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. 1995 Jan;84(1):105–110.

Interaction between gamma delta T cells and B cells regulating IgG production.

G Häcker 1, S Adam 1, H Wagner 1
PMCID: PMC1415197  PMID: 7890294

Abstract

Despite profound knowledge about the molecular structure of the gamma delta T-cell receptor (TCR), the physiological function of gamma delta T cells remains enigmatic. Participation of these cells in complex immune reactions, however, is suggested by the appearance of gamma delta T cells in sites of infectious and autoimmune-induced inflammations. Only a few in vitro models of gamma delta T-cell stimulation have been established: besides a reactivity in the presence of microbial ligands, human gamma delta T cells proliferate upon in vitro challenge with cells from an allogeneic B-lymphoblastic cell line (B-LCL). We present data here demonstrating that this reactivity is not confined to allogenic B-LCL. Autologous B-LCL are also very strong stimulators for gamma delta T cells; more important, autologous B cells can stimulate gamma delta T cells after a period of mitogen-activation but not in a resting state. This activation seems to address a subgroup of gamma delta T cells, as the percentage of V delta 1+ cells is increased after stimulation. Activated gamma delta T cells, on the other hand, are able to exert an influence on B cells by inhibiting the secretion of IgG in coculture experiments. These data define a simple regulatory circle of B cells and gamma delta T cells in vitro and propose a model for gamma delta T-cell function which could explain many in vivo observations of gamma delta T-cell activation.

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Selected References

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

  1. Amadori A., Zamarchi R., Ciminale V., Del Mistro A., Siervo S., Alberti A., Colombatti M., Chieco-Bianchi L. HIV-1-specific B cell activation. A major constituent of spontaneous B cell activation during HIV-1 infection. J Immunol. 1989 Oct 1;143(7):2146–2152. [PubMed] [Google Scholar]
  2. Bluestone J. A., Cron R. Q., Cotterman M., Houlden B. A., Matis L. A. Structure and specificity of T cell receptor gamma/delta on major histocompatibility complex antigen-specific CD3+, CD4-, CD8- T lymphocytes. J Exp Med. 1988 Nov 1;168(5):1899–1916. doi: 10.1084/jem.168.5.1899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Born W., O'Brien R. The gamma delta cell response to stress: unresolved issues and possible significance. Res Immunol. 1990 Sep;141(7):595–600. doi: 10.1016/0923-2494(90)90063-5. [DOI] [PubMed] [Google Scholar]
  4. Carding S. R., Allan W., Kyes S., Hayday A., Bottomly K., Doherty P. C. Late dominance of the inflammatory process in murine influenza by gamma/delta + T cells. J Exp Med. 1990 Oct 1;172(4):1225–1231. doi: 10.1084/jem.172.4.1225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. De Paoli P., Gennari D., Martelli P., Basaglia G., Crovatto M., Battistin S., Santini G. A subset of gamma delta lymphocytes is increased during HIV-1 infection. Clin Exp Immunol. 1991 Feb;83(2):187–191. doi: 10.1111/j.1365-2249.1991.tb05612.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Emoto M., Danbara H., Yoshikai Y. Induction of gamma/delta T cells in murine salmonellosis by an avirulent but not by a virulent strain of Salmonella choleraesuis. J Exp Med. 1992 Aug 1;176(2):363–372. doi: 10.1084/jem.176.2.363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fujihashi K., Taguchi T., Aicher W. K., McGhee J. R., Bluestone J. A., Eldridge J. H., Kiyono H. Immunoregulatory functions for murine intraepithelial lymphocytes: gamma/delta T cell receptor-positive (TCR+) T cells abrogate oral tolerance, while alpha/beta TCR+ T cells provide B cell help. J Exp Med. 1992 Mar 1;175(3):695–707. doi: 10.1084/jem.175.3.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Goerlich R., Häcker G., Pfeffer K., Heeg K., Wagner H. Plasmodium falciparum merozoites primarily stimulate the V gamma 9 subset of human gamma/delta T cells. Eur J Immunol. 1991 Oct;21(10):2613–2616. doi: 10.1002/eji.1830211045. [DOI] [PubMed] [Google Scholar]
  9. Hara T., Mizuno Y., Nagata M., Okabe Y., Taniguchi S., Harada M., Niho Y., Oshimi K., Ohga S., Yoshikai Y. Human gamma delta T-cell receptor-positive cell-mediated inhibition of erythropoiesis in vitro in a patient with type I autoimmune polyglandular syndrome and pure red blood cell aplasia. Blood. 1990 Feb 15;75(4):941–950. [PubMed] [Google Scholar]
  10. Havran W. L., Chien Y. H., Allison J. P. Recognition of self antigens by skin-derived T cells with invariant gamma delta antigen receptors. Science. 1991 Jun 7;252(5011):1430–1432. doi: 10.1126/science.1828619. [DOI] [PubMed] [Google Scholar]
  11. Holoshitz J., Koning F., Coligan J. E., De Bruyn J., Strober S. Isolation of CD4- CD8- mycobacteria-reactive T lymphocyte clones from rheumatoid arthritis synovial fluid. Nature. 1989 May 18;339(6221):226–229. doi: 10.1038/339226a0. [DOI] [PubMed] [Google Scholar]
  12. Holoshitz J. Potential role of gamma delta T cells in autoimmune diseases. Res Immunol. 1990 Sep;141(7):651–657. doi: 10.1016/0923-2494(90)90076-b. [DOI] [PubMed] [Google Scholar]
  13. Howard C. J., Sopp P., Parsons K. R., Finch J. In vivo depletion of BoT4 (CD4) and of non-T4/T8 lymphocyte subsets in cattle with monoclonal antibodies. Eur J Immunol. 1989 Apr;19(4):757–764. doi: 10.1002/eji.1830190428. [DOI] [PubMed] [Google Scholar]
  14. Häcker G., Kromer S., Falk M., Heeg K., Wagner H., Pfeffer K. V delta 1+ subset of human gamma delta T cells responds to ligands expressed by EBV-infected Burkitt lymphoma cells and transformed B lymphocytes. J Immunol. 1992 Dec 15;149(12):3984–3989. [PubMed] [Google Scholar]
  15. Häcker G., Kromer S., Heeg K., Ivanyi J., Wagner H., Pfeffer K. Opportunist mycobacteria express ligands that stimulate production of human V gamma 9V delta 2 T lymphocytes. Infect Immun. 1992 Jul;60(7):2753–2757. doi: 10.1128/iai.60.7.2753-2757.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Janeway C. A., Jr Gamma delta T cells: research on the frontlines of defence. Res Immunol. 1990 Sep;141(7):688–695. doi: 10.1016/0923-2494(90)90094-f. [DOI] [PubMed] [Google Scholar]
  17. Kabelitz D., Bender A., Prospero T., Wesselborg S., Janssen O., Pechhold K. The primary response of human gamma/delta + T cells to Mycobacterium tuberculosis is restricted to V gamma 9-bearing cells. J Exp Med. 1991 Jun 1;173(6):1331–1338. doi: 10.1084/jem.173.6.1331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kabelitz D., Bender A., Schondelmaier S., Schoel B., Kaufmann S. H. A large fraction of human peripheral blood gamma/delta + T cells is activated by Mycobacterium tuberculosis but not by its 65-kD heat shock protein. J Exp Med. 1990 Mar 1;171(3):667–679. doi: 10.1084/jem.171.3.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kabelitz D., Pechhold K., Bender A., Wesselborg S., Wesch D., Friese K., Janssen O. Activation and activation-driven death of human gamma/delta T cells. Immunol Rev. 1991 Apr;120:71–88. doi: 10.1111/j.1600-065x.1991.tb00588.x. [DOI] [PubMed] [Google Scholar]
  20. McClure S. J., Emery D. L., Wagland B. M., Jones W. O. A serial study of rejection of Trichostrongylus colubriformis by immune sheep. Int J Parasitol. 1992 Apr;22(2):227–234. doi: 10.1016/0020-7519(92)90106-u. [DOI] [PubMed] [Google Scholar]
  21. McMenamin C., Oliver J., Girn B., Holt B. J., Kees U. R., Thomas W. R., Holt P. G. Regulation of T-cell sensitization at epithelial surfaces in the respiratory tract: suppression of IgE responses to inhaled antigens by CD3+ Tcr alpha-/beta- lymphocytes (putative gamma/delta T cells). Immunology. 1991 Oct;74(2):234–239. [PMC free article] [PubMed] [Google Scholar]
  22. Mizuma H., Litwin S., Zolla-Pazner S. B-cell activation in HIV infection: relationship of spontaneous immunoglobulin secretion to various immunological parameters. Clin Exp Immunol. 1988 Mar;71(3):410–416. [PMC free article] [PubMed] [Google Scholar]
  23. O'Brien R. L., Happ M. P., Dallas A., Palmer E., Kubo R., Born W. K. Stimulation of a major subset of lymphocytes expressing T cell receptor gamma delta by an antigen derived from Mycobacterium tuberculosis. Cell. 1989 May 19;57(4):667–674. doi: 10.1016/0092-8674(89)90135-9. [DOI] [PubMed] [Google Scholar]
  24. Pfeffer K., Schoel B., Gulle H., Kaufmann S. H., Wagner H. Primary responses of human T cells to mycobacteria: a frequent set of gamma/delta T cells are stimulated by protease-resistant ligands. Eur J Immunol. 1990 May;20(5):1175–1179. doi: 10.1002/eji.1830200534. [DOI] [PubMed] [Google Scholar]
  25. Porcelli S., Brenner M. B., Greenstein J. L., Balk S. P., Terhorst C., Bleicher P. A. Recognition of cluster of differentiation 1 antigens by human CD4-CD8-cytolytic T lymphocytes. Nature. 1989 Oct 5;341(6241):447–450. doi: 10.1038/341447a0. [DOI] [PubMed] [Google Scholar]
  26. Quere P., Cooper M. D., Thorbecke G. J. Characterization of suppressor T cells for antibody production by chicken spleen cells. I. Antigen-induced suppressor cells are CT8+, TcR1+ (gamma delta) T cells. Immunology. 1990 Dec;71(4):517–522. [PMC free article] [PubMed] [Google Scholar]
  27. Roberts K., Shevach E. M. Immunoregulatory role of gamma delta T cells. Ann N Y Acad Sci. 1991 Dec 30;636:1–8. doi: 10.1111/j.1749-6632.1991.tb33432.x. [DOI] [PubMed] [Google Scholar]
  28. Roberts K., Yokoyama W. M., Kehn P. J., Shevach E. M. The vitronectin receptor serves as an accessory molecule for the activation of a subset of gamma/delta T cells. J Exp Med. 1991 Jan 1;173(1):231–240. doi: 10.1084/jem.173.1.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rust C., Peña S., Kluin P., Koning F. Gamma delta T cells in coeliac disease. Res Immunol. 1990 Sep;141(7):668–671. doi: 10.1016/0923-2494(90)90079-e. [DOI] [PubMed] [Google Scholar]
  30. Saito H., Kranz D. M., Takagaki Y., Hayday A. C., Eisen H. N., Tonegawa S. Complete primary structure of a heterodimeric T-cell receptor deduced from cDNA sequences. 1984 Jun 28-Jul 4Nature. 309(5971):757–762. doi: 10.1038/309757a0. [DOI] [PubMed] [Google Scholar]
  31. Schild H., Mavaddat N., Litzenberger C., Ehrich E. W., Davis M. M., Bluestone J. A., Matis L., Draper R. K., Chien Y. H. The nature of major histocompatibility complex recognition by gamma delta T cells. Cell. 1994 Jan 14;76(1):29–37. doi: 10.1016/0092-8674(94)90170-8. [DOI] [PubMed] [Google Scholar]
  32. Spits H. Human T cell receptor gamma delta + T cells. Semin Immunol. 1991 Mar;3(2):119–129. [PubMed] [Google Scholar]
  33. Taguchi T., Aicher W. K., Fujihashi K., Yamamoto M., McGhee J. R., Bluestone J. A., Kiyono H. Novel function for intestinal intraepithelial lymphocytes. Murine CD3+, gamma/delta TCR+ T cells produce IFN-gamma and IL-5. J Immunol. 1991 Dec 1;147(11):3736–3744. [PubMed] [Google Scholar]
  34. Tonegawa S., Berns A., Bonneville M., Farr A., Ishida I., Ito K., Itohara S., Janeway C. A., Jr, Kanagawa O., Katsuki M. Diversity, development, ligands, and probable functions of gamma delta T cells. Cold Spring Harb Symp Quant Biol. 1989;54(Pt 1):31–44. doi: 10.1101/sqb.1989.054.01.005. [DOI] [PubMed] [Google Scholar]
  35. Uyemura K., Deans R. J., Band H., Ohmen J., Panchamoorthy G., Morita C. T., Rea T. H., Modlin R. L. Evidence for clonal selection of gamma/delta T cells in response to a human pathogen. J Exp Med. 1991 Sep 1;174(3):683–692. doi: 10.1084/jem.174.3.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Vidović D., Roglić M., McKune K., Guerder S., MacKay C., Dembić Z. Qa-1 restricted recognition of foreign antigen by a gamma delta T-cell hybridoma. Nature. 1989 Aug 24;340(6235):646–650. doi: 10.1038/340646a0. [DOI] [PubMed] [Google Scholar]
  37. Vroom T. M., Scholte G., Ossendorp F., Borst J. Tissue distribution of human gamma delta T cells: no evidence for general epithelial tropism. J Clin Pathol. 1991 Dec;44(12):1012–1017. doi: 10.1136/jcp.44.12.1012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. van Vlasselaer P., Gascan H., de Waal Malefyt R., de Vries J. E. IL-2 and a contact-mediated signal provided by TCR alpha beta + or TCR gamma delta + CD4+ T cells induce polyclonal Ig production by committed human B cells. Enhancement by IL-5, specific inhibition of IgA synthesis by IL-4. J Immunol. 1992 Mar 15;148(6):1674–1684. [PubMed] [Google Scholar]

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