Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1997 Dec;65(12):5244–5249. doi: 10.1128/iai.65.12.5244-5249.1997

Cellular changes and cytokine expression in the ilea of gnotobiotic piglets resulting from peroral Salmonella typhimurium challenge.

I Trebichavský 1, V Dlabac 1, Z Reháková 1, M Zahradnícková 1, I Splíchal 1
PMCID: PMC175755  PMID: 9393822

Abstract

Two stable rough mutants of Salmonella spp. were studied as live peroral vaccines. The SF1591 mutant of S. typhimurium (Ra chemotype) protected germ-free piglets against subsequent infection with virulent smooth S. typhimurium LT2, whereas a deep-rough mutant of S. minnesota mR595 (Re chemotype) did not. We investigated cytokine and leukocyte profiles in the ilea of gnotobiotic piglets colonized for 1 week either with rough mutants alone or with rough mutants followed by S. typhimurium LT2. The ileal mucosae of piglets associated with strain SF1591 alone were not inflamed. Villi contained activated macrophages, and enterocytes expressed transforming growth factor beta (TGF-beta). Subsequent infection of piglets with S. typhimurium LT2 resulted in immigration of alphabeta T cells and immunoglobulin A (IgA) response. In contrast, the ileal mucosae of piglets associated with strain mR595 alone expressed heat shock proteins and inflammatory cytokines but not TGF-beta. Acellular villi contained numerous gammadelta T cells but no alphabeta T cells. After subsequent challenge with the LT2 strain, most piglets died of sepsis. Intestinal mucosae contained IgG but no IgA. These findings suggest the importance of cytokine signals in the regulation of intestinal responses against Salmonella infection.

Full Text

The Full Text of this article is available as a PDF (935.0 KB).

Selected References

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

  1. Arnold J. W., Klimpel G. R., Niesel D. W. Tumor necrosis factor (TNF alpha) regulates intestinal mucus production during salmonellosis. Cell Immunol. 1993 Oct 15;151(2):336–344. doi: 10.1006/cimm.1993.1243. [DOI] [PubMed] [Google Scholar]
  2. Binns R. M., Duncan I. A., Powis S. J., Hutchings A., Butcher G. W. Subsets of null and gamma delta T-cell receptor+ T lymphocytes in the blood of young pigs identified by specific monoclonal antibodies. Immunology. 1992 Oct;77(2):219–227. [PMC free article] [PubMed] [Google Scholar]
  3. Bukholm G., Degré M. Effect of human gamma interferon on invasiveness of Salmonella typhimurium in HEp-2 cell cultures. J Interferon Res. 1985 Winter;5(1):45–53. doi: 10.1089/jir.1985.5.45. [DOI] [PubMed] [Google Scholar]
  4. Dlabac V., Trebichavský I., Reháková Z., Hofmanová B., Splíchal I., Cukrowska B. Pathogenicity and protective effect of rough mutants of Salmonella species in germ-free piglets. Infect Immun. 1997 Dec;65(12):5238–5243. doi: 10.1128/iai.65.12.5238-5243.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Eckmann L., Kagnoff M. F., Fierer J. Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect Immun. 1993 Nov;61(11):4569–4574. doi: 10.1128/iai.61.11.4569-4574.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Galán J. E., Pace J., Hayman M. J. Involvement of the epidermal growth factor receptor in the invasion of cultured mammalian cells by Salmonella typhimurium. Nature. 1992 Jun 18;357(6379):588–589. doi: 10.1038/357588a0. [DOI] [PubMed] [Google Scholar]
  7. Kagnoff M. F. Mucosal immunology: new frontiers. Immunol Today. 1996 Feb;17(2):57–59. doi: 10.1016/0167-5699(96)80579-2. [DOI] [PubMed] [Google Scholar]
  8. Kelly N. M., Young L., Cross A. S. Differential induction of tumor necrosis factor by bacteria expressing rough and smooth lipopolysaccharide phenotypes. Infect Immun. 1991 Dec;59(12):4491–4496. doi: 10.1128/iai.59.12.4491-4496.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Klimpel G. R., Asuncion M., Haithcoat J., Niesel D. W. Cholera toxin and Salmonella typhimurium induce different cytokine profiles in the gastrointestinal tract. Infect Immun. 1995 Mar;63(3):1134–1137. doi: 10.1128/iai.63.3.1134-1137.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Klimpel G. R., Langley K. E., Wypych J., Abrams J. S., Chopra A. K., Niesel D. W. A role for stem cell factor (SCF): c-kit interaction(s) in the intestinal tract response to Salmonella typhimurium infection. J Exp Med. 1996 Jul 1;184(1):271–276. doi: 10.1084/jem.184.1.271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. McGhee J. R., Kiyono H. New perspectives in vaccine development: mucosal immunity to infections. Infect Agents Dis. 1993 Apr;2(2):55–73. [PubMed] [Google Scholar]
  12. Pabst R., Geist M., Rothkötter H. J., Fritz F. J. Postnatal development and lymphocyte production of jejunal and ileal Peyer's patches in normal and gnotobiotic pigs. Immunology. 1988 Jul;64(3):539–544. [PMC free article] [PubMed] [Google Scholar]
  13. Ramarathinam L., Shaban R. A., Niesel D. W., Klimpel G. R. Interferon gamma (IFN-gamma) production by gut-associated lymphoid tissue and spleen following oral Salmonella typhimurium challenge. Microb Pathog. 1991 Nov;11(5):347–356. doi: 10.1016/0882-4010(91)90020-b. [DOI] [PubMed] [Google Scholar]
  14. Saalmüller A. Characterization of swine leukocyte differentiation antigens. Immunol Today. 1996 Aug;17(8):352–354. doi: 10.1016/S0167-5699(96)90273-X. [DOI] [PubMed] [Google Scholar]
  15. Sasaki H., Pollard R. B., Schmitt D., Suzuki F. Transforming growth factor-beta in the regulation of the immune response. Clin Immunol Immunopathol. 1992 Oct;65(1):1–9. doi: 10.1016/0090-1229(92)90241-f. [DOI] [PubMed] [Google Scholar]
  16. Tlaskalová-Hogenová H., Mandel L., Stepánková R., Bártová J., Barot R., Leclerc M., Kovárů F., Trebichavský I. Autoimmunity: from physiology to pathology. Natural antibodies, mucosal immunity and development of B cell repertoire. Folia Biol (Praha) 1992;38(3-4):202–215. [PubMed] [Google Scholar]
  17. Trávnícek J., Mandel L., Trebichavský I., Talafantová M. Immunological state of adult germfree miniature Minnesota pigs. Folia Microbiol (Praha) 1989;34(2):157–164. doi: 10.1007/BF02823696. [DOI] [PubMed] [Google Scholar]
  18. Wahl S. M. Transforming growth factor beta (TGF-beta) in inflammation: a cause and a cure. J Clin Immunol. 1992 Mar;12(2):61–74. doi: 10.1007/BF00918135. [DOI] [PubMed] [Google Scholar]
  19. Whyte A., Haskard D. O., Binns R. M. Infiltrating gamma delta T-cells and selectin endothelial ligands in the cutaneous phytohaemagglutinin-induced inflammatory reaction. Vet Immunol Immunopathol. 1994 May;41(1-2):31–40. doi: 10.1016/0165-2427(94)90055-8. [DOI] [PubMed] [Google Scholar]

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

RESOURCES