Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1995 Jul;63(7):2743–2754. doi: 10.1128/iai.63.7.2743-2754.1995

Characterization of intestinal invasion by Salmonella typhimurium and Salmonella dublin and effect of a mutation in the invH gene.

P R Watson 1, S M Paulin 1, A P Bland 1, P W Jones 1, T S Wallis 1
PMCID: PMC173367  PMID: 7790093

Abstract

The relative levels of invasiveness of two bovine isolates each of Salmonella typhimurium and Salmonella dublin and of invH mutants of S. typhimurium were determined in MDCK and Int 407 cultured-cell assays and in bovine ileal loops. S. dublin was found to be significantly less invasive in cultured cells than S. typhimurium, but this difference was not observed in bovine intestines. The invH mutants exhibited a significant reduction in invasion in both cultured cells and bovine intestines. The invasive phenotypes of the strains were confirmed by fluorescent microscopy and scanning and transmission electron microscopy. The wild-type strains were observed in the laminae propriae of the intestinal villi, while in contrast the invH mutants were generally associated with the enterocyte layer. The degree of damage in the bovine ileum was related to the magnitude of the invasion. There was no difference in the amount of S. typhimurium or S. dublin recovered from the bovine ileum either with or without Peyer's patches 3 h after inoculation of the loop.

Full Text

The Full Text of this article is available as a PDF (4.6 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altmeyer R. M., McNern J. K., Bossio J. C., Rosenshine I., Finlay B. B., Galán J. E. Cloning and molecular characterization of a gene involved in Salmonella adherence and invasion of cultured epithelial cells. Mol Microbiol. 1993 Jan;7(1):89–98. doi: 10.1111/j.1365-2958.1993.tb01100.x. [DOI] [PubMed] [Google Scholar]
  2. Amin I. I., Douce G. R., Osborne M. P., Stephen J. Quantitative studies of invasion of rabbit ileal mucosa by Salmonella typhimurium strains which differ in virulence in a model of gastroenteritis. Infect Immun. 1994 Feb;62(2):569–578. doi: 10.1128/iai.62.2.569-578.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Finlay B. B., Ruschkowski S., Dedhar S. Cytoskeletal rearrangements accompanying salmonella entry into epithelial cells. J Cell Sci. 1991 Jun;99(Pt 2):283–296. doi: 10.1242/jcs.99.2.283. [DOI] [PubMed] [Google Scholar]
  4. Finlay B. B., Starnbach M. N., Francis C. L., Stocker B. A., Chatfield S., Dougan G., Falkow S. Identification and characterization of TnphoA mutants of Salmonella that are unable to pass through a polarized MDCK epithelial cell monolayer. Mol Microbiol. 1988 Nov;2(6):757–766. doi: 10.1111/j.1365-2958.1988.tb00087.x. [DOI] [PubMed] [Google Scholar]
  5. Francis C. L., Ryan T. A., Jones B. D., Smith S. J., Falkow S. Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature. 1993 Aug 12;364(6438):639–642. doi: 10.1038/364639a0. [DOI] [PubMed] [Google Scholar]
  6. Galán J. E., Curtiss R., 3rd Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6383–6387. doi: 10.1073/pnas.86.16.6383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Galán J. E. Interactions of bacteria with non-phagocytic cells. Curr Opin Immunol. 1994 Aug;6(4):590–595. doi: 10.1016/0952-7915(94)90146-5. [DOI] [PubMed] [Google Scholar]
  8. Giannasca P. J., Neutra M. R. Interactions of microorganisms with intestinal M cells: mucosal invasion and induction of secretory immunity. Infect Agents Dis. 1993 Aug;2(4):242–248. [PubMed] [Google Scholar]
  9. Giannella R. A., Formal S. B., Dammin G. J., Collins H. Pathogenesis of salmonellosis. Studies of fluid secretion, mucosal invasion, and morphologic reaction in the rabbit ileum. J Clin Invest. 1973 Feb;52(2):441–453. doi: 10.1172/JCI107201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Giannella R. A., Washington O., Gemski P., Formal S. B. Invasion of HeLa cells by Salmonella typhimurium: a model for study of invasiveness of Salmonella. J Infect Dis. 1973 Jul;128(1):69–75. doi: 10.1093/infdis/128.1.69. [DOI] [PubMed] [Google Scholar]
  11. Ginocchio C., Pace J., Galán J. E. Identification and molecular characterization of a Salmonella typhimurium gene involved in triggering the internalization of salmonellae into cultured epithelial cells. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5976–5980. doi: 10.1073/pnas.89.13.5976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Groisman E. A., Ochman H. Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and Shigella flexneri. EMBO J. 1993 Oct;12(10):3779–3787. doi: 10.1002/j.1460-2075.1993.tb06056.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grützkau A., Hanski C., Hahn H., Riecken E. O. Involvement of M cells in the bacterial invasion of Peyer's patches: a common mechanism shared by Yersinia enterocolitica and other enteroinvasive bacteria. Gut. 1990 Sep;31(9):1011–1015. doi: 10.1136/gut.31.9.1011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hohmann A. W., Schmidt G., Rowley D. Intestinal colonization and virulence of Salmonella in mice. Infect Immun. 1978 Dec;22(3):763–770. doi: 10.1128/iai.22.3.763-770.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jones B. D., Ghori N., Falkow S. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med. 1994 Jul 1;180(1):15–23. doi: 10.1084/jem.180.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jones P. W., Dougan G., Hayward C., Mackensie N., Collins P., Chatfield S. N. Oral vaccination of calves against experimental salmonellosis using a double aro mutant of Salmonella typhimurium. Vaccine. 1991 Jan;9(1):29–34. doi: 10.1016/0264-410x(91)90313-u. [DOI] [PubMed] [Google Scholar]
  17. Kohbata S., Yokoyama H., Yabuuchi E. Cytopathogenic effect of Salmonella typhi GIFU 10007 on M cells of murine ileal Peyer's patches in ligated ileal loops: an ultrastructural study. Microbiol Immunol. 1986;30(12):1225–1237. doi: 10.1111/j.1348-0421.1986.tb03055.x. [DOI] [PubMed] [Google Scholar]
  18. Lodge J., Douce G. R., Amin I. I., Bolton A. J., Martin G. D., Chatfield S., Dougan G., Brown N. L., Stephen J. Biological and genetic characterization of TnphoA mutants of Salmonella typhimurium TML in the context of gastroenteritis. Infect Immun. 1995 Mar;63(3):762–769. doi: 10.1128/iai.63.3.762-769.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mounier J., Vasselon T., Hellio R., Lesourd M., Sansonetti P. J. Shigella flexneri enters human colonic Caco-2 epithelial cells through the basolateral pole. Infect Immun. 1992 Jan;60(1):237–248. doi: 10.1128/iai.60.1.237-248.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Parsons K. R., Bland A. P., Hall G. A. Follicle associated epithelium of the gut associated lymphoid tissue of cattle. Vet Pathol. 1991 Jan;28(1):22–29. doi: 10.1177/030098589102800104. [DOI] [PubMed] [Google Scholar]
  21. Perdomo O. J., Cavaillon J. M., Huerre M., Ohayon H., Gounon P., Sansonetti P. J. Acute inflammation causes epithelial invasion and mucosal destruction in experimental shigellosis. J Exp Med. 1994 Oct 1;180(4):1307–1319. doi: 10.1084/jem.180.4.1307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pospischil A., Wood R. L., Anderson T. D. Peroxidase-antiperoxidase and immunogold labeling of Salmonella typhimurium and Salmonella choleraesuis var kunzendorf in tissues of experimentally infected swine. Am J Vet Res. 1990 Apr;51(4):619–624. [PubMed] [Google Scholar]
  23. Reed W. M., Olander H. J., Thacker H. L. Studies on the pathogenesis of Salmonella typhimurium and Salmonella choleraesuis var kunzendorf infection in weanling pigs. Am J Vet Res. 1986 Jan;47(1):75–83. [PubMed] [Google Scholar]
  24. Smith H. W., Halls S. Observations by the ligated intestinal segment and oral inoculation methods on Escherichia coli infections in pigs, calves, lambs and rabbits. J Pathol Bacteriol. 1967 Apr;93(2):499–529. doi: 10.1002/path.1700930211. [DOI] [PubMed] [Google Scholar]
  25. Smith H. W., Jones J. E. Observations on experimental oral infection with Salmonella dublin in calves and Salmonella choleraesuis in pigs. J Pathol Bacteriol. 1967 Jan;93(1):141–156. doi: 10.1002/path.1700930114. [DOI] [PubMed] [Google Scholar]
  26. Takeuchi A. Electron microscope studies of experimental Salmonella infection. I. Penetration into the intestinal epithelium by Salmonella typhimurium. Am J Pathol. 1967 Jan;50(1):109–136. [PMC free article] [PubMed] [Google Scholar]
  27. Turnbull P. C., Richmond J. E. A model of salmonella enteritis: the behaviour of Salmonella enteritidis in chick intestine studies by light and electron microscopy. Br J Exp Pathol. 1978 Feb;59(1):64–75. [PMC free article] [PubMed] [Google Scholar]
  28. Verjans G. M., Ringrose J. H., van Alphen L., Feltkamp T. E., Kusters J. G. Entrance and survival of Salmonella typhimurium and Yersinia enterocolitica within human B- and T-cell lines. Infect Immun. 1994 Jun;62(6):2229–2235. doi: 10.1128/iai.62.6.2229-2235.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wallis T. S., Paulin S. M., Plested J. S., Watson P. R., Jones P. W. The Salmonella dublin virulence plasmid mediates systemic but not enteric phases of salmonellosis in cattle. Infect Immun. 1995 Jul;63(7):2755–2761. doi: 10.1128/iai.63.7.2755-2761.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wallis T. S., Starkey W. G., Stephen J., Haddon S. J., Osborne M. P., Candy D. C. The nature and role of mucosal damage in relation to Salmonella typhimurium-induced fluid secretion in the rabbit ileum. J Med Microbiol. 1986 Aug;22(1):39–49. doi: 10.1099/00222615-22-1-39. [DOI] [PubMed] [Google Scholar]
  31. Wassef J. S., Keren D. F., Mailloux J. L. Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis. Infect Immun. 1989 Mar;57(3):858–863. doi: 10.1128/iai.57.3.858-863.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Worton K. J., Candy D. C., Wallis T. S., Clarke G. J., Osborne M. P., Haddon S. J., Stephen J. Studies on early association of Salmonella typhimurium with intestinal mucosa in vivo and in vitro: relationship to virulence. J Med Microbiol. 1989 Aug;29(4):283–294. doi: 10.1099/00222615-29-4-283. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES