Linking molecular and cellular events in T-cell activation and synapse formation

Seminars in Immunology

Volumn 15, Issue 6, 2003, Pages 307-315

  Krogsgaard, Michelle ^a   Huppa, Johannes B ^a   Purbhoo, Marco A ^a   Davis, Mark M ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Immunological synapse; Peptide MHC; T cell activation; T cell receptor; T cell recognition

Indexed keywords

CD28 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CYTOCHALASIN D; DNA; GLUTAMIC ACID; INTERCELLULAR ADHESION MOLECULE 1; LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN; PEPTIDE; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR;

ANTIGEN BINDING; ARTICLE; B LYMPHOCYTE; CELL CONTACT; CELL INTERACTION; CELL KINETICS; CELL STIMULATION; CELL STRUCTURE; CELL SURFACE; CROSS REACTION; CRYSTALLOGRAPHY; CYTOTOXICITY; DNA SEQUENCE; EFFECTOR CELL; FLUORESCENCE MICROSCOPY; HELPER CELL; IMMUNE SYSTEM; IMMUNOLOGICAL SYNAPSE; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR INTERACTION; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; SYNAPSE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THERMODYNAMICS;

EID: 0742305009     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.smim.2003.09.002     Document Type: Article

References (63)

1. Davis M.M., Boniface J.J., Reich Z., Lyons D., Hampl J., Arden B.et al. Ligand recognition by αβ T cell receptors. Annu. Rev. Immunol. 16:1998;523-524.
2. Harding C.V., Unanue E.R. Quantitation of antigen-presenting cell MHC class II/peptide complexes necessary for T-cell stimulation. Nature. 346:1990;574-576.
3. Demotz S., Grey H.M., Sette A. The minimal number of class II MHC-antigen complexes needed for T cell activation. Science. 249:1990;1028-1030.
4. Christinck E.R., Luscher M.A., Barber B.H., Williams D.B. Peptide binding to class I MHC on living cells and quantitation of complexes required for CTL lysis. Nature. 352:1991;67-70.
5. Sykulev Y., Joo M., Vturina I., Tsomides T.J., Eisen H.N. Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T-cell response. Immunity. 4:1996;565-571.
6. + CTL. Mol. Immunol. 31:1994;1285-1293.
7. Reay P.A., Matsui K., Haase K., Wülfing C., Chien Y.H., Davis M.M. Determination of the relationship between T cell responsiveness and the number of MHC-peptide complexes using specific monoclonal antibodies. J. Immunol. 164:2000;5626-5634.
8. Irvine D.J., Purbhoo M.A., Krogsgaard M., Davis M.M. Direct observation of ligand recognition by T cells. Nature. 419:2002;845-849.
9. Wülfing C., Sumen C., Sjaastad M.D., Wu L.C., Dustin M.L., Davis M.M. Costimulation and endogenous MHC ligands contribute to T cell recognition. Nat. Immunol. 3:2002;42-47.
10. Wang J.H., Meijers R., Xiong Y., Liu J.H., Sakihama T., Zhang R.et al. Crystal structure of the human CD4 N-terminal two-domain fragment complexed to a class II MHC molecule. Proc. Natl. Acad. Sci. U.S.A. 98:2001;10799-10804.
11. Germain R.N., Stefanova I. The dynamics of T cell receptor signaling: complex orchestration and the key roles of tempo and cooperation. Annu. Rev. Immunol. 17:1999;467-522.
12. Gascoigne NRJ, Zal T, Alam SM. T-cell receptor binding kinetics in T-cell development and activation. Exp Rev Mol Med 2001. http://www-ermm.cbcu. cam.ac.uk/01002502h.htm .
13. van der Merwe P.A. The TCR triggering puzzle. Immunity. 14:2001;665-668.
14. Matsui K., Boniface J.J., Steffner P., Reay P.A., Davis M.M. Kinetics of T-cell receptor binding to peptide/I-Ek complexes: correlation of the dissociation rate with T-cell responsiveness. Proc. Natl. Acad. Sci. U.S.A. 91:1994;12862-12866.
15. Al-Ramadi B.K., Jelonek M.T., Boyd L.F., Margulies D.H., Bothwell A.L. Lack of strict correlation of functional sensitization with the apparent affinity of MHC/peptide complexes for the TCR. J. Immunol. 155:1995;662-673.
16. Alam S.M., Travers P.J., Wung J.L., Nasholds W., Redpath S., Jameson S.C.et al. T cell receptor affinity and thymocyte positive selection. Nature. 381:1996;616-620.
17. Kersh G.J., Kersh E.N., Fremont D.H., Allen P.M. High- and low-potency ligands with similar affinities for the TCR: the importance of kinetics in TCR signaling. Immunity. 9:1998;817-826.
18. Sykulev Y., Vugmeyster Y., Brunmark A., Ploegh H.L., Eisen H.N. Peptide antagonism and T cell receptor interactions with peptide-MHC complexes. Immunity. 9:1998;475-483.
19. Baker B.M., Gagnon S.J., Biddison W.E., Wiley D.C. Conversion of a T cell antagonist into an agonist by repairing a defect in the TCR/peptide/MHC interface: implications for TCR signaling. Immunity. 13:2000;475-484.
20. Degano M., Garcia K.C., Apostolopoulos V., Rudolph M.G., Teyton L., Wilson I.A. A functional hotspot for antigen recognition in a superagonist TCR/MHC complex. Immunity. 12:2000;251-261.
21. Kalergis A.M., Boucheron N., Doucey M., Palmieri E., Goyarts E.C., Vegh Z.et al. Efficient T cell activation requires an optimal dwell-time of interaction between the TCR and the pMHC complex. Nat. Immunol. 2:2001;229-234.
22. Rudolph M.G., Wilson I.A. The specificity of TCR/pMHC interaction. Curr. Opin. Immunol. 14:2002;52-65.
23. - T cell transfectants that express a high affinity T cell receptor exhibit enhanced peptide-dependent activation. J. Exp. Med. 194:2002;1043-1052.
24. Holler P.D., Kranz D.M. Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity. 18:2003;255-264.
25. Davis M.M., Bjorkman P.J. T-cell antigen receptor genes and T-cell recognition. Nature. 334:1988;395-402.
26. Garcia K.C., Teyton L., Wilson I.A. Structural basis of T cell recognition. Annu. Rev. Immunol. 17:1999;369-397.
27. Ding Y.H., Baker B.M., Garboczi D.N., Biddison W.E., Wiley D.C. Four A6-TCR/peptide/HLA-A2 structures that generate very different T cell signals are nearly identical. Immunity. 11:1999;45-56.
28. Degano M., Garcia K.C., Apostolopoulos V., Rudolph M.G., Teyton L., Wilson I.A. A functional hotspot for antigen recognition in a superagonist TCR/MHC complex. Immunity. 12:2000;251-261.
29. Rojo J.M., Janeway C.A. The biologic activity of anti-T cell receptor V region monoclonal antibodies is determined by the epitope recognized. J. Immunol. 140:1988;1081-1088.
30. Garcia K.C., Degano M., Pease L.R., Huang M., Peterson P.A., Teyton L. Structural basis of plasticity in T cell receptor recognition of a self peptide-MHC antigen. Science. 279:1998;1166-1172.
31. Reiser J.B., Gregoire C., Darnault C., Moser T., Guimezanes A., Schmitt-Verhulst A.M., Fontecilla-Camps J.C., Mazza G., Malissen B., Honsset D. A T cell receptor CDR3β loop undergoes conformational changes of unprecedented magnitude upon binding to a peptide/MHC class I complex. Immunity. 16:2002;345-354.
32. Reiser J.B., Darnault C., Gregoire C., Mosser T., Mazza G., Kearney A., van der Merwe P.A., Fontecilla-Camps J.C., Honsset D., Malissen B. CDR3 loop flexibility contributes to the degeneracy of TCR recognition. Nat. Immunol. 4:2003;241-247.
33. Kjer-Nielsen L., Clements C.S., Purcell A.W., Brooks A.G., Whisstock J.C., Burrows S.R.et al. A structural basis for the selection of dominant alphabeta T cell receptors in antiviral immunity. Immunity. 18:2003;53-64.
34. Willcox B.E., Gao G.F., Wyer J.R., Ladbury J.E., Bell J.I., Jakobsen B.K., van der Merwe P.A. TCR binding to peptide-MHC stabilizes a flexible recognition interface. Immunity. 10:1999;357-365.
35. Boniface J.J., Reich Z., Lyons D.S., Davis M.M. Thermodynamics of T cell receptor binding to peptide-MHC: evidence for a general mechanism of molecular scanning. Proc. Natl. Acad. Sci. U.S.A. 96:1999;11446-11451.
36. Garcia K.C., Radu C.G., Ho J., Ober R.J., Ward S.E. Kinetics and thermodynamics of T cell receptor-autoantigen interactions in murine experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. U.S.A. 98:2001;6818-6823.
37. Wu L.C., Tuot D.S., Lyons D.S., Garcia K.C., Davis M.M. Two-step binding mechanism for T-cell receptor recognition of peptide MHC. Nature. 418:2002;552-556.
38. Fersht A.R. Nucleation mechanisms in protein folding. Curr. Opin. Struct. Biol. 7:1997;3-9.
39. Schreiber G., Fersht A.R. Rapid, electrostatically assisted association of proteins. Nat. Struct. Biol. 3:1996;427-431.
40. Stites W.E. Protein-protein interactions: interface structure, binding thermodynamics, and mutational analysis. Chem. Rev. 97:1997;1233-1250.
41. Maeneka K., Juji T., Wyer J.R., Gao G.F., Maenaka T., Zaccai N.R.et al. Killer cell immunoglobulin receptors and T cell receptors bind peptide-major histocompability complex class I with distinct thermodynamic and kinetic properties. J. Biol. Chem. 274:1999;28329-28334.
42. Maenaka K., van der Merwe P.A., Stuart D.I., Jones E.Y., Sondermann P. The human low affinity Fcγ receptors IIa, IIb, and III bind IgG with fast kinetics and distinct thermodynamic properties. J. Biol. Chem. 276:2001;44898-45004.
43. James L.C., Roversi P., Tawfik D.S. Antibody multispecificity mediated by conformational diversity. Science. 299:2003;1362-1367.
44. Spolar R.S., Record M.T. Coupling of local folding to site-specific binding of proteins to DNA. Science. 263:1994;777-784.
45. Monks C.R.F., Kupfer H., Tamir I., Barlow A., Kupfer A. Selective modulation of protein kinase C-theta during T-cell activation. Nature. 385:1997;83-86.
46. Monks C.R.F., Freiberg A., Kupfer H., Sciaky N., Kupfer A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature. 395:1998;82-86.
47. Wülfing C., Davis M.M. A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science. 282:1998;2266-2269.
48. Dustin M.L., Olszowy M.W., Holdorf A.D., Li J., Bromley S., Desai N.A.et al. A novel adaptor protein orchestrates receptor patterning and cytoskeletal polarity in T-cell contacts. Cell. 94:1998;667-677.
49. Grakoui A., Bromley S.K., Sumen C., Davis M.M., Shaw A.S., Allen P.M.et al. The immunological synapse: a molecular machine controlling T cell activation. Science. 285:1999;221-227.
50. + T cells after engagement of the T cell antigen receptor and CD8 by antigen-presenting cells. Proc. Natl. Acad. Sci. U.S.A. 98:2001;12624-12629.
51. Krummel M.F., Sjaastad M., Wülfing C., Davis M.M. Differential clustering of CD4 and CD3zeta during T cell recognition. Science. 289:2000;1349-1352.
52. Kupfer A., Singer S.J., Dennert G. On the mechanism of unidirectional killing in mixtures of two cytotoxic T lymphocytes. Unidirectional polarization of cytoplasmic organelles and the membrane-associated cytoskeleton in the effector cell. J. Exp. Med. 163:1986;489-498.
53. Kupfer A., Swain S.L., Singer S.J. The specific direct interaction of helper T cells and antigen-presenting B cells. II. Reorientation of the microtubule organizing center and reorganization of the membrane-associated cytoskeleton inside the bound helper T cells. J. Exp. Med. 165:1987;1565-1580.
54. Kupfer A., Mosmann T.R., Kupfer H. Polarized expression of cytokines in cell conjugates of helper T cells and splenic B cells. Proc. Natl. Acad. Sci. U.S.A. 88:1991;775-779.
55. Huppa J.B., Gleimer M., Sumen C., Davis M.M. T cell receptor signalling maintains the immunological synapse and exerts a cumulative effect on T cell effector potential. Nat. Immunol. 4:2003;749-755.
56. Viola A., Schroeder S., Sakakibara Y., Lanzavecchia A. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science. 283:1991;680-682.
57. Moss W.C., Irvine D.J., Davis M.M., Krummel M.F. Quantifying signaling-induced reorientation of T cell receptors during immunological synapse formation. Proc. Natl. Acad. Sci. U.S.A. 99:2002;15024-15029.
58. Davis M.M., Krogsgaard M., Huppa J.B., Sumen C., Purbhoo M.A., Irvine D.J.et al. Dynamics of cell surface molecules during T-cell recognition. Ann. Rev. Biochem. 72:2003;717-742.
59. Karttunen J., Shastri N. Measurement of ligand-induced activation in single viable T cells using the lacZ reporter gene. Proc. Natl. Acad. Sci. U.S.A. 88:1991;3972-3976.
60. Iezzi G., Karjalainen K., Lanzavecchia A. The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity. 8:1998;89-95.
61. Lee J.E., Cossoy M.B., Chau L.A., Singh B., Madrenas J. Inactivation of lck and loss of TCR-mediated signaling upon persistent engagement with complexes of peptide:MHC molecules. J. Immunol. 159:1997;61-69.
62. + T cell effector mechanisms in resistance to infection. Annu. Rev. Immunol. 18:2000;275-308.
63. Krogsgaard M, Prado N, Adams EJ, He X, Chow D, Wilson DB, Garcia KC, Davis MM. Evidence that structural rearrangements and/or flexibility during TCR binding can contribute to T-cell activation. Mol Cell, 2003, in press.