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. 1991 Dec;44(12):1012–1017. doi: 10.1136/jcp.44.12.1012

Tissue distribution of human gamma delta T cells: no evidence for general epithelial tropism.

T M Vroom 1, G Scholte 1, F Ossendorp 1, J Borst 1
PMCID: PMC494970  PMID: 1838746

Abstract

In man and mice only a small proportion of T cells in the peripheral lymphoid compartment express the gamma delta T cell receptor (TCR). In mice, however, gamma delta T cells comprise the predominant population at particular epithelial sites--in epidermis and epithelia of intestine, reproductive organs, and tongue. The distribution of gamma delta T cells in normal human tissues was investigated, paying particular attention to epithelial layers. In all lymphatic organs and in epithelia of a wide variety of non-lymphatic organs, including the respiratory tract, male and female reproductive organs and tongue, gamma delta T cells constituted less than 5% of total T cells, with the remainder expressing TCR alpha beta. The only exception was the intestine, where gamma delta T cells were preferentially situated in the columnar epithelium of the crypts, rather than in the lamina propria. It is concluded, therefore, that human gamma delta T cells do not display a general epithelial tropism and are, in terms of relative numbers, no more able than alpha beta T cells to carry out continuous surveillance of the immune system against infection or transformation in epithelia. gamma delta T cells may, however, have a specialised function in the epithelium of the intestinal tract.

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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., Goodman T., LeFrancois L., Allison J. P. Distinct antigen receptor repertoires of two classes of murine epithelium-associated T cells. Nature. 1989 Sep 7;341(6237):60–62. doi: 10.1038/341060a0. [DOI] [PubMed] [Google Scholar]
  2. Augustin A., Kubo R. T., Sim G. K. Resident pulmonary lymphocytes expressing the gamma/delta T-cell receptor. Nature. 1989 Jul 20;340(6230):239–241. doi: 10.1038/340239a0. [DOI] [PubMed] [Google Scholar]
  3. Bandeira A., Mota-Santos T., Itohara S., Degermann S., Heusser C., Tonegawa S., Coutinho A. Localization of gamma/delta T cells to the intestinal epithelium is independent of normal microbial colonization. J Exp Med. 1990 Jul 1;172(1):239–244. doi: 10.1084/jem.172.1.239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bonyhadi M., Weiss A., Tucker P. W., Tigelaar R. E., Allison J. P. Delta is the Cx-gene product in the gamma/delta antigen receptor of dendritic epidermal cells. Nature. 1987 Dec 10;330(6148):574–576. doi: 10.1038/330574a0. [DOI] [PubMed] [Google Scholar]
  5. Borst J., van Dongen J. J., Bolhuis R. L., Peters P. J., Hafler D. A., de Vries E., van de Griend R. J. Distinct molecular forms of human T cell receptor gamma/delta detected on viable T cells by a monoclonal antibody. J Exp Med. 1988 May 1;167(5):1625–1644. doi: 10.1084/jem.167.5.1625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bos J. D., Teunissen M. B., Cairo I., Krieg S. R., Kapsenberg M. L., Das P. K., Borst J. T-cell receptor gamma delta bearing cells in normal human skin. J Invest Dermatol. 1990 Jan;94(1):37–42. doi: 10.1111/1523-1747.ep12873333. [DOI] [PubMed] [Google Scholar]
  7. Brenner M. B., McLean J., Scheft H., Warnke R. A., Jones N., Strominger J. L. Characterization and expression of the human alpha beta T cell receptor by using a framework monoclonal antibody. J Immunol. 1987 Mar 1;138(5):1502–1509. [PubMed] [Google Scholar]
  8. Brenner M. B., Strominger J. L., Krangel M. S. The gamma delta T cell receptor. Adv Immunol. 1988;43:133–192. [PubMed] [Google Scholar]
  9. Bucy R. P., Chen C. L., Cihak J., Lösch U., Cooper M. D. Avian T cells expressing gamma delta receptors localize in the splenic sinusoids and the intestinal epithelium. J Immunol. 1988 Oct 1;141(7):2200–2205. [PubMed] [Google Scholar]
  10. Bucy R. P., Chen C. L., Cooper M. D. Tissue localization and CD8 accessory molecule expression of T gamma delta cells in humans. J Immunol. 1989 May 1;142(9):3045–3049. [PubMed] [Google Scholar]
  11. Carding S. R., Kyes S., Jenkinson E. J., Kingston R., Bottomly K., Owen J. J., Hayday A. C. Developmentally regulated fetal thymic and extrathymic T-cell receptor gamma delta gene expression. Genes Dev. 1990 Aug;4(8):1304–1315. doi: 10.1101/gad.4.8.1304. [DOI] [PubMed] [Google Scholar]
  12. Chien Y. H., Iwashima M., Wettstein D. A., Kaplan K. B., Elliott J. F., Born W., Davis M. M. T-cell receptor delta gene rearrangements in early thymocytes. Nature. 1987 Dec 24;330(6150):722–727. doi: 10.1038/330722a0. [DOI] [PubMed] [Google Scholar]
  13. Clevers H., Alarcon B., Wileman T., Terhorst C. The T cell receptor/CD3 complex: a dynamic protein ensemble. Annu Rev Immunol. 1988;6:629–662. doi: 10.1146/annurev.iy.06.040188.003213. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Falini B., Flenghi L., Pileri S., Pelicci P., Fagioli M., Martelli M. F., Moretta L., Ciccone E. Distribution of T cells bearing different forms of the T cell receptor gamma/delta in normal and pathological human tissues. J Immunol. 1989 Oct 15;143(8):2480–2488. [PubMed] [Google Scholar]
  16. 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]
  17. Groh V., Porcelli S., Fabbi M., Lanier L. L., Picker L. J., Anderson T., Warnke R. A., Bhan A. K., Strominger J. L., Brenner M. B. Human lymphocytes bearing T cell receptor gamma/delta are phenotypically diverse and evenly distributed throughout the lymphoid system. J Exp Med. 1989 Apr 1;169(4):1277–1294. doi: 10.1084/jem.169.4.1277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Halstensen T. S., Scott H., Brandtzaeg P. Intraepithelial T cells of the TcR gamma/delta+ CD8- and V delta 1/J delta 1+ phenotypes are increased in coeliac disease. Scand J Immunol. 1989 Dec;30(6):665–672. doi: 10.1111/j.1365-3083.1989.tb02474.x. [DOI] [PubMed] [Google Scholar]
  19. Haregewoin A., Soman G., Hom R. C., Finberg R. W. Human gamma delta+ T cells respond to mycobacterial heat-shock protein. Nature. 1989 Jul 27;340(6231):309–312. doi: 10.1038/340309a0. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Havran W. L., Allison J. P. Origin of Thy-1+ dendritic epidermal cells of adult mice from fetal thymic precursors. Nature. 1990 Mar 1;344(6261):68–70. doi: 10.1038/344068a0. [DOI] [PubMed] [Google Scholar]
  22. Hirt W., Saalmüller A., Reddehase M. J. Distinct gamma/delta T cell receptors define two subsets of circulating porcine CD2-CD4-CD8- T lymphocytes. Eur J Immunol. 1990 Feb;20(2):265–269. doi: 10.1002/eji.1830200206. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Itohara S., Farr A. G., Lafaille J. J., Bonneville M., Takagaki Y., Haas W., Tonegawa S. Homing of a gamma delta thymocyte subset with homogeneous T-cell receptors to mucosal epithelia. Nature. 1990 Feb 22;343(6260):754–757. doi: 10.1038/343754a0. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. 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]
  28. 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]
  29. Lafaille J. J., DeCloux A., Bonneville M., Takagaki Y., Tonegawa S. Junctional sequences of T cell receptor gamma delta genes: implications for gamma delta T cell lineages and for a novel intermediate of V-(D)-J joining. Cell. 1989 Dec 1;59(5):859–870. doi: 10.1016/0092-8674(89)90609-0. [DOI] [PubMed] [Google Scholar]
  30. Lawetzky A., Tiefenthaler G., Kubo R., Hünig T. Identification and characterization of rat T cell subpopulations expressing T cell receptors alpha/beta and gamma/delta. Eur J Immunol. 1990 Feb;20(2):343–349. doi: 10.1002/eji.1830200217. [DOI] [PubMed] [Google Scholar]
  31. Lefrancois L., LeCorre R., Mayo J., Bluestone J. A., Goodman T. Extrathymic selection of TCR gamma delta + T cells by class II major histocompatibility complex molecules. Cell. 1990 Oct 19;63(2):333–340. doi: 10.1016/0092-8674(90)90166-c. [DOI] [PubMed] [Google Scholar]
  32. Li C. Y., Yam L. T., Crosby W. H. Histochemical characterization of cellular and structural elements of the human spleen. J Histochem Cytochem. 1972 Dec;20(12):1049–1058. doi: 10.1177/20.12.1049. [DOI] [PubMed] [Google Scholar]
  33. Mackay C. R., Beya M. F., Matzinger P. Gamma/delta T cells express a unique surface molecule appearing late during thymic development. Eur J Immunol. 1989 Aug;19(8):1477–1483. doi: 10.1002/eji.1830190820. [DOI] [PubMed] [Google Scholar]
  34. Mackay C. R., Hein W. R. A large proportion of bovine T cells express the gamma delta T cell receptor and show a distinct tissue distribution and surface phenotype. Int Immunol. 1989;1(5):540–545. doi: 10.1093/intimm/1.5.540. [DOI] [PubMed] [Google Scholar]
  35. Raulet D. H. Immunology. Antigens for gamma/delta T cells. Nature. 1989 Jun 1;339(6223):342–343. doi: 10.1038/339342a0. [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. Spencer J., Isaacson P. G., Diss T. C., MacDonald T. T. Expression of disulfide-linked and non-disulfide-linked forms of the T cell receptor gamma/delta heterodimer in human intestinal intraepithelial lymphocytes. Eur J Immunol. 1989 Jul;19(7):1335–1338. doi: 10.1002/eji.1830190728. [DOI] [PubMed] [Google Scholar]
  38. Stingl G., Koning F., Yamada H., Yokoyama W. M., Tschachler E., Bluestone J. A., Steiner G., Samelson L. E., Lew A. M., Coligan J. E. Thy-1+ dendritic epidermal cells express T3 antigen and the T-cell receptor gamma chain. Proc Natl Acad Sci U S A. 1987 Jul;84(13):4586–4590. doi: 10.1073/pnas.84.13.4586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Takagaki Y., DeCloux A., Bonneville M., Tonegawa S. Diversity of gamma delta T-cell receptors on murine intestinal intra-epithelial lymphocytes. Nature. 1989 Jun 29;339(6227):712–714. doi: 10.1038/339712a0. [DOI] [PubMed] [Google Scholar]

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