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. 1992 Feb;60(2):450–454. doi: 10.1128/iai.60.2.450-454.1992

Role of gamma interferon and tumor necrosis factor alpha in resistance to Salmonella typhimurium infection.

C Nauciel 1, F Espinasse-Maes 1
PMCID: PMC257648  PMID: 1730475

Abstract

In mice infected with a sublethal dose of Salmonella typhimurium, the injection of an anti-gamma interferon (IFN-gamma) monoclonal antibody increased bacterial proliferation in the spleen and led to death on day 7 or 8. Depletion of both CD4+ and CD8+ T cells with monoclonal antibodies in vivo had a much less marked effect during the first week of infection than the administration of anti-IFN-gamma antibodies, suggesting that cells other than T lymphocytes participate in the production of IFN-gamma at this time. Administration of anti-tumor necrosis factor alpha (TNF-alpha) antibodies to mice infected with a sublethal dose of S. typhimurium induced the same effect as anti-IFN-gamma antibodies, while the administration of both antibodies resulted in a synergistic interaction. When mice were infected with an avirulent strain of S. typhimurium and challenged on day 7 either with a virulent strain of S. typhimurium or with Listeria monocytogenes, their resistance to reinfection was slightly depressed by anti-IFN-gamma or anti-TNF-alpha antibodies given 1 day before challenge and much more strongly depressed by the simultaneous administration of both antibodies. Taken together, these results indicate that IFN-gamma and TNF-alpha play an essential role in acquired resistance during the early phase of S. typhimurium infection.

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Selected References

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

  1. Aggarwal B. B., Eessalu T. E., Hass P. E. Characterization of receptors for human tumour necrosis factor and their regulation by gamma-interferon. Nature. 1985 Dec 19;318(6047):665–667. doi: 10.1038/318665a0. [DOI] [PubMed] [Google Scholar]
  2. Bancroft G. J., Schreiber R. D., Bosma G. C., Bosma M. J., Unanue E. R. A T cell-independent mechanism of macrophage activation by interferon-gamma. J Immunol. 1987 Aug 15;139(4):1104–1107. [PubMed] [Google Scholar]
  3. Bancroft G. J., Sheehan K. C., Schreiber R. D., Unanue E. R. Tumor necrosis factor is involved in the T cell-independent pathway of macrophage activation in scid mice. J Immunol. 1989 Jul 1;143(1):127–130. [PubMed] [Google Scholar]
  4. Benjamin W. H., Jr, Hall P., Roberts S. J., Briles D. E. The primary effect of the Ity locus is on the rate of growth of Salmonella typhimurium that are relatively protected from killing. J Immunol. 1990 Apr 15;144(8):3143–3151. [PubMed] [Google Scholar]
  5. Bermudez L. E., Young L. S. Tumor necrosis factor, alone or in combination with IL-2, but not IFN-gamma, is associated with macrophage killing of Mycobacterium avium complex. J Immunol. 1988 May 1;140(9):3006–3013. [PubMed] [Google Scholar]
  6. Buchmeier N. A., Schreiber R. D. Requirement of endogenous interferon-gamma production for resolution of Listeria monocytogenes infection. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7404–7408. doi: 10.1073/pnas.82.21.7404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Collart M. A., Belin D., Vassalli J. D., de Kossodo S., Vassalli P. Gamma interferon enhances macrophage transcription of the tumor necrosis factor/cachectin, interleukin 1, and urokinase genes, which are controlled by short-lived repressors. J Exp Med. 1986 Dec 1;164(6):2113–2118. doi: 10.1084/jem.164.6.2113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Collins F. M. Vaccines and cell-mediated immunity. Bacteriol Rev. 1974 Dec;38(4):371–402. doi: 10.1128/br.38.4.371-402.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Denis M. Modulation of Mycobacterium lepraemurium growth in murine macrophages: beneficial effect of tumor necrosis factor alpha and granulocyte-macrophage colony-stimulating factor. Infect Immun. 1991 Feb;59(2):705–707. doi: 10.1128/iai.59.2.705-707.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Eisenstein T. K., Killar L. M., Stocker B. A., Sultzer B. M. Cellular immunity induced by avirulent Salmonella in LPS-defective C3H/HeJ mice. J Immunol. 1984 Aug;133(2):958–961. [PubMed] [Google Scholar]
  11. Eisenstein T. K., Sultzer B. M. Immunity to Salmonella infection. Adv Exp Med Biol. 1983;162:261–296. doi: 10.1007/978-1-4684-4481-0_26. [DOI] [PubMed] [Google Scholar]
  12. Fisch H., Gifford G. E. In vitro production of rabbit macrophage tumor cell cytotoxin. Int J Cancer. 1983 Jul 15;32(1):105–112. doi: 10.1002/ijc.2910320117. [DOI] [PubMed] [Google Scholar]
  13. Havell E. A. Production of tumor necrosis factor during murine listeriosis. J Immunol. 1987 Dec 15;139(12):4225–4231. [PubMed] [Google Scholar]
  14. Hori K., Ehrke M. J., Mace K., Mihich E. Effect of recombinant tumor necrosis factor on tumoricidal activation of murine macrophages: synergism between tumor necrosis factor and gamma-interferon. Cancer Res. 1987 Nov 15;47(22):5868–5874. [PubMed] [Google Scholar]
  15. Hormaeche C. E., Harrington K. A., Joysey H. S. Natural resistance to salmonellae in mice: control by genes within the major histocompatibility complex. J Infect Dis. 1985 Nov;152(5):1050–1056. doi: 10.1093/infdis/152.5.1050. [DOI] [PubMed] [Google Scholar]
  16. Hormaeche C. E., Mastroeni P., Arena A., Uddin J., Joysey H. S. T cells do not mediate the initial suppression of a Salmonella infection in the RES. Immunology. 1990 Jun;70(2):247–250. [PMC free article] [PubMed] [Google Scholar]
  17. Hormaeche C. E., Pettifor R. A., Brock J. The fate of temperature-sensitive salmonella mutants in vivo in naturally resistant and susceptible mice. Immunology. 1981 Apr;42(4):569–576. [PMC free article] [PubMed] [Google Scholar]
  18. Hsu H. S. Pathogenesis and immunity in murine salmonellosis. Microbiol Rev. 1989 Dec;53(4):390–409. doi: 10.1128/mr.53.4.390-409.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kagaya K., Watanabe K., Fukazawa Y. Capacity of recombinant gamma interferon to activate macrophages for Salmonella-killing activity. Infect Immun. 1989 Feb;57(2):609–615. doi: 10.1128/iai.57.2.609-615.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Killar L. M., Eisenstein T. K. Immunity to Salmonella typhimurium infection in C3H/HeJ and C3H/HeNCrlBR mice: studies with an aromatic-dependent live S. typhimurium strain as a vaccine. Infect Immun. 1985 Mar;47(3):605–612. doi: 10.1128/iai.47.3.605-612.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Liew F. Y., Li Y., Millott S. Tumor necrosis factor-alpha synergizes with IFN-gamma in mediating killing of Leishmania major through the induction of nitric oxide. J Immunol. 1990 Dec 15;145(12):4306–4310. [PubMed] [Google Scholar]
  22. Matsumura H., Onozuka K., Terada Y., Nakano Y., Nakano M. Effect of murine recombinant interferon-gamma in the protection of mice against Salmonella. Int J Immunopharmacol. 1990;12(1):49–56. doi: 10.1016/0192-0561(90)90067-w. [DOI] [PubMed] [Google Scholar]
  23. Mosmann T. R., Coffman R. L. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol. 1989;7:145–173. doi: 10.1146/annurev.iy.07.040189.001045. [DOI] [PubMed] [Google Scholar]
  24. Muotiala A., Mäkelä P. H. The role of IFN-gamma in murine Salmonella typhimurium infection. Microb Pathog. 1990 Feb;8(2):135–141. doi: 10.1016/0882-4010(90)90077-4. [DOI] [PubMed] [Google Scholar]
  25. Nakane A., Minagawa T., Kohanawa M., Chen Y., Sato H., Moriyama M., Tsuruoka N. Interactions between endogenous gamma interferon and tumor necrosis factor in host resistance against primary and secondary Listeria monocytogenes infections. Infect Immun. 1989 Nov;57(11):3331–3337. doi: 10.1128/iai.57.11.3331-3337.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nakano Y., Onozuka K., Terada Y., Shinomiya H., Nakano M. Protective effect of recombinant tumor necrosis factor-alpha in murine salmonellosis. J Immunol. 1990 Mar 1;144(5):1935–1941. [PubMed] [Google Scholar]
  27. Nathan C. F., Murray H. W., Wiebe M. E., Rubin B. Y. Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J Exp Med. 1983 Sep 1;158(3):670–689. doi: 10.1084/jem.158.3.670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nauciel C. Role of CD4+ T cells and T-independent mechanisms in acquired resistance to Salmonella typhimurium infection. J Immunol. 1990 Aug 15;145(4):1265–1269. [PubMed] [Google Scholar]
  29. Nauciel C., Ronco E., Guenet J. L., Pla M. Role of H-2 and non-H-2 genes in control of bacterial clearance from the spleen in Salmonella typhimurium-infected mice. Infect Immun. 1988 Sep;56(9):2407–2411. doi: 10.1128/iai.56.9.2407-2411.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nauciel C., Vilde F., Ronco E. Host response to infection with a temperature-sensitive mutant of Salmonella typhimurium in a susceptible and a resistant strain of mice. Infect Immun. 1985 Sep;49(3):523–527. doi: 10.1128/iai.49.3.523-527.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. O'Brien A. D. Influence of host genes on resistance of inbred mice to lethal infection with Salmonella typhimurium. Curr Top Microbiol Immunol. 1986;124:37–48. [PubMed] [Google Scholar]
  32. Spitalny G. L., Havell E. A. Monoclonal antibody to murine gamma interferon inhibits lymphokine-induced antiviral and macrophage tumoricidal activities. J Exp Med. 1984 May 1;159(5):1560–1565. doi: 10.1084/jem.159.5.1560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tsujimoto M., Yip Y. K., Vilcek J. Interferon-gamma enhances expression of cellular receptors for tumor necrosis factor. J Immunol. 1986 Apr 1;136(7):2441–2444. [PubMed] [Google Scholar]
  34. Wietzerbin J., Stefanos S., Falcoff R., Lucero M., Catinot L., Falcoff E. Immune interferon induced by phytohemagglutinin in nude mouse spleen cells. Infect Immun. 1978 Sep;21(3):966–972. doi: 10.1128/iai.21.3.966-972.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Williams D. M., Magee D. M., Bonewald L. F., Smith J. G., Bleicker C. A., Byrne G. I., Schachter J. A role in vivo for tumor necrosis factor alpha in host defense against Chlamydia trachomatis. Infect Immun. 1990 Jun;58(6):1572–1576. doi: 10.1128/iai.58.6.1572-1576.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Young H. A., Ortaldo J. R. One-signal requirement for interferon-gamma production by human large granular lymphocytes. J Immunol. 1987 Aug 1;139(3):724–727. [PubMed] [Google Scholar]
  37. van Dissel J. T., Stikkelbroeck J. J., Michel B. C., van den Barselaar M. T., Leijh P. C., van Furth R. Inability of recombinant interferon-gamma to activate the antibacterial activity of mouse peritoneal macrophages against Listeria monocytogenes and Salmonella typhimurium. J Immunol. 1987 Sep 1;139(5):1673–1678. [PubMed] [Google Scholar]

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