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. 1977 Jul 1;146(1):184–200. doi: 10.1084/jem.146.1.184

Functional analysis of two human T-cell subpopulations: help and suppression of B-cell responses by T cells bearing receptors for IgM or IgG

PMCID: PMC2180738  PMID: 301544

Abstract

Subpopulations of thymus-derived T lymphocytes bearing receptors for either IgM or IgG molecules were isolated from human peripheral blood. Those with receptors for IgM (T.M) provided help in a cell dose- dependent fashion for the pokeweed mitogen-induced differentiation of B lymphocytes in vitro, whereas cells with receptors for IgG (T.G) did not. T.G cells, on the hand, efficiently suppressed the differentiation and proliferation of B cells in the pokeweed system in the presence of helper T.M cells. This suppressive activity of T.G cells required prior interaction of the T.G cells with immune complexes. The helper activity of T.M cells was relatively radioresistant while the suppressor activity of T.G cells was radiosensitive. The results indicate that helper and suppressor functions of human T lymphocytes in this model system are mediated by different subpopulations of T cells which can be distinguished by their ability to bind IgM or IgG immune complexes, respectively.

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Selected References

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

  1. Anderson C. L., Grey H. M. Receptors for aggregated IgG on mouse lymphocytes: their presence on thymocytes, thymus-derived, and bone marrow-derived lymphocytes. J Exp Med. 1974 May 1;139(5):1175–1188. doi: 10.1084/jem.139.5.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bentwich Z., Douglas S. D., Skutelsky E., Kunkel H. G. Sheep red cell binding to human lymphocytes treated with neuraminidase; enhancement of T cell binding and identification of a subpopulation of B cells. J Exp Med. 1973 Jun 1;137(6):1532–1537. doi: 10.1084/jem.137.6.1532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boyle W. An extension of the 51Cr-release assay for the estimation of mouse cytotoxins. Transplantation. 1968 Sep;6(6):761–764. doi: 10.1097/00007890-196809000-00002. [DOI] [PubMed] [Google Scholar]
  4. Brown G., Greaves M. F. Cell surface markers for human T and B lymphocytes. Eur J Immunol. 1974 Apr;4(4):302–310. doi: 10.1002/eji.1830040414. [DOI] [PubMed] [Google Scholar]
  5. Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl. 1968;97:77–89. [PubMed] [Google Scholar]
  6. Cantor H., Boyse E. A. Functional subclasses of T lymphocytes bearing different Ly antigens. II. Cooperation between subclasses of Ly+ cells in the generation of killer activity. J Exp Med. 1975 Jun 1;141(6):1390–1399. doi: 10.1084/jem.141.6.1390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cantor H., Boyse E. A. Functional subclasses of T-lymphocytes bearing different Ly antigens. I. The generation of functionally distinct T-cell subclasses is a differentiative process independent of antigen. J Exp Med. 1975 Jun 1;141(6):1376–1389. doi: 10.1084/jem.141.6.1376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cantor H., Simpson E., Sato V. L., Fathman C. G., Herzenberg L. A. Characterization of subpopulations of T lymphocytes. I. Separation and functional studies of peripheral T-cells binding different amounts of fluorescent anti-Thy 1.2 (theta) antibody using a fluorescence-activated cell sorter (FACS). Cell Immunol. 1975 Jan;15(1):180–196. doi: 10.1016/0008-8749(75)90174-4. [DOI] [PubMed] [Google Scholar]
  9. Chess L., MacDermott R. P., Schlossman S. F. Immunologic functions of isolated human lymphocyte subpopulations. I. Quantitative isolation of human T and B cells and response to mitogens. J Immunol. 1974 Oct;113(4):1113–1121. [PubMed] [Google Scholar]
  10. Dickler H. B., Adkinson N. F., Jr, Terry W. D. Evidence for individual human peripheral blood lymphocytes bearing both B and T cell markers. Nature. 1974 Jan 25;247(5438):213–215. doi: 10.1038/247213a0. [DOI] [PubMed] [Google Scholar]
  11. Ferrarini M., Moretta L., Abrile R., Durante M. L. Receptors for IgG molecules on human lymphocytes forming spontaneous rosettes with sheep red cells. Eur J Immunol. 1975 Jan;5(1):70–72. doi: 10.1002/eji.1830050115. [DOI] [PubMed] [Google Scholar]
  12. Ferrarini M., Moretta L., Mingari M. C., Tonda P., Pernis B. Human T cell receptor for IgM: specificity for the pentameric Fc fragment. Eur J Immunol. 1976 Jul;6(7):520–521. doi: 10.1002/eji.1830060714. [DOI] [PubMed] [Google Scholar]
  13. Ferrarini M., Tonda G. P., Risso A., Viale G. Lymphocyte membrane receptors in human lymphoid leukemias. Eur J Immunol. 1975 Feb;5(2):89–93. doi: 10.1002/eji.1830050204. [DOI] [PubMed] [Google Scholar]
  14. Geha R. S., Schneeberger E., Merler E., Rosen F. S. Heterogeneity of "acquired" or common variable agammaglobulinemia. N Engl J Med. 1974 Jul 4;291(1):1–6. doi: 10.1056/NEJM197407042910101. [DOI] [PubMed] [Google Scholar]
  15. Gershon R. K., Mokyr M. B., Mitchell M. S. Activation of suppressor T cells by tumour cells and specific antibody. Nature. 1974 Aug 16;250(467):594–596. doi: 10.1038/250594a0. [DOI] [PubMed] [Google Scholar]
  16. Gmelig-Meyling F., Van der Ham M., Ballieux R. E. Binding of IgM by human T lymphocytes. Scand J Immunol. 1976;5(5):487–495. doi: 10.1111/j.1365-3083.1976.tb00303.x. [DOI] [PubMed] [Google Scholar]
  17. Goldschneider I., Cogen R. B. Immunoglobulin molecules on the surface of activated T lymphocytes in the rat. J Exp Med. 1973 Jul 1;138(1):163–175. doi: 10.1084/jem.138.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gorczynski R., Kontiainen S., Mitchison N. A., Tigelaar R. E. Antigen--antibody complexes as blocking factors on the T lymphocyte surface. Soc Gen Physiol Ser. 1974;29:143–154. [PubMed] [Google Scholar]
  19. Greaves M., Janossy G., Doenhoff M. Selective triggering of human T and B lymphocytes in vitro by polyclonal mitogens. J Exp Med. 1974 Jul 1;140(1):1–18. doi: 10.1084/jem.140.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hirst J. A., Beverley P. C., Kisielow P., Hoffmann M. K., Oettgen H. F. Ly antigens: markers of T cell function on mouse spleen cells. J Immunol. 1975 Dec;115(6):1555–1557. [PubMed] [Google Scholar]
  21. Janossy G., Greaves M. Functional analysis of murine and human B lymphocyte subsets. Transplant Rev. 1975;24:177–236. doi: 10.1111/j.1600-065x.1975.tb00169.x. [DOI] [PubMed] [Google Scholar]
  22. Kearney J. F., Lawton A. R. B lymphocyte differentiation induced by lipopolysaccharide. I. Generation of cells synthesizing four major immunoglobulin classes. J Immunol. 1975 Sep;115(3):671–676. [PubMed] [Google Scholar]
  23. Keightley R. G., Cooper M. D., Lawton A. R. The T cell dependence of B cell differentiation induced by pokeweed mitogen. J Immunol. 1976 Nov;117(5 Pt 1):1538–1544. [PubMed] [Google Scholar]
  24. Kreth H. W., Herzenberg L. A. Fluorescence-activated cell sorting of human T and B lymphocytes. I. Direct evidence that lymphocytes with a high density of membrane-bound immunoglobulin are precursors of plasmacytes. Cell Immunol. 1974 Jun;12(3):396–406. doi: 10.1016/0008-8749(74)90096-3. [DOI] [PubMed] [Google Scholar]
  25. Lamon E. W., Andersson B., Whitten H. D., Hurst M. M., Ghanta V. IgM complex receptors on subpopulations of murine lymphocytes. J Immunol. 1976 May;116(5):1199–1203. [PubMed] [Google Scholar]
  26. Lamon E. W., Shaw M. W., Goodson S., Lidin B., Walia A. S., Fuson E. W. Antibody-dependent cell-mediated cytotoxicity in the Moloney sarcoma virus system: differential activity of IgG and IgM with different subpopulations of lymphocytes. J Exp Med. 1977 Feb 1;145(2):302–313. doi: 10.1084/jem.145.2.302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lawler S. D., Ukaejiofo E. O., Reeves B. R. Interaction of maternal and neonatal cells in mixed-lymphocyte cultures. Lancet. 1975 Dec 13;2(7946):1185–1187. doi: 10.1016/s0140-6736(75)92663-x. [DOI] [PubMed] [Google Scholar]
  28. Lee S. T., Paraskevas F. Cell surface-associated gamma globulins in lymphocytes. IV. Lack of detection of surface globulin on B-cells and acquisition of surface G globulin by T-cells during primary response. J Immunol. 1972 Dec;109(6):1262–1271. [PubMed] [Google Scholar]
  29. McBride R. A., Schierman L. W. Thymus dependency of antibody-mediated helper effect. J Immunol. 1973 Jun;110(6):1710–1712. [PubMed] [Google Scholar]
  30. McConnell I., Hurd C. M. Lymphocyte receptors. II. Receptors for rabbit IgM on human T lymphocytes. Immunology. 1976 Jun;30(6):835–839. [PMC free article] [PubMed] [Google Scholar]
  31. Moretta L., Ferrarini M., Durante M. L., Mingari M. C. Expression of a receptor for IgM by human T cells in vitro. Eur J Immunol. 1975 Aug;5(8):565–569. doi: 10.1002/eji.1830050812. [DOI] [PubMed] [Google Scholar]
  32. Moretta L., Ferrarini M., Mingari M. C., Moretta A., Webb S. R. Subpopulations of human T cells identified by receptors for immunoglobulins and mitogen responsiveness. J Immunol. 1976 Dec;117(6):2171–2174. [PubMed] [Google Scholar]
  33. Nicholas R., Sinclair S. C. Regulation of the immune response. I. Reduction in ability of specific antibody to inhibit long-lasting IgG immunological priming after removal of the Fc fragment. J Exp Med. 1969 Jun 1;129(6):1183–1201. doi: 10.1084/jem.129.6.1183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Niederhuber J. E., Frelinger J. A., Dine M. S., Shoffner P., Dugan E., Shreffler D. C. Effects of anti-Ia sera on mitogenic responses. II. Differential expression of the Ia marker on phytohemagglutinin and concanavalin A-reactive T cells. J Exp Med. 1976 Feb 1;143(2):372–381. doi: 10.1084/jem.143.2.372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Olding L. B., Oldstone B. A. Thymus-derived peripheral lymphocytes from human newborns inhibit division of their mothers' lymphocytes. J Immunol. 1976 Mar;116(3):682–686. [PubMed] [Google Scholar]
  36. Playfair J. H., Marshall-Clarke S., Hudson L. Cooperation by mouse T lymphocytes: the role of antibody in T cell specificity. Eur J Immunol. 1974 Jan;4(1):54–56. doi: 10.1002/eji.1830040114. [DOI] [PubMed] [Google Scholar]
  37. Playfair J. H. The role of antibody in T-cell responses. Clin Exp Immunol. 1974 May;17(1):1–18. [PMC free article] [PubMed] [Google Scholar]
  38. Saal J. G., Rieber E. P., Hadam M., Riethmuller G. Lymphocytes with T-cell markers cooperate with IgG antibodies in the lysis of human tumour cells. Nature. 1977 Jan 13;265(5590):158–160. doi: 10.1038/265158a0. [DOI] [PubMed] [Google Scholar]
  39. Siegal F. P., Siegal M., Good R. A. Suppression of B-cell differentiation by leukocytes from hypogammaglobulinemic patients. J Clin Invest. 1976 Jul;58(1):109–122. doi: 10.1172/JCI108439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Soteriades-Vlachos C., Gyöngyössy M. I., Playfair J. H. Rosette formation by mouse lymphocytes. III. Receptors for immunoglobulin on normal and activated T cells. Clin Exp Immunol. 1974 Oct;18(2):187–192. [PMC free article] [PubMed] [Google Scholar]
  41. Stobo J. D., Paul S., Van Scoy R. E., Hermans P. E. Suppressor thymus-derived lymphocytes in fungal infection. J Clin Invest. 1976 Feb;57(2):319–328. doi: 10.1172/JCI108283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Stout R. D., Herzenberg L. A. The Fc receptor on thymus-derived lymphocytes. I. Detection of a subpopulation of murine T lymphocytes bearing the Fc receptor. J Exp Med. 1975 Sep 1;142(3):611–621. doi: 10.1084/jem.142.3.611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Stout R. D., Herzenberg L. A. The Fc receptor on thymus-derived lymphocytes: II. Mitogen responsiveness of T lymphocytes bearing the Fc receptor. J Exp Med. 1975 Nov 1;142(5):1041–1051. doi: 10.1084/jem.142.5.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Stout R. D., Murphy D. B., McDevitt H. O., Herzenberg L. A. The Fc receptor on thymus-derived lymphocytes. IV. Inhibition of binding of antigen-antibody complexes to Fc receptor-positive T cells by anti-Ia sera. J Exp Med. 1977 Jan 1;145(1):187–203. doi: 10.1084/jem.145.1.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Stout R. D., Waksal S. D., Herzenberg L. A. The Fc receptor on thymus-derived lymphocytes. III. Mixed lymphocyte reactivity and cell-mediated lympholytic activity of Fc- and Fc+ T lymphocytes. J Exp Med. 1976 Jul 1;144(1):54–68. doi: 10.1084/jem.144.1.54. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Twomey J. J., Laughter A. H., Farrow S., Douglass C. C. Hodgkin's disease. An immunodepleting and immunosuppressive disorder. J Clin Invest. 1975 Aug;56(2):467–475. doi: 10.1172/JCI108113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Van Boxel J. A., Rosenstreich D. L. Binding of aggregated gamma-globulin to activated T lymphocytes in the guinea pig. J Exp Med. 1974 Apr 1;139(4):1002–1012. doi: 10.1084/jem.139.4.1002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Waldmann T. A., Broder S. Suppressor cells in the regulation of the immune response. Prog Clin Immunol. 1977;3:155–199. [PubMed] [Google Scholar]
  49. Waldmann T. A., Durm M., Broder S., Blackman M., Blaese R. M., Strober W. Role of suppressor T cells in pathogenesis of common variable hypogammaglobulinaemia. Lancet. 1974 Sep 14;2(7881):609–613. doi: 10.1016/s0140-6736(74)91940-0. [DOI] [PubMed] [Google Scholar]
  50. Winchester R. J., Fu S. M., Hoffman T., Kunkel H. G. IgG on lymphocyte surfaces; technical problems and the significance of a third cell population. J Immunol. 1975 Apr;114(4):1210–1212. [PubMed] [Google Scholar]
  51. Wåhlin B., Perlmann H., Perlmann P. Analysis by a plaque assay of IgG- or IgM- dependent cytolytic lymphocytes in human blood. J Exp Med. 1976 Nov 2;144(5):1375–1380. doi: 10.1084/jem.144.5.1375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Yoshida T. O., Andersson B. Evidence for a receptor recognizing antigen complexed immunoglobulin on the surface of activated mouse thymus lymphocytes. Scand J Immunol. 1972;1(4):401–408. doi: 10.1111/j.1365-3083.1972.tb03306.x. [DOI] [PubMed] [Google Scholar]
  53. de la Concha E. G., Oldham G., Webster A. D., Asherson G. L., Platts-Mills T. A. Quantitative measurements of T- and B-cell function in "variable" primary hypogammaglobulinaemia: evidence for a consistent B-cell defect. Clin Exp Immunol. 1977 Feb;27(2):208–215. [PMC free article] [PubMed] [Google Scholar]

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