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. 1995 Dec 1;182(6):1921–1930. doi: 10.1084/jem.182.6.1921

Ontogenic development and tissue distribution of V gamma 1-expressing gamma/delta T lymphocytes in normal mice

PMCID: PMC2192273  PMID: 7500038

Abstract

A hamster monoclonal antibody (mAb) recognizing an epitope in the V gamma 1-J gamma 4-C gamma 4 chain of the gamma/delta T cell receptor has been generated. Using this mAb, we have quantitated the occurrence of V gamma 1-bearing gamma/delta T cells in the developing thymus and in the lymphoid organs and several epithelia of adult mice. The V gamma 1-expressing cells constitute a minor gamma/delta T cell subpopulation during fetal and early postnatal life, but they constitute a major population of gamma/delta T cells in the thymus and in the peripheral lymphoid organs in adult mice. In addition, we found that V gamma 1- bearing cells comprise a large proportion (15-60%) of the gamma/delta T cells present in the intestinal epithelium (i-IEL) in all strains of mice tested. V gamma 1+ i-IEL are present in athymic (nude) mice and in antigen-free mice, demonstrating that they can develop extrathymically and that their presence in the intestinal epithelium is independent of the antigenic load of the gut. Our results show that V gamma 1-bearing lymphocytes account for the largest population of gamma/delta T cells in the mouse. This population includes a thymus-dependent component that homes to the secondary lymphoid organs and a thymus-independent component that constitutes a major fraction of the gamma/delta i-IELs.

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Selected References

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  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. 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]
  3. 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]
  4. Bandeira A., Itohara S., Bonneville M., Burlen-Defranoux O., Mota-Santos T., Coutinho A., Tonegawa S. Extrathymic origin of intestinal intraepithelial lymphocytes bearing T-cell antigen receptor gamma delta. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):43–47. doi: 10.1073/pnas.88.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bluestone J. A., Cron R. Q., Barrett T. A., Houlden B., Sperling A. I., Dent A., Hedrick S., Rellahan B., Matis L. A. Repertoire development and ligand specificity of murine TCR gamma delta cells. Immunol Rev. 1991 Apr;120:5–33. doi: 10.1111/j.1600-065x.1991.tb00585.x. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Born W., Hall L., Dallas A., Boymel J., Shinnick T., Young D., Brennan P., O'Brien R. Recognition of a peptide antigen by heat shock--reactive gamma delta T lymphocytes. Science. 1990 Jul 6;249(4964):67–69. doi: 10.1126/science.1695022. [DOI] [PubMed] [Google Scholar]
  8. Coffman R. L., Weissman I. L. A monoclonal antibody that recognizes B cells and B cell precursors in mice. J Exp Med. 1981 Feb 1;153(2):269–279. doi: 10.1084/jem.153.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cron R. Q., Gajewski T. F., Sharrow S. O., Fitch F. W., Matis L. A., Bluestone J. A. Phenotypic and functional analysis of murine CD3+,CD4-,CD8- TCR-gamma delta-expressing peripheral T cells. J Immunol. 1989 Jun 1;142(11):3754–3762. [PubMed] [Google Scholar]
  10. De Libero G., Casorati G., Giachino C., Carbonara C., Migone N., Matzinger P., Lanzavecchia A. Selection by two powerful antigens may account for the presence of the major population of human peripheral gamma/delta T cells. J Exp Med. 1991 Jun 1;173(6):1311–1322. doi: 10.1084/jem.173.6.1311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dialynas D. P., Quan Z. S., Wall K. A., Pierres A., Quintáns J., Loken M. R., Pierres M., Fitch F. W. Characterization of the murine T cell surface molecule, designated L3T4, identified by monoclonal antibody GK1.5: similarity of L3T4 to the human Leu-3/T4 molecule. J Immunol. 1983 Nov;131(5):2445–2451. [PubMed] [Google Scholar]
  12. Emoto M., Danbara H., Yoshikai Y. Induction of gamma/delta T cells in murine salmonellosis by an avirulent but not by a virulent strain of Salmonella choleraesuis. J Exp Med. 1992 Aug 1;176(2):363–372. doi: 10.1084/jem.176.2.363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Findly R. C., Roberts S. J., Hayday A. C. Dynamic response of murine gut intraepithelial T cells after infection by the coccidian parasite Eimeria. Eur J Immunol. 1993 Oct;23(10):2557–2564. doi: 10.1002/eji.1830231027. [DOI] [PubMed] [Google Scholar]
  14. Fisch P., Malkovsky M., Kovats S., Sturm E., Braakman E., Klein B. S., Voss S. D., Morrissey L. W., DeMars R., Welch W. J. Recognition by human V gamma 9/V delta 2 T cells of a GroEL homolog on Daudi Burkitt's lymphoma cells. Science. 1990 Nov 30;250(4985):1269–1273. doi: 10.1126/science.1978758. [DOI] [PubMed] [Google Scholar]
  15. Fisch P., Oettel K., Fudim N., Surfus J. E., Malkovsky M., Sondel P. M. MHC-unrestricted cytotoxic and proliferative responses of two distinct human gamma/delta T cell subsets to Daudi cells. J Immunol. 1992 Apr 15;148(8):2315–2323. [PubMed] [Google Scholar]
  16. 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]
  17. Gaynor J. J., Unkenholz K. M. Sequence analysis of a genomic clone encoding an endochitinase from Solanum tuberosum. Nucleic Acids Res. 1989 Jul 25;17(14):5855–5856. doi: 10.1093/nar/17.14.5855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Guy-Grand D., Cerf-Bensussan N., Malissen B., Malassis-Seris M., Briottet C., Vassalli P. Two gut intraepithelial CD8+ lymphocyte populations with different T cell receptors: a role for the gut epithelium in T cell differentiation. J Exp Med. 1991 Feb 1;173(2):471–481. doi: 10.1084/jem.173.2.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Haas W., Pereira P., Tonegawa S. Gamma/delta cells. Annu Rev Immunol. 1993;11:637–685. doi: 10.1146/annurev.iy.11.040193.003225. [DOI] [PubMed] [Google Scholar]
  22. Happ M. P., Kubo R. T., Palmer E., Born W. K., O'Brien R. L. Limited receptor repertoire in a mycobacteria-reactive subset of gamma delta T lymphocytes. Nature. 1989 Dec 7;342(6250):696–698. doi: 10.1038/342696a0. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. 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]
  25. 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]
  26. Holoshitz J., Koning F., Coligan J. E., De Bruyn J., Strober S. Isolation of CD4- CD8- mycobacteria-reactive T lymphocyte clones from rheumatoid arthritis synovial fluid. Nature. 1989 May 18;339(6221):226–229. doi: 10.1038/339226a0. [DOI] [PubMed] [Google Scholar]
  27. Ikuta K., Kina T., MacNeil I., Uchida N., Peault B., Chien Y. H., Weissman I. L. A developmental switch in thymic lymphocyte maturation potential occurs at the level of hematopoietic stem cells. Cell. 1990 Sep 7;62(5):863–874. doi: 10.1016/0092-8674(90)90262-d. [DOI] [PubMed] [Google Scholar]
  28. Inoue T., Yoshikai Y., Matsuzaki G., Nomoto K. Early appearing gamma/delta-bearing T cells during infection with Calmétte Guérin bacillus. J Immunol. 1991 Apr 15;146(8):2754–2762. [PubMed] [Google Scholar]
  29. Ishikawa H., Li Y., Abeliovich A., Yamamoto S., Kaufmann S. H., Tonegawa S. Cytotoxic and interferon gamma-producing activities of gamma delta T cells in the mouse intestinal epithelium are strain dependent. Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8204–8208. doi: 10.1073/pnas.90.17.8204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. 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]
  33. 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]
  34. Kabelitz D., Bender A., Prospero T., Wesselborg S., Janssen O., Pechhold K. The primary response of human gamma/delta + T cells to Mycobacterium tuberculosis is restricted to V gamma 9-bearing cells. J Exp Med. 1991 Jun 1;173(6):1331–1338. doi: 10.1084/jem.173.6.1331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kabelitz D., Bender A., Schondelmaier S., Schoel B., Kaufmann S. H. A large fraction of human peripheral blood gamma/delta + T cells is activated by Mycobacterium tuberculosis but not by its 65-kD heat shock protein. J Exp Med. 1990 Mar 1;171(3):667–679. doi: 10.1084/jem.171.3.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kelly K. A., Pearse M., Lefrancois L., Scollay R. Emigration of selected subsets of gamma delta + T cells from the adult murine thymus. Int Immunol. 1993 Apr;5(4):331–335. doi: 10.1093/intimm/5.4.331. [DOI] [PubMed] [Google Scholar]
  37. Kikuchi G. E., Roberts K., Shevach E. M., Coligan J. E. Gene transfer demonstrates that the V gamma 1.1C gamma 4V delta 6C delta T cell receptor is essential for autoreactivity. J Immunol. 1992 Mar 1;148(5):1302–1307. [PubMed] [Google Scholar]
  38. 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]
  39. Koning F., Yokoyama W. M., Maloy W. L., Stingl G., McConnell T. J., Cohen D. I., Shevach E. M., Coligan J. E. Expression of C gamma 4 T cell receptors and lack of isotype exclusion by dendritic epidermal T cell lines. J Immunol. 1988 Sep 15;141(6):2057–2062. [PubMed] [Google Scholar]
  40. Krangel M. S., Yssel H., Brocklehurst C., Spits H. A distinct wave of human T cell receptor gamma/delta lymphocytes in the early fetal thymus: evidence for controlled gene rearrangement and cytokine production. J Exp Med. 1990 Sep 1;172(3):847–859. doi: 10.1084/jem.172.3.847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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]
  42. 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]
  43. Kyes S., Carew E., Carding S. R., Janeway C. A., Jr, Hayday A. Diversity in T-cell receptor gamma gene usage in intestinal epithelium. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5527–5531. doi: 10.1073/pnas.86.14.5527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Kyes S., Hayday A. Disparate types of gamma delta T cell. Res Immunol. 1990 Sep;141(7):582–587. doi: 10.1016/0923-2494(90)90060-c. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. Ledbetter J. A., Herzenberg L. A. Xenogeneic monoclonal antibodies to mouse lymphoid differentiation antigens. Immunol Rev. 1979;47:63–90. doi: 10.1111/j.1600-065x.1979.tb00289.x. [DOI] [PubMed] [Google Scholar]
  47. 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]
  48. 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]
  49. Lefrancois L. Phenotypic complexity of intraepithelial lymphocytes of the small intestine. J Immunol. 1991 Sep 15;147(6):1746–1751. [PubMed] [Google Scholar]
  50. Modlin R. L., Pirmez C., Hofman F. M., Torigian V., Uyemura K., Rea T. H., Bloom B. R., Brenner M. B. Lymphocytes bearing antigen-specific gamma delta T-cell receptors accumulate in human infectious disease lesions. Nature. 1989 Jun 15;339(6225):544–548. doi: 10.1038/339544a0. [DOI] [PubMed] [Google Scholar]
  51. Mosley R. L., Styre D., Klein J. R. Differentiation and functional maturation of bone marrow-derived intestinal epithelial T cells expressing membrane T cell receptor in athymic radiation chimeras. J Immunol. 1990 Sep 1;145(5):1369–1375. [PubMed] [Google Scholar]
  52. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983 Dec 16;65(1-2):55–63. doi: 10.1016/0022-1759(83)90303-4. [DOI] [PubMed] [Google Scholar]
  53. O'Brien R. L., Fu Y. X., Cranfill R., Dallas A., Ellis C., Reardon C., Lang J., Carding S. R., Kubo R., Born W. Heat shock protein Hsp60-reactive gamma delta cells: a large, diversified T-lymphocyte subset with highly focused specificity. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4348–4352. doi: 10.1073/pnas.89.10.4348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. O'Brien R. L., Happ M. P., Dallas A., Palmer E., Kubo R., Born W. K. Stimulation of a major subset of lymphocytes expressing T cell receptor gamma delta by an antigen derived from Mycobacterium tuberculosis. Cell. 1989 May 19;57(4):667–674. doi: 10.1016/0092-8674(89)90135-9. [DOI] [PubMed] [Google Scholar]
  55. Ohmen J. D., Barnes P. F., Uyemura K., Lu S. Z., Grisso C. L., Modlin R. L. The T cell receptors of human gamma delta T cells reactive to Mycobacterium tuberculosis are encoded by specific V genes but diverse V-J junctions. J Immunol. 1991 Nov 15;147(10):3353–3359. [PubMed] [Google Scholar]
  56. Ohteki T., Abo T., Seki S., Kobata T., Yagita H., Okumura K., Kumagai K. Predominant appearance of gamma/delta T lymphocytes in the liver of mice after birth. Eur J Immunol. 1991 Jul;21(7):1733–1740. doi: 10.1002/eji.1830210722. [DOI] [PubMed] [Google Scholar]
  57. Ota Y., Kobata T., Seki M., Yagita H., Shimada S., Huang Y. Y., Takagaki Y., Okumura K. Extrathymic origin of V gamma 1/V delta 6 T cells in the skin. Eur J Immunol. 1992 Feb;22(2):595–598. doi: 10.1002/eji.1830220245. [DOI] [PubMed] [Google Scholar]
  58. Panchamoorthy G., McLean J., Modlin R. L., Morita C. T., Ishikawa S., Brenner M. B., Band H. A predominance of the T cell receptor V gamma 2/V delta 2 subset in human mycobacteria-responsive T cells suggests germline gene encoded recognition. J Immunol. 1991 Nov 15;147(10):3360–3369. [PubMed] [Google Scholar]
  59. Roark C. E., Vollmer M. K., Cranfill R. L., Carding S. R., Born W. K., O'Brien R. L. Liver gamma delta T cells. TCR junctions reveal differences in heat shock protein-60-reactive cells in liver and spleen. J Immunol. 1993 Jun 1;150(11):4867–4875. [PubMed] [Google Scholar]
  60. Sperling A. I., Cron R. Q., Decker D. C., Stern D. A., Bluestone J. A. Peripheral T cell receptor gamma delta variable gene repertoire maps to the T cell receptor loci and is influenced by positive selection. J Immunol. 1992 Nov 15;149(10):3200–3207. [PubMed] [Google Scholar]
  61. Springer T., Galfrè G., Secher D. S., Milstein C. Monoclonal xenogeneic antibodies to murine cell surface antigens: identification of novel leukocyte differentiation antigens. Eur J Immunol. 1978 Aug;8(8):539–551. doi: 10.1002/eji.1830080802. [DOI] [PubMed] [Google Scholar]
  62. 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]
  63. Sturm E., Braakman E., Fisch P., Vreugdenhil R. J., Sondel P., Bolhuis R. L. Human V gamma 9-V delta 2 T cell receptor-gamma delta lymphocytes show specificity to Daudi Burkitt's lymphoma cells. J Immunol. 1990 Nov 15;145(10):3202–3208. [PubMed] [Google Scholar]
  64. 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]
  65. Takagaki Y., Nakanishi N., Ishida I., Kanagawa O., Tonegawa S. T cell receptor-gamma and -delta genes preferentially utilized by adult thymocytes for the surface expression. J Immunol. 1989 Mar 15;142(6):2112–2121. [PubMed] [Google Scholar]
  66. Uehira M., Matsuda H., Hikita I., Sakata T., Fujiwara H., Nishimoto H. The development of dermatitis infiltrated by gamma delta T cells in IL-7 transgenic mice. Int Immunol. 1993 Dec;5(12):1619–1627. doi: 10.1093/intimm/5.12.1619. [DOI] [PubMed] [Google Scholar]
  67. Viney J. L., Kilshaw P. J., MacDonald T. T. Cytotoxic alpha/beta+ and gamma/delta+ T cells in murine intestinal epithelium. Eur J Immunol. 1990 Jul;20(7):1623–1626. doi: 10.1002/eji.1830200734. [DOI] [PubMed] [Google Scholar]
  68. Whetsell M., Mosley R. L., Whetsell L., Schaefer F. V., Miller K. S., Klein J. R. Rearrangement and junctional-site sequence analyses of T-cell receptor gamma genes in intestinal intraepithelial lymphocytes from murine athymic chimeras. Mol Cell Biol. 1991 Dec;11(12):5902–5909. doi: 10.1128/mcb.11.12.5902. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. White J., Blackman M., Bill J., Kappler J., Marrack P., Gold D. P., Born W. Two better cell lines for making hybridomas expressing specific T cell receptors. J Immunol. 1989 Sep 15;143(6):1822–1825. [PubMed] [Google Scholar]
  70. Wilde D. B., Roberts K., Sturmhöfel K., Kikuchi G., Coligan J. E., Shevach E. M. Mouse autoreactive gamma/delta T cells. I. Functional properties of autoreactive T cell hybridomas. Eur J Immunol. 1992 Feb;22(2):483–489. doi: 10.1002/eji.1830220229. [DOI] [PubMed] [Google Scholar]
  71. Wright A., Lee J. E., Link M. P., Smith S. D., Carroll W., Levy R., Clayberger C., Krensky A. M. Cytotoxic T lymphocytes specific for self tumor immunoglobulin express T cell receptor delta chain. J Exp Med. 1989 May 1;169(5):1557–1564. doi: 10.1084/jem.169.5.1557. [DOI] [PMC free article] [PubMed] [Google Scholar]

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