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. 1990 Dec;87(24):9727–9731. doi: 10.1073/pnas.87.24.9727

Expression of the thymus leukemia antigen in mouse intestinal epithelium.

R Hershberg 1, P Eghtesady 1, B Sydora 1, K Brorson 1, H Cheroutre 1, R Modlin 1, M Kronenberg 1
PMCID: PMC55246  PMID: 2263622

Abstract

The Qa and Tla regions of the mouse major histocompatibility complex contain a series of genes encoding proteins with structural similarity to the class I transplantation antigens of the same complex. In contrast to the genes encoding the transplantation antigens, the Qa and Tla genes show very little polymorphism. Function(s) of the proteins encoded by the Qa and Tla loci remain an enigma. Recently, the protein products of the Qa and Tla loci, often referred to as class Ib major histocompatibility complex molecules, have been proposed to present antigen to gamma delta T cells. In mice, gamma delta T cells have been found concentrated in several epithelial barriers and in the skin; yet, expression of serologically detectable Tla antigens is believed restricted to thymocytes, activated T lymphocytes, and some T-cell leukemias. Here we report that luminal epithelial cells of the mouse small intestine express the thymus leukemia antigen (TLA). We also find that, unlike T cells in Peyer's patches, a significant fraction of intestinal epithelial lymphocytes also express TLA. RNA prepared from intestinal cells contains transcripts of the T18d gene, which encodes TLA. These data extend the known expression profile of TLA molecules to mature lymphocytes and to nonhematopoietic cells. These data also demonstrate the specific expression of TLA on antigen-presenting cells in a site enriched for T cells that express gamma delta T-cell antigen receptor.

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Selected References

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

  1. 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]
  2. Bonneville M., Ito K., Krecko E. G., Itohara S., Kappes D., Ishida I., Kanagawa O., Janeway C. A., Murphy D. B., Tonegawa S. Recognition of a self major histocompatibility complex TL region product by gamma delta T-cell receptors. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5928–5932. doi: 10.1073/pnas.86.15.5928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bonneville M., Itohara S., Krecko E. G., Mombaerts P., Ishida I., Katsuki M., Berns A., Farr A. G., Janeway C. A., Jr, Tonegawa S. Transgenic mice demonstrate that epithelial homing of gamma/delta T cells is determined by cell lineages independent of T cell receptor specificity. J Exp Med. 1990 Apr 1;171(4):1015–1026. doi: 10.1084/jem.171.4.1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brorson K. A., Richards S., Hunt S. W., 3rd, Cheroutre H., Lindahl K. F., Hood L. Analysis of a new class I gene mapping to the Hmt region of the mouse. Immunogenetics. 1989;30(4):273–283. doi: 10.1007/BF02421331. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  7. Chorney M. J., Mashimo H., Bushkin Y., Nathenson S. G. Characterization of the thymus leukemia (TL) product encoded by the BALB/c T3c gene by DNA-mediated gene transfer. Comparison to the T13c product and BALB/c leukemia TL. J Immunol. 1989 Dec 1;143(11):3762–3768. [PubMed] [Google Scholar]
  8. Cook R. G., Landolfi N. F. Expression of the thymus leukemia antigen by activated peripheral T lymphocytes. J Exp Med. 1983 Sep 1;158(3):1012–1017. doi: 10.1084/jem.158.3.1012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Dent A. L., Matis L. A., Hooshmand F., Widacki S. M., Bluestone J. A., Hedrick S. M. Self-reactive gamma delta T cells are eliminated in the thymus. Nature. 1990 Feb 22;343(6260):714–719. doi: 10.1038/343714a0. [DOI] [PubMed] [Google Scholar]
  11. Fisher D. A., Hunt S. W., 3rd, Hood L. Structure of a gene encoding a murine thymus leukemia antigen, and organization of Tla genes in the BALB/c mouse. J Exp Med. 1985 Aug 1;162(2):528–545. doi: 10.1084/jem.162.2.528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Goodenow R. S., McMillan M., Nicolson M., Sher B. T., Eakle K., Davidson N., Hood L. Identification of the class I genes of the mouse major histocompatibility complex by DNA-mediated gene transfer. Nature. 1982 Nov 18;300(5889):231–237. doi: 10.1038/300231a0. [DOI] [PubMed] [Google Scholar]
  13. Goodman T., Lefrancois L. Intraepithelial lymphocytes. Anatomical site, not T cell receptor form, dictates phenotype and function. J Exp Med. 1989 Nov 1;170(5):1569–1581. doi: 10.1084/jem.170.5.1569. [DOI] [PMC free article] [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. Guesdon J. L., Ternynck T., Avrameas S. The use of avidin-biotin interaction in immunoenzymatic techniques. J Histochem Cytochem. 1979 Aug;27(8):1131–1139. doi: 10.1177/27.8.90074. [DOI] [PubMed] [Google Scholar]
  16. Hedley M. L., Drake B. L., Head J. R., Tucker P. W., Forman J. Differential expression of the class I MHC genes in the embryo and placenta during midgestational development in the mouse. J Immunol. 1989 Jun 1;142(11):4046–4053. [PubMed] [Google Scholar]
  17. Hood L., Steinmetz M., Malissen B. Genes of the major histocompatibility complex of the mouse. Annu Rev Immunol. 1983;1:529–568. doi: 10.1146/annurev.iy.01.040183.002525. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Kroczek R. A., Gunter K. C., Germain R. N., Shevach E. M. Thy-1 functions as a signal transduction molecule in T lymphocytes and transfected B lymphocytes. Nature. 1986 Jul 10;322(6075):181–184. doi: 10.1038/322181a0. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Lefrancois L., Goodman T. In vivo modulation of cytolytic activity and Thy-1 expression in TCR-gamma delta+ intraepithelial lymphocytes. Science. 1989 Mar 31;243(4899):1716–1718. doi: 10.1126/science.2564701. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Mayer L., Shlien R. Evidence for function of Ia molecules on gut epithelial cells in man. J Exp Med. 1987 Nov 1;166(5):1471–1483. doi: 10.1084/jem.166.5.1471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Modlin R. L., Segal G. P., Hofman F. M., Walley M. S., Johnson R. H., Taylor C. R., Rea T. H. In situ localization of T lymphocytes in disseminated coccidioidomycosis. J Infect Dis. 1985 Feb;151(2):314–319. doi: 10.1093/infdis/151.2.314. [DOI] [PubMed] [Google Scholar]
  26. Obata Y., Chen Y. T., Stockert E., Old L. J. Structural analysis of TL genes of the mouse. Proc Natl Acad Sci U S A. 1985 Aug;82(16):5475–5479. doi: 10.1073/pnas.82.16.5475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Obata Y., Stockert E., Chen Y. T., Takahashi T., Old L. J. Influence of 5' flanking sequences on TL and H-2 expression in transfected L cells. Proc Natl Acad Sci U S A. 1988 May;85(10):3541–3545. doi: 10.1073/pnas.85.10.3541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ostrand-Rosenberg S., Nickerson D. A., Clements V. K., Garcia E. P., Lamouse-Smith E., Hood L., Stroynowski I. Embryonal carcinoma cells express Qa and Tla class I genes of the major histocompatibility complex. Proc Natl Acad Sci U S A. 1989 Jul;86(13):5084–5088. doi: 10.1073/pnas.86.13.5084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rowden G., Misra B., Higley H., Howard R. Antigens specified by the Tla locus are expressed on the surface of murine Langerhans cells. J Invest Dermatol. 1983 Jul;81(1):2–6. doi: 10.1111/1523-1747.ep12537381. [DOI] [PubMed] [Google Scholar]
  30. Sharrow S. O., Arn J. S., Stroynowski I., Hood L., Sachs D. H. Epitope clusters of Qa-2 antigens defined by a panel of new monoclonal antibodies. J Immunol. 1989 May 15;142(10):3495–3502. [PubMed] [Google Scholar]
  31. Shen F. W., Chorney M. J., Boyse E. A. Further polymorphism of the Tla locus defined by monoclonal TL antibodies. Immunogenetics. 1982;15(6):573–578. doi: 10.1007/BF00347051. [DOI] [PubMed] [Google Scholar]
  32. Strominger J. L. The gamma delta T cell receptor and class Ib MHC-related proteins: enigmatic molecules of immune recognition. Cell. 1989 Jun 16;57(6):895–898. doi: 10.1016/0092-8674(89)90326-7. [DOI] [PubMed] [Google Scholar]
  33. Stroynowski I. Molecules related to class-I major histocompatibility complex antigens. Annu Rev Immunol. 1990;8:501–530. doi: 10.1146/annurev.iy.08.040190.002441. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Vidović D., Roglić M., McKune K., Guerder S., MacKay C., Dembić Z. Qa-1 restricted recognition of foreign antigen by a gamma delta T-cell hybridoma. Nature. 1989 Aug 24;340(6235):646–650. doi: 10.1038/340646a0. [DOI] [PubMed] [Google Scholar]

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