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. 1978 Apr 1;147(4):1142–1158. doi: 10.1084/jem.147.4.1142

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

PMCID: PMC2184238  PMID: 306407

Abstract

Unprimed (CBA X C57BL/6)F1 lymph node T cells were transferred with sheep erythrocytes (SRC) into heavily irradiated F1 or parental strain mice and recovered from thoracic duct lymph or spleens of the recipients 5 days later. To study their helper function, the harvested F1 T cells were transferred with antigen into irradiated F1 mice plus B cells from either the two parental strains or from F1 mice. F1 T cells activated in F1 mice gave high IgM and IgG anti-SRC responses with all three populations of B cells. By contrast, F1 T cells activated in mice of one parental strain collaborated well with B cells of this strain, but poorly with B cells of the opposite strain. Active suppression was considered an unlikely explanation for this result since (a) good responses were found with F1 B cells, and (b) addition experiments showed that the poor response with B cells of the opposite parental strain (which was equivalent to that produced by unprimed F1 T cells) could be converted to a high response by a supplemental injection of F1 T cells activated in F1 mice. The phenomenon (a) was specific for the antigen used for activation (criss-cross experiments were performed with horse erythrocytes), (b) was reflected in levels of serum hemagglutinins as well as in numbers of splenic plaque-forming cells, (c) applied also to comparable activation of (DBA/2 X C57BL/6)F1 T cells, and (d) could be prevented by activating F1 T cells in mice of one parental strain in the presence of peritoneal exudate cells of the opposite parental strain. The hypothesis was advanced that F1 T cells contain two discrete subpopulations of antigen-reactive cells, each subject to restrictions acting at two different levels: (a) during T- macrophage interactions and (b) during T-B collaboration. It was suggested that when F1 T cells are activated to antigen in a parental strain environment, radioresistant macrophages activate only one of the two subgroups of T cells, and this subgroup is able to collaborate with B cells of the strain used for activation (and with F1 B cells) but not with B cells of the opposite parental strain. The other subgroup of T cells remains in an unprimed (nonactivated) state.

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Selected References

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  1. Anderson R. E., Warner N. L. Ionizing radiation and the immune response. Adv Immunol. 1976;24:215–335. doi: 10.1016/s0065-2776(08)60331-4. [DOI] [PubMed] [Google Scholar]
  2. Cudkowicz G., Bennett M. Peculiar immunobiology of bone marrow allografts. II. Rejection of parental grafts by resistant F 1 hybrid mice. J Exp Med. 1971 Dec 1;134(6):1513–1528. doi: 10.1084/jem.134.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cunningham A. J., Szenberg A. Further improvements in the plaque technique for detecting single antibody-forming cells. Immunology. 1968 Apr;14(4):599–600. [PMC free article] [PubMed] [Google Scholar]
  4. Dietrich F. M. The immune response to heterologous red cells in mice. Immunology. 1966 Apr;10(4):365–376. [PMC free article] [PubMed] [Google Scholar]
  5. Erb P., Feldmann M. The role of macrophages in the generation of T-helper cells. I. The requirement for macrophages in helper cell induction and characteristics of the macrophage-T cell interaction. Cell Immunol. 1975 Oct;19(2):356–367. doi: 10.1016/0008-8749(75)90217-8. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Feldmann M., Beverley P. C., Woody J., McKenzie I. F. T-T interactions in the induction of suppressor and helper T cells: analysis of membrane phenotype of precursor and amplifier cells. J Exp Med. 1977 Apr 1;145(4):793–801. doi: 10.1084/jem.145.4.793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ford W. L., Atkins R. C. Specific unresponsiveness of recirculating lymphocytes ater exposure to histocompatibility antigen in F 1 hybrid rats. Nat New Biol. 1971 Dec 8;234(49):178–180. doi: 10.1038/newbio234178a0. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Julius M. H., Simpson E., Herzenberg L. A. A rapid method for the isolation of functional thymus-derived murine lymphocytes. Eur J Immunol. 1973 Oct;3(10):645–649. doi: 10.1002/eji.1830031011. [DOI] [PubMed] [Google Scholar]
  11. Matzinger P., Bevan M. J. Induction of H-2-restricted cytotoxic T cells: in vivo induction has the appearance of being unrestricted. Cell Immunol. 1977 Sep;33(1):92–100. doi: 10.1016/0008-8749(77)90137-x. [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. 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]
  14. Skidmore B. J., Katz D. H. Haplotype preference in lymphocyte differentiation. I. Development of haplotype-specific helper and suppressor activities in F1 hybrid-activated T cell populations. J Immunol. 1977 Aug;119(2):694–701. [PubMed] [Google Scholar]
  15. Sprent J. Circulating T and B lymphocytes of the mouse. I. Migratory properties. Cell Immunol. 1973 Apr;7(1):10–39. doi: 10.1016/0008-8749(73)90180-9. [DOI] [PubMed] [Google Scholar]
  16. Sprent J., Miller J. F. Activation of thymus cells by histocompatibility antigens. Nat New Biol. 1971 Sep 15;234(50):195–198. doi: 10.1038/newbio234195a0. [DOI] [PubMed] [Google Scholar]
  17. Sprent J., Miller J. F., Mitchell G. F. Antigen-induced selective recruitment of circulating lymphocytes. Cell Immunol. 1971 Apr;2(2):171–181. doi: 10.1016/0008-8749(71)90036-0. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Vadas M. A., Miller J. F., McKenzie I. F., Chism S. E., Shen F. W., Boyse E. A., Gamble J. R., Whitelaw A. M. Ly and Ia antigen phenotypes of T cells involved in delayed-type hypersensitivity and in suppression. J Exp Med. 1976 Jul 1;144(1):10–19. doi: 10.1084/jem.144.1.10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Zinkernagel R. M., Doherty P. C. H-2 compatability requirement for T-cell-mediated lysis of target cells infected with lymphocytic choriomeningitis virus. Different cytotoxic T-cell specificities are associated with structures coded for in H-2K or H-2D;. J Exp Med. 1975 Jun 1;141(6):1427–1436. doi: 10.1084/jem.141.6.1427. [DOI] [PMC free article] [PubMed] [Google Scholar]

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