Continuous T cell receptor signaling required for synapse maintenance and full effector potential

Nature Immunology

Volumn 4, Issue 8, 2003, Pages 749-755

  Huppa, Johannes B ^a,b   Gleimer, Michael ^a   Sumen, Cenk ^a,c   Davis, Mark M ^a,b  

^a STANFORD UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; INTERLEUKIN 2; PHOSPHATIDYLINOSITOL 3 KINASE; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CELL TRANSPORT; COMPLEX FORMATION; CONJUGATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISSOLUTION; ENZYME ACTIVITY; IMMUNE SYSTEM; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SYNAPSE; T LYMPHOCYTE; THREE DIMENSIONAL IMAGING; VIDEORECORDING;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, CD3; CALCIUM; CELL COMMUNICATION; LYMPHOCYTE ACTIVATION; MICE; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 0041695164     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/ni951     Document Type: Article

References (49)

1. Grakoui, A. et al. The immunological synapse: a molecular machine controlling T cell activation. Science 285, 221-227 (1999).
2. Dustin, M.L., Bromley, S.K., Davis, M.M. & Zhu, C. Identification of self through two-dimensional chemistry and synapses. Annu. Rev. Cell. Dev. Biol. 17, 133-157 (2001).
3. Monks, C.R., Freiberg, B.A., Kupfer, H., Sciaky, N. & Kupfer, A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395, 82-86 (1998).
4. Lee, K.H. et al. T cell receptor signaling precedes immunological synapse formation. Science 295, 1539-1342 (2002).
5. Kupfer, H., Monks, C.R. & Kupfer, A. Small splenic B cells that bind to antigen-specific T helper (Th) cells and face the site of cytokine production in the Th cells selectively proliferate: immunofluorescence microscopic studies of Th-B antigen-presenting cell interactions. J. Exp. Med. 179, 1507-1515 (1994).
6. Delon, J., Stoll, S. & Germain, R.N. Imaging of T-cell interactions with antigen presenting cells in culture and in intact lymphoid tissue. Immunol. Rev. 189, 51-63 (2002).
7. Richie, L.I. et al. Imaging synapse formation during thymocyte selection: inability of CD3z to form a stable central accumulation during negative selection. Immunity 16, 595-606 (2002).
8. Stinchcombe, J.C., Bossi, G., Booth, S. & Griffiths, G.M. The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 15, 751-761 (2001).
9. Kane, L.P., Lin, J. & Weiss, A. Signal transduction by the TCR for antigen. Curr. Opin. Immunol. 12, 242-249 (2000).
10. Valitutti, S., Muller, S., Cella, M., Padovan, E. & Lanzavecchia, A. Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature 375, 148-151 (1995).
11. Liu, H., Rhodes, M., Wiest, D.L. & Vignali, D.A. On the dynamics of TCR:CD3 complex cell surface expression and downmodulation. Immunity 13, 665-675 (2000).
12. Iezzi, G., Karjalainen, K. & Lanzavecchia, A. The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 8, 89-95 (1998).
13. Zal, T., Zal, M.A. & Gascoigne, N.R. Inhibition of T cell receptor-coreceptor interactions by antagonist ligands visualized by live FRET imaging of the T-hybridoma immunological synapse. Immunity 16, 521-534 (2002).
14. Bunnell, S.C. et al. T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J. Cell. Biol. 158, 1263-1275 (2002).
15. Krummel, M.F., Sjaastad, M.D., Wulfing, C. & Davis, M.M. Differential clustering of CD4 and CD3zeta during T cell recognition. Science 289, 1349-1352 (2000).
16. Botelho, R.J. et al. Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. J. Cell. Biol. 151, 1353-1368 (2000).
17. Costello, P.S., Gallagher, M. & Cantrell, D.A. Sustained and dynamic inositol lipid metabolism inside and outside the immunological synapse. Nat. Immunol. 3, 1082-1089 (2002).
18. Harriague, J. & Bismuth, G. Imaging antigen-induced PI3K activation in T cells. Nat. Immunol. 3, 1090-1096 (2002).
19. Marshall, J.G. et al. Restricted accumulation of phosphatidylinositol 3-kinase products in a plasmalemmal subdomain during Fc g receptor-mediated phagocytosis. J. Cell Biol. 153, 1369-1380 (2001).
20. Valitutti, S., Muller, S., Salio, M. & Lanzavecchia, A. Degradation of T cell receptor (TCR)-CD3-z complexes after antigenic stimulation. J. Exp. Med 185, 1859-1864 (1997).
21. Ward, S.G. & Cantrell, D.A. Phosphoinositide 3-kinases in T lymphocyte activation. Curr. Opin. Immunol. 13, 332-338 (2001).
22. Feske, S., Giltnane, J., Dolmetsch, R., Staudt, L.M. & Rao, A. Gene regulation mediated by calcium signals in T lymphocytes. Nat. Immunol. 2, 316-324 (2001).
23. Valitutti, S., Dessing, M., Aktories, K., Gallati, H. & Lanzavecchia, A. Sustained signaling leading to T cell activation results from prolonged T cell receptor occupancy. Role of T cell actin cytoskeleton. J. Exp. Med. 181, 577-584 (1995).
24. Lollo, B.A., Chan, K.W,, Hanson, E.M., Moy, V.T. & Brian, A.A. Direct evidence for two affinity states for lymphocyte function- associated antigen 1 on activated T cells. J. Biol. Chem. 268, 21693-21700 (1993).
25. Labadia, M.E., Jeanfavre, D.D., Caviness, G.O. & Morelock, M.M. Molecular regulation of the interaction between leukocyte function- associated antigen-1 and soluble ICAM-1 by divalent metal cations. J. Immunol. 161, 836-842 (1998).
26. Lyons, A.B. & Parish, C.R. Determination of lymphocyte division by flow cytometry. J. Immunol. Methods 171, 131-137 (1994).
27. Banchereau, J. & Steinman, R.M. Dendritic cells and the control of immunity. Nature 392, 245-252 (1998).
28. Mellman, I., Turley, S.J. & Steinman, R.M. Antigen processing for amateurs and professionals. Trends Cell Biol. 8, 231-237 (1998).
29. Gunzer, M. et al. Antigen presentation in extracellular matrix: interactions of T cells with dendritic cells are dynamic, short lived, and sequential. Immunity 13, 323-332 (2000).
30. Miller, M.J., Wei, S.H., Parker, I. & Cahalan, M.D. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296, 1869-1873 (2002).
31. Stoll, S., Delon, J., Brotz, T.M. & Germain, R.N. Dynamic imaging of T cell-dendritic cell interactions in lymph nodes. Science 296, 1873-1876 (2002).
32. + T cells is amplified by prolonged T cell antigen receptor triggering. J. Exp. Med. 196, 793-803 (2002).
33. Bird, J.J. et al. Helper T cell differentiation is controlled by the cell cycle. Immunity 9, 229-237 (1998).
34. Iezzi, G., Scotet, E., Scheidegger, D. & Lanzavecchia, A. The interplay between the duration of TCR and cytokine signaling determines T cell polarization. Eur. J. Immunol. 29, 4092-4101 (1999).
35. Lee, K.M. et al. Molecular basis of T cell inactivation by CTLA-4. Science 282, 2263-2266 (1998).
36. Egen, J.G., Kuhns, M.S. & Allison, J.P. CTLA-4: new insights into its biological function and use in tumor immunotherapy. Nat. Immunol. 3, 611-618 (2002).
37. Egen, J.G. & Allison, J.P. Cytotoxic T lymphocyte antigen-4 accumulation in the immunological synapse is regulated by TCR signal strength. Immunity 16, 23-135 (2002).
38. + T cell effector mechanisms in resistance to infection. Annu. Rev. Immunol. 18, 275-308 (2000).
39. + T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat. Immunol. 2, 415-222 (2001).
40. van Stipdonk, M.J., Lemmens, E.E. & Schoenberger, S.P. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat. Immunol. 2, 423-429 (2001).
41. Carbone, F.R., Kurts, C., Bennett, S.R., Miller, J.F. & Heath, W.R. Cross-presentation: a general mechanism for CTL immunity and tolerance. Immunol. Today 19, 368-373 (1998).
42. Schoenberger, S.P., Toes, R.E., van der Voort, E.I., Offringa, R. & Melief, C.J. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393, 480-483 (1998).
43. Bennett, S.R. et al. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393, 478-480 (1998).
44. Ozato, K., Mayer, N. & Sachs, D.H. Hybridoma cell lines secreting monoclonal antibodies to mouse H-2 and Ia antigens. J. Immunol. 124, 533-540 (1980).
45. Reay, P.A. et al. Determination of the relationship between T cell responsiveness and the number of MHC-peptide complexes using specific monoclonal antibodies. J. Immunol. 164, 5626-5634 (2000).
46. Fredrickson, G.G. & Basch, R.S. Early thymic regeneration after irradiation. Dev. Comp. Immunol. 18, 251-263 (1994).
47. Pawelec, G., Ziegler, A. & Wernet, P. Dissection of human allostimulatory determinants with cloned T cells: stimulation inhibition by monoclonal antibodies TU22, 34, 35, 36, 37, 39, 43, and 58 against distinct human MHC class II molecules. Hum Immunol. 12, 165-176 (1985).
48. Unkeless, J.C. Characterization of a monoclonal antibody directed against mouse macrophage and lymphocyte Fc receptors. J. Exp. Med. 150, 580-596 (1979).
49. Irvine, D.J., Purbhoo, M.A., Krogsgaard, M. & Davis, M.M. Direct observation of ligand recognition by T cells. Nature 419, 845-849 (2002).