The related effector proteins SopD and SopD2 from Salmonella enterica serovar Typhimurium contribute to virulence during systemic infection of mice. Mol Microbiol 54:1186–1198 [CrossRef]
    [Google Scholar]
  16. Jones B. D., Ghori N., Falkow S. 1994; Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med 180:15–23 [CrossRef]
    [Google Scholar]
  17. Jones M. A., Wood M. W., Mullan P. B., Watson P. R., Wallis T. S., Galyov E. E. 1998; Secreted effector proteins of Salmonella dublin act in concert to induce enteritis. Infect Immun 66:5799–5804
    [Google Scholar]
  18. Kubori T., Galan J. E. 2003; Temporal regulation of salmonella virulence effector function by proteasome-dependent protein degradation. Cell 115:333–342 [CrossRef]
    [Google Scholar]
  19. Lawley T. D., Chan K., Thompson L. J., Kim C. C., Govoni G. R., Monack D. M. 2006; Genome-wide screen for salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2:e11 [CrossRef]
    [Google Scholar]
  20. Layton A. N., Brown P. J., Edouard E., Galyov E. E. 2005; The Salmonella translocated effector SopA is targeted to the mitochondria of infected cells. J Bacteriol 187:3565–3571 [CrossRef]
    [Google Scholar]
  21. Lucas R. L., Lee C. A. 2000; Unravelling the mysteries of virulence gene regulation in Salmonella typhimurium . Mol Microbiol 36:1024–1033 [CrossRef]
    [Google Scholar]
  22. Marcus S. L., Brumell J. H., Pfeifer C. G., Finlay B. B. 2000; Salmonella pathogenicity islands: big virulence in small packages. Microbes Infect 2:145–156 [CrossRef]
    [Google Scholar]
  23. Miki T., Okada N., Danbara H. 2004; Two periplasmic disulfide oxidoreductases, DsbA and SrgA, target outer membrane protein SpiA, a component of the Salmonella pathogenicity island 2 type III secretion system. J Biol Chem 279:34631–34642 [CrossRef]
    [Google Scholar]
  24. Mirold S., Ehrbar K., Prager R., Hardt W.-D., Weissmüller A., Tschäpe H., Rüssmann H. 2001; Salmonella host cell invasion emerged by acquisition of a mosaic of separate genetic elements, including Salmonella pathogenicity island1 (SPI1), SPI5, and sopE2 . J Bacteriol 183:2348–2358 [CrossRef]
    [Google Scholar]
  25. Patel J. C., Galan J. E. 2005; Manipulation of the host actin cytoskeleton by Salmonella : all in the name of entry. Curr Opin Microbiol 8:10–15 [CrossRef]
    [Google Scholar]
  26. Pfeifer C. G., Marcus S. L., Steele-Mortimer O., Knodler L. A., Finlay B. B. 1999; Salmonella typhimurium virulence genes are induced upon bacterial invasion into phagocytic and nonphagocytic cells. Infect Immun 67:5690–5698
    [Google Scholar]
  27. Pucciarelli M. G., Prieto A. I., Casadesús J., García-Del Portillo F. 2002; Envelope instability in DNA adenine methylase mutants of Salmonella enterica . Microbiology 148:1171–1182
    [Google Scholar]
  28. Raffatellu M., Wilson R. P., Chessa D., Andrews-Polymenis H., Tran Q. T., Lawhon S., Khare S., Adams L. G., Bäumler A. J. 2005; SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype typhimurium invasion of epithelial cells. Infect Immun 73:146–154 [CrossRef]
    [Google Scholar]
  29. Reed L. J., Muench H. 1938; A simple method of estimating fifty per cent endpoints. Am J Hyg 27:493–499
    [Google Scholar]
  30. Reis B. P., Zhang S., Tsolis R. M., Santos R. L., Baümler A. J., Adams L. G. 2003; The attenuated sopB mutant of Salmonella enterica serovar Typhimurium has the same tissue distribution and host chemokine response as the wild type in bovine Peyer's patches. Vet Microbiol 97:269–277 [CrossRef]
    [Google Scholar]
  31. Santos R. L., Bäumler A. J. 2004; Cell tropism of Salmonella enterica . Int J Med Microbiol 294:225–233 [CrossRef]
    [Google Scholar]
  32. Schlumberger M. C., Hardt W. D. 2006; Salmonella type III secretion effectors: pulling the host cell's strings. Curr Opin Microbiol 9:1–9 [CrossRef]
    [Google Scholar]
  33. Steele-Mortimer O., Brumell J. H., Knodler L. A., Meresse S., Lopez A., Finlay B. B. 2002; The invasion-associated type III secretion system of Salmonella enterica serovar Typhimurium is necessary for intracellular proliferation and vacuole biogenesis in epithelial cells. Cell Microbiol 4:43–54 [CrossRef]
    [Google Scholar]
  34. Streckel W., Wolff A. C., Prager R., Tietze E., Tschäpe H. 2004; Expression profiles of effector proteins SopB, SopD1, SopE1, and AvrA differ with systemic, enteric, and epidemic strains of Salmonella enterica . Mol Nutr Food Res 48:496–503 [CrossRef]
    [Google Scholar]
  35. Tsolis R. M., Kingsley R. A., Townsend S. M., Ficht T. A., Adams L. G., Baumler A. J. 1999; Of mice, calves, and men. Comparison of the mouse typhoid model with other Salmonella infections. Adv Exp Med Biol 473:261–274
    [Google Scholar]
  36. Uzzau S., Figueroa-Bossi N., Rubino S., Bossi L. 2001; Epitope tagging of chromosomal genes in Salmonella . Proc Natl Acad Sci U S A 26:15264–15269
    [Google Scholar]
  37. Vazquez-Torres A., Jones-Carson J., Baümler A. J. 1999; Extraintestinal dissemination of Salmonella via CD18-expressing phagocytes. Nature 401:804–808 [CrossRef]
    [Google Scholar]
  38. Wallis T. S., Galyov E. E. 2000; Molecular basis of Salmonella -induced enteritis. Mol Microbiol 36:997–1005 [CrossRef]
    [Google Scholar]
  39. Waterman S. R., Holden D. W. 2003; Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol 5:501–511 [CrossRef]
    [Google Scholar]
  40. Wood M. W., Jones M. A., Watson P. R., Siber A. M., McCormick B. A., Hedges S., Rosqvist R., Wallis T. S., Galyov E. E. 2000; The secreted effector protein of Salmonella dublin , SopA, is translocated into eukaryotic cells and influences the induction of enteritis. Cell Microbiol 2:293–303 [CrossRef]
    [Google Scholar]
  41. Zhang S., Santos S. R. L., Tsolis R. M., Stender S., Hardt W.-D., Adams L. G., Baümler A. J. 2002; The Salmonella enterica serotype Typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infect Immun 70:3843–3855 [CrossRef]
    [Google Scholar]
  42. Zhang S., Adams L. G., Nunes J., Khare S., Tsolis R. M., Bäumler A. J. 2003; Secreted effector proteins of Salmonella enterica serotype typhimurium elicit host-specific chemokine profiles in animal models of typhoid fever and enterocolitis. Infect Immun 71:4795–4803 [CrossRef]
    [Google Scholar]
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