Skip to main content
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1980 May 1;151(5):1103–1113. doi: 10.1084/jem.151.5.1103

Role of I-region gene products in macrophage induction of an antibody response. II. Restriction at the level of T cell in recognition of I-J- subregion macrophage determinants

PMCID: PMC2185866  PMID: 6768830

Abstract

The effect of specific anti-I-J reagents on macrophage-T cell interactions was studied in an in vitro antibody response to burro erythrocytes. Macrophages were prepared from the spleens of F1 hybrid mice whose parental strains differed at the I-J subregion. Two F1 hybrids were used for these experiments, [B10.A(3R) X B10.A(5R)]F1 and [B10.S(9R) X B10.HTT]F1. F1 macrophages responded equally well with F1 T-B cells or with T-B cells of either parental strain. When F1 macrophages were pretreated with anti-I-J serum (without complement) specific for one parental haplotype, they were only able to cooperate with T helper (TH) cells of the unblocked haplotype and with F1 TH cells. Identical results were obtained with (Jb X Jk)F1 and (Js X Jk)F1 mice. The results indicate that TH cells possess genetically restricted receptors for macrophage I-J-subregion gene products and that the interaction between this receptor and the macrophage I-J-subregion determinants is essential for the initiation of a primary in vitro antibody response to an erythrocyte antigen.

Full Text

The Full Text of this article is available as a PDF (629.3 KB).

Selected References

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

  1. Bullock W. W., Möller E. "Spontaneous" B cell activation due to loss of normal mouse serum suppressor. Eur J Immunol. 1972 Dec;2(6):514–517. doi: 10.1002/eji.1830020609. [DOI] [PubMed] [Google Scholar]
  2. David C. S. Serologic and genetic aspects of murine Ia antigens. Transplant Rev. 1976;30:299–302. doi: 10.1111/j.1600-065x.1976.tb00224.x. [DOI] [PubMed] [Google Scholar]
  3. David C. S., Shreffler D. C., Frelinger J. A. New lymphocyte antigen system (Lna) controlled by the Ir region of the mouse H-2 complex. Proc Natl Acad Sci U S A. 1973 Sep;70(9):2509–2514. doi: 10.1073/pnas.70.9.2509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ellner J. J., Lipsky P. E., Rosenthal A. S. Antigen handling by guinea pig macrophages: further evidence for the sequestration of antigen relevant for activation of primed T lymphocytes. J Immunol. 1977 Jun;118(6):2053–2057. [PubMed] [Google Scholar]
  5. Erb P., Feldmann M. The role of macrophages in the generation of T-helper cells. II. The genetic control of the macrophage-T-cell interaction for helper cell induction with soluble antigens. J Exp Med. 1975 Aug 1;142(2):460–472. doi: 10.1084/jem.142.2.460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Erb P., Meier B., Kraus D., von Boehmer H., Feldmann M. Nature of T cell-macrophage interaction in helper cell induction in vitro. I. Evidence for genetic restriction of T cell-macrophage interactions prior to T cell priming. Eur J Immunol. 1978 Nov;8(11):786–792. doi: 10.1002/eji.1830081107. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Frelinger J. A., Neiderhuber J. E., David C. S., Shreffler D. C. Evidence for the expression of Ia (H-2-associated) antigens on thymus-derived lymphocytes. J Exp Med. 1974 Nov 1;140(5):1273–1284. doi: 10.1084/jem.140.5.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Frelinger J. A., Niederhuber J. E., Shreffler D. C. Inhibition of immune responses in vitro by specific antiserums to Ia antigens. Science. 1975 Apr 18;188(4185):268–270. doi: 10.1126/science.1118728. [DOI] [PubMed] [Google Scholar]
  10. Jerne N. K., Nordin A. A. Plaque Formation in Agar by Single Antibody-Producing Cells. Science. 1963 Apr 26;140(3565):405–405. doi: 10.1126/science.140.3565.405. [DOI] [PubMed] [Google Scholar]
  11. Kappler J. W., Marrack P. C. Helper T cells recognise antigen and macrophage surface components simultaneously. Nature. 1976 Aug 26;262(5571):797–799. doi: 10.1038/262797a0. [DOI] [PubMed] [Google Scholar]
  12. Miller J. F., Vadas M. A., Whitelaw A., Gamble J. Role of major histocompatibility complex gene products in delayed-type hypersensitivity. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2486–2490. doi: 10.1073/pnas.73.7.2486. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mishell R. I., Dutton R. W. Immunization of dissociated spleen cell cultures from normal mice. J Exp Med. 1967 Sep 1;126(3):423–442. doi: 10.1084/jem.126.3.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Niederhuber J. E., Allen P., Mayo L. The expression of Ia antigenic determinants on macrophages required for the in vitro antibody response. J Immunol. 1979 Apr;122(4):1342–1349. [PubMed] [Google Scholar]
  15. Niederhuber J. E. The role of I region gene products in macrophage - T lymphocyte interaction. Immunol Rev. 1978;40:28–52. doi: 10.1111/j.1600-065x.1978.tb00400.x. [DOI] [PubMed] [Google Scholar]
  16. Pierce C. W., Kapp J. A., Benacerraf B. Regulation by the H-2 gene complex of macrophage-lymphoid cell interactions in secondary antibody responses in vitro. J Exp Med. 1976 Aug 1;144(2):371–381. doi: 10.1084/jem.144.2.371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Rosenthal A. S., Shevach E. M. Function of macrophages in antigen recognition by guinea pig T lymphocytes. I. Requirement for histocompatible macrophages and lymphocytes. J Exp Med. 1973 Nov 1;138(5):1194–1212. doi: 10.1084/jem.138.5.1194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Schwartz R. H., David C. S., Dorf M. E., Benacerraf B., Paul W. E. Inhibition of dual Ir gene-controlled T-lymphocyte proliferative response to poly (Glu56Lys35Phe9)n with anti-Ia antisera directed against products of either I-A or I-C subregion. Proc Natl Acad Sci U S A. 1978 May;75(5):2387–2391. doi: 10.1073/pnas.75.5.2387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Shevach E. M., Paul W. E., Green I. Histocompatibility-linked immune response gene function in guinea pigs. Specific inhibition of antigen-induced lymphocyte proliferation by alloantisera. J Exp Med. 1972 Nov 1;136(5):1207–1221. doi: 10.1084/jem.136.5.1207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Shevach E. M., Rosenthal A. S. Function of macrophages in antigen recognition by guinea pig T lymphocytes. II. Role of the macrophage in the regulation of genetic control of the immune response. J Exp Med. 1973 Nov 1;138(5):1213–1229. doi: 10.1084/jem.138.5.1213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Singer A., Hathcock K. S., Hodes R. J. Cellular and genetic control of antibody responses. V. Helper T-cell recognition of H-2 determinants on accessory cells but not B cells. J Exp Med. 1979 May 1;149(5):1208–1226. doi: 10.1084/jem.149.5.1208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sprent J. Restricted helper function of F1 hybrid T cells positively selected to heterologous erythrocytes in irradiated parental strain mice. II. Evidence for restrictions affecting helper cell induction and T-B collaboration, both mapping to the K-end of the H-2 complex. J Exp Med. 1978 Apr 1;147(4):1159–1174. doi: 10.1084/jem.147.4.1159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Thomas D. W., Clement L., Shevach E. M. T lymphocyte stimulation by hapten-conjugated macrophages: a model system for the study of immunocompetent cell interactions. Immunol Rev. 1978;40:181–204. doi: 10.1111/j.1600-065x.1978.tb00406.x. [DOI] [PubMed] [Google Scholar]
  25. Thomas D. W., Shevach E. M. Nature of the antigenic complex recognized by T lymphocytes II. T-cell activation by direct modification of macrophage histocompatibility antigens. J Exp Med. 1977 Apr 1;145(4):907–915. doi: 10.1084/jem.145.4.907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Thomas D. W., Shevach E. M. Nature of the antigenic complex recognized by T lymphocytes. I. Analysis with an in vitro primary response to soluble protein antigens. J Exp Med. 1976 Nov 2;144(5):1263–1273. doi: 10.1084/jem.144.5.1263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Yamashita U., Shevach E. M. The histocompatibility restrictions on macrophage T-helper cell interaction determine the histocompatibility restrictions on T-helper cell B-cell interaction. J Exp Med. 1978 Nov 1;148(5):1171–1185. doi: 10.1084/jem.148.5.1171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yano A., Schwartz R. H., Paul W. E. Antigen presentation in the murine T-lymphocyte proliferative response. I. Requirement for genetic identity at the major histocompatibility complex. J Exp Med. 1977 Sep 1;146(3):828–843. doi: 10.1084/jem.146.3.828. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES