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. 1995 Sep;63(9):3302–3308. doi: 10.1128/iai.63.9.3302-3308.1995

CD4+ T cells play a significant role in adoptive immunity to Chlamydia trachomatis infection of the mouse genital tract.

H Su 1, H D Caldwell 1
PMCID: PMC173455  PMID: 7642259

Abstract

The ability of CD4+ and CD8+ T cells to adoptively immunize mice against Chlamydia trachomatis infection of the mouse genital tract was studied. Adoptive transfer experiments were performed with splenic CD4+ or CD8+ T cells obtained from mice following resolution of a primary genital tract infection and after a secondary chlamydial challenge. The results show that donor CD4+ T cells, but not CD8+ T cells, obtained from mice following resolution of a primary infection or after secondary challenge were effective in transferring significant antichlamydial immunity to the genital tracts of naive animals. The lymphokine profiles in the culture supernatants of proliferating Chlamydia-specific CD4+ T cells obtained from mice following resolution of a primary infection and after secondary challenge were assayed by an enzyme-linked immunoadsorbent assay. Protective CD4+ T cells restimulated in vitro secreted interleukin 2, gamma interferon, and interleukin 6, lymphokine profiles characteristic of both Th1- and Th2-like responses. Resting CD4+ T cells obtained from mice 4 months following resolution of a primary infection were also capable of conferring significant levels of adoptive protective immunity to naive mice. These findings support an important role for CD4+ T cells in acquired immunity to chlamydial infection of the genital tract and indicate that protective CD4+ immune responses in this model are relatively long lived.

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Selected References

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  1. Barron A. L., White H. J., Rank R. G., Soloff B. L., Moses E. B. A new animal model for the study of Chlamydia trachomatis genital infections: infection of mice with the agent of mouse pneumonitis. J Infect Dis. 1981 Jan;143(1):63–66. doi: 10.1093/infdis/143.1.63. [DOI] [PubMed] [Google Scholar]
  2. Beagley K. W., Eldridge J. H., Lee F., Kiyono H., Everson M. P., Koopman W. J., Hirano T., Kishimoto T., McGhee J. R. Interleukins and IgA synthesis. Human and murine interleukin 6 induce high rate IgA secretion in IgA-committed B cells. J Exp Med. 1989 Jun 1;169(6):2133–2148. doi: 10.1084/jem.169.6.2133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bishop D. K., Hinrichs D. J. Adoptive transfer of immunity to Listeria monocytogenes. The influence of in vitro stimulation on lymphocyte subset requirements. J Immunol. 1987 Sep 15;139(6):2005–2009. [PubMed] [Google Scholar]
  4. Brunt L. M., Portnoy D. A., Unanue E. R. Presentation of Listeria monocytogenes to CD8+ T cells requires secretion of hemolysin and intracellular bacterial growth. J Immunol. 1990 Dec 1;145(11):3540–3546. [PubMed] [Google Scholar]
  5. Buzoni-Gatel D., Guilloteau L., Bernard F., Bernard S., Chardès T., Rocca A. Protection against Chlamydia psittaci in mice conferred by Lyt-2+ T cells. Immunology. 1992 Oct;77(2):284–288. [PMC free article] [PubMed] [Google Scholar]
  6. Byrne G. I., Carlin J. M., Merkert T. P., Arter D. L. Long-term effects of gamma interferon on chlamydia-infected host cells: microbicidal activity follows microbistasis. Infect Immun. 1989 Apr;57(4):1318–1320. doi: 10.1128/iai.57.4.1318-1320.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Byrne G. I., Lehmann L. K., Landry G. J. Induction of tryptophan catabolism is the mechanism for gamma-interferon-mediated inhibition of intracellular Chlamydia psittaci replication in T24 cells. Infect Immun. 1986 Aug;53(2):347–351. doi: 10.1128/iai.53.2.347-351.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Flesch I. E., Kaufmann S. H. Activation of tuberculostatic macrophage functions by gamma interferon, interleukin-4, and tumor necrosis factor. Infect Immun. 1990 Aug;58(8):2675–2677. doi: 10.1128/iai.58.8.2675-2677.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Grayston J. T., Wang S. New knowledge of chlamydiae and the diseases they cause. J Infect Dis. 1975 Jul;132(1):87–105. doi: 10.1093/infdis/132.1.87. [DOI] [PubMed] [Google Scholar]
  10. Harding C. V., Pfeifer J. D. Antigen expressed by Salmonella typhimurium is processed for class I major histocompatibility complex presentation by macrophages but not infected epithelial cells. Immunology. 1994 Dec;83(4):670–674. [PMC free article] [PubMed] [Google Scholar]
  11. Heinzel F. P., Sadick M. D., Holaday B. J., Coffman R. L., Locksley R. M. Reciprocal expression of interferon gamma or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets. J Exp Med. 1989 Jan 1;169(1):59–72. doi: 10.1084/jem.169.1.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Igietseme J. U., Magee D. M., Williams D. M., Rank R. G. Role for CD8+ T cells in antichlamydial immunity defined by Chlamydia-specific T-lymphocyte clones. Infect Immun. 1994 Nov;62(11):5195–5197. doi: 10.1128/iai.62.11.5195-5197.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Igietseme J. U., Ramsey K. H., Magee D. M., Williams D. M., Kincy T. J., Rank R. G. Resolution of murine chlamydial genital infection by the adoptive transfer of a biovar-specific, Th1 lymphocyte clone. Reg Immunol. 1993 Nov-Dec;5(6):317–324. [PubMed] [Google Scholar]
  14. Igietseme J. U., Wyrick P. B., Goyeau D., Rank R. G. An in vitro model for immune control of chlamydial growth in polarized epithelial cells. Infect Immun. 1994 Aug;62(8):3528–3535. doi: 10.1128/iai.62.8.3528-3535.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jones B. R. The prevention of blindness from trachoma. Trans Ophthalmol Soc U K. 1975 Apr;95(1):16–33. [PubMed] [Google Scholar]
  16. Kaufmann S. H., Flesch I. E. The role of T cell--macrophage interactions in tuberculosis. Springer Semin Immunopathol. 1988;10(4):337–358. doi: 10.1007/BF02053845. [DOI] [PubMed] [Google Scholar]
  17. Kaufmann S. H. Immunity against intracellular bacteria: biological effector functions and antigen specificity of T lymphocytes. Curr Top Microbiol Immunol. 1988;138:141–176. [PubMed] [Google Scholar]
  18. Kazar J., Gillmore J. D., Gordon F. B. Effect of Interferon and Interferon Inducers on Infections with a Nonviral Intracellular Microorganism, Chlamydia trachomatis. Infect Immun. 1971 Jun;3(6):825–832. doi: 10.1128/iai.3.6.825-832.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lukacs K., Kurlander R. Lyt-2+ T cell-mediated protection against listeriosis. Protection correlates with phagocyte depletion but not with IFN-gamma production. J Immunol. 1989 Apr 15;142(8):2879–2886. [PubMed] [Google Scholar]
  20. Mayer J., Woods M. L., Vavrin Z., Hibbs J. B., Jr Gamma interferon-induced nitric oxide production reduces Chlamydia trachomatis infectivity in McCoy cells. Infect Immun. 1993 Feb;61(2):491–497. doi: 10.1128/iai.61.2.491-497.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Mutis T., Cornelisse Y. E., Ottenhoff T. H. Mycobacteria induce CD4+ T cells that are cytotoxic and display Th1-like cytokine secretion profile: heterogeneity in cytotoxic activity and cytokine secretion levels. Eur J Immunol. 1993 Sep;23(9):2189–2195. doi: 10.1002/eji.1830230921. [DOI] [PubMed] [Google Scholar]
  23. Orme I. M. Active and memory immunity to Listeria monocytogenes infection in mice is mediated by phenotypically distinct T-cell populations. Immunology. 1989 Sep;68(1):93–95. [PMC free article] [PubMed] [Google Scholar]
  24. Patton D. L., Landers D. V., Schachter J. Experimental Chlamydia trachomatis salpingitis in mice: initial studies on the characterization of the leukocyte response to chlamydial infection. J Infect Dis. 1989 Jun;159(6):1105–1110. doi: 10.1093/infdis/159.6.1105. [DOI] [PubMed] [Google Scholar]
  25. Polsinelli T., Meltzer M. S., Fortier A. H. Nitric oxide-independent killing of Francisella tularensis by IFN-gamma-stimulated murine alveolar macrophages. J Immunol. 1994 Aug 1;153(3):1238–1245. [PubMed] [Google Scholar]
  26. Rakhmilevich A. L. Evidence for a significant role of CD4+ T cells in adoptive immunity to Listeria monocytogenes in the liver. Immunology. 1994 Jun;82(2):249–254. [PMC free article] [PubMed] [Google Scholar]
  27. Ramsey K. H., Rank R. G. Resolution of chlamydial genital infection with antigen-specific T-lymphocyte lines. Infect Immun. 1991 Mar;59(3):925–931. doi: 10.1128/iai.59.3.925-931.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rank R. G., Soderberg L. S., Barron A. L. Chronic chlamydial genital infection in congenitally athymic nude mice. Infect Immun. 1985 Jun;48(3):847–849. doi: 10.1128/iai.48.3.847-849.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rossi-Bergmann B., Müller I., Godinho E. B. TH1 and TH2 T-cell subsets are differentially activated by macrophages and B cells in murine leishmaniasis. Infect Immun. 1993 May;61(5):2266–2269. doi: 10.1128/iai.61.5.2266-2269.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schachter J. Chlamydial infections (third of three parts). N Engl J Med. 1978 Mar 9;298(10):540–549. doi: 10.1056/NEJM197803092981005. [DOI] [PubMed] [Google Scholar]
  31. Shemer Y., Sarov I. Inhibition of growth of Chlamydia trachomatis by human gamma interferon. Infect Immun. 1985 May;48(2):592–596. doi: 10.1128/iai.48.2.592-596.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Starnbach M. N., Bevan M. J., Lampe M. F. Protective cytotoxic T lymphocytes are induced during murine infection with Chlamydia trachomatis. J Immunol. 1994 Dec 1;153(11):5183–5189. [PubMed] [Google Scholar]
  33. Su H., Caldwell H. D. Kinetics of chlamydial antigen processing and presentation to T cells by paraformaldehyde-fixed murine bone marrow-derived macrophages. Infect Immun. 1995 Mar;63(3):946–953. doi: 10.1128/iai.63.3.946-953.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Swenson C. E., Donegan E., Schachter J. Chlamydia trachomatis-induced salpingitis in mice. J Infect Dis. 1983 Dec;148(6):1101–1107. doi: 10.1093/infdis/148.6.1101. [DOI] [PubMed] [Google Scholar]
  35. Van Snick J. Interleukin-6: an overview. Annu Rev Immunol. 1990;8:253–278. doi: 10.1146/annurev.iy.08.040190.001345. [DOI] [PubMed] [Google Scholar]
  36. de la Maza L. M., Peterson E. M., Goebel J. M., Fennie C. W., Czarniecki C. W. Interferon-induced inhibition of Chlamydia trachomatis: dissociation from antiviral and antiproliferative effects. Infect Immun. 1985 Mar;47(3):719–722. doi: 10.1128/iai.47.3.719-722.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]

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