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. 1979 Nov 1;150(5):1143–1160. doi: 10.1084/jem.150.5.1143

The specific binding of Listeria monocytogenes-immune T lymphocytes to macrophages. I. Quantitation and role of H-2 gene products

PMCID: PMC2185700  PMID: 115958

Abstract

A system was developed to study the binding of Listeria monocytogenes- specific T cells to L. monocytogenes-pulsed macrophages as an analogue of the initial phase of T-cell activation: antigen recognition. Specific binding, demonstrable after a brief (1 h) contact, was quantitated by the depletion of L. monocytogenes-specific T-cell activity in the cells nonadherent to L. monocytogenes-pulsed macrophage monolayers. L. monocytogenes-specific T-cell function was measured by its ability to activate L. monocytogenes-pulsed macrophages, both to secrete a protein mitogenic for thymocytes and to effect nonspecific tumoricidal activity. These manifestations of T-cell function are known to be regulated by products of I region of the H-2 gene complex. Studies designed to determine the role of H-2 gene products in specific T-cell-macrophage binding have revealed the following. T cells bind specifically to syngeneic macrophages and poorly to allogeneic macrophages. The binding ability appears to map to the K end of the H-2 gene complex (K through I-E). At least two distinct populations of B6AF1 T cells with binding avidity for L. monocytogenes presented on parental macrophages can be identified. Finally, the binding of a given parental-reactive B6AF1 T-cell clone can be specifically inhibited by pretreatment of the antigen-pulsed B6AF1 binding macrophage with anti-H- 2 (anti-Ia) antibodies reactive with the appropriate parental haplotype. These results strongly suggest that H-2 gene products play a direct role in mediating the specific binding of T cells to macrophages and imply that the antigen-dependent physical interaction between T cells and macrophages is the initial, and determining, event in some forms of H-2 gene control of immune reactivity.

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Selected References

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  1. Bach F. H., Kuperman O. J., Sollinger H. W., Zarling J. M., Sondel P. M., Alter B. J., Bach M. L. Cellular immunogenetics and LD-CD collaboration. Transplant Proc. 1977 Mar;9(1):859–863. [PubMed] [Google Scholar]
  2. Benacerraf B. A hypothesis to relate the specificity of T lymphocytes and the activity of I region-specific Ir genes in macrophages and B lymphocytes. J Immunol. 1978 Jun;120(6):1809–1812. [PubMed] [Google Scholar]
  3. Benacerraf B., Germain R. N. The immune response genes of the major histocompatibility complex. Immunol Rev. 1978;38:70–119. doi: 10.1111/j.1600-065x.1978.tb00385.x. [DOI] [PubMed] [Google Scholar]
  4. Benacerraf B., McDevitt H. O. Histocompatibility-linked immune response genes. Science. 1972 Jan 21;175(4019):273–279. doi: 10.1126/science.175.4019.273. [DOI] [PubMed] [Google Scholar]
  5. Cohn Z. A. Activation of mononuclear phagocytes: fact, fancy, and future. J Immunol. 1978 Sep;121(3):813–816. [PubMed] [Google Scholar]
  6. Doherty P. C., Blanden R. V., Zinkernagel R. M. Specificity of virus-immune effector T cells for H-2K or H-2D compatible interactions: implications for H-antigen diversity. Transplant Rev. 1976;29:89–124. doi: 10.1111/j.1600-065x.1976.tb00198.x. [DOI] [PubMed] [Google Scholar]
  7. Farr A. G., Dorf M. E., Unanue E. R. Secretion of mediators following T lymphocyte-macrophage interaction is regulated by the major histocompatibility complex. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3542–3546. doi: 10.1073/pnas.74.8.3542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Farr A. G., Kiely J. M., Unanue E. R. Macrophage-T cell interactions involving Listeria monocytogenes--role of the H-2 gene complex. J Immunol. 1979 Jun;122(6):2395–2404. [PubMed] [Google Scholar]
  9. Farr A. G., Wechter W. J., Kiely J. M., Unanue E. R. Induction of cytocidal macrophages after in vitro interactions between Listeria-immune T cells and macrophages--role of H-2. J Immunol. 1979 Jun;122(6):2405–2412. [PubMed] [Google Scholar]
  10. Fathman C. G., Nabholz M. In vitro secondary mixed leukocyte reaction (MLR). II. Interaction MLR determinants expressed by F1 cells. Eur J Immunol. 1977 Jun;7(6):370–374. doi: 10.1002/eji.1830070609. [DOI] [PubMed] [Google Scholar]
  11. Green I., Paul W. E., Benacerraf B. The behavior of hapten-poly-L-lysine conjugates as complete antigens in genetic responder and as haptens in nonresponder guinea pigs. J Exp Med. 1966 May 1;123(5):859–879. doi: 10.1084/jem.123.5.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Greenberg P. D., Bluestein H. G. Antigen recognition by primed T lymphocytes in vitro. I. Separation of recognitive and proliferative phases of antigen-induced T cell activation. J Immunol. 1978 Jul;121(1):239–244. [PubMed] [Google Scholar]
  13. Jerne N. K. The somatic generation of immune recognition. Eur J Immunol. 1971 Jan;1(1):1–9. doi: 10.1002/eji.1830010102. [DOI] [PubMed] [Google Scholar]
  14. Jones P. P., Murphy D. B., McDevitt H. O. Two-gene control of the expression of a murine Ia antigen. J Exp Med. 1978 Oct 1;148(4):925–939. doi: 10.1084/jem.148.4.925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Karnovsky M. L., Lazdins J. K. Biochemical criteria for activated macrophages. J Immunol. 1978 Sep;121(3):809–813. [PubMed] [Google Scholar]
  16. Lipscomb M. F., Ben-Sasson S. Z., Uhr J. W. Specific binding of T lymphocytes to macrophages. I. Kinetics of binding. J Immunol. 1977 May;118(5):1748–1754. [PubMed] [Google Scholar]
  17. Lipsky P. E., Rosenthal A. S. Macrophage-lymphocyte interaction. II. Antigen-mediated physical interactions between immune guinea pig lymph node lymphocytes and syngeneic macrophages. J Exp Med. 1975 Jan 1;141(1):138–154. doi: 10.1084/jem.141.1.138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lyons C. R., Tucker T. F., Uhr J. W. Specific binding of T lymphocytes to macrophages. V. The role of Ia antigens on Mphi in the binding. J Immunol. 1979 Apr;122(4):1598–1600. [PubMed] [Google Scholar]
  19. Miller J. F., Vadas M. A., Whitelaw A., Gamble J., Bernard C. Histocompatibility linked immune responsiveness and restrictions imposed on sensitized lymphocytes. J Exp Med. 1977 Jun 1;145(6):1623–1628. doi: 10.1084/jem.145.6.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mozes E., Schwartz M., Sela M. Antibody response of inbred mouse strains to ordered tetrapeptides of tyrosine and glutamic acid attached to multichain polyalanine or polyproline. Tyr-Tyr-Glu-Glu is a major determinant of the random poly-(Tyr, Glu)-polyDLAla--polyLys. J Exp Med. 1974 Aug 1;140(2):349–355. doi: 10.1084/jem.140.2.349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Paul W. E., Shevach E. M., Pickeral S., Thomas D. W., Rosenthal A. S. Independent populations of primed F1 guinea pig T lymphocytes respond to antigen-pulsed parental peritoneal exudate cells. J Exp Med. 1977 Mar 1;145(3):618–630. doi: 10.1084/jem.145.3.618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rosenthal A. S. Determinant selection and macrophage function in genetic control of the immune response. Immunol Rev. 1978;40:136–152. doi: 10.1111/j.1600-065x.1978.tb00404.x. [DOI] [PubMed] [Google Scholar]
  23. Schwartz R. H., Paul W. E. T-lymphocyte-enriched murine peritoneal exudate cells. II. Genetic control of antigen-induced T-lymphocyte proliferation. J Exp Med. 1976 Mar 1;143(3):529–540. doi: 10.1084/jem.143.3.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Schwartz R. H., Yano A., Paul W. E. Interaction between antigen-presenting cells and primed T lymphocytes: an assessment of Ir gene expression in the antigen-presenting cell. Immunol Rev. 1978;40:153–180. doi: 10.1111/j.1600-065x.1978.tb00405.x. [DOI] [PubMed] [Google Scholar]
  25. Schwartz R. H., Yano A., Stimpfling J. H., Paul W. E. Gene complementation in the T-lymphocyte proliferative response to poly (Glu55Lys36Phe9)n. A demonstration that both immune response gene products must be expressed in the same antigen-presenting cell. J Exp Med. 1979 Jan 1;149(1):40–57. doi: 10.1084/jem.149.1.40. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sprent J. Two subgroups of T helper cells in F1 hybrid mice revealed by negative selection to heterologous erythrocytes in vivo. J Immunol. 1978 Nov;121(5):1691–1695. [PubMed] [Google Scholar]
  27. Thomas D. W., Shevach E. M. Nature of the antigenic complex recognized by T lymphocytes. VII. Evidence for an association between TNP-conjugated macrophage membrane components and Ia antigens. J Immunol. 1978 Sep;121(3):1152–1156. [PubMed] [Google Scholar]
  28. Ziegler H. K., Geyer C., Henney C. S. Studies on the cytolytic activity of human lymphocytes. III. An analysis of requirements for K cell-target interaction. J Immunol. 1977 Nov;119(5):1821–1829. [PubMed] [Google Scholar]
  29. Zinkernagel R. M., Althage A., Adler B., Blanden R. V., Davidson W. F., Kees U., Dunlop M. B., Shreffler D. C. H-2 restriction of cell-mediated immunity to an intracellular bacterium: effector T cells are specific for Listeria antigen in association with H-21 region-coded self-markers. J Exp Med. 1977 May 1;145(5):1353–1367. doi: 10.1084/jem.145.5.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]

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