Skip to main content
Immunology logoLink to Immunology
. 1998 Aug;94(4):469–475. doi: 10.1046/j.1365-2567.1998.00549.x

Different roles are played by alpha beta and gamma delta T cells in acquired immunity to Chlamydia trachomatis pulmonary infection.

X Yang 1, K T Hayglass 1, R C Brunham 1
PMCID: PMC1364223  PMID: 9767433

Abstract

Using gene knockout and wild-type C57BL/6 mice, we examined the role of alpha beta and gamma delta T cells in the resolution of Chlamydia trachomatis mouse pneumonitis (MoPn) biovar pulmonary infection. The results show that alpha beta T-cell-deficient (alpha-/-) mice, when compared with wild-type control mice, have dramatically increased mortality rate and greater in vivo growth of MoPn. The alpha beta T-cell-deficient mice were as susceptible to MoPn infection as T- and B-lymphocyte-deficient (RAG-1-/-) mice. Moreover, both alpha beta T-cell-deficient and RAG-1 mutant mice failed to mount delayed-type hypersensitivity (DTH) responses to organism-specific challenge and showed undetectable interferon-gamma (IFN-gamma) production by spleen cells upon in vitro organism-specific restimulation. In contrast, gamma delta T-cell-deficient mice exhibited intact DTH responses and their mortality rate and in vivo chlamydial growth were comparable to those in wild-type controls. More interestingly, gamma delta T-cell-deficient mice showed significantly higher levels of IFN-gamma production than did wild-type mice. The data indicate that the alpha beta T cell is the major T-cell population for acquired immunity to chlamydial infection and that gamma delta T cells may play an ancillary role in regulating the magnitude of alpha beta T-cell responses.

Full text

PDF
469

Selected References

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

  1. Abbas A. K., Murphy K. M., Sher A. Functional diversity of helper T lymphocytes. Nature. 1996 Oct 31;383(6603):787–793. doi: 10.1038/383787a0. [DOI] [PubMed] [Google Scholar]
  2. Beatty P. R., Stephens R. S. CD8+ T lymphocyte-mediated lysis of Chlamydia-infected L cells using an endogenous antigen pathway. J Immunol. 1994 Nov 15;153(10):4588–4595. [PubMed] [Google Scholar]
  3. Cardillo F., Falcão R. P., Rossi M. A., Mengel J. An age-related gamma delta T cell suppressor activity correlates with the outcome of autoimmunity in experimental Trypanosoma cruzi infection. Eur J Immunol. 1993 Oct;23(10):2597–2605. doi: 10.1002/eji.1830231033. [DOI] [PubMed] [Google Scholar]
  4. Carding S. R., Allan W., McMickle A., Doherty P. C. Activation of cytokine genes in T cells during primary and secondary murine influenza pneumonia. J Exp Med. 1993 Feb 1;177(2):475–482. doi: 10.1084/jem.177.2.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. D'Souza C. D., Cooper A. M., Frank A. A., Mazzaccaro R. J., Bloom B. R., Orme I. M. An anti-inflammatory role for gamma delta T lymphocytes in acquired immunity to Mycobacterium tuberculosis. J Immunol. 1997 Feb 1;158(3):1217–1221. [PubMed] [Google Scholar]
  6. Emoto M., Nishimura H., Sakai T., Hiromatsu K., Gomi H., Itohara S., Yoshikai Y. Mice deficient in gamma delta T cells are resistant to lethal infection with Salmonella choleraesuis. Infect Immun. 1995 Sep;63(9):3736–3738. doi: 10.1128/iai.63.9.3736-3738.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fu Y. X., Roark C. E., Kelly K., Drevets D., Campbell P., O'Brien R., Born W. Immune protection and control of inflammatory tissue necrosis by gamma delta T cells. J Immunol. 1994 Oct 1;153(7):3101–3115. [PubMed] [Google Scholar]
  8. Hanano R., Reifenberg K., Kaufmann S. H. Naturally acquired Pneumocystis carinii pneumonia in gene disruption mutant mice: roles of distinct T-cell populations in infection. Infect Immun. 1996 Aug;64(8):3201–3209. doi: 10.1128/iai.64.8.3201-3209.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Itohara S., Mombaerts P., Lafaille J., Iacomini J., Nelson A., Clarke A. R., Hooper M. L., Farr A., Tonegawa S. T cell receptor delta gene mutant mice: independent generation of alpha beta T cells and programmed rearrangements of gamma delta TCR genes. Cell. 1993 Feb 12;72(3):337–348. doi: 10.1016/0092-8674(93)90112-4. [DOI] [PubMed] [Google Scholar]
  11. Kimani J., Maclean I. W., Bwayo J. J., MacDonald K., Oyugi J., Maitha G. M., Peeling R. W., Cheang M., Nagelkerke N. J., Plummer F. A. Risk factors for Chlamydia trachomatis pelvic inflammatory disease among sex workers in Nairobi, Kenya. J Infect Dis. 1996 Jun;173(6):1437–1444. doi: 10.1093/infdis/173.6.1437. [DOI] [PubMed] [Google Scholar]
  12. Landers D. V., Erlich K., Sung M., Schachter J. Role of L3T4-bearing T-cell populations in experimental murine chlamydial salpingitis. Infect Immun. 1991 Oct;59(10):3774–3777. doi: 10.1128/iai.59.10.3774-3777.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mabey D., Bailey R. Immunity to Chlamydia trachomatis: lessons from a Gambian village. J Med Microbiol. 1996 Jul;45(1):1–2. doi: 10.1099/00222615-45-1-1. [DOI] [PubMed] [Google Scholar]
  14. Magee D. M., Williams D. M., Smith J. G., Bleicker C. A., Grubbs B. G., Schachter J., Rank R. G. Role of CD8 T cells in primary Chlamydia infection. Infect Immun. 1995 Feb;63(2):516–521. doi: 10.1128/iai.63.2.516-521.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mombaerts P., Clarke A. R., Rudnicki M. A., Iacomini J., Itohara S., Lafaille J. J., Wang L., Ichikawa Y., Jaenisch R., Hooper M. L. Mutations in T-cell antigen receptor genes alpha and beta block thymocyte development at different stages. Nature. 1992 Nov 19;360(6401):225–231. doi: 10.1038/360225a0. [DOI] [PubMed] [Google Scholar]
  16. Mombaerts P., Iacomini J., Johnson R. S., Herrup K., Tonegawa S., Papaioannou V. E. RAG-1-deficient mice have no mature B and T lymphocytes. Cell. 1992 Mar 6;68(5):869–877. doi: 10.1016/0092-8674(92)90030-g. [DOI] [PubMed] [Google Scholar]
  17. Morrison R. P., Feilzer K., Tumas D. B. Gene knockout mice establish a primary protective role for major histocompatibility complex class II-restricted responses in Chlamydia trachomatis genital tract infection. Infect Immun. 1995 Dec;63(12):4661–4668. doi: 10.1128/iai.63.12.4661-4668.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mosmann T. R., Sad S. The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today. 1996 Mar;17(3):138–146. doi: 10.1016/0167-5699(96)80606-2. [DOI] [PubMed] [Google Scholar]
  19. Nagasawa H., Hisaeda H., Maekawa Y., Fujioka H., Ito Y., Aikawa M., Himeno K. gamma delta T cells play a crucial role in the expression of 65,000 MW heat-shock protein in mice immunized with Toxoplasma antigen. Immunology. 1994 Nov;83(3):347–352. [PMC free article] [PubMed] [Google Scholar]
  20. Perry L. L., Feilzer K., Caldwell H. D. Immunity to Chlamydia trachomatis is mediated by T helper 1 cells through IFN-gamma-dependent and -independent pathways. J Immunol. 1997 Apr 1;158(7):3344–3352. [PubMed] [Google Scholar]
  21. 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]
  22. Santos Lima E. C., Minoprio P. Chagas' disease is attenuated in mice lacking gamma delta T cells. Infect Immun. 1996 Jan;64(1):215–221. doi: 10.1128/iai.64.1.215-221.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Skeen M. J., Ziegler H. K. Intercellular interactions and cytokine responsiveness of peritoneal alpha/beta and gamma/delta T cells from Listeria-infected mice: synergistic effects of interleukin 1 and 7 on gamma/delta T cells. J Exp Med. 1993 Sep 1;178(3):985–996. doi: 10.1084/jem.178.3.985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Su H., Caldwell H. D. CD4+ T cells play a significant role in adoptive immunity to Chlamydia trachomatis infection of the mouse genital tract. Infect Immun. 1995 Sep;63(9):3302–3308. doi: 10.1128/iai.63.9.3302-3308.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tuffrey M., Alexander F., Woods C., Taylor-Robinson D. Genetic susceptibility to chlamydial salpingitis and subsequent infertility in mice. J Reprod Fertil. 1992 May;95(1):31–38. doi: 10.1530/jrf.0.0950031. [DOI] [PubMed] [Google Scholar]
  27. Williams D. M., Grubbs B. G., Kelly K., Pack E., Rank R. G. Role of gamma-delta T cells in murine Chlamydia trachomatis infection. Infect Immun. 1996 Sep;64(9):3916–3919. doi: 10.1128/iai.64.9.3916-3919.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Williams D. M., Schachter J., Drutz D. J., Sumaya C. V. Pneumonia due to Chlamydia trachomatis in the immunocompromised (nude) mouse. J Infect Dis. 1981 Feb;143(2):238–241. doi: 10.1093/infdis/143.2.238. [DOI] [PubMed] [Google Scholar]
  29. Williams D. M., Schachter J. Role of cell-mediated immunity in chlamydial infection: implications for ocular immunity. Rev Infect Dis. 1985 Nov-Dec;7(6):754–759. doi: 10.1093/clinids/7.6.754. [DOI] [PubMed] [Google Scholar]
  30. Yamamoto S., Russ F., Teixeira H. C., Conradt P., Kaufmann S. H. Listeria monocytogenes-induced gamma interferon secretion by intestinal intraepithelial gamma/delta T lymphocytes. Infect Immun. 1993 May;61(5):2154–2161. doi: 10.1128/iai.61.5.2154-2161.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Yang X., Gieni R. S., Mosmann T. R., HayGlass K. T. Chemically modified antigen preferentially elicits induction of Th1-like cytokine synthesis patterns in vivo. J Exp Med. 1993 Jul 1;178(1):349–353. doi: 10.1084/jem.178.1.349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Yang X., HayGlass K. T., Brunham R. C. Genetically determined differences in IL-10 and IFN-gamma responses correlate with clearance of Chlamydia trachomatis mouse pneumonitis infection. J Immunol. 1996 Jun 1;156(11):4338–4344. [PubMed] [Google Scholar]

Articles from Immunology are provided here courtesy of British Society for Immunology

RESOURCES