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. 1993 Jul 1;178(1):1–16. doi: 10.1084/jem.178.1.1

Analysis of T cell antigen receptor (TCR) expression by human peripheral blood CD4-8- alpha/beta T cells demonstrates preferential use of several V beta genes and an invariant TCR alpha chain

PMCID: PMC2191070  PMID: 8391057

Abstract

CD4-CD8- (double negative [DN]) alpha/beta T cells are a largely uncharacterized subpopulation of unknown function. To investigate whether these cells are selected to recognize particular antigens or antigen-presenting molecules, DN alpha/beta T cells were purified from the peripheral blood of five normal donors and their T cell receptor (TCR) alpha and beta chains were examined. Random cloning of TCR alpha chains by single-sided polymerase chain reaction (PCR) amplification identified an invariant rearrangement between V alpha 24 and J alpha Q, with no N region diversity, which was expressed preferentially by DN alpha/beta T cells from all donors. Random cloning also identified a precise V alpha 7.2-J alpha (IGRJa14) rearrangement, with two variable amino acids encoded in the V-J junction, which was enriched in the DN alpha/beta T cell preparations from some, but not all, donors. Analysis of TCR beta chains by quantitative PCR amplification demonstrated that the expression of four V beta gene families, V beta 2, 8, 11, and 13, was markedly increased in these DN alpha/beta T cell preparations. The expression of particular TCRs by DN alpha/beta T cells from multiple donors indicates that these cells, or at least a subpopulation of cells with this phenotype, recognize a limited spectrum of antigens and suggests that they may use nonpolymorphic antigen-presenting molecules.

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Selected References

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  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. Balk S. P., Bleicher P. A., Terhorst C. Isolation and characterization of a cDNA and gene coding for a fourth CD1 molecule. Proc Natl Acad Sci U S A. 1989 Jan;86(1):252–256. doi: 10.1073/pnas.86.1.252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Balk S. P., Ebert E. C., Blumenthal R. L., McDermott F. V., Wucherpfennig K. W., Landau S. B., Blumberg R. S. Oligoclonal expansion and CD1 recognition by human intestinal intraepithelial lymphocytes. Science. 1991 Sep 20;253(5026):1411–1415. doi: 10.1126/science.1716785. [DOI] [PubMed] [Google Scholar]
  4. Band H., Hochstenbach F., McLean J., Hata S., Krangel M. S., Brenner M. B. Immunochemical proof that a novel rearranging gene encodes the T cell receptor delta subunit. Science. 1987 Oct 30;238(4827):682–684. doi: 10.1126/science.3672118. [DOI] [PubMed] [Google Scholar]
  5. Bogue M., Gilfillan S., Benoist C., Mathis D. Regulation of N-region diversity in antigen receptors through thymocyte differentiation and thymus ontogeny. Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):11011–11015. doi: 10.1073/pnas.89.22.11011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brenner M. B., Strominger J. L., Krangel M. S. The gamma delta T cell receptor. Adv Immunol. 1988;43:133–192. [PubMed] [Google Scholar]
  7. Brooks E. G., Wirt D. P., Goldblum R. M., Vaidya S., Asuncion M. T., Patterson J. C., Ware C. F., Klimpel G. R. Double-negative (CD4- CD8-) T cells with an alpha/beta T cell receptor. Non-MHC-restricted cytolytic activity and lymphokine production. J Immunol. 1990 Jun 15;144(12):4507–4512. [PubMed] [Google Scholar]
  8. Budd R. C., Miescher G. C., Howe R. C., Lees R. K., Bron C., MacDonald H. R. Developmentally regulated expression of T cell receptor beta chain variable domains in immature thymocytes. J Exp Med. 1987 Aug 1;166(2):577–582. doi: 10.1084/jem.166.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Calabi F., Bradbury A. The CD1 system. Tissue Antigens. 1991 Jan;37(1):1–9. doi: 10.1111/j.1399-0039.1991.tb01836.x. [DOI] [PubMed] [Google Scholar]
  10. Calman A. F., Peterlin B. M. Expression of T cell receptor genes in human B cells. J Exp Med. 1986 Dec 1;164(6):1940–1957. doi: 10.1084/jem.164.6.1940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ceredig R., Lynch F., Newman P. Phenotypic properties, interleukin 2 production, and developmental origin of a "mature" subpopulation of Lyt-2- L3T4- mouse thymocytes. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8578–8582. doi: 10.1073/pnas.84.23.8578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Choi Y. W., Kotzin B., Herron L., Callahan J., Marrack P., Kappler J. Interaction of Staphylococcus aureus toxin "superantigens" with human T cells. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8941–8945. doi: 10.1073/pnas.86.22.8941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Clark J. M. Novel non-templated nucleotide addition reactions catalyzed by procaryotic and eucaryotic DNA polymerases. Nucleic Acids Res. 1988 Oct 25;16(20):9677–9686. doi: 10.1093/nar/16.20.9677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Crispe I. N., Moore M. W., Husmann L. A., Smith L., Bevan M. J., Shimonkevitz R. P. Differentiation potential of subsets of CD4-8- thymocytes. Nature. 1987 Sep 24;329(6137):336–339. doi: 10.1038/329336a0. [DOI] [PubMed] [Google Scholar]
  15. Davidson W. F., Dumont F. J., Bedigian H. G., Fowlkes B. J., Morse H. C., 3rd Phenotypic, functional, and molecular genetic comparisons of the abnormal lymphoid cells of C3H-lpr/lpr and C3H-gld/gld mice. J Immunol. 1986 Jun 1;136(11):4075–4084. [PubMed] [Google Scholar]
  16. Delfau M. H., Hance A. J., Lecossier D., Vilmer E., Grandchamp B. Restricted diversity of V gamma 9-JP rearrangements in unstimulated human gamma/delta T lymphocytes. Eur J Immunol. 1992 Sep;22(9):2437–2443. doi: 10.1002/eji.1830220937. [DOI] [PubMed] [Google Scholar]
  17. Egerton M., Scollay R. Intrathymic selection of murine TCR alpha beta+CD4-CD8- thymocytes. Int Immunol. 1990;2(2):157–163. doi: 10.1093/intimm/2.2.157. [DOI] [PubMed] [Google Scholar]
  18. Fowlkes B. J., Kruisbeek A. M., Ton-That H., Weston M. A., Coligan J. E., Schwartz R. H., Pardoll D. M. A novel population of T-cell receptor alpha beta-bearing thymocytes which predominantly expresses a single V beta gene family. Nature. 1987 Sep 17;329(6136):251–254. doi: 10.1038/329251a0. [DOI] [PubMed] [Google Scholar]
  19. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Groh V., Fabbi M., Hochstenbach F., Maziarz R. T., Strominger J. L. Double-negative (CD4-CD8-) lymphocytes bearing T-cell receptor alpha and beta chains in normal human skin. Proc Natl Acad Sci U S A. 1989 Jul;86(13):5059–5063. doi: 10.1073/pnas.86.13.5059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Guidos C. J., Weissman I. L., Adkins B. Developmental potential of CD4-8- thymocytes. Peripheral progeny include mature CD4-8- T cells bearing alpha beta T cell receptor. J Immunol. 1989 Jun 1;142(11):3773–3780. [PubMed] [Google Scholar]
  23. 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]
  24. Havran W. L., Chien Y. H., Allison J. P. Recognition of self antigens by skin-derived T cells with invariant gamma delta antigen receptors. Science. 1991 Jun 7;252(5011):1430–1432. doi: 10.1126/science.1828619. [DOI] [PubMed] [Google Scholar]
  25. Herman A., Kappler J. W., Marrack P., Pullen A. M. Superantigens: mechanism of T-cell stimulation and role in immune responses. Annu Rev Immunol. 1991;9:745–772. doi: 10.1146/annurev.iy.09.040191.003525. [DOI] [PubMed] [Google Scholar]
  26. Huang L., Crispe I. N. Distinctive selection mechanisms govern the T cell receptor repertoire of peripheral CD4-CD8- alpha/beta T cells. J Exp Med. 1992 Sep 1;176(3):699–706. doi: 10.1084/jem.176.3.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Klein M. H., Concannon P., Everett M., Kim L. D., Hunkapiller T., Hood L. Diversity and structure of human T-cell receptor alpha-chain variable region genes. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6884–6888. doi: 10.1073/pnas.84.19.6884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Koseki H., Asano H., Inaba T., Miyashita N., Moriwaki K., Lindahl K. F., Mizutani Y., Imai K., Taniguchi M. Dominant expression of a distinctive V14+ T-cell antigen receptor alpha chain in mice. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7518–7522. doi: 10.1073/pnas.88.17.7518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kubota H., Okazaki H., Onuma M., Kano S., Hattori M., Minato N. CD3+4-8- alpha beta T cell population with biased T cell receptor V gene usage. Presence in bone marrow and possible involvement of IL-3 for their extrathymic development. J Immunol. 1992 Aug 15;149(4):1143–1150. [PubMed] [Google Scholar]
  30. Kusunoki Y., Hirai Y., Kyoizumi S., Akiyama M. Evidence for in vivo clonal proliferation of unique population of blood CD4-/CD8- T cells bearing T-cell receptor alpha and beta chains in two normal men. Blood. 1992 Jun 1;79(11):2965–2972. [PubMed] [Google Scholar]
  31. Köhler G., Milstein C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature. 1975 Aug 7;256(5517):495–497. doi: 10.1038/256495a0. [DOI] [PubMed] [Google Scholar]
  32. Lanier L. L., Cwirla S., Federspiel N., Phillips J. H. Human natural killer cells isolated from peripheral blood do not rearrange T cell antigen receptor beta chain genes. J Exp Med. 1986 Jan 1;163(1):209–214. doi: 10.1084/jem.163.1.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ledbetter J. A., Evans R. L., Lipinski M., Cunningham-Rundles C., Good R. A., Herzenberg L. A. Evolutionary conservation of surface molecules that distinguish T lymphocyte helper/inducer and cytotoxic/suppressor subpopulations in mouse and man. J Exp Med. 1981 Feb 1;153(2):310–323. doi: 10.1084/jem.153.2.310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Loh E. Y., Elliott J. F., Cwirla S., Lanier L. L., Davis M. M. Polymerase chain reaction with single-sided specificity: analysis of T cell receptor delta chain. Science. 1989 Jan 13;243(4888):217–220. doi: 10.1126/science.2463672. [DOI] [PubMed] [Google Scholar]
  35. Londei M., Verhoef A., De Berardinis P., Kissonerghis M., Grubeck-Loebenstein B., Feldmann M. Definition of a population of CD4-8- T cells that express the alpha beta T-cell receptor and respond to interleukins 2, 3, and 4. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8502–8506. doi: 10.1073/pnas.86.21.8502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Malissen B., Rebai N., Liabeuf A., Mawas C. Human cytotoxic T cell structures associated with expression of cytolysis. I. Analysis at the clonal cell level of the cytolysis-inhibiting effect of 7 monoclonal antibodies. Eur J Immunol. 1982 Sep;12(9):739–747. doi: 10.1002/eji.1830120908. [DOI] [PubMed] [Google Scholar]
  37. Martin L. H., Calabi F., Lefebvre F. A., Bilsland C. A., Milstein C. Structure and expression of the human thymocyte antigens CD1a, CD1b, and CD1c. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9189–9193. doi: 10.1073/pnas.84.24.9189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Mieno M., Suto R., Obata Y., Udono H., Takahashi T., Shiku H., Nakayama E. CD4-CD8- T cell receptor alpha beta T cells: generation of an in vitro major histocompatibility complex class I specific cytotoxic T lymphocyte response and allogeneic tumor rejection. J Exp Med. 1991 Jul 1;174(1):193–201. doi: 10.1084/jem.174.1.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Morisset J., Trannoy E., De Talance A., Spinella S., Debré P., Godet P., Seman M. Genetics and strain distribution of concanavalin A-reactive Ly-2-, L3T4- peripheral precursors of autoreactive T cells. Eur J Immunol. 1988 Mar;18(3):387–394. doi: 10.1002/eji.1830180311. [DOI] [PubMed] [Google Scholar]
  40. Oksenberg J. R., Stuart S., Begovich A. B., Bell R. B., Erlich H. A., Steinman L., Bernard C. C. Limited heterogeneity of rearranged T-cell receptor V alpha transcripts in brains of multiple sclerosis patients. Nature. 1990 May 24;345(6273):344–346. doi: 10.1038/345344a0. [DOI] [PubMed] [Google Scholar]
  41. Porcelli S., Brenner M. B., Greenstein J. L., Balk S. P., Terhorst C., Bleicher P. A. Recognition of cluster of differentiation 1 antigens by human CD4-CD8-cytolytic T lymphocytes. Nature. 1989 Oct 5;341(6241):447–450. doi: 10.1038/341447a0. [DOI] [PubMed] [Google Scholar]
  42. Porcelli S., Morita C. T., Brenner M. B. CD1b restricts the response of human CD4-8- T lymphocytes to a microbial antigen. Nature. 1992 Dec 10;360(6404):593–597. doi: 10.1038/360593a0. [DOI] [PubMed] [Google Scholar]
  43. Quaratino S., Murison G., Knyba R. E., Verhoef A., Londei M. Human CD4- CD8- alpha beta+ T cells express a functional T cell receptor and can be activated by superantigens. J Immunol. 1991 Nov 15;147(10):3319–3323. [PubMed] [Google Scholar]
  44. Reinherz E. L., Kung P. C., Goldstein G., Levey R. H., Schlossman S. F. Discrete stages of human intrathymic differentiation: analysis of normal thymocytes and leukemic lymphoblasts of T-cell lineage. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1588–1592. doi: 10.1073/pnas.77.3.1588. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Rivas A., Koide J., Laus R., Engleman E. G. Alloantigen-specific cytotoxic clones bearing the alpha,beta T cell antigen receptor but not CD4 or CD8 molecules. J Immunol. 1990 Jul 15;145(2):470–476. [PubMed] [Google Scholar]
  46. Roman-Roman S., Ferradini L., Azocar J., Genevée C., Hercend T., Triebel F. Studies on the human T cell receptor alpha/beta variable region genes. I. Identification of 7 additional V alpha subfamilies and 14 J alpha gene segments. Eur J Immunol. 1991 Apr;21(4):927–933. doi: 10.1002/eji.1830210411. [DOI] [PubMed] [Google Scholar]
  47. Sakamoto A., Sumida T., Maeda T., Itoh M., Asai T., Takahashi H., Yoshida S., Koike T., Tomioka H., Yoshida S. T cell receptor V beta repertoire of double-negative alpha/beta T cells in patients with systemic sclerosis. Arthritis Rheum. 1992 Aug;35(8):944–948. doi: 10.1002/art.1780350815. [DOI] [PubMed] [Google Scholar]
  48. Schlitt H. J., Kurrle R., Wonigeit K. T cell activation by monoclonal antibodies directed to different epitopes on the human T cell receptor/CD3 complex: evidence for two different modes of activation. Eur J Immunol. 1989 Sep;19(9):1649–1655. doi: 10.1002/eji.1830190920. [DOI] [PubMed] [Google Scholar]
  49. Scott B., Blüthmann H., Teh H. S., von Boehmer H. The generation of mature T cells requires interaction of the alpha beta T-cell receptor with major histocompatibility antigens. Nature. 1989 Apr 13;338(6216):591–593. doi: 10.1038/338591a0. [DOI] [PubMed] [Google Scholar]
  50. Seman M., Boudaly S., Roger T., Morisset J., Pham G. Autoreactive T cells in normal mice: unrestricted recognition of self peptides on dendritic cell I-A molecules by CD4-CD8- T cell receptor alpha/beta+ T cell clones expressing V beta 8.1 gene segments. Eur J Immunol. 1990 Jun;20(6):1265–1272. doi: 10.1002/eji.1830200611. [DOI] [PubMed] [Google Scholar]
  51. Servenius B., Rask L., Peterson P. A. Class II genes of the human major histocompatibility complex. The DO beta gene is a divergent member of the class II beta gene family. J Biol Chem. 1987 Jun 25;262(18):8759–8766. [PubMed] [Google Scholar]
  52. Shivakumar S., Tsokos G. C., Datta S. K. T cell receptor alpha/beta expressing double-negative (CD4-/CD8-) and CD4+ T helper cells in humans augment the production of pathogenic anti-DNA autoantibodies associated with lupus nephritis. J Immunol. 1989 Jul 1;143(1):103–112. [PubMed] [Google Scholar]
  53. Singer P. A., Balderas R. S., McEvilly R. J., Bobardt M., Theofilopoulos A. N. Tolerance-related V beta clonal deletions in normal CD4-8-, TCR-alpha/beta + and abnormal lpr and gld cell populations. J Exp Med. 1989 Dec 1;170(6):1869–1877. doi: 10.1084/jem.170.6.1869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Strober S., Dejbachsh-Jones S., Van Vlasselaer P., Duwe G., Salimi S., Allison J. P. Cloned natural suppressor cell lines express the CD3+CD4-CD8- surface phenotype and the alpha, beta heterodimer of the T cell antigen receptor. J Immunol. 1989 Aug 15;143(4):1118–1122. [PubMed] [Google Scholar]
  55. 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]
  56. Sykes M. Unusual T cell populations in adult murine bone marrow. Prevalence of CD3+CD4-CD8- and alpha beta TCR+NK1.1+ cells. J Immunol. 1990 Nov 15;145(10):3209–3215. [PubMed] [Google Scholar]
  57. Takahama Y., Kosugi A., Singer A. Phenotype, ontogeny, and repertoire of CD4-CD8- T cell receptor alpha beta + thymocytes. Variable influence of self-antigens on T cell receptor V beta usage. J Immunol. 1991 Feb 15;146(4):1134–1141. [PubMed] [Google Scholar]
  58. Takahama Y., Shores E. W., Singer A. Negative selection of precursor thymocytes before their differentiation into CD4+CD8+ cells. Science. 1992 Oct 23;258(5082):653–656. doi: 10.1126/science.1357752. [DOI] [PubMed] [Google Scholar]
  59. Takahama Y., Singer A. Post-transcriptional regulation of early T cell development by T cell receptor signals. Science. 1992 Nov 27;258(5087):1456–1462. doi: 10.1126/science.1439838. [DOI] [PubMed] [Google Scholar]
  60. Tonnelle C., DeMars R., Long E. O. DO beta: a new beta chain gene in HLA-D with a distinct regulation of expression. EMBO J. 1985 Nov;4(11):2839–2847. doi: 10.1002/j.1460-2075.1985.tb04012.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Toyonaga B., Mak T. W. Genes of the T-cell antigen receptor in normal and malignant T cells. Annu Rev Immunol. 1987;5:585–620. doi: 10.1146/annurev.iy.05.040187.003101. [DOI] [PubMed] [Google Scholar]
  62. Watanabe-Fukunaga R., Brannan C. I., Copeland N. G., Jenkins N. A., Nagata S. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature. 1992 Mar 26;356(6367):314–317. doi: 10.1038/356314a0. [DOI] [PubMed] [Google Scholar]
  63. Wilson A., Ewing T., Owens T., Scollay R., Shortman K. T cell antigen receptor expression by subsets of Ly-2-L3T4- (CD8-CD4-) thymocytes. J Immunol. 1988 Mar 1;140(5):1470–1476. [PubMed] [Google Scholar]
  64. Wirt D. P., Brooks E. G., Vaidya S., Klimpel G. R., Waldmann T. A., Goldblum R. M. Novel T-lymphocyte population in combined immunodeficiency with features of graft-versus-host disease. N Engl J Med. 1989 Aug 10;321(6):370–374. doi: 10.1056/NEJM198908103210606. [DOI] [PubMed] [Google Scholar]
  65. Yankelevich B., Knobloch C., Nowicki M., Dennert G. A novel cell type responsible for marrow graft rejection in mice. T cells with NK phenotype cause acute rejection of marrow grafts. J Immunol. 1989 May 15;142(10):3423–3430. [PubMed] [Google Scholar]
  66. Yui K., Hashimoto Y., Wadsworth S., Greene M. I. Characterization of Lyt-2-, L3T4- class I-specific cytolytic clones in C3H-gld/gld mice. Implications for functions of accessory molecules and programmed development. J Exp Med. 1987 Oct 1;166(4):1026–1040. doi: 10.1084/jem.166.4.1026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Yui K., Wadsworth S., Yellen A., Hashimoto Y., Kokai Y., Greene M. I. Molecular and functional properties of novel T cell subsets in C3H-gld/gld and nude mice. Implications for thymic and extrathymic maturation. Immunol Rev. 1988 Aug;104:121–155. doi: 10.1111/j.1600-065x.1988.tb00761.x. [DOI] [PubMed] [Google Scholar]
  68. de Talance A., Regnier D., Spinella S., Morisset J., Seman M. Origin of autoreactive T helper cells. I. Characterization of Thy-1+, Lyt-, L3T4- precursors in the spleen of normal mice. J Immunol. 1986 Aug 15;137(4):1101–1108. [PubMed] [Google Scholar]
  69. von Boehmer H., Kirberg J., Rocha B. An unusual lineage of alpha/beta T cells that contains autoreactive cells. J Exp Med. 1991 Nov 1;174(5):1001–1008. doi: 10.1084/jem.174.5.1001. [DOI] [PMC free article] [PubMed] [Google Scholar]

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