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. 1979 Jul 1;150(1):20–30. doi: 10.1084/jem.150.1.20

Adaptive differentiation of murine lymphocytes. IV. (Responder × Nonresponder) F(1) T cells can be taught to preferentially help nonresponder,rather than responder, B cells

DH Katz, LR Katz, CA Bogowitz, PH Maurer
PMCID: PMC2185606  PMID: 109573

Abstract

Responses to the synthetic terpolymer L-glutamic acid, L-lysine, L-tyrosine (GLT) in the mouse are controlled by H-2-1inked Ir-GLTgenes. (Responder × nonresponder) F(1) hybrid mice, themselves phenotypic responders, can be primed with GLT to develop specific helper cells capable of interacting with 2,4-dinitrophenyl hapten (DNP)-primed F(1) B cells in response to DNP-GLT. Unlike the indiscriminant ability of F(1) helper T cells for conventional antigens (i.e. not Ir gene-controlled), which can help B cells of either parental type (as well as F(1)) equally well, GLT-primed F(1) T cells can only provide help under normal circumstances for B lymphocytes of responder parent origin; they are unable to communicate effectively with nonresponder parental B cells (1, and the present studies). The present studies reveal, however, that the induction of a parental cell-induced allogeneic effect during priming of F(1) mice to GLT actually dictates the direction of cooperating preference that will be displayed by such F(1) helper cells for B cells of one parental type or the other. Thus, F(1) T cells, primed to GLT under the influence of an allogeneic effect induced by parental BALB/c cells, develop into effective helpers for nonresponder A/J B cells, but fail to develop effective helpers for responder BALB/c B cells, and vice-versa. In contrast, F(1) T cells, primed to GLT under the influence of an allogeneic effect induced by either parental type, display significantly enhanced levels of helper activity for B cells derived from F(1) donors. These results are interpreted to reflect the existence of two interdependent events provoked by the allogeneic effect: one event augments the differentiation of GLT-specific helper T cells belonging to the subset corresponding to the opposite parental type; this would explain the development of increased helper activity provided to partner B cells of opposite parental type (as well as of F(1) origin). The second event, we postulate, involves the production of responses against the receptors which normally self-recognize native cell interaction determinants; this form of anti-idiotype response is restricted against self- recognizing receptors of the same parental type used for induction of the allogeneic effect, hence explaining diminished helper activity of such F(1) cells for partner B lymphocytes of corresponding parental type.

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Selected References

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

  1. Bellgrau D., Wilson D. B. Immunological studies of T-cell receptors. I. Specifically induced resistance to graft-versus-host disease in rats mediated by host T-cell immunity to alloreactive parental T cells. J Exp Med. 1978 Jul 1;148(1):103–114. doi: 10.1084/jem.148.1.103. [DOI] [PMC free article] [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. 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]
  4. Katz D. H., Davie J. M., Paul W. E., Benacerraf B. Carrier function in anti-hapten antibody responses. IV. Experimental conditions for the induction of hapten-specific tolerance or for the stimulation of anti-hapten anamnestic responses by "nonimmunogenic" hapten-polypeptide conjugates. J Exp Med. 1971 Jul 1;134(1):201–223. doi: 10.1084/jem.134.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Katz D. H., Hamaoka T., Dorf M. E., Maurer P. H., Benacerraf B. Cell interactions between histoincompatible T and B lymphocytes. IV. Involvement of the immune response (Ir) gene in the control of lymphocyte interactions in responses controlled by the gene. J Exp Med. 1973 Sep 1;138(3):734–739. doi: 10.1084/jem.138.3.734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Katz D. H. The allogeneic effect on immune responses: model for regulatory influences of T lymphocytes on the immune system. Transplant Rev. 1972;12:141–179. doi: 10.1111/j.1600-065x.1972.tb00055.x. [DOI] [PubMed] [Google Scholar]
  8. Katz D. H. The role of the histocompatibilty gene complex in lymphocyte defferetiation. Cold Spring Harb Symp Quant Biol. 1977;41(Pt 2):611–624. doi: 10.1101/sqb.1977.041.01.070. [DOI] [PubMed] [Google Scholar]
  9. McDougal J. S., Cort S. P. Generation of T helper cells in vitro. IV. F1 T helper cells primed with antigen-pulsed parental macrophages are genetically restricted in their antigen-specific helper activity. J Immunol. 1978 Feb;120(2):445–451. [PubMed] [Google Scholar]
  10. Miller J. F., Vadas M. A. The major histocompatibility complex: influence on immune reactivity and T-lymphocyte activation. Scand J Immunol. 1977;6(8):771–778. doi: 10.1111/j.1365-3083.1977.tb02150.x. [DOI] [PubMed] [Google Scholar]
  11. Ordal J. C., Grumet F. C. Genetic control of the immune response. The effect of graft-versus-host reaction on the antibody response to poly-L(Tyr, Glu)-poly-D,L-Ala--poly-L-Lys in nonresponder mice. J Exp Med. 1972 Nov 1;136(5):1195–1206. doi: 10.1084/jem.136.5.1195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Osborne D. P., Jr, Katz D. H. The allogeneic effect in inbred mice. 3. Unique antigenic structural requirements in the expression of the phenomenon on unprimed cell populations in vivo. J Exp Med. 1973 Apr 1;137(4):991–1008. doi: 10.1084/jem.137.4.991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Osborne D. P., Jr, Katz D. H. The allogeneic effect in inbred mice. IV. Regulatory influences of graft-vs.-host reactions on host T lymphocyte functions. J Exp Med. 1973 Oct 1;138(4):825–838. doi: 10.1084/jem.138.4.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Paul W. E., Shevach E. M., Thomas D. W., Pickeral S. F., Rosenthal A. S. Genetic restriction in T-lymphocyte activation by antigen-pulse peritoneal exudate cells. Cold Spring Harb Symp Quant Biol. 1977;41(Pt 2):571–578. doi: 10.1101/sqb.1977.041.01.066. [DOI] [PubMed] [Google Scholar]
  15. Press J. L., McDevitt H. O. Allotype-specific analysis of anti-(Tyr,Glu)-Ala-Lys antibodies produced by Ir-1A high and low responder chimeric mice. J Exp Med. 1977 Dec 1;146(6):1815–1820. doi: 10.1084/jem.146.6.1815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Schwartz R. H. A clonal deletion model for Ir gene control of the immune response. Scand J Immunol. 1978;7(1):3–10. doi: 10.1111/j.1365-3083.1978.tb00420.x. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Thomas D. W., Shevach E. M. Nature of the antigenic complex recognized by T lymphocytes. V. Genetic predisposition of independent F1 T cell subpopulations responsive to antigen-pulsed parental macrophages. J Immunol. 1978 Feb;120(2):638–640. [PubMed] [Google Scholar]
  21. 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]

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