Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1989 Aug;86(15):5928–5932. doi: 10.1073/pnas.86.15.5928

Recognition of a self major histocompatibility complex TL region product by gamma delta T-cell receptors.

M Bonneville 1, K Ito 1, E G Krecko 1, S Itohara 1, D Kappes 1, I Ishida 1, O Kanagawa 1, C A Janeway 1, D B Murphy 1, S Tonegawa 1
PMCID: PMC297744  PMID: 2788280

Abstract

Ligand specificity of a murine gammadelta T-cell receptor-expressing hybridoma (KN6) derived from adult thymocytes has been analyzed in detail. The molecule recognized by the KN6 gammadelta T-cell receptor is expressed on syngeneic cells of various sources (peritoneal macrophages, thymocytes, spleen cells, and Abelson murine leukemia virus-transformed cell lines) and on transformed cells arrested at an early stage of development (e.g., PCC3 embryonal carcinoma cells). Linkage of the gene coding for the KN6 ligand to the major histocompatibility complex genes could be demonstrated by testing KN6 hybridoma reactivity to cells from congenic strains that differ only at H-2. In addition, analysis of recombinant strains indicates that the gene controlling the KN6 ligand is located in or distal to the TL region. Involvement of the KN6 gammadelta T-cell receptor in this recognition process could be directly demonstrated by transferring the KN6 TL specificity after introduction of the productively rearranged KN6 gamma and delta genes into an alphabeta T-cell clone or into the germ line in transgenic mice. These observations raise the possibility that at least some gammadelta cells regulate hemopoietic cell maturation and activation.

Full text

PDF
5928

Selected References

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

  1. Andreason G. L., Evans G. A. Introduction and expression of DNA molecules in eukaryotic cells by electroporation. Biotechniques. 1988 Jul-Aug;6(7):650–660. [PubMed] [Google Scholar]
  2. Ashwell J. D., Cunningham R. E., Noguchi P. D., Hernandez D. Cell growth cycle block of T cell hybridomas upon activation with antigen. J Exp Med. 1987 Jan 1;165(1):173–194. doi: 10.1084/jem.165.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bank I., DePinho R. A., Brenner M. B., Cassimeris J., Alt F. W., Chess L. A functional T3 molecule associated with a novel heterodimer on the surface of immature human thymocytes. Nature. 1986 Jul 10;322(6075):179–181. doi: 10.1038/322179a0. [DOI] [PubMed] [Google Scholar]
  4. Bluestone J. A., Cron R. Q., Cotterman M., Houlden B. A., Matis L. A. Structure and specificity of T cell receptor gamma/delta on major histocompatibility complex antigen-specific CD3+, CD4-, CD8- T lymphocytes. J Exp Med. 1988 Nov 1;168(5):1899–1916. doi: 10.1084/jem.168.5.1899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bonneville M., Janeway C. A., Jr, Ito K., Haser W., Ishida I., Nakanishi N., Tonegawa S. Intestinal intraepithelial lymphocytes are a distinct set of gamma delta T cells. Nature. 1988 Dec 1;336(6198):479–481. doi: 10.1038/336479a0. [DOI] [PubMed] [Google Scholar]
  6. Brenner M. B., McLean J., Dialynas D. P., Strominger J. L., Smith J. A., Owen F. L., Seidman J. G., Ip S., Rosen F., Krangel M. S. Identification of a putative second T-cell receptor. Nature. 1986 Jul 10;322(6075):145–149. doi: 10.1038/322145a0. [DOI] [PubMed] [Google Scholar]
  7. Chen Y. T., Obata Y., Stockert E., Takahashi T., Old L. J. Tla-region genes and their products. Immunol Res. 1987;6(1-2):30–45. doi: 10.1007/BF02918102. [DOI] [PubMed] [Google Scholar]
  8. Chorney M. J., Shen F. W., Tung J. S., Boyse E. A. Additional products of the Tla locus of the mouse. Proc Natl Acad Sci U S A. 1985 Oct;82(20):7044–7047. doi: 10.1073/pnas.82.20.7044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cook R. G., Rich R. R., Flaherty L. The Qa-1 alloantigens. I. Identification and molecular weight characterization of glycoproteins controlled by the Qa-1a and Qa-1b alleles. J Immunol. 1981 Nov;127(5):1894–1898. [PubMed] [Google Scholar]
  10. Goodman T., Lefrançois L. Expression of the gamma-delta T-cell receptor on intestinal CD8+ intraepithelial lymphocytes. Nature. 1988 Jun 30;333(6176):855–858. doi: 10.1038/333855a0. [DOI] [PubMed] [Google Scholar]
  11. Grosschedl R., Baltimore D. Cell-type specificity of immunoglobulin gene expression is regulated by at least three DNA sequence elements. Cell. 1985 Jul;41(3):885–897. doi: 10.1016/s0092-8674(85)80069-6. [DOI] [PubMed] [Google Scholar]
  12. Ito K., Bonneville M., Takagaki Y., Nakanishi N., Kanagawa O., Krecko E. G., Tonegawa S. Different gamma delta T-cell receptors are expressed on thymocytes at different stages of development. Proc Natl Acad Sci U S A. 1989 Jan;86(2):631–635. doi: 10.1073/pnas.86.2.631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Itohara S., Nakanishi N., Kanagawa O., Kubo R., Tonegawa S. Monoclonal antibodies specific to native murine T-cell receptor gamma delta: analysis of gamma delta T cells during thymic ontogeny and in peripheral lymphoid organs. Proc Natl Acad Sci U S A. 1989 Jul;86(13):5094–5098. doi: 10.1073/pnas.86.13.5094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jakob H., Boon T., Gaillard J., Nicolas J., Jacob F. Tératocarcinome de la spuris: isolement, culture et propriétés de cellules a potentialités multiples. Ann Microbiol (Paris) 1973 Oct;124(3):269–282. [PubMed] [Google Scholar]
  15. Janeway C. A., Jr Frontiers of the immune system. Nature. 1988 Jun 30;333(6176):804–806. doi: 10.1038/333804a0. [DOI] [PubMed] [Google Scholar]
  16. Janeway C. A., Jr T-cell development. Accessories or coreceptors? Nature. 1988 Sep 15;335(6187):208–210. doi: 10.1038/335208a0. [DOI] [PubMed] [Google Scholar]
  17. Jones B., Tite J. P., Janeway C. A., Jr Different phenotypic variants of the mouse B cell tumor A20/2J are selected by antigen- and mitogen-triggered cytotoxicity of L3T4-positive, I-A-restricted T cell clones. J Immunol. 1986 Jan;136(1):348–356. [PubMed] [Google Scholar]
  18. Kaye J., Porcelli S., Tite J., Jones B., Janeway C. A., Jr Both a monoclonal antibody and antisera specific for determinants unique to individual cloned helper T cell lines can substitute for antigen and antigen-presenting cells in the activation of T cells. J Exp Med. 1983 Sep 1;158(3):836–856. doi: 10.1084/jem.158.3.836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kubo R. T., Born W., Kappler J. W., Marrack P., Pigeon M. Characterization of a monoclonal antibody which detects all murine alpha beta T cell receptors. J Immunol. 1989 Apr 15;142(8):2736–2742. [PubMed] [Google Scholar]
  20. Kuziel W. A., Takashima A., Bonyhadi M., Bergstresser P. R., Allison J. P., Tigelaar R. E., Tucker P. W. Regulation of T-cell receptor gamma-chain RNA expression in murine Thy-1+ dendritic epidermal cells. Nature. 1987 Jul 16;328(6127):263–266. doi: 10.1038/328263a0. [DOI] [PubMed] [Google Scholar]
  21. Lanier L. L., Weiss A. Presence of Ti (WT31) negative T lymphocytes in normal blood and thymus. Nature. 1986 Nov 20;324(6094):268–270. doi: 10.1038/324268a0. [DOI] [PubMed] [Google Scholar]
  22. Leo O., Foo M., Sachs D. H., Samelson L. E., Bluestone J. A. Identification of a monoclonal antibody specific for a murine T3 polypeptide. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1374–1378. doi: 10.1073/pnas.84.5.1374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lew A. M., Pardoll D. M., Maloy W. L., Fowlkes B. J., Kruisbeek A., Cheng S. F., Germain R. N., Bluestone J. A., Schwartz R. H., Coligan J. E. Characterization of T cell receptor gamma chain expression in a subset of murine thymocytes. Science. 1986 Dec 12;234(4782):1401–1405. doi: 10.1126/science.3787252. [DOI] [PubMed] [Google Scholar]
  24. Maher L. J., 3rd, Dove W. F. Overt expression of H-2 serotypes on EC cells is not necessary for host rejection. Immunogenetics. 1984;19(4):343–347. doi: 10.1007/BF00345407. [DOI] [PubMed] [Google Scholar]
  25. Matis L. A., Cron R., Bluestone J. A. Major histocompatibility complex-linked specificity of gamma delta receptor-bearing T lymphocytes. Nature. 1987 Nov 19;330(6145):262–264. doi: 10.1038/330262a0. [DOI] [PubMed] [Google Scholar]
  26. Michaelson J. S. Qa/Tla antigens. Immunol Ser. 1989;43:379–398. [PubMed] [Google Scholar]
  27. Michaelson J., Boyse E. A., Ciccia L., Flaherty L., Fleissner E., Garnick E., Hämmerling U., Lawrence M., Mauch P., Shen F. W. Biochemical genetics of TL antigens. Immunogenetics. 1986;24(2):103–114. doi: 10.1007/BF00373117. [DOI] [PubMed] [Google Scholar]
  28. Moingeon P., Jitsukawa S., Faure F., Troalen F., Triebel F., Graziani M., Forestier F., Bellet D., Bohuon C., Hercend T. A gamma-chain complex forms a functional receptor on cloned human lymphocytes with natural killer-like activity. Nature. 1987 Feb 19;325(6106):723–726. doi: 10.1038/325723a0. [DOI] [PubMed] [Google Scholar]
  29. Nakanishi N., Maeda K., Ito K., Heller M., Tonegawa S. T gamma protein is expressed on murine fetal thymocytes as a disulphide-linked heterodimer. Nature. 1987 Feb 19;325(6106):720–723. doi: 10.1038/325720a0. [DOI] [PubMed] [Google Scholar]
  30. Pampeno C., Meruelo D. Genomic organization of the mouse Tla locus: study of an endogenous retroviruslike locus reveals polymorphisms related to different Tla haplotypes. Immunogenetics. 1988;28(4):247–254. doi: 10.1007/BF00345501. [DOI] [PubMed] [Google Scholar]
  31. Pardoll D. M., Fowlkes B. J., Bluestone J. A., Kruisbeek A., Maloy W. L., Coligan J. E., Schwartz R. H. Differential expression of two distinct T-cell receptors during thymocyte development. Nature. 1987 Mar 5;326(6108):79–81. doi: 10.1038/326079a0. [DOI] [PubMed] [Google Scholar]
  32. Saito H., Kranz D. M., Takagaki Y., Hayday A. C., Eisen H. N., Tonegawa S. Complete primary structure of a heterodimeric T-cell receptor deduced from cDNA sequences. 1984 Jun 28-Jul 4Nature. 309(5971):757–762. doi: 10.1038/309757a0. [DOI] [PubMed] [Google Scholar]
  33. Singer D. S., Hare J., Golding H., Flaherty L., Rudikoff S. Characterization of a new subfamily of class I genes in the H-2 complex of the mouse. Immunogenetics. 1988;28(1):13–21. doi: 10.1007/BF00372524. [DOI] [PubMed] [Google Scholar]
  34. Stern P. L., Beresford N., Bell S. M., Thompson S., Jones K., Mellor A. Murine embryonal carcinoma cells express class I MHC-like antigens. J Immunogenet. 1986 Apr-Jun;13(2-3):133–140. doi: 10.1111/j.1744-313x.1986.tb01094.x. [DOI] [PubMed] [Google Scholar]
  35. Stingl G., Gunter K. C., Tschachler E., Yamada H., Lechler R. I., Yokoyama W. M., Steiner G., Germain R. N., Shevach E. M. Thy-1+ dendritic epidermal cells belong to the T-cell lineage. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2430–2434. doi: 10.1073/pnas.84.8.2430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Transy C., Nash S. R., David-Watine B., Cochet M., Hunt S. W., 3rd, Hood L. E., Kourilsky P. A low polymorphic mouse H-2 class I gene from the Tla complex is expressed in a broad variety of cell types. J Exp Med. 1987 Aug 1;166(2):341–361. doi: 10.1084/jem.166.2.341. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES