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. 1980 Aug 1;152(2):336–349. doi: 10.1084/jem.152.2.336

Role of the major histocompatibility gene products in regulating the antibody response to dinitrophenylated poly(L-Glu55,L-Ala35,L-Phe9)n

PMCID: PMC2185948  PMID: 6156986

Abstract

These studies were carried out to investigate the potential helper T cell repertoire specific for the random copolymer poly(L-Glu55,L-Ala35, L-Phe9)n(GL phi 9) of responder, nonresponder, and (responder x nonresponder)F1 murine strains. We tested the ability of these T cells to collaborate with dinitrophenyl (DNP)-specific primary and secondary B lymphocytes of each strain in response to the antigen CNP-GL phi 9 in the splenic-fragment culture system. The results of these experiments show that there are GL phi 9-specific T lymphocytes in the responder, nonresponder, and F1 strains; but that these three GL phi 9-specific T cell populations differ in their collaborative potential. Responder T cells are able to collaborate with their own syngeneic responder B cells as well as the allogeneic nonresponder B cells in a syngeneic fashion. The F1 T cell population resembles that of the nonresponder in its ability to collaborate with only responder B cells in a syngeneic fashion. Analysis carried out using appropriately selected mouse strains indicate that these results are unlikely to be a result of positive or negative allogeneic effects. The results obtained suggest that individuals within a given murine strain do possess the capacity to collaborate in a syngeneic fashion with B cells of any other MHC- allogeneic strain as well as their own MHC-identical B cells. The nonresponder status in the response to GL phi 9 appears to be the result of a deletion of T cells capable of recognizing antigen in the context of B cells of the nonresponder haplotype. Thus, the MHC gene products appear to play a determinative role in shaping the expressed helper T cell specificity repertoire within an individual mouse strain.

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Selected References

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

  1. Dorf M. E., Benacerraf B. Complementation of H-2-linked Ir genes in the mouse. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3671–3675. doi: 10.1073/pnas.72.9.3671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Heber-Katz E., Wilson D. B. Collaboration of allogeneic T and B lymphocytes in the primary antibody response to sheep erythrocytes in vitro. J Exp Med. 1975 Oct 1;142(4):928–935. doi: 10.1084/jem.142.4.928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Hodes R. J., Ahmann G. B., Hathcock K. S., Dickler H. B., Singer A. Cellular and genetic control of antibody responses in vitro. IV. Expression of Ia antigens on accessory cells required for responses to soluble antigens including a response under Ir gene control. J Immunol. 1978 Oct;121(4):1501–1509. [PubMed] [Google Scholar]
  5. KATCHALSKI E., SELA M. Synthesis and chemical properties of poly-alpha-amino acids. Adv Protein Chem. 1958;13:243–492. doi: 10.1016/s0065-3233(08)60600-2. [DOI] [PubMed] [Google Scholar]
  6. Katz D. H., Hamaoka T., Benacerraf B. Cell interactions between histoincompatible T and B lymphocytes. II. Failure of physiologic cooperative interactions between T and B lymphocytes from allogeneic donor strains in humoral response to hapten-protein conjugates. J Exp Med. 1973 Jun 1;137(6):1405–1418. doi: 10.1084/jem.137.6.1405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Katz D. H., Osborne D. P., Jr The allogeneic effect in inbred mice. II. Establishment of the cellular interactions required for enhancement of antibody production by the graft-versus-host reaction. J Exp Med. 1972 Sep 1;136(3):455–465. doi: 10.1084/jem.136.3.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Katz D. H., Skidmore B. J., Katz L. R., Bogowitz C. A. Adaptive differentiation of murine lymphocytes. I. Both T and B lymphocytes differentiating in F1 transplanted to parental chimeras manifest preferential cooperative activity for partner lymphocytes derived from the same parental type corresponding to the chimeric host. J Exp Med. 1978 Sep 1;148(3):727–745. doi: 10.1084/jem.148.3.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Katz D. H., Skidmore B. J. Self-recognition as a means of cell communication in biologic systems: the immune system is not an exception to the general rule. Birth Defects Orig Artic Ser. 1978;14(2):327–341. [PubMed] [Google Scholar]
  10. Kindred B., Shreffler D. C. H-2 dependence of co-operation between T and B cells in vivo. J Immunol. 1972 Nov;109(5):940–943. [PubMed] [Google Scholar]
  11. Klinman N. R. The mechanism of antigenic stimulation of primary and secondary clonal precursor cells. J Exp Med. 1972 Aug 1;136(2):241–260. doi: 10.1084/jem.136.2.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Merryman C. F., Maurer P. H., Bailey D. W. Genetic control of immune response in mice to a glutamic acid, lysine, phenylalanine copolymer. 3. Use of recombinant inbred strains of mice to establish association of immune response genes with H-2 genotype. J Immunol. 1972 Apr;108(4):937–940. [PubMed] [Google Scholar]
  13. 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]
  14. Pierce S. K., Cancro M. P., Klinman N. R. Individual antigen-specific T lymphocytes: helper function in enabling the expression of multiple antibody isotypes. J Exp Med. 1978 Sep 1;148(3):759–765. doi: 10.1084/jem.148.3.759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Pierce S. K., Klinman N. R. Allogeneic carrier-specific enhancement of hapten-specific secondary B-cell responses. J Exp Med. 1976 Nov 2;144(5):1254–1262. doi: 10.1084/jem.144.5.1254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Pierce S. K., Klinman N. R. The allogeneic bisection of carrier-specific enhancement of monoclonal B-cell responses. J Exp Med. 1975 Nov 1;142(5):1165–1179. doi: 10.1084/jem.142.5.1165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. 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]
  20. 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]
  21. Smith F. I., Miller J. F. Suppression of T cells specific for the nonthymic parental H-2 haplotype in thymus-grafted chimeras. J Exp Med. 1980 Jan 1;151(1):246–251. doi: 10.1084/jem.151.1.246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sprent J. Restricted helper function of F1 hybrid T cells positively selected to heterologous erythrocytes in irradiated parental strain mice. I. Failure to collaborate with B cells of the opposite parental strain not associated with active suppression. J Exp Med. 1978 Apr 1;147(4):1142–1158. doi: 10.1084/jem.147.4.1142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Swain S. L., Trefts P. E., Tse H. Y., Dutton R. W. The significance of T-B collaboration across haplotype barriers. Cold Spring Harb Symp Quant Biol. 1977;41(Pt 2):597–609. doi: 10.1101/sqb.1977.041.01.069. [DOI] [PubMed] [Google Scholar]
  24. Swierkosz J. E., Rock K., Marrack P., Kappler J. W. The role of H-2 linked genes in helper T-cell function. II. Isolation on antigen-pulsed macrophages of two separate populations of F1 helper T cells each specific for antigen and one set of parental H-2 products. J Exp Med. 1978 Feb 1;147(2):554–570. doi: 10.1084/jem.147.2.554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Zinkernagel R. M., Callahan G. N., Althage A., Cooper S., Klein P. A., Klein J. On the thymus in the differentiation of "H-2 self-recognition" by T cells: evidence for dual recognition? J Exp Med. 1978 Mar 1;147(3):882–896. doi: 10.1084/jem.147.3.882. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. von Boehmer H., Hudson L., Sprent J. Collaboration of histoincompatible T and B lymphocytes using cells from tetraparental bone marrow chimeras. J Exp Med. 1975 Oct 1;142(4):989–997. doi: 10.1084/jem.142.4.989. [DOI] [PMC free article] [PubMed] [Google Scholar]

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