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. 1989 Jul;86(14):5527–5531. doi: 10.1073/pnas.86.14.5527

Diversity in T-cell receptor gamma gene usage in intestinal epithelium.

S Kyes 1, E Carew 1, S R Carding 1, C A Janeway Jr 1, A Hayday 1
PMCID: PMC297656  PMID: 2546157

Abstract

The intraepithelial cells of the murine small intestine include a significant number of CD3+ T cells that use T-cell receptor gamma genes rather than T-cell receptor beta genes. As with other sites of T-cell receptor gamma expression, combinatorial diversity is limited, but there is junctional diversity, and this, together with the specific variable region gamma gene segments used, distinguishes gamma gene expression in the gut epithelium from that in cells derived from the dermal epithelium. The restriction of productive gamma gene expression largely to one V-J-C (V, variable; J, joining; C, constant) gene combination may result from nonproductive joining of other V-J combinations and from productively rearranged genes rendered nonfunctional by incorrect splicing.

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Selected References

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

  1. Asarnow D. M., Kuziel W. A., Bonyhadi M., Tigelaar R. E., Tucker P. W., Allison J. P. Limited diversity of gamma delta antigen receptor genes of Thy-1+ dendritic epidermal cells. Cell. 1988 Dec 2;55(5):837–847. doi: 10.1016/0092-8674(88)90139-0. [DOI] [PubMed] [Google Scholar]
  2. Azuma T., Igras V., Reilly E. B., Eisen H. N. Diversity at the variable-joining region boundary of lambda light chains has a pronounced effect on immunoglobulin ligand-binding activity. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6139–6143. doi: 10.1073/pnas.81.19.6139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Born W., Rathbun G., Tucker P., Marrack P., Kappler J. Synchronized rearrangement of T-cell gamma and beta chain genes in fetal thymocyte development. Science. 1986 Oct 24;234(4775):479–482. doi: 10.1126/science.3020688. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Brenner M. B., McLean J., Scheft H., Riberdy J., Ang S. L., Seidman J. G., Devlin P., Krangel M. S. Two forms of the T-cell receptor gamma protein found on peripheral blood cytotoxic T lymphocytes. Nature. 1987 Feb 19;325(6106):689–694. doi: 10.1038/325689a0. [DOI] [PubMed] [Google Scholar]
  7. Carding S. R., Jenkinson E. J., Kingston R., Hayday A. C., Bottomly K., Owen J. J. Developmental control of lymphokine gene expression in fetal thymocytes during T-cell ontogeny. Proc Natl Acad Sci U S A. 1989 May;86(9):3342–3345. doi: 10.1073/pnas.86.9.3342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chien Y. H., Iwashima M., Kaplan K. B., Elliott J. F., Davis M. M. A new T-cell receptor gene located within the alpha locus and expressed early in T-cell differentiation. 1987 Jun 25-Jul 1Nature. 327(6124):677–682. doi: 10.1038/327677a0. [DOI] [PubMed] [Google Scholar]
  9. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  10. Davies M. D., Parrott D. M. Preparation and purification of lymphocytes from the epithelium and lamina propria of murine small intestine. Gut. 1981 Jun;22(6):481–488. doi: 10.1136/gut.22.6.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Davis M. M., Bjorkman P. J. T-cell antigen receptor genes and T-cell recognition. Nature. 1988 Aug 4;334(6181):395–402. doi: 10.1038/334395a0. [DOI] [PubMed] [Google Scholar]
  12. Forster A., Huck S., Ghanem N., Lefranc M. P., Rabbitts T. H. New subgroups in the human T cell rearranging V gamma gene locus. EMBO J. 1987 Jul;6(7):1945–1950. doi: 10.1002/j.1460-2075.1987.tb02456.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Garman R. D., Doherty P. J., Raulet D. H. Diversity, rearrangement, and expression of murine T cell gamma genes. Cell. 1986 Jun 6;45(5):733–742. doi: 10.1016/0092-8674(86)90787-7. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Havran W. L., Allison J. P. Developmentally ordered appearance of thymocytes expressing different T-cell antigen receptors. Nature. 1988 Sep 29;335(6189):443–445. doi: 10.1038/335443a0. [DOI] [PubMed] [Google Scholar]
  16. Hayday A. C., Saito H., Gillies S. D., Kranz D. M., Tanigawa G., Eisen H. N., Tonegawa S. Structure, organization, and somatic rearrangement of T cell gamma genes. Cell. 1985 Feb;40(2):259–269. doi: 10.1016/0092-8674(85)90140-0. [DOI] [PubMed] [Google Scholar]
  17. Heilig J. S., Tonegawa S. Diversity of murine gamma genes and expression in fetal and adult T lymphocytes. 1986 Aug 28-Sep 3Nature. 322(6082):836–840. doi: 10.1038/322836a0. [DOI] [PubMed] [Google Scholar]
  18. Janeway C. A., Jr, Jones B., Hayday A. Specificity and function of T cells bearing gamma delta receptors. Immunol Today. 1988 Mar;9(3):73–76. doi: 10.1016/0167-5699(88)91267-4. [DOI] [PubMed] [Google Scholar]
  19. Jones B., Carding S., Kyes S., Mjolsness S., Janeway C., Jr, Hayday A. Molecular analysis of T cell receptor gamma gene expression in allo-activated splenic T cells of adult mice. Eur J Immunol. 1988 Dec;18(12):1907–1915. doi: 10.1002/eji.1830181207. [DOI] [PubMed] [Google Scholar]
  20. Jones B., Mjolsness S., Janeway C., Jr, Hayday A. C. Transcripts of functionally rearranged gamma genes in primary T cells of adult immunocompetent mice. Nature. 1986 Oct 16;323(6089):635–638. doi: 10.1038/323635a0. [DOI] [PubMed] [Google Scholar]
  21. Koning F., Stingl G., Yokoyama W. M., Yamada H., Maloy W. L., Tschachler E., Shevach E. M., Coligan J. E. Identification of a T3-associated gamma delta T cell receptor on Thy-1+ dendritic epidermal Cell lines. Science. 1987 May 15;236(4803):834–837. doi: 10.1126/science.2883729. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Lacy M. J., McNeil L. K., Roth M. E., Kranz D. M. T-cell receptor delta-chain diversity in peripheral lymphocytes. Proc Natl Acad Sci U S A. 1989 Feb;86(3):1023–1026. doi: 10.1073/pnas.86.3.1023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Laski F. A., Rio D. C., Rubin G. M. Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell. 1986 Jan 17;44(1):7–19. doi: 10.1016/0092-8674(86)90480-0. [DOI] [PubMed] [Google Scholar]
  25. Lefrancois L. Carbohydrate differentiation antigens of murine T cells: expression on intestinal lymphocytes and intestinal epithelium. J Immunol. 1987 May 15;138(10):3375–3384. [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Mullis K. B., Faloona F. A. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 1987;155:335–350. doi: 10.1016/0076-6879(87)55023-6. [DOI] [PubMed] [Google Scholar]
  29. Oettgen H. C., Pettey C. L., Maloy W. L., Terhorst C. A T3-like protein complex associated with the antigen receptor on murine T cells. Nature. 1986 Mar 20;320(6059):272–275. doi: 10.1038/320272a0. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Pelkonen J., Traunecker A., Karjalainen K. A new mouse TCR V gamma gene that shows remarkable evolutionary conservation. EMBO J. 1987 Jul;6(7):1941–1944. doi: 10.1002/j.1460-2075.1987.tb02455.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Quertermous T., Murre C., Dialynas D., Duby A. D., Strominger J. L., Waldman T. A., Seidman J. G. Human T-cell gamma chain genes: organization, diversity, and rearrangement. Science. 1986 Jan 17;231(4735):252–255. doi: 10.1126/science.3079918. [DOI] [PubMed] [Google Scholar]
  33. Roth M. E., Lacy M. J., McNeil L. K., Kranz D. M. Selection of variable-joining region combinations in the alpha chain of the T cell receptor. Science. 1988 Sep 9;241(4871):1354–1358. doi: 10.1126/science.2970673. [DOI] [PubMed] [Google Scholar]
  34. Saito H., Kranz D. M., Takagaki Y., Hayday A. C., Eisen H. N., Tonegawa S. A third rearranged and expressed gene in a clone of cytotoxic T lymphocytes. Nature. 1984 Nov 1;312(5989):36–40. doi: 10.1038/312036a0. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Sowder J. T., Chen C. L., Ager L. L., Chan M. M., Cooper M. D. A large subpopulation of avian T cells express a homologue of the mammalian T gamma/delta receptor. J Exp Med. 1988 Feb 1;167(2):315–322. doi: 10.1084/jem.167.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Staerz U. D., Rammensee H. G., Benedetto J. D., Bevan M. J. Characterization of a murine monoclonal antibody specific for an allotypic determinant on T cell antigen receptor. J Immunol. 1985 Jun;134(6):3994–4000. [PubMed] [Google Scholar]
  38. 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]
  39. Toneguzzo F., Glynn S., Levi E., Mjolsness S., Hayday A. Use of a chemically modified T7 DNA polymerase for manual and automated sequencing of supercoiled DNA. Biotechniques. 1988 May;6(5):460–469. [PubMed] [Google Scholar]

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