Cd3 ligation on immature thymocytes generates antagonist-like signals appropriate for CD8 lineage commitment, independently of T cell receptor specificity

Journal of Experimental Medicine

Volumn 187, Issue 8, 1998, Pages 1249-1260

  Basson, M Albert ^a   Bommhardt, Ursula ^a   Cole, Michael S ^b   Tso, J Yun ^b   Zamoyska, Rose ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b PROTEIN DESIGN LABS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; IMMUNOGLOBULIN F(AB')2 FRAGMENT; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCLONAL ANTIBODY; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DENDRITIC CELL; LYMPHOCYTE DIFFERENTIATION; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMOCYTE;

ANIMALS; ANTIGENS, CD3; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINEAGE; CYTOTOXICITY TESTS, IMMUNOLOGIC; HEMATOPOIETIC STEM CELLS; HISTOCOMPATIBILITY ANTIGENS; IMMUNOGLOBULIN FRAGMENTS; IMMUNOLOGIC CAPPING; LIGANDS; LYMPHOCYTE ACTIVATION; MICE; MICE, MUTANT STRAINS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, CYTOTOXIC; THYMUS GLAND; TYROSINE; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 0032550367     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.187.8.1249     Document Type: Article

References (65)

1. Müller, K.-P., and B.A. Kyewski. 1995. T cell receptor (TcR) targeting in mice lacking CD4 or major histocompatibility complex (MHC) class II: rescue of CD4 T cell lineage without co-engagement of TcR/CD4 by MHC class II. Eur. J. Immunol. 25:896-902.
2. + T cells by TcR ligation without aggregation even in the absence of MHC. Nature. 371:67-70.
3. Cibotti, R., J.A. Punt, K.S. Dash, S.O. Sharrow, and A. Singer. 1997. Surface molecules that drive T cell development in vitro in the absence of thymic epithelium and in the absence of lineage-specific signals. Immunity. 6:245-255.
4. Bommhardt, U., M.S. Cole, J. Yun Tso, and R. Zamoyska. 1997. Signals through CD8 or CD4 can induce commitment to the CD4 lineage in the thymus. Eur. J. Immunol. 27:1152-1163.
5. Hogquist, K.A., S.C. Jameson, W.R. Heath, J.L. Howard, M.J. Bevan, and F.R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell. 76:17-27.
6. Ashton-Rickardt, P.G., A. Bandeira, J.R. Delaney, L. Van Kaer, H.-P. Pircher, R.M. Zinkernagel, and S. Tonegawa. 1994. Evidence for a differential avidity model of T cell selection in the thymus. Cell. 76:651-663.
7. Spain, L.M., J.L. Jorgensen, M.M. Davis, and L.J. Berg. 1994. A peptide antigen antagonist prevents the differentiation of T cell receptor transgenic thymocytes. J. Immunol. 152:1709-1717.
8. Sebzda, E., V.A. Wallace, J. Mayer, R.S.M. Yeung, T.W. Mak, and P.S. Ohashi. 1994. Positive and negative thymocyte selection induced by different concentrations of a single peptide. Science. 263:1615-1618.
9. Sebzda, E., T.M. Kundig, C.T. Thomson, K. Aoki, S.-Y. Mak, J.P. Mayer, T. Zamborelli, S.G. Nathenson, and P.M. Ohashi. 1996. Mature T cell reactivity altered by peptide agonist that induces positive selection. J. Exp. Med. 183:1093-1104.
10. + T cells. Immunity. 3:79-86.
11. + thymocytes to the CD4 lineage without TcR engagement. Int. Immunol. 8:297-306.
12. Takahama, Y., and H. Nakauchi. 1996. Phorbol ester and calcium ionophore can replace TCR signals that induce positive selection of CD4 T cells. J. Immunol. 157:1508-1513.
13. Henrickson, M., J. Reid, J.S. Bellet, S.S. Sawchuk, and R. Hirsch. 1995. Comparison of in vivo efficacy and mechanism of action of antimurine monoclonal antibodies directed against TCR αβ (H57-597) and CD3 (145-2C11). Transplantation (Baltimore). 60:828-835.
14. 2) anti-CD3 monoclonal antibody. Transplantation (Baltimore). 60:1331-1337.
15. Chatenoud, L., J. Primo, and J.-F. Bach. 1997. CD3 antibody-induced dominant self-tolerance in overtly diabetic NOD mice. J. Immunol. 158:2947-2954.
16. Madrenas, J., L.A. Chau, J. Smith, J.A. Bluestone, and R.N. Germain. 1997. The efficiency of CD4 recruitment to ligand-engaged TCR controls the agonist/partial agonist properties of peptide-MHC molecule ligands. J. Exp. Med. 185:219-229.
17. Smith, J.A., J. Yun Tso, M.R. Clark, M.S. Cole, and J.A. Bluestone. 1997. Nonmitogenic anti-CD3 monoclonal antibodies deliver a partial T cell receptor signal and induce clonal anergy. J. Exp. Med. 185:1413-1422.
18. Itano, A., P. Salmon, D. Kioussis, M. Tolaini, P. Corbella, and E. Robey. 1996. The cytoplasmic domain of CD4 promotes the development of CD4 lineage T cells. J. Exp. Med. 183:731-741.
19. Veillette, A., J.C. Zuniga-Pflucker, J.B. Bolen, and A.M. Kruisbeek. 1989. Engagement of CD4 and CD8 expressed on immature thymocytes induces activation of intracellular tyrosine phosphorylation pathways. J. Exp. Med. 170:1671-1680.
20. Kostelny, S.A., M.S. Cole, and J. Yun Tso. 1992. Formation of a bispecific antibody by the use of leucine zippers. J. Immunol. 148:1547-1553.
21. + cytolytic T cells, Nature. 344:742-746.
22. Cosgrove, D., D. Gray, A. Dierich, J. Kaufman, M. Lemeur, C. Benoist, and D. Mathis. 1991. Mice lacking MHC class II molecules. Cell. 66:1051-1066.
23. Spanopoulou, E., C. Roman, L. Corcoran, M. Schlissel, D. Silver, D. Nemazee, M. Nussenweig, S. Shinton, R. Hardy, and D. Baltimore. 1994. Functional immunoglobulin transgenes guide ordered B-cell differentiation in Rag-1 deficient mice. Genes Dev. 8:1030-1042.
24. Mamalaki, C., J. Elliot, T. Norton, N. Yannoutsos, A.R. Townsend, P. Chandler, E. Simpson, and D. Kioussis. 1993. Positive and negative selection in transgenic mice expressing a T-cell receptor specific for influenza nucleoprotein and endogenous superantigen. Dev. Immunol. 3:159-174.
25. Zal, T., A. Volkmann, and B. Stockinger. 1994. Mechanisms of tolerance induction in major histocompatibility complex class II-restricted T cells specific for a blood-borne self-antigen. J. Exp. Med. 180:2089-2099.
26. Inaba, K., M. Inaba, N. Romani, H. Aya, M. Deguchi, S. Ikehara, S. Muramatsu, and R.M. Steinman. 1992. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176:1693-1702.
27. Bluestone, J.A., R.Q. Cron, T.A. Barrett, B. Houlden, A.I. Sperling, A. Dent, S. Hedrick, B. Rellahan, and L.A. Matis. 1991. Repertoire development and ligand specificity of murine TCRγδ cells. Immunol. Rev. 120:5-33.
28. Hogquist, K.A., A.J. Tomlinson, W.C. Kieper, M.A. McGargill, M.C. Hart, S. Naylor, and S.C. Jameson. 1997. Identification of a naturally occurring ligand for thymic positive selection. Immunity. 6:389-399.
29. + T cells in the thymus. Cell. 73:1041-1049.
30. Lucas, B., F. Vasseur, and C. Penit. 1993. Normal sequence of phenotypic transitions in one cohort of 5-bromo-2′-deoxyurine-pulse-labelled thymocytes. J. Immunol. 151:4574-4582.
31. Levelt, C.N., A. Ehrfield, and K. Eichmann. 1993. Regulation of thymocyte development through CD3. I. Timepoint of ligation of CD3∈ determines clonal deletion or induction of developmental program. J. Exp. Med. 177:707-716.
32. -/- mice in the absence of TCRβ chain expression. Int. Immunol. 6:995-1001.
33. Luton, F., M. Buferne, J. Davoust, A.-M. Schmitt-Verhulst, and C. Boyer. 1994. Evidence for protein tyrosine kinase involvement in ligand-induced TCR/CD3 internalization and surface redistribution. J. Immunol. 153:63-72.
34. Valitutti, S., S. Müller, M. Cella, E. Padovan, and A. Lanzavecchia. 1995. Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature. 375:148-151.
35. + T cells. J. Exp. Med. 185:641-651.
36. Sloan-Lancaster, J., B.D. Evavold, and P.M. Allen. 1993. Induction of T-cell anergy by altered T-cell-receptor ligand on live antigen-presenting cells. Nature. 363:156-159.
37. De Magistris, M.T., J. Alexander, M. Coggeshal, A. Altman, F.C.A. Gaeta, H.M. Grey, and A. Sette. 1992. Antigen-analog-major histocompatibility complexes act as antagonists of the T cell receptor. Cell. 68:625-634.
38. Sloan-Lancaster, J., A.S. Shaw, J. Rothbard, and P.M. Allen. 1994. Partial T cell signalling: altered phospho-ζ and lack of ZAP70 recruitment in APL-induced T cell anergy. Cell. 79: 913-922.
39. Jameson, S.C., and M.J. Bevan. 1995. T cell receptor antagonists and partial agonists. Immunity. 2:1-11.
40. + thymocytes results in tyrosine phosphorylation of the T-cell receptor zeta chain. Nature. 341:651-654.
41. van Oers, N.S.C., W. Tao, J.D. Watts, P. Johnson, R. Aebersold, and H.-S. Teh. 1993. Constitutive tyrosine phosphorylation of the T cell receptor (TCR) ζ subunit: regulation of TCR-associated protein kinase activity by TCR ζ. Mol. Cell. Biol. 13:5771-5780.
42. Osman, N., H. Turner, S. Lucas, K. Reif, and D.A. Cantrell. 1996. The protein interactions of the immunoglobulin receptor family tyrosine-based activation motifs present in the T cell receptor ζ subunits and the CD3 γ, δ and ∈ chains. Eur. J. Immunol. 26:1063-1068.
43. Jensen, W.A., C.M. Pleiman, P. Beaufils, A.-M.K. Wegener, B. Malissen, and J.C. Cambier. 1997. Qualitatively distinct signaling through T cell antigen receptor subunits. Eur. J. Immunol. 27:707-716.
44. Madrenas, J., R.L. Wange, J.L. Wang, N. Isakov, L.E. Samelson, and R.N. Germain. 1995. ζ-phosphorylation without ZAP-70 activation induced by TcR antagonists or partial agonists. Science. 267:515-518.
45. + T cells in response to antagonist ligands. J. Exp. Med. 184:149-157.
46. Negishi, L. N. Motoyama, K. Nakayama, S. Senju, S. Hatakeyama, Q. Zhang, A.C. Chan, and D.Y. Loh. 1995. Essential role for ZAP-70 in both positive and negative selection of thymocytes. Nature. 376:435-438.
47. van Oers, N.S.C., N. Killeen, and A. Weiss. 1996. Lck regulates the tyrosine phosphorylation of the T cell receptor subunits and ZAP-70 in murine thymocytes. J. Exp. Med. 183: 1053-1062.
48. + T cell lineages: a new perspective on thymic commitment and selection. Immunity. 2: 413-425.
49. Matechak, E.O., N. Killeen, S.M. Hedrick, and B.J. Fowlkes. 1996. MHC class II-specific T cells can develop in the CD8 lineage when CD4 is absent. Immunity. 4:337-347
50. Corbella, P., D. Moskophidis, E. Spanopoulou, C. Mamalaki, M. Tolaini, A. Itano, D. Lans, D. Baltimore, E. Robey, and D. Kioussis. 1994. Functional commitment to helper T cell lineage precedes positive selection and is independent of T cell receptor MHC specificity. Immunity. 1: 269-276.
51. Goldrath, A.W., K.A. Hogquist, and M.J. Bevan. 1997. CD8 lineage commitment in the absence of CD8. Immunity. 6: 633-642.
52. Fung-Leung, W.-P., M. Schillham, A. Rahemtulla, T. Kündig, M. Vollenweider, J. Potter, W. van Ewijk, and T. Mak. 1991. CD8 is needed for development of cytotoxic T cells but not helper T cells. Cell. 65:443-449.
53. + T cells in CD8β gene-targeted mice. J. Exp. Med. 180:959-967.
54. Crooks, M., and D. Littman. 1994. Disruption of T lymphocyte positive and negative selection in mice lacking the CD8β chain. Immunity. 1:277-286.
55. Nakayama, K., K. Nakayama, I. Negishi, K. Kuida, M.C. Louie, O. Kanagawa, H. Nakauchi, and D.Y. Loh. 1994. Requirement for CD8 β chain in positive selection of CD8-lineage T cells. Science. 263:1131-1133.
56. Sebzda, E., M. Choi, W.P. Fung-Leung, T.W. Mak, and P.S. Ohashi. 1997. Peptide-induced positive selection of TCR transgenic thymocytes in a co-receptor-independent manner. Immunity. 6:643-653.
57. lck correlates with impaired function in vitro and lack of expression in vivo. Nature. 342:278-281.
58. Nakano, N., R. Rooke, C. Benoist, and D. Mathis. 1997. Positive selection of T cells induced by viral delivery of neopeptides to the thymus. Science. 275:678-683.
59. lck. Nature. 338:257-259.
60. Zerrahn, J., W. Held, and D.H. Raulet. 1997. The MHC reactivity of the T cell repertoire prior to positive and negative selection. Cell. 88:627-636.
61. Sloan-Lancaster, J., and P.M. Allen. 1996. Altered peptide ligand-induced partial T cell activation: molecular mechanisms and role in T cell biology. Annu. Rev. Immunol. 14:1-27.
62. Miceli, M., and J. Parnes. 1993. Role of CD4 and CD8 in T cell activation and differentiation. Adv. Immunol. 53:59-122.
63. Kwan Lim, G., T. Ong, F. Aosai, H. Stauss, and R. Zamoyska. 1993. Is CD8 dependence a true reflection of TCR affinity for antigen? Int. Immunol. 5:1219-1228.
64. Straus, D.B., and A. Weiss. 1992. Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell. 70:585-593.
65. Ignatowicz, L., J. Kappler, D. Parker, and P. Marrack. 1996. The responses of mature T cells are not necessarily antagonized by their positively selecting peptide. J. Immunol. 157: 1827-1831.