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PMID: 6770025 Published · ppublish English Journal Article

Gene complementation. Neither Ir-GLphi gene need be present in the proliferative T cell to generate an immune response to Poly(Glu55Lys36Phe9)n.

The Journal of experimental medicine ·Vol. 151 ·No. 6 ·1980-06-01 ·Pages 1452-67

Longo DL, Schwartz RH

Abstract

The cellular requirements for immune response (Ir) gene expression in a T cell proliferative response under dual Ir gene control were examined with radiation-induced bone marrow chimeras. The response to poly(Glu55Lys36Phe9)n (GLphi) requires two responder alleles that in the [B10.A X B10.A(18R)]F1 map in I-Ab and I-Ek/Cd. Chimeras in which a mixture of the nonresponder B10.A parental cells (which possess only I-Ek/Cd) and the nonresponder B10.A(18R) parental cells (which possess only I-Ab) were allowed to mature in a responder F1 environment did not respond to GLphi, which suggests that at least one cell participating in the response needed to possess both responder alleles to function. When T cells from such A + 18R leads to F1 chimeras were primed in the presence of responder antigen-presenting cells (APC), the chimeric T cells responded to GLphi, which suggests that both responder alleles must be expressed in the APC but not necessarily in the T cell. Interestingly, acutely irradiated F1 animals were found not to be an adequate source of responder APC for priming the proliferating T cell because of the rapid turnover of peripheral APC after irradiation. In adoptive transfer experiments, T cell-depleted bone marrow had to be used as a source of responder APC. When bone marrow cells from (B10.A X B10)F1 responder animals were allowed to mature in a low-responder B10 of B10.A parental environment, neither chimera, F1 leads to A or F1 leads to B, could respond to GLphi. This demonstrated that the presence of high-responder APC, which derive from the donor bone marrow, was not sufficient to generate a GLphi response. It appears that in addition it is essential for the T lymphocytes to mature in a high-responder environment. Finally, B10.A(4R) T cells, which possess neither Ir-GLphi responder allele, could be educated to mount a GLphi-proliferative response provided that they matured in a responder environment and were primed with APC expressing both responder alleles. Therefore, the gene products of the complementing Ir-GLphi responder alleles appear to function as a single restriction element at the level of the APC. T cells that do not possess responder alleles are not intrinsically defective, because they could be made phenotypic responders if they developed in an environment in which responder major histocompatibility complex (MHC) products were learned as self and if antigen was presented to them by APC expressing responder MHC products.

MeSH Terms
Animals Antigens Bone Marrow Cells Cell Differentiation Genes, MHC Class II Genetic Complementation Test Glutamates Lymphocyte Activation Lysine Mice Peptides/immunology Phenylalanine Radiation Chimera T-Lymphocytes/immunology
Chemicals
Antigens Glutamates Peptides Phenylalanine Lysine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Longo D L
Schwartz R H
References (32)
32 references, click to expand
  1. Peculiar immunobiology of bone marrow allografts. I. Graft rejection by irradiated responder mice.
    J Exp Med. 1971 Jul 1;134(1):83-102 PMID: 4397663
  2. T lymphocyte-enriched murine peritoneal exudate cells. I. A reliable assay for antigen-induced T lymphocyte proliferation.
    J Immunol. 1975 Nov;115(5):1330-8 PMID: 51890
  3. The requirement for two complementing Ir-GLphi immune response genes in the T-lymphocyte proliferative response to poly-(Glu53Lys36Phe11).
    J Exp Med. 1976 Apr 1;143(4):897-905 PMID: 1082919
  4. Virus and trinitrophenol hapten-specific T-cell-mediated cytotoxicity against H-2 incompatible target cells.
    J Exp Med. 1976 Apr 1;143(4):999-1004 PMID: 1082923
  5. T lymphocyte-enriched murine peritoneal exudate cells. III. Inhibition of antigen-induced T lymphocyte Proliferation with anti-Ia antisera.
    J Immunol. 1976 Aug;117(2):531-40 PMID: 1084902
  6. 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):828-43 PMID: 70497
  7. Influence of the major histocompatibility complex on lymphocyte interactions in antibody formation.
    Nature. 1978 Jul 13;274(5667):166-8 PMID: 307186
  8. Major histocompatibility complex-linked immune-responsiveness is acquired by lymphocytes of low-responder mice differentiating in thymus of high-responder mice.
    Proc Natl Acad Sci U S A. 1978 May;75(5):2439-42 PMID: 307765
  9. Genetic control of cytolytic t-lymphocyte responses. II. The role of the host genotype in parental leads to F1 radiation chimeras in the control of the specificity of cytolytic T-lymphocyte responses to trinitrophenyl-modified syngeneic cells.
    J Exp Med. 1978 Aug 1;148(2):352-9 PMID: 100568
  10. 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):727-45 PMID: 308984
  11. Two-gene control of the expression of a murine Ia antigen.
    J Exp Med. 1978 Oct 1;148(4):925-39 PMID: 100572
  12. Thymic macrophages modulate one stage of T cell differentiation in vitro.
    J Immunol. 1978 Nov;121(5):1861-4 PMID: 152329
  13. Immunologic functions of Ia-bearing epidermal Langerhans cells.
    J Immunol. 1978 Nov;121(5):2005-13 PMID: 81860
  14. 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):786-92 PMID: 309821
  15. The role of H-2 linked genes in helper T-cell function. IV. Importance of T-cell genotype and host environment in I-region and Ir gene expression.
    J Exp Med. 1978 Dec 1;148(6):1510-22 PMID: 102728
  16. H-2 complementation in anti-H-Y cytotoxic T-cell responses can occur in chimeric mice.
    Proc Natl Acad Sci U S A. 1978 Dec;75(12):6207-10 PMID: 310553
  17. Role of H-2 gene products in the function of T helper cells from normal and chimeric mice in vivo.
    Immunol Rev. 1978;42:108-37 PMID: 83698
  18. Intrathymic and extrathymic T cell maturation.
    Immunol Rev. 1978;42:138-84 PMID: 32648
  19. The influence of the major histocompatibility complex on the function of T-helper cells in antibody formation.
    Immunol Rev. 1978;42:202-23 PMID: 83700
  20. Thymus and lymphohemopoietic cells: their role in T cell maturation in selection of T cells' H-2-restriction-specificity and in H-2 linked Ir gene control.
    Immunol Rev. 1978;42:224-70 PMID: 83701
  21. The influence of thymus H-2 antigens on the specificity of maturing killer and helper cells.
    Immunol Rev. 1978;42:3-19 PMID: 83702
  22. Structural studies on the murine Ia alloantigens. V. Evidence that the structural gene for the I-E/C beta polypeptide is encoded within the I-A subregion.
    J Exp Med. 1979 Apr 1;149(4):981-6 PMID: 429967
  23. Search for suppression of T cells specific for the second nonhost H-2 haplotype in F1 leads to P irradiation bone marrow chimeras.
    J Immunol. 1979 May;122(5):1742-9 PMID: 156219
  24. 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):1208-26 PMID: 109564
  25. Trans gene complementation of I-E subregion antigens.
    J Immunol. 1979 Sep;123(3):1423-5 PMID: 469258
  26. Genetic control of the immune response to collagen. II. Antibody responses produced in fetal liver restored radiation chimeras and thymus reconstituted F1 hybrid nude mice.
    J Exp Med. 1979 Sep 19;150(3):646-52 PMID: 113479
  27. Thymic reconstitution of nude F1 mice with one or both parental thymus grafts.
    J Exp Med. 1979 Sep 19;150(3):693-7 PMID: 314490
  28. The murine Kupffer cell. I. Characterization of the cell serving accessory function in antigen-specific T cell proliferation.
    J Immunol. 1979 Dec;123(6):2602-9 PMID: 91637
  29. Cellular and genetic control of antibody responses. VI. Expression of Ir gene function by H-2a accessory cells, but not H-2a T or B cells in responses to TNP-(T,G)-A--L.
    J Immunol. 1979 Dec;123(6):2823-9 PMID: 115922
  30. Mouse epidermal Ia molecules have a bone marrow origin.
    Nature. 1979 Nov 15;282(5736):321-3 PMID: 503207
  31. Epidermal Langerhans cells are derived from cells originating in bone marrow.
    Nature. 1979 Nov 15;282(5736):324-6 PMID: 503208
  32. T-lymphocyte response to cytochrome c. I. Demonstration of a T-cell heteroclitic proliferative response and identification of a topographic antigenic determinant on pigeon cytochrome c whose immune recognition requires two complementing major histocompatibility complex-linked immune response genes.
    J Exp Med. 1979 Oct 1;150(4):830-48 PMID: 92520
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
1980-06-01
Pages
1452-67
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2185878
Subset
IM
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