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. 1993 Nov;80(3):388–394.

Gamma delta T-cell lines isolated from intestinal epithelium respond to a B-cell lymphoma.

Y Sano 1, E Dudley 1, S Carding 1, R H Lin 1, A C Hayday 1, C A Janeway Jr 1
PMCID: PMC1422228  PMID: 8288315

Abstract

gamma delta T-cell hybrid clones were obtained from intestinal intraepithelial lymphocytes (i-IEL) by fusion with the BW5147 thymoma line. Four clones which expressed different V gamma/V delta genes were selected for further study. All of the gamma delta clones secreted interleukin-2 (IL-2) in the presence of the BALB/c-derived B-lymphoma line, A20. No alpha beta T-cell hybrid clones derived from spleen or i-IEL responded to A20. We obtained several pieces of evidence which strongly suggest that these responses are mediated by the gamma delta T-cell receptor (TcR). Class II major histocompatibility complex (MHC), FcR and surface Ig expressed on A20 are not involved in the response. Native i-IEL derived from BALB/c selectively survive in culture in the presence of A20 cells. The ligand may be a superantigen-like molecule because all our gamma delta T-cell clones responded to A20 in spite of their different combinations of V gamma/V delta gene segments.

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Selected References

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  1. Asarnow D. M., Kuziel W. A., Bonyhadi M., Tigelaar R. E., Tucker P. W., Allison J. P. Limited diversity of gamma delta antigen receptor genes of Thy-1+ dendritic epidermal cells. Cell. 1988 Dec 2;55(5):837–847. doi: 10.1016/0092-8674(88)90139-0. [DOI] [PubMed] [Google Scholar]
  2. Band H., Panchamoorthy G., Mclean J., Morita C. T., Ishikawa S., Modlin R., Brenner M. B. Recognition of mycobacterial antigens by gamma delta T cells. Res Immunol. 1990 Sep;141(7):645–651. doi: 10.1016/0923-2494(90)90075-a. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Bonneville M., Ito K., Krecko E. G., Itohara S., Kappes D., Ishida I., Kanagawa O., Janeway C. A., Murphy D. B., Tonegawa S. Recognition of a self major histocompatibility complex TL region product by gamma delta T-cell receptors. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5928–5932. doi: 10.1073/pnas.86.15.5928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cole B. C., Daynes R. A., Ward J. R. Stimulation of mouse lymphocytes by a mitogen derived from Mycoplasma arthritidis. I. Transformation is associated with an H-2-linked gene that maps to the I-E/I-C subregion. J Immunol. 1981 Nov;127(5):1931–1936. [PubMed] [Google Scholar]
  6. Davies M. D., Parrott D. M. Preparation and purification of lymphocytes from the epithelium and lamina propria of murine small intestine. Gut. 1981 Jun;22(6):481–488. doi: 10.1136/gut.22.6.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fisch P., Malkovsky M., Kovats S., Sturm E., Braakman E., Klein B. S., Voss S. D., Morrissey L. W., DeMars R., Welch W. J. Recognition by human V gamma 9/V delta 2 T cells of a GroEL homolog on Daudi Burkitt's lymphoma cells. Science. 1990 Nov 30;250(4985):1269–1273. doi: 10.1126/science.1978758. [DOI] [PubMed] [Google Scholar]
  8. Fleischer B., Schrezenmeier H. T cell stimulation by staphylococcal enterotoxins. Clonally variable response and requirement for major histocompatibility complex class II molecules on accessory or target cells. J Exp Med. 1988 May 1;167(5):1697–1707. doi: 10.1084/jem.167.5.1697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Frankel W. N., Rudy C., Coffin J. M., Huber B. T. Linkage of Mls genes to endogenous mammary tumour viruses of inbred mice. Nature. 1991 Feb 7;349(6309):526–528. doi: 10.1038/349526a0. [DOI] [PubMed] [Google Scholar]
  10. Harwell L., Skidmore B., Marrack P., Kappler J. Concanavalin A-inducible, interleukin-2-producing T cell hybridoma. J Exp Med. 1980 Oct 1;152(4):893–904. doi: 10.1084/jem.152.4.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Itohara S., Farr A. G., Lafaille J. J., Bonneville M., Takagaki Y., Haas W., Tonegawa S. Homing of a gamma delta thymocyte subset with homogeneous T-cell receptors to mucosal epithelia. Nature. 1990 Feb 22;343(6260):754–757. doi: 10.1038/343754a0. [DOI] [PubMed] [Google Scholar]
  13. Itohara S., Nakanishi N., Kanagawa O., Kubo R., Tonegawa S. Monoclonal antibodies specific to native murine T-cell receptor gamma delta: analysis of gamma delta T cells during thymic ontogeny and in peripheral lymphoid organs. Proc Natl Acad Sci U S A. 1989 Jul;86(13):5094–5098. doi: 10.1073/pnas.86.13.5094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Janeway C. A., Jr, Jones B., Hayday A. Specificity and function of T cells bearing gamma delta receptors. Immunol Today. 1988 Mar;9(3):73–76. doi: 10.1016/0167-5699(88)91267-4. [DOI] [PubMed] [Google Scholar]
  15. Janeway C. A., Jr, Yagi J., Conrad P. J., Katz M. E., Jones B., Vroegop S., Buxser S. T-cell responses to Mls and to bacterial proteins that mimic its behavior. Immunol Rev. 1989 Feb;107:61–88. doi: 10.1111/j.1600-065x.1989.tb00003.x. [DOI] [PubMed] [Google Scholar]
  16. Jenkins M. K., Pardoll D. M., Mizuguchi J., Quill H., Schwartz R. H. T-cell unresponsiveness in vivo and in vitro: fine specificity of induction and molecular characterization of the unresponsive state. Immunol Rev. 1987 Feb;95:113–135. doi: 10.1111/j.1600-065x.1987.tb00502.x. [DOI] [PubMed] [Google Scholar]
  17. Kaye J., Janeway C. A., Jr The Fab fragment of a directly activating monoclonal antibody that precipitates a disulfide-linked heterodimer from a helper T cell clone blocks activation by either allogeneic Ia or antigen and self-Ia. J Exp Med. 1984 May 1;159(5):1397–1412. doi: 10.1084/jem.159.5.1397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Koning F., Stingl G., Yokoyama W. M., Yamada H., Maloy W. L., Tschachler E., Shevach E. M., Coligan J. E. Identification of a T3-associated gamma delta T cell receptor on Thy-1+ dendritic epidermal Cell lines. Science. 1987 May 15;236(4803):834–837. doi: 10.1126/science.2883729. [DOI] [PubMed] [Google Scholar]
  19. Lefrancois L., LeCorre R., Mayo J., Bluestone J. A., Goodman T. Extrathymic selection of TCR gamma delta + T cells by class II major histocompatibility complex molecules. Cell. 1990 Oct 19;63(2):333–340. doi: 10.1016/0092-8674(90)90166-c. [DOI] [PubMed] [Google Scholar]
  20. Liu Y., Janeway C. A., Jr Microbial induction of co-stimulatory activity for CD4 T-cell growth. Int Immunol. 1991 Apr;3(4):323–332. doi: 10.1093/intimm/3.4.323. [DOI] [PubMed] [Google Scholar]
  21. Marrack P., Kappler J. The staphylococcal enterotoxins and their relatives. Science. 1990 May 11;248(4956):705–711. doi: 10.1126/science.2185544. [DOI] [PubMed] [Google Scholar]
  22. McVay L. D., Carding S. R., Bottomly K., Hayday A. C. Regulated expression and structure of T cell receptor gamma/delta transcripts in human thymic ontogeny. EMBO J. 1991 Jan;10(1):83–91. doi: 10.1002/j.1460-2075.1991.tb07923.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Munk M. E., Schoel B., Modrow S., Karr R. W., Young R. A., Kaufmann S. H. T lymphocytes from healthy individuals with specificity to self-epitopes shared by the mycobacterial and human 65-kilodalton heat shock protein. J Immunol. 1989 Nov 1;143(9):2844–2849. [PubMed] [Google Scholar]
  24. 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]
  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. Porcelli S., Morita C. T., Brenner M. B. CD1b restricts the response of human CD4-8- T lymphocytes to a microbial antigen. Nature. 1992 Dec 10;360(6404):593–597. doi: 10.1038/360593a0. [DOI] [PubMed] [Google Scholar]
  27. Richman A., Hayday A. Serum-inducible expression of transfected human c-myc genes. Mol Cell Biol. 1989 Nov;9(11):4962–4969. doi: 10.1128/mcb.9.11.4962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rippmann F., Taylor W. R., Rothbard J. B., Green N. M. A hypothetical model for the peptide binding domain of hsp70 based on the peptide binding domain of HLA. EMBO J. 1991 May;10(5):1053–1059. doi: 10.1002/j.1460-2075.1991.tb08044.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rust C. J., Verreck F., Vietor H., Koning F. Specific recognition of staphylococcal enterotoxin A by human T cells bearing receptors with the V gamma 9 region. Nature. 1990 Aug 9;346(6284):572–574. doi: 10.1038/346572a0. [DOI] [PubMed] [Google Scholar]
  30. Stadler B. M., Dougherty S. F., Farrar J. J., Oppenheim J. J. Relationship of cell cycle to recovery of IL 2 activity from human mononuclear cells, human and mouse T cell lines. J Immunol. 1981 Nov;127(5):1936–1940. [PubMed] [Google Scholar]
  31. Takagaki Y., DeCloux A., Bonneville M., Tonegawa S. Diversity of gamma delta T-cell receptors on murine intestinal intra-epithelial lymphocytes. Nature. 1989 Jun 29;339(6227):712–714. doi: 10.1038/339712a0. [DOI] [PubMed] [Google Scholar]
  32. Toneguzzo F., Glynn S., Levi E., Mjolsness S., Hayday A. Use of a chemically modified T7 DNA polymerase for manual and automated sequencing of supercoiled DNA. Biotechniques. 1988 May;6(5):460–469. [PubMed] [Google Scholar]
  33. Viney J. L., MacDonald T. T. Selective death of T cell receptor gamma/delta+ intraepithelial lymphocytes by apoptosis. Eur J Immunol. 1990 Dec;20(12):2809–2812. doi: 10.1002/eji.1830201242. [DOI] [PubMed] [Google Scholar]
  34. White J., Blackman M., Bill J., Kappler J., Marrack P., Gold D. P., Born W. Two better cell lines for making hybridomas expressing specific T cell receptors. J Immunol. 1989 Sep 15;143(6):1822–1825. [PubMed] [Google Scholar]
  35. Zijlstra M., Bix M., Simister N. E., Loring J. M., Raulet D. H., Jaenisch R. Beta 2-microglobulin deficient mice lack CD4-8+ cytolytic T cells. Nature. 1990 Apr 19;344(6268):742–746. doi: 10.1038/344742a0. [DOI] [PubMed] [Google Scholar]

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