Initiation ofTCR phosphorylation and signal transduction

Frontiers in Immunology

Volumn 2, Issue DEC, 2011, Pages

  Gascoigne, Nicholas R J ^a   Casas, Javier ^a   Brzostek, Joanna ^a   Rybakin, Vasily ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

CD8; Fyn; Lck; Src family kinases; T cell receptor

Indexed keywords

EID: 84874485209     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2011.00072     Document Type: Review

References (88)

1. Acuto, O., Di Bartolo, V., and Micheli, F. (2008). Tailoring T-cell receptor sig-nals by proximal negative feedback mechanisms. Nat. Rev. Immunol. 8, 699-712.
2. Appleby, M. W., Gross, J. A., Cooke, M. W., Levin, S. D., Qian, X., and Perlmutter, R. (1992). Defective T cell receptor signaling in mice lack-ing the thymic isoform of p59-fyn. Cell 70, 751-763.
3. Artyomov, M. N., Lis, M., Devadas, S., Davis, M. M., and Chakraborty, A. K. (2010). CD4 and CD8 binding to MHC molecules primarily acts to enhance Lck delivery. Proc. Natl. Acad. Sci. U.S.A. 107, 16916-16921.
4. Beddoe, T., Chen, Z., Clements, C. S., Ely, L. K., Bushell, S. R., Vivian, J. P., Kjer-Nielsen, L., Pang, S. S., Dun-Stone, M. A., Liu, Y. C., Macdonald, W. A., Perugini, M. A., Wilce, M. C., Burrows, S. R., Purcell, A. W., Tiga-Nis, T., Bottomley, S. P., McCluskey, J., and Rossjohn, J. (2009). Antigen ligation triggers a conformational change within the constant domain of the αβ T cell receptor. Immunity 30, 777-788.
5. Boniface, J. J., Rabinowitz, J. D., Wulf-Ing, C., Hampl, J., Reich, Z., Alt-Man, J. D., Kantor, R. M., Beeson, C., McConnell, H. M., and Davis, M. M. (1998). Initiation of signal trans-duction through the T cell receptor requires the multivalent engagement of peptide/MHC ligands. Immunity 9, 459-466.
6. Call, M. E., Pyrdol, J., Wiedmann, M., and Wucherpfennig, K. W. (2002). The organizing principle in the formation of the T cell receptor-CD3 complex. Cell 111, 967-979.
7. Cebecauer, M., Guillaume, P., Mark, S., Michielin, O., Boucheron, N., Bezard, M., Meyer, B. H., Segura, J. M., Vogel, H., and Luescher, I. F. (2005). CD8+ cytotoxic T lymphocyte activation by soluble major histocompatibility complex-peptide dimers. J. Biol. Chem. 280, 23820-23828.
8. Chau, L. A., and Madrenas, J. (1999). Phospho-LAT-independent activa-tion of the ras-mitogen-activated protein kinase pathway:a differential recruitment model of TCR partial agonist signaling. J. Immunol. 163, 1853-1858.
9. Cheroutre, H., and Lambolez, F. (2008). Doubting the TCR coreceptor func-tion of CD8alphaalpha. Immunity 28, 149-159.
10. Cho, B. K., Lian, K. C., Lee, P., Brunmark, A., McKinley, C., Chen, J., Kranz, D. M., and Eisen, H. N. (2001). Differences in antigen recognition and cytolytic activity of CD8+ and CD8- T cells that express the same antigen-specific receptor. Proc. Natl. Acad. Sci. U.S.A. 98, 1723-1727.
11. Cochran, J. R., Cameron, T. O., and Stern, L. J. (2000). The rela-tionship of MHC-peptide bind-ing and T cell activation probed using chemically defined MHC class II oligomers. Immunity 12, 241-250.
12. Collins, T. L., and Burakoff, S. J. (1993). Tyrosine kinase activity of CD4-associated p56lck may not be required for CD4-dependent T-cell activation. Proc. Natl. Acad. Sci. U.S.A. 90, 11885-11889.
13. Cornely, R., Rentero, C., Enrich, C., Gre-Wal,T.,and Gaus,K. (2011).Annexin A6 is an organizer of membrane microdomains to regulate receptor localization and signalling. IUBMB Life 63, 1009-1017.
14. Davis, S. J., and van der Merwe, P. A. (2006). The kinetic-segregation model: TCR triggering and beyond. Nat. Immunol. 7, 803-809.
15. Doucey, M. A., Goffin, L., Naeher, D., Michielin, O., Baumgartner, P., Guil-Laume, P., Palmer, E., and Luescher, I. F. (2003). CD3δ establishes a func-tional link between the T cell recep-tor and CD8. J. Biol. Chem. 278, 3257-3264.
16. Douglass, A. D., and Vale, R. D. (2005). Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein net-works that exclude or trap signal-ing molecules in T cells. Cell 121, 937-950.
17. Dower, N. A., Stang, S. L., Bot-Torff, D. A., Ebinu, J. O., Dickie, P., Ostergaard, H. L., and Stone, J. C. (2000). RasGRP is essential for mouse thymocyte differentiation and TCR signaling. Nat. Immunol. 1, 317-321.
18. Ehrlich,L. I.,Ebert,P. J.,Krummel,M. F., Weiss, A., and Davis, M. M. (2002). Dynamics of p56lck translocation to the T cell immunological synapse following agonist and antagonist stimulation. Immunity 17, 809-822.
19. Filby, A., Seddon, B., Kleczkowska, J., Salmond, R., Tomlinson, P., Smida, M., Lindquist, J. A., Schraven, B., and Zamoyska, R. (2007). Fyn reg-ulates the duration of TCR engage-ment needed for commitment to effector function. J. Immunol. 179, 4635-4644.
20. Fusaki, N., Matsuda, S., Nishizumi, H., Umemori, H., and Yamamoto, T. (1996). Physical and functional interactions of protein tyrosine kinases, p59fyn and ZAP-70, in T cell signaling. J. Immunol. 156, 1369-1377.
21. Gascoigne, N. R. J. (2008). Do T cells need endogenous peptides for activation? Nat. Rev. Immunol. 8, 895-900.
22. Gascoigne, N. R. J., Ampudia, J., Clamme, J. P., Fu, G., Lotz, C., Mal-Laun, M., Niederberger, N., Palmer, E., Rybakin, V., Yachi, P. P., and Zal, T. (2009). Visualizing intermolecu-lar interactions in T cells. Curr. Top. Microbiol. Immunol. 334, 31-46.
23. Gascoigne, N. R. J., and Zal, T. (2004). Molecular interactions at the T cell-antigen-presenting cell interface. Curr. Opin. Immunol. 16, 114-119.
24. Gascoigne, N. R. J., Zal, T., Yachi, P. P., and Hoerter, J. A. H. (2010). Co-receptors and recognition of self at the immunological synapse. Curr. Top. Microbiol. Immunol. 340, 171-189.
25. Germain, R. N. (2001). The T cell recep-tor for antigen: signaling and ligand discrimination. J. Biol. Chem. 276, 35223-35226.
26. Gil, D., Schamel,W. W. A., Montoya, M., Sanchez-Madrid, F., and Alarcon, B. (2002). Recruitment of Nck by CD3ε reveals a ligand-induced conformational change essen-tial for T cell receptor signaling and synapse formation. Cell 109, 901-912.
27. Groves, T., Smiley, P., Cooke, M. P., Forbush, K., Perlmutter, R. M., and Guidos, C. J. (1996). Fyn can par-tially substitute for Lck in T lym-phocyte development. Immunity 5, 417-428.
28. Holler, P. D., and Kranz, D. M. (2003). Quantitative analysis of the con-tribution of TCR/pepMHC affin-ity and CD8 to T cell activation. Immunity 18, 255-264.
29. Huang, J., Edwards, L. J., Evavold, B. D., and Zhu, C. (2007). Kinetics of MHC-CD8 interaction at the T cell membrane. J. Immunol. 179, 7653-7662.
30. Huang, J., Zarnitsyna, V. I., Liu, B., Edwards, L. J., Jiang, N., Evavold, B. D., and Zhu, C. (2010). The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 464, 932-936.
31. Huse, M., Klein, L. O., Girvin, A. T., Faraj, J. M., Li, Q. J., Kuhns, M. S., and Davis, M. M. (2007). Spatial and temporal dynamics of T cell recep-tor signaling with a photoactivatable agonist. Immunity 27, 76-88.
32. Ike, H., Kosugi, A., Kato, A., Iino, R., Hirano, H., Fujiwara, T., Ritchie, K., and Kusumi, A. (2003). Mecha-nism of Lck recruitment to the T-cell receptor cluster as studied by single-molecule-fluorescence video imaging. Chemphyschem 4,620-626.
33. Jiang, N., Huang, J., Edwards, L. J., Liu, B., Zhang, Y., Beal, C. D., Evavold, B. D., and Zhu, C. (2011). Two-stage cooperative T cell receptor-peptide major histocompatibility complex-CD8 trimolecular interac-tions amplify antigen discrimina-tion. Immunity 34, 13-23.
34. Kim, S. T., Takeuchi, K., Sun, Z. Y., Touma, M., Castro, C. E., Fahmy, A., Lang, M. J., Wagner, G., and Reinherz, E. L. (2009). The αβ T cell receptor is an anisotropic mechanosensor. J. Biol. Chem. 284, 31028-31037.
35. Kim, S. T., Touma, M., Takeuchi, K., Sun, Z. Y., Dave, V. P., Kappes, D. J., Wagner, G., and Reinherz, E. L. (2010). Distinctive CD3 het-erodimeric ectodomain topologies maximize antigen-triggered activa-tion of αβ T cell receptors. J. Immunol. 185, 2951-2959.
36. Kjer-Nielsen, L., Clements, C. S., Pur-cell, A. W., Brooks, A. G., Whisstock, J. C., Burrows, S. R., McCluskey, J., and Rossjohn, J. (2003). A struc-tural basis for the selection of dom-inant αβ T cell receptors in antiviral immunity. Immunity 18, 53-64.
37. Krogsgaard, M., and Davis, M. M. (2005). How T cells 'see' antigen. Nat. Immunol. 6, 239-245.
38. Krogsgaard, M., Juang, J., and Davis, M. M. (2007). A role for "self" in T-cell activation. Semin. Immunol. 19, 236-244.
39. Kuhns, M. S., and Davis, M. M. (2007). Disruption of extracellular inter-actions impairs T cell receptor-CD3 complex stability and signaling. Immunity 26, 357-369.
40. Kumar, R., Ferez, M., Swamy, M., Arechaga, I., Rejas, M. T., Valpuesta, J. M., Schamel, W. W., Alarcon, B., and van Santen, H. M. (2011). Increased sensitivity of antigen-experienced T cells through the enrichment of oligomeric T cell receptor complexes. Immunity 35, 375-387.
41. Legname, G., Seddon, B., Lovatt, M., Tomlinson, P., Sarner, N., Tolaini, M., Williams, K., Norton, T., Kious-Sis, D., and Zamoyska, R. (2000). Inducible expression of a p56Lck transgene reveals a central role for Lck in the differentiation of CD4 SP thymocytes. Immunity 12, 537-546.
42. Li, Y. C., Chen, B. M., Wu, P. C., Cheng, T. L., Kao, L. S., Tao, M. H., Lieber, A., and Roffler, S. R. (2010). Cut-ting Edge: mechanical forces acting on T cells immobilized via the TCR complex can trigger TCR signaling. J. Immunol. 184, 5959-5963.
43. Lillemeier, B. F., Mortelmaier, M. A., Forstner, M. B., Huppa, J. B., Groves, J. T., and Davis, M. M. (2010). TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation. Nat. Immunol. 11, 90-96.
44. Lillemeier, B. F., Pfeiffer, J. R., Survi-Ladze, Z., Wilson, B. S., and Davis, M. M. (2006). Plasma membrane-associated proteins are clustered into islands attached to the cytoskele-ton. Proc. Natl. Acad. Sci. U.S.A. 103, 18992-18997
45. Lovatt, M., Filby, A., Parravicini, V., Werlen, G., Palmer, E., and Zamoyska, R. (2006). Lck regulates the threshold of activation in pri-mary T cells, while both Lck and Fyn contribute to the magnitude of the extracellular signal-related kinase response. Mol. Cell. Biol. 26, 8655-8665.
46. Mallaun, M., Naeher, D., Daniels, M. A., Yachi, P. P., Hausmann, B., Luescher, I. F., Gascoigne, N. R. J., and Palmer, E. (2008). The T cell receptor's α-chain connecting peptide motif pro-motes close approximation of the CD8 coreceptor allowing efficient signal initiation. J. Immunol. 180, 8211-8221.
47. Martin, M. W., and Machacek, M. R. (2010). Update on lymphocyte spe-cific kinase inhibitors: a patent sur-vey. Expert Opin. Ther. Pat. 20, 1573-1593.
48. Methi, T., Ngai, J., Vang, T., Torgersen, K. M., and Tasken, K. (2007). Hypophosphorylated TCR/CD3ζ signals through a Grb2-SOS1-Ras pathway in Lck knockdown cells. Eur. J. Immunol. 37, 2539-2548.
49. Molina, T. J., Kishihara, K., Siderovski, D. P., van Ewijk, W., Timms, A. N., Wakeham, A., Paige, C. J., Hartman, K. U., Veillette, A., Davidson, D., and Mak, T. W. (1992). Profound block in thymocyte development in mice lacking p56lck. Nature 357, 161-164.
50. Naeher, D., Luescher, I. F., and Palmer, E. (2002). A role for the α-chain con-necting peptide motif in mediating TCR-CD8 cooperation. J. Immunol. 169, 2964-2970.
51. Nika, K., Soldani, C., Salek, M., Paster, W., Gray, A., Etzensperger, R., Fug-ger, L., Polzella, P., Cerundolo, V., Dushek, O., Höfer, T., Viola, A., and Acuto, O. (2010). Constitutively active Lck kinase in T cells dri-ves antigen receptor signal transduc-tion. Immunity 32, 766-777.
52. O'Rourke, A. M., and Mescher, M. F. (1992). Cytotoxic T-lymphocyte activation involves a cascade of sig-nalling and adhesion events. Nature 358, 253-255.
53. O'Rourke, A. M., Rogers, J., and Mescher, M. F. (1990). Activated CD8 binding to class I protein mediated by the T cell receptor results in signalling. Nature 346, 187-189.
54. Palacios, E. H., and Weiss, A. (2004). Function of the Src-family kinases, Lck and Fyn, in T-cell develop-ment and activation. Oncogene 23, 7990-8000.
55. Palmer, E., and Naeher, D. (2009). Affin-ity threshold for thymic selection through a T-cell receptor-co-receptor zipper. Nat. Rev. Immunol. 9, 207-213.
56. Priatel, J. J., Teh, S. J., Dower, N. A., Stone, J. C., and Teh, H. S. (2002). RasGRP1 transduces low-grade TCR signals which are critical for T cell development, homeostasis, and differentiation. Immunity 17, 617-627.
57. Qian,D.,Lev,S.,van Oers,N. S.,Dikic,I., Schlessinger, J., and Weiss, A. (1997). Tyrosine phosphorylation of Pyk2 is selectively regulated by Fyn dur-ing TCR signaling. J. Exp. Med. 185, 1253-1259.
58. Rybakin, V., Clamme, J.-P., Ampudia, J., Yachi, P. P., and Gascoigne, N. R. J. (2011). CD8αα and CD8αβ isotypes are equally recruited to the immuno-logical synapse through their abil-ity to bind MHC class I. EMBO Rep. doi: 10.1038/embor.2011.209. [Epub ahead of print].
59. Salmond, R. J., Emery, J., Okkenhaug, K., and Zamoyska, R. (2009a). MAPK, phosphatidylinositol 3-kinase, and mammalian target of rapamycin pathways converge at the level of ribosomal protein S6 phos-phorylation to control metabolic signaling in CD8 T cells. J. Immunol. 183, 7388-7397.
60. Salmond, R. J., Filby, A., Qureshi, I., Caserta, S., and Zamoyska, R. (2009b). T-cell receptor proximal signaling via the Src-family kinases, Lck and Fyn,influences T-cell activa-tion, differentiation, and tolerance. Immunol. Rev. 228, 9-22.
61. Samelson, L. E., Phillips, A. F., Luong, E. T., and Klausner, R. D. (1990). Asso-ciation of the fyn protein-tyrosine kinase with the T-cell antigen recep-tor. Proc. Natl. Acad. Sci. U.S.A. 87, 4358-4362.
62. Schamel, W. W., Arechaga, I., Risueno, R. M., van Santen, H. M., Cabezas, P., Risco, C., Valpuesta, J. M., and Alarcon, B. (2005). Coexistence of multivalent and monovalent TCRs explains high sensitivity and wide range of response. J. Exp. Med. 202, 493-503.
63. Schilham, M. W., Fung-Leung, W. P., Rahemtulla, A., Kuendig, T., Zhang, L., Potter, J., Miller, R. G., Hengartner, H., and Mak, T. W. (1993). Alloreactive cytotoxic T cells can develop and func-tion in mice lacking both CD4 and CD8. Eur. J. Immunol. 23, 1299-1304.
64. Schraven, B.,Wild, M., Kirchgessner, H., Siebert, B., Wallich, R., Henning, S., Samstag, Y., and Meuer, S. C. (1993). Alterations of CD2 association with T cell receptor signaling molecules in "CD2 unresponsive" human T lymphocytes. Eur. J. Immunol. 23, 119-123.
65. Seddon, B., Legname, G., Tomlinson, P., and Zamoyska, R. (2000). Long-term survival but impaired homeo-static proliferation of Naive T cells in the absence of p56lck. Science 290, 127-131.
66. Seddon, B., and Zamoyska, R. (2002). TCR signals mediated by Src family kinases are essential for the survival of naive T cells. J. Immunol. 169, 2997-3005.
67. Sohn, H. W., Tolar, P., and Pierce, S. K. (2008). Membrane heterogeneities in the formation of B cell receptor-Lyn kinase microclusters and the immune synapse. J. Cell Biol. 182, 367-379.
68. Stefanova, I., Hemmer, B., Vergelli, M., Martin, R., Biddison,W. E., and Ger-main, R. N. (2003). TCR ligand dis-crimination is enforced by compet-ing ERK positive and SHP-1 negative feedback pathways. Nat. Immunol. 4, 248-254.
69. Stein, P. L., Lee, H.-M., Rich, S., and Soriano, P. (1992). pp59-fyn Mutant mice display differential signaling in thymocytes and peripheral T cells. Cell 70, 741-750.
70. Sun, Z. Y., Kim, S. T., Kim, I. C., Fahmy, A., Reinherz, E. L., and Wagner, G. (2004). Solution structure of the CD3εδ ectodomain and comparison with CD3εγ as a basis for modeling T cell receptor topology and signal-ing. Proc. Natl. Acad. Sci. U.S.A. 101, 16867-16872.
71. Thome, M., Duplay, P., Guttinger, M., and Acuto, O. (1995). Syk and ZAP-70 mediate recruit-ment of p56lck/CD4 to the activated T cell receptor/CD3/ζ complex. J. Exp. Med. 181, 1997-2006.
72. Thome, M., Germain, V., DiSanto, J. P., and Acuto, O. (1996). The p56lck SH2 domain mediates recruitment of CD8/p56lck to the activated T cell receptor/CD3/ζ complex. Eur. J. Immunol. 26, 2093-2100.
73. Timson Gauen, L. K., Kong, A. N., Samelson, L. E., and Shaw, A. S. (1992). p59fyn Tyrosine kinase asso-ciates with multiple T-cell receptor subunits through its unique amino-terminal domain. Mol. Cell. Biol. 12, 5438-5446.
74. van der Merwe, P. A., and Dushek, O. (2011). Mechanisms for T cell recep-tor triggering. Nat. Rev. Immunol. 11, 47-55.
75. Van Laethem, F., Sarafova, S. D., Park, J. H., Tai, X., Pobezin-sky, L., Guinter, T. I., Adoro, S., Adams, A., Sharrow, S. O., Feigen-baum, L., and Singer, A. (2007). Deletion of CD4 and CD8 corecep-tors permits generation of αβTcells that recognize antigens indepen-dently of the MHC. Immunity 27, 735-750.
76. van Oers, N. S., Lowin-Kropf, B., Fin-lay, D., Connolly, K., and Weiss, A. (1996a). αβ T cell development is abolished in mice lacking both Lck and Fyn protein tyrosine kinases. Immunity 5, 429-436.
77. Van Oers, N. S. C., Killeen, N., and Weiss, A. (1996b). Lck regulates the tyrosine phosphorylation of the T cell receptor subunits and ZAP-70 in murine thymocytes. J. Exp. Med. 183, 1053-1062.
78. van't Hof, W., and Resh, M. D. (1999). Dual fatty acylation of p59(Fyn) is required for associa-tion with the T cell receptor ζ chain through phosphotyrosine-Src homology domain-2 interactions. J. Cell Biol. 145, 377-389.
79. Varma, R., Campi, G., Yokosuka, T., Saito, T., and Dustin, M. L. (2006). T cell receptor-proximal signals are sustained in periph-eral microclusters and terminated in the central supramolecular activation cluster. Immunity 25, 117-127.
80. Werlen, G., Hausmann, B., and Palmer, E. (2000). A motif in the αβ T-cell receptor controls positive selection by modulating ERK activity. Nature 406, 422-426.
81. Wulfing, C., and Davis, M. M. (1998). A receptor/cytoskeletal movement triggered by costimulation dur-ing T cell activation. Science 282, 2266-2269.
82. Xu, C., Gagnon, E., Call, M. E., Schnell, J. R., Schwieters, C. D., Carman, C. V., Chou, J. J., and Wucherpfen-nig, K. W. (2008). Regulation of T cell receptor activation by dynamic membrane binding of the CD3ε cytoplasmic tyrosine-based motif. Cell 135, 702-713.
83. Xu, H., and Littman, D. R. (1993). A kinase-independent function of Lck in potentiating antigen-specific T cell activation. Cell 74, 633-643.
84. Yachi, P. P., Ampudia, J., Gascoigne, N. R. J., and Zal, T. (2005). Non-stimulatory peptides contribute to antigen-induced CD8-T cell recep-tor interaction at the immuno-logical synapse. Nat. Immunol. 6, 785-792.
85. Yachi, P. P., Ampudia, J., Zal, T., and Gascoigne, N. R. J. (2006). Altered peptide ligands induce delayed and reduced CD8-TCR interaction - a role for CD8 in distinguish-ing antigen quality. Immunity 25, 203-211
86. Yasuda, K., Nagafuku, M., Shima, T., Okada, M., Yagi, T., Yamada, T., Minaki, Y., Kato, A., Tani-Ichi, S., Hamaoka, T., and Kosugi, A. (2002). Cutting edge: Fyn is essential for tyrosine phosphorylation of Csk-binding protein/phosphoprotein associated with glycolipid-enriched microdomains in lipid rafts in resting T cells. J. Immunol. 169, 2813-2817.
87. Yokosuka, T., Sakata-Sogawa, K., Kobayashi, W., Hiroshima, M., Hashimoto-Tane, A., Tokunaga, M., Dustin, M. L., and Saito, T. (2005). Newly generated T cell receptor microclusters initiate and sustain T cell activation by recruitment of Zap70 and SLP-76. Nat. Immunol. 6, 1253-1262.
88. Zal, T., Zal, M. A., and Gas-Coigne, N. R. J. (2002). Inhibition of T-cell receptor-coreceptor interactions by antagonist ligands visualized by live FRET imaging of the T-hybridoma immuno-logical synapse. Immunity 16, 521-534.;