Skip to main content
PMC home page
Immunology logoLink to Immunology
. 1996 May;88(1):116–123. doi: 10.1046/j.1365-2567.1996.d01-649.x

Modulation of WC1, a lineage-specific cell surface molecule of gamma/delta T cells augments cellular proliferation.

M D Hanby-Flarida 1, O J Trask 1, T J Yang 1, C L Baldwin 1
PMCID: PMC1456450  PMID: 8707336

Abstract

WC1, also known as T19, is the only unique gamma/delta T-cell differentiation antigen described to date other than the gamma/delta T-cell receptor. We present evidence that modulation of WC1 results in augmented proliferation of gamma/delta T cells. Immobilized IL-A29, a monoclonal antibody (mAb) specific for WC1, augmented proliferation of gamma/delta T cells in the autologous mixed leucocyte reaction (AMLR) as well as proliferation induced by either anti-CD3 or anti-CD5 mAb. In contrast, anti-CD5 mAb did not increase proliferation in the AMLR even though both CD5 and WC1 are members of the scavenger receptor cysteine-rich family of proteins and are expressed by bovine peripheral blood gamma/delta T cells. IL-A29 did not induce proliferation when assessed alone or in the presence of either phorbol myristate acetate (PMA) or interleukin-2. IL-A29 also did not induce detectable calcium mobilization when evaluated in the presence of monocytes, PMA, or following cross-linking of IL-A29 with anti-immunoglobulin antibody. We conclude that WC1 is a gamma/delta T-cell lineage-specific cell-surface differentiation antigen which is involved in activation of gamma/delta T cells using an as yet unidentified pathway.

Full text

PDF
116

Images in this article

119Figure 1
on p.119

Selected References

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

  1. Alberola-Ila J., Places L., Cantrell D. A., Vives J., Lozano F. Intracellular events involved in CD5-induced human T cell activation and proliferation. J Immunol. 1992 Mar 1;148(5):1287–1293. [PubMed] [Google Scholar]
  2. Baldwin C. L., Machugh N. D., Ellis J. A., Naessens J., Newson J., Morrison W. I. Monoclonal antibodies which react with bovine T-lymphocyte antigens and induce blastogenesis: tissue distribution and functional characteristics of the target antigens. Immunology. 1988 Mar;63(3):439–446. [PMC free article] [PubMed] [Google Scholar]
  3. Baldwin C. L., Teale A. J., Naessens J. G., Goddeeris B. M., MacHugh N. D., Morrison W. I. Characterization of a subset of bovine T lymphocytes that express BoT4 by monoclonal antibodies and function: similarity to lymphocytes defined by human T4 and murine L3T4. J Immunol. 1986 Jun 15;136(12):4385–4391. [PubMed] [Google Scholar]
  4. Bank I., DePinho R. A., Brenner M. B., Cassimeris J., Alt F. W., Chess L. A functional T3 molecule associated with a novel heterodimer on the surface of immature human thymocytes. Nature. 1986 Jul 10;322(6075):179–181. doi: 10.1038/322179a0. [DOI] [PubMed] [Google Scholar]
  5. Borst J., van de Griend R. J., van Oostveen J. W., Ang S. L., Melief C. J., Seidman J. G., Bolhuis R. L. A T-cell receptor gamma/CD3 complex found on cloned functional lymphocytes. Nature. 1987 Feb 19;325(6106):683–688. doi: 10.1038/325683a0. [DOI] [PubMed] [Google Scholar]
  6. Clevers H., MacHugh N. D., Bensaid A., Dunlap S., Baldwin C. L., Kaushal A., Iams K., Howard C. J., Morrison W. I. Identification of a bovine surface antigen uniquely expressed on CD4-CD8- T cell receptor gamma/delta+ T lymphocytes. Eur J Immunol. 1990 Apr;20(4):809–817. doi: 10.1002/eji.1830200415. [DOI] [PubMed] [Google Scholar]
  7. Ellis J. A., Baldwin C. L., MacHugh N. D., Bensaid A., Teale A. J., Goddeeris B. M., Morrison W. I. Characterization by a monoclonal antibody and functional analysis of a subset of bovine T lymphocytes that express BoT8, a molecule analogous to human CD8. Immunology. 1986 Jul;58(3):351–358. [PMC free article] [PubMed] [Google Scholar]
  8. Gangemi R. M., Swack J. A., Gaviria D. M., Romain P. L. Anti-T12, an anti-CD6 monoclonal antibody, can activate human T lymphocytes. J Immunol. 1989 Oct 15;143(8):2439–2447. [PubMed] [Google Scholar]
  9. Gay D., Maddon P., Sekaly R., Talle M. A., Godfrey M., Long E., Goldstein G., Chess L., Axel R., Kappler J. Functional interaction between human T-cell protein CD4 and the major histocompatibility complex HLA-DR antigen. Nature. 1987 Aug 13;328(6131):626–629. doi: 10.1038/328626a0. [DOI] [PubMed] [Google Scholar]
  10. Goddeeris B. M., Baldwin C. L., ole-MoiYoi O., Morrison W. I. Improved methods for purification and depletion of monocytes from bovine peripheral blood mononuclear cells. Functional evaluation of monocytes in responses to lectins. J Immunol Methods. 1986 May 22;89(2):165–173. doi: 10.1016/0022-1759(86)90354-6. [DOI] [PubMed] [Google Scholar]
  11. Haas W., Pereira P., Tonegawa S. Gamma/delta cells. Annu Rev Immunol. 1993;11:637–685. doi: 10.1146/annurev.iy.11.040193.003225. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Inghirami G., Zhu B. Y., Chess L., Knowles D. M. Flow cytometric and immunohistochemical characterization of the gamma/delta T-lymphocyte population in normal human lymphoid tissue and peripheral blood. Am J Pathol. 1990 Feb;136(2):357–367. [PMC free article] [PubMed] [Google Scholar]
  14. June C. H., Ledbetter J. A., Linsley P. S., Thompson C. B. Role of the CD28 receptor in T-cell activation. Immunol Today. 1990 Jun;11(6):211–216. doi: 10.1016/0167-5699(90)90085-n. [DOI] [PubMed] [Google Scholar]
  15. June C. H., Rabinovitch P. S. Flow cytometric measurement of cellular ionized calcium concentration. Pathol Immunopathol Res. 1988;7(5):409–432. doi: 10.1159/000157133. [DOI] [PubMed] [Google Scholar]
  16. Lalor P. A., Morrison W. I., Goddeeris B. M., Jack R. M., Black S. J. Monoclonal antibodies identify phenotypically and functionally distinct cell types in the bovine lymphoid system. Vet Immunol Immunopathol. 1986 Sep;13(1-2):121–140. doi: 10.1016/0165-2427(86)90054-1. [DOI] [PubMed] [Google Scholar]
  17. Ledbetter J. A., Martin P. J., Spooner C. E., Wofsy D., Tsu T. T., Beatty P. G., Gladstone P. Antibodies to Tp67 and Tp44 augment and sustain proliferative responses of activated T cells. J Immunol. 1985 Oct;135(4):2331–2336. [PubMed] [Google Scholar]
  18. Mackay C. R., Beya M. F., Matzinger P. Gamma/delta T cells express a unique surface molecule appearing late during thymic development. Eur J Immunol. 1989 Aug;19(8):1477–1483. doi: 10.1002/eji.1830190820. [DOI] [PubMed] [Google Scholar]
  19. Mackay C. R., Maddox J. F., Brandon M. R. Three distinct subpopulations of sheep T lymphocytes. Eur J Immunol. 1986 Jan;16(1):19–25. doi: 10.1002/eji.1830160105. [DOI] [PubMed] [Google Scholar]
  20. Morimoto C., Rudd C. E., Letvin N. L., Hagan M., Schlossman S. F. 2H1--a novel antigen involved in T lymphocyte triggering. J Immunol. 1988 Apr 1;140(7):2165–2170. [PubMed] [Google Scholar]
  21. Newell M. K., Haughn L. J., Maroun C. R., Julius M. H. Death of mature T cells by separate ligation of CD4 and the T-cell receptor for antigen. Nature. 1990 Sep 20;347(6290):286–289. doi: 10.1038/347286a0. [DOI] [PubMed] [Google Scholar]
  22. Penninger J., Kishihara K., Molina T., Wallace V. A., Timms E., Hedrick S. M., Mak T. W. Requirement for tyrosine kinase p56lck for thymic development of transgenic gamma delta T cells. Science. 1993 Apr 16;260(5106):358–361. doi: 10.1126/science.8469988. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Rabinovitch P. S., June C. H., Grossmann A., Ledbetter J. A. Heterogeneity among T cells in intracellular free calcium responses after mitogen stimulation with PHA or anti-CD3. Simultaneous use of indo-1 and immunofluorescence with flow cytometry. J Immunol. 1986 Aug 1;137(3):952–961. [PubMed] [Google Scholar]
  25. Ratcliffe M. J., Coggeshall K. M., Newell M. K., Julius M. H. T cell receptor aggregation, but not dimerization, induces increased cytosolic calcium concentrations and reveals a lack of stable association between CD4 and the T cell receptor. J Immunol. 1992 Mar 15;148(6):1643–1651. [PubMed] [Google Scholar]
  26. Rubinstein S., Familletti P. C., Pestka S. Convenient assay for interferons. J Virol. 1981 Feb;37(2):755–758. doi: 10.1128/jvi.37.2.755-758.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rudd C. E., Trevillyan J. M., Dasgupta J. D., Wong L. L., Schlossman S. F. The CD4 receptor is complexed in detergent lysates to a protein-tyrosine kinase (pp58) from human T lymphocytes. Proc Natl Acad Sci U S A. 1988 Jul;85(14):5190–5194. doi: 10.1073/pnas.85.14.5190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Shimonkevitz R., Luescher B., Cerottini J. C., MacDonald H. R. Clonal analysis of cytolytic T lymphocyte-mediated lysis of target cells with inducible antigen expression: correlation between antigen density and requirement for Lyt-2/3 function. J Immunol. 1985 Aug;135(2):892–899. [PubMed] [Google Scholar]
  29. Spour E. F., Leemhuis T., Jenski L., Redmond R., Fillak D., Jansen J. Characterization of normal human CD3+ CD5- and gamma delta T cell receptor positive T lymphocytes. Clin Exp Immunol. 1990 Apr;80(1):114–121. doi: 10.1111/j.1365-2249.1990.tb06450.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Strominger J. L. The gamma delta T cell receptor and class Ib MHC-related proteins: enigmatic molecules of immune recognition. Cell. 1989 Jun 16;57(6):895–898. doi: 10.1016/0092-8674(89)90326-7. [DOI] [PubMed] [Google Scholar]
  31. Suttles J., Carruth L. M., Mizel S. B. Detection of IL-1 alpha and IL-1 beta in the supernatants of paraformaldehyde-treated human monocytes. Evidence against a membrane form of IL-1. J Immunol. 1990 Jan 1;144(1):170–174. [PubMed] [Google Scholar]
  32. Van Neerven J., Coligan J. E., Koning F. Structural comparison of alpha/beta and gamma/delta T cell receptor-CD3 complexes reveals identical subunit interactions but distinct cross-linking patterns of T cell receptor chains. Eur J Immunol. 1990 Sep;20(9):2105–2111. doi: 10.1002/eji.1830200932. [DOI] [PubMed] [Google Scholar]
  33. Vandenberghe P., Ceuppens J. L. Immobilized anti-CD5 together with prolonged activation of protein kinase C induce interleukin 2-dependent T cell growth: evidence for signal transduction through CD5. Eur J Immunol. 1991 Feb;21(2):251–259. doi: 10.1002/eji.1830210203. [DOI] [PubMed] [Google Scholar]
  34. Veillette A., Bookman M. A., Horak E. M., Samelson L. E., Bolen J. B. Signal transduction through the CD4 receptor involves the activation of the internal membrane tyrosine-protein kinase p56lck. Nature. 1989 Mar 16;338(6212):257–259. doi: 10.1038/338257a0. [DOI] [PubMed] [Google Scholar]
  35. Walcheck B., Watts G., Jutila M. A. Bovine gamma/delta T cells bind E-selectin via a novel glycoprotein receptor: first characterization of a lymphocyte/E-selectin interaction in an animal model. J Exp Med. 1993 Sep 1;178(3):853–863. doi: 10.1084/jem.178.3.853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wesselborg S., Janssen O., Pechhold K., Kabelitz D. Selective activation of gamma/delta + T cell clones by single anti-CD2 antibodies. J Exp Med. 1991 Feb 1;173(2):297–304. doi: 10.1084/jem.173.2.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wijngaard P. L., Metzelaar M. J., MacHugh N. D., Morrison W. I., Clevers H. C. Molecular characterization of the WC1 antigen expressed specifically on bovine CD4-CD8- gamma delta T lymphocytes. J Immunol. 1992 Nov 15;149(10):3273–3277. [PubMed] [Google Scholar]
  38. Wilde D. B., Marrack P., Kappler J., Dialynas D. P., Fitch F. W. Evidence implicating L3T4 in class II MHC antigen reactivity; monoclonal antibody GK1.5 (anti-L3T4a) blocks class II MHC antigen-specific proliferation, release of lymphokines, and binding by cloned murine helper T lymphocyte lines. J Immunol. 1983 Nov;131(5):2178–2183. [PubMed] [Google Scholar]
  39. Williams D. J., Newson J., Naessens J. Quantitation of bovine immunoglobulin isotypes and allotypes using monoclonal antibodies. Vet Immunol Immunopathol. 1990 Mar;24(3):267–283. doi: 10.1016/0165-2427(90)90042-q. [DOI] [PubMed] [Google Scholar]
  40. Yang S. Y., Chouaib S., Dupont B. A common pathway for T lymphocyte activation involving both the CD3-Ti complex and CD2 sheep erythrocyte receptor determinants. J Immunol. 1986 Aug 15;137(4):1097–1100. [PubMed] [Google Scholar]
  41. Yang T. J., Baldwin C. L., Hanby-Flarida M., Mather J. F., Rabinovsky E. D. Monoclonal antibody BLT-1, specific for the bovine homologue of CD5, reacts with the majority of mature T cells, a subpopulation of B cells and stimulates T cell proliferation. Dev Comp Immunol. 1995 Jul-Aug;19(4):337–346. doi: 10.1016/0145-305x(95)00014-k. [DOI] [PubMed] [Google Scholar]

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

RESOURCES