T cells expressing two different T cell receptors form a heterogeneous population containing autoreactive clones

Molecular Immunology

Volumn 48, Issue 1-3, 2010, Pages 211-218

  Kekäläinen, Eliisa ^a   Hänninen, Arno ^b   Maksimow, Mikael ^c   Arstila, T Petteri ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

^c UNIVERSITY OF TURKU   (Finland)

Author keywords

Allelic exclusion; Autoimmunity; T cell receptor; T cells; Tolerance

Indexed keywords

T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNITY; CELL HETEROGENEITY; CELL SELECTION; FLOW CYTOMETRY; GENETIC TRANSFECTION; IMMUNOPATHOLOGY; LYMPHOCYTOPENIA; MOLECULAR CLONING; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN CELL; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE;

ANIMALS; AUTOIMMUNITY; CELL SEPARATION; FLOW CYTOMETRY; GENE REARRANGEMENT, T-LYMPHOCYTE; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; RECEPTORS, ANTIGEN, T-CELL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES;

MUS MUSCULUS;

EID: 78649526747     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2010.08.008     Document Type: Article

References (44)

1. Arstila T.P., Casrouge A., Baron V., Even J., Kanellopoulos J., Kourilsky P. A direct estimate of the human alphabeta T cell receptor diversity. Science 1999, 286:958-961.
2. Baccala R., Theofilopoulos A.N. The new paradigm of T-cell homeostatic proliferation-induced autoimmunity. Trends. Immunol. 2005, 26:5-8.
3. Bouneaud C., Kourilsky P., Bousso P. Impact of negative selection on the T cell repertoire reactive to a self-peptide: a large fraction of T cell clones escapes clonal deletion. Immunity 2000, 13:829-840.
4. Casanova J.L., Romero P., Widmann C., Kourilsky P., Maryanski J.L. T cell receptor genes in a series of class I major histocompatibility complex-restricted cytotoxic T lymphocyte clones specific for a plasmodium berghei nonapeptide: implications for T cell allelic exclusion and antigen-specific repertoire. J. Exp. Med. 1991, 174:1371-1383.
5. Cho B.K., Rao V.P., Ge Q., Eisen H.N., Chen J. Homeostasis-stimulated proliferation drives naive T cells to differentiate directly into memory T cells. J. Exp. Med. 2000, 192:549-556.
6. Corthay A., Nandakumar K.S., Holmdahl R. Evaluation of the percentage of peripheral T cells with two different T cell receptor alpha-chains and of their potential role in autoimmunity. J. Autoimmun. 2001, 16:423-429.
7. Curotto de Lafaille M.A., Lino A.C., Kutchukhidze N., Lafaille J.J. CD25-T cells generate CD25+Foxp3+ regulatory T cells by peripheral expansion. J. Immunol. 2004, 173:7259-7268.
8. Elliott J.I. Selection of dual Valpha T cells. Eur. J. Immunol. 1998, 28:2115-2123.
9. Elliott J.I., Altmann D.M. Dual T cell receptor alpha chain T cells in autoimmunity. J. Exp. Med. 1995, 182:953-959.
10. Ernst B., Lee D.S., Chang J.M., Sprent J., Surh C.D. The peptide ligands mediating positive selection in the thymus control T cell survival and homeostatic proliferation in the periphery. Immunity 1999, 11:173-181.
11. Fossati G., Cooke A., Papafio R.Q., Haskins K., Stockinger B. Triggering a second T cell receptor on diabetogenic T cells can prevent induction of diabetes. J. Exp. Med. 1999, 190:577-583.
12. Gavin M.A., Clarke S.R., Negrou E., Gallegos A., Rudensky A. Homeostasis and anergy of CD4(+)CD25(+) suppressor T cells in vivo. Nat. Immunol. 2002, 3:33-41.
13. Ge Q., Hu H., Eisen H.N., Chen J. Different contributions of thymopoiesis and homeostasis-driven proliferation to the reconstitution of naive and memory T cell compartments. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:2989-2994.
14. Ge Q., Rao V.P., Cho B.K., Eisen H.N., Chen J. Dependence of lymphopenia-induced T cell proliferation on the abundance of peptide/MHC epitopes and strength of their interaction with T cell receptors. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:1728-1733.
15. Gladow M., Uckert W., Blankenstein T. Dual T cell receptor T cells with two defined specificities mediate tumor suppression via both receptors. Eur. J. Immunol. 2004, 34:1882-1891.
16. Goldrath A.W., Bevan M.J. Low-affinity ligands for the TCR drive proliferation of mature CD8+ T cells in lymphopenic hosts. Immunity 1999, 11:183-190.
17. Gorochov G., Neumann A.U., Kereveur A., Parizot C., Li T., Katlama C., Karmochkine M., Raguin G., Autran B., Debré P. Perturbation of CD4+ and CD8+ T-cell repertoires during progression to AIDS and regulation of the CD4+ repertoire during antiviral therapy. Nat. Med. 1998, 4:215-221.
18. Hardardottir F., Baron J.L., Janeway C.A. T cells with two functional antigen-specific receptors. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:354-358.
19. He X., Janeway C.A., Levine M., Robinson E., Preston-Hurlburt P., Viret C., Bottomly K. Dual receptor T cells extend the immune repertoire for foreign antigens. Nat. Immunol. 2002, 3:127-134.
20. Hazenberg M.D., Verschuren M.C., Hamann D., Miedema F., van Dongen J.J. T cell receptor excision circles as markers for recent thymic emigrants: basic aspects, technical approach, and guidelines for interpretation. J. Mol. Med. 2001, 79:631-640.
21. Heath W.R., Carbone F.R., Bertolino P., Kelly J., Cose S., Miller J.F. Expression of two T cell receptor alpha chains on the surface of normal murine T cells. Eur. J. Immunol. 1995, 25:1617-1623.
22. Herman A.E., Freeman G.J., Mathis D., Benoist C. CD4+CD25+ T regulatory cells dependent on ICOS promote regulation of effector cells in the prediabetic lesion. J. Exp. Med. 2004, 199:1479-1489.
23. Hsieh C.S., Liang Y., Tyznik A.J., Self S.G., Liggitt D., Rudensky A.Y. Recognition of the peripheral self by naturally arising CD25+ CD4+ T cell receptors. Immunity 2004, 21:267-277.
24. JAX staff, 2000. Immunodeficient model selection: choosing a nude, scid or Rag1 strain. JAX Communication - Scientific Publication for Users of JAX Mice.
25. Jordan M.S., Boesteanu A., Reed A.J., Petrone A.L., Holenbeck A.E., Lerman M.A., Naji A., Caton A.J. Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat. Immunol. 2001, 2:301-306.
26. Kieper W.C., Troy A., Burghardt J.T., Ramsey C., Lee J.Y., Jiang H.Q., Dummer W., Shen H., Cebra J.J., Surh C.D. Recent immune status determines the source of antigens that drive homeostatic T cell expansion. J. Immunol. 2005, 174:3158-3163.
27. King C., Ilic A., Koelsch K., Sarvetnick N. Homeostatic expansion of T cells during immune insufficiency generates autoimmunity. Cell 2004, 117:265-277.
28. Lacorazza H.D., Nikolich-Zugich J. Exclusion and inclusion of TCR alpha proteins during T cell development in TCR-transgenic and normal mice. J. Immunol. 2004, 173:5591-5600.
29. La Gruta N.L., Driel I.R., Gleeson P.A. Peripheral T cell expansion in lymphopenic mice results in a restricted T cell repertoire. Eur. J. Immunol. 2000, 30:3380-3386.
30. Le Campion A., Gagnerault M.C., Auffray C., Becourt C., Poitrasson-Riviere M., Lallemand E., Bienvenu B., Martin B., Lepault F., Lucas B. Lymphopenia-induced spontaneous T-cell proliferation as a cofactor for autoimmune disease development. Blood 2009, 114(9):1784-1793.
31. Malissen M., Trucy J., Jouvin-Marche E., Cazenave P.A., Scollay R., Malissen B. Regulation of TCR alpha and beta gene allelic exclusion during T-cell development. Immunol. Today 1992, 13:315-322.
32. Morris G.P., Allen P.M. Cutting edge: highly alloreactive dual TCR T cells play a dominant role in graft-versus-host disease. J. Immunol. 2009, 182:6639-6643.
33. Moses C.T., Thorstenson K.M., Jameson S.C., Khoruts A. Competition for self ligands restrains homeostatic proliferation of naive CD4 T cells. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:1185-1190.
34. Olivares-Villagomez D., Wang Y., Lafaille J.J. Regulatory CD4(+) T cells expressing endogenous T cell receptor chains protect myelin basic protein-specific transgenic mice from spontaneous autoimmune encephalomyelitis. J. Exp. Med. 1998, 188:1883-1894.
35. Padovan E., Casorati G., Dellabona P., Meyer S., Brockhaus M., Lanzavecchia A. Expression of two T cell receptor alpha chains: dual receptor T cells. Science 1993, 262:422-424.
36. Petrie H.T., Livak F., Schatz D.G., Strasser A., Crispe I.N., Shortman K. Multiple rearrangements in T cell receptor alpha chain genes maximize the production of useful thymocytes. J. Exp. Med. 1993, 178:615-622.
37. Peng Y., Laouar Y., Li M.O., Green E.A., Flavell R.A. TGF-beta regulates in vivo expansion of Foxp3-expressing CD4+CD25+ regulatory T cells responsible for protection against diabetes. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:4572-4577.
38. Piper H., Litwin S., Mehr R. Models for antigen receptor gene rearrangement. II. Multiple rearrangement in the TCR: allelic exclusion or inclusion?. J. Immunol. 1999, 163:1799-1808.
39. Shultz L.D., Schweitzer P.A., Christianson S.W., Gott B., Schweitzer I.B., Tennent B., McKenna S., Mobraaten L., Rajan T.V., Greiner D.L. Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J. Immunol. 1995, 154:180-191.
40. Szanya V., Ermann J., Taylor C., Holness C., Fathman C.G. The subpopulation of CD4+CD25+ splenocytes that delays adoptive transfer of diabetes expresses l-selectin and high levels of CCR7. J. Immunol. 2002, 169:2461-2465.
41. Tuovinen H., Salminen J.T., Arstila T.P. Most human thymic and peripheral-blood CD4+ CD25+ regulatory T cells express 2 T-cell receptors. Blood 2006, 108:4063-4070.
42. Van de Keere F., Tonegawa S. CD4(+) T cells prevent spontaneous experimental autoimmune encephalomyelitis in anti-myelin basic protein T cell receptor transgenic mice. J. Exp. Med. 1998, 188:1875-1882.
43. Zal T., Weiss S., Mellor A., Stockinger B. Expression of a second receptor rescues self-specific T cells from thymic deletion and allows activation of autoreactive effector function. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:9102-9107.
44. Zerrahn J., Held W., Raulet D.H. The MHC reactivity of the T cell repertoire prior to positive and negative selection. Cell 1997, 88:627-636.