Adaptors as central mediators of signal transduction in immune cells

Nature Immunology

Volumn 4, Issue 2, 2003, Pages 110-116

  Jordan, Martha S ^a   Singer, Andrew L ^a   Koretzky, Gary A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN;

BIOCHEMISTRY; CELL ACTIVATION; CELL FUNCTION; EFFECTOR CELL; GENETICS; HUMAN; IMAGING; IMMUNOCOMPETENT CELL; MEDIATOR; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; B-LYMPHOCYTES; BLOOD PLATELETS; CARRIER PROTEINS; HUMANS; LYMPHOCYTE ACTIVATION; MEMBRANE PROTEINS; MICE; MODELS, IMMUNOLOGICAL; PHOSPHOPROTEINS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 0037318720     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/ni0203-110     Document Type: Review

References (89)

1. Weiss, A. & Littman, D.R. Signal transduction by lymphocyte antigen receptors. Cell 76, 263-274 (1994).
2. Finco, T.S., Kadlecek, T., Zhang, W., Samelson, L.E. & Weiss, A. LAT is required for TCR-mediated activation of PLCγl and the Ras pathway. Immunity 9, 617-626 (1998).
3. Zhang, W., Irvin, B.J., Trible, R.P., Abraham, R.T. & Samelson, L.E. Functional analysis of LAT in TCR-mediated signaling pathways using a LAT-deficient Jurkat cell line. Int. Immunol 11, 943-950 (1999).
4. Yablonski, D., Kuhne, M.R., Kadlecek, T. & Weiss, A. Uncoupling of nonreceptor tyrosine kinases from PLC-γl in an SLP-76-deficient T cell. Science 281, 413-416 (1998).
5. Zhang, W., Trible, R.P. & Samelson, L.E. LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity 9, 239-246 (1998).
6. Zhang, W., Sloan-Lancaster, J., Kitchen, J., Tribe, R.P. & Samelson, L.E. Lat: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 92, 83-92 (1998).
7. Asada, H. et al. Grf40, A novel Grb2 family member, is involved in T cell signaling through interaction with SLP-76 and LAT. J. Exp. Med. 189, 1383-1390 (1999).
8. Liu, S.K., Fang, N., Koretzky, G.A. & McGlade, C.J. The hematopoietic-specific adaptor protein gads functions in T-cell signaling via interactions with the SLP-76 and LAT adaptors. Curr. Biol 9, 67-75 (1999).
9. Wardenburg, J.B. et al. Phosphorylation of SLP-76 by the ZAP-70 protein-tyrosine kinase is required for T-cell receptor function. J. Biol Chem. 271, 19641-19644 (1996).
10. Fang, N. & Koretzky, G.A. SLP-76 and Vav function in separate, but overlapping pathways to augment interleukin-2 promoter activity. J. Biol. Chem. 274, 16206-16212 (1999).
11. Wu, J., Motto, D.G., Koretzky, G.A. & Weiss, A. Vav and SLP-76 interact and functionally cooperate in IL-2 gene activation. Immunity 4, 593-602 (1996).
12. Wunderlich, L., Farago, A., Downward, J. & Buday, L. Association of Nck with tyrosine-phosphorylated SLP-76 in activated T lymphocytes. Eur. J. Immunol. 29, 1068-1075 (1999).
13. Bunnell, S.C. et al. Biochemical interactions integrating Itk with the T cell receptor-initiated signaling cascade. J. Biol. Chem. 275, 2219-2230 (2000).
14. Su, Y.W. et al. Interaction of SLP adaptors with the SH2 domain of Tec family kinases. Eur. J. Immunol. 29, 3702-3711 (1999).
15. da Silva, A.J. et al. Cloning of a novel T-cell protein FYB that binds FYN and SH2-domain- containing leukocyte protein 76 and modulates interleukin 2 production. Proc. Natl. Acad. Sci. USA 94, 7493-7498 (1997).
16. Musci, M.A. et al. Molecular cloning of SLAP-130, an SLP-76-associated substrate of the T cell antigen receptor-stimulated protein tyrosine kinases. J. Biol. Chem. 272, 11674-11677 (1997).
17. Sauer, K. et al. Hematopoietic progenitor kinase I associates physically and functionally with the adaptor proteins B cell linker protein and SLP-76 in lymphocytes. J. Biol. Chem. 276, 45207-45216 (2001).
18. Zhang, W. et al. Association of Grb2, Gads, and phospholipase C-γ I with phosphorylated LAT tyrosine residues. Effect of LAT tyrosine mutations on T cell antigen receptor-mediated signaling. J. Biol. Chem. 275, 23355-23361 (2000).
19. Yablonski, D., Kadlecek, T. & Weiss, A. Identification of a phospholipase C-γI (PLC-γI) SH3 domain-binding site in SLP-76 required for T-cell receptor-mediated activation of PLC-γI and NFAT. Mol. Cell. Biol. 21, 4208-4218 (2001).
20. Veri, M.C. et al. Membrane raft-dependent regulation of phospholipase Cγ-I activation in T lymphocytes. Mol. Cell. Biol. 21, 6939-6950 (2001).
21. Buday, L., Egan, S.E., Rodriguez Viciana, P., Cantrell, D.A. & Downward, J. A complex of Grb2 adaptor protein, Sos exchange factor, and a 36-kDa membrane-bound tyrosine phosphoprotein is implicated in ras activation in T cells. J. Biol. Chem. 269, 9019-9023 (1994).
22. Lin, J. & Weiss, A. Identification of the minimal tyrosine residues required for linker for activation of T cell function. J. Biol. Chem. 276, 29588-29595 (2001).
23. Paz, P.E. et al. Mapping the Zap-70 phosphorylation sites on LAT (linker for activation of T cells) required for recruitment and activation of signalling proteins in T cells. Biochem. J. 356, 461-471 (2001).
24. Dower, N.A. et al. RasGRP is essential for mouse thymocyte differentiation and TCR signaling. Nat. Immunol. 1, 317-321 (2000).
25. Clements, J.L. et al. Requirements for the leukocyte-specific adapter protein SLP-76 for normal T cell development. Science 281, 416-419 (1998).
26. Pivniouk, V. et al. Impaired viability and profound block in thymocyte development in mice lacking the adaptor protein SLP-76. Cell 94, 229-238 (1998).
27. Zhang, W. et al. Essential role of LAT in T cell development. Immunity 10, 323-332. (1999).
28. Aguado, E. et al. Induction of T helper type 2 immunity by a point mutation in the LAT adaptor. Science 296, 2039-2040 (2002).
29. Kumar, L., Pivniouk, V., de la Fuente, M.A., Laouini, D. & Gaha, R.S. Differential role of SLP-76 domains in T cell development and function. Proc. Natl. Acad. Sci. USA 99, 884-889 (2002).
30. Myung, P.S. et al. Differential requirement for SLP-76 domains in T cell development and function. Immunity 15, 1011-1026 (2001).
31. Sommers, C.L. et al. A LAT mutation that inhibits T cell development yet induces lymphoproliferation. Science 296, 2040-2043 (2002).
32. Turner, M. et al. A requirement for the Rho-family GTP exchange factor Vav in positive and negative selection of thymocytes. Immunity 7, 451-460 (1997).
33. Yoder, J. et al. Requirement for the SLP-76 adaptor GADs in T cell development. Science 291, 1987-1991 (2001).
34. Griffiths, E.K. et al. Positive regulation of T cell activation and integrin adhesion by the adapter Fyb/Slap. Science 293, 2260-2263 (2001).
35. Peterson, E.J. et al. Coupling of the TCR to integrin activation by Slap-130/Fyb. Science 293, 2263-2265 (2001).
36. Leo, A. & Schraven, B. Adapters in lymphocyte signalling. Curr. Opin. Immunol. 13, 307-316 (2001).
37. Brdicka, T. et al. Phosphoprotein associated with glycosphingolipid-enriched microdomains (PAG), a novel ubiquitously transmembrane adaptor protein, binds the protein tyrosine kinase csk and is involved in regulation of T cell activation. J. Exp. Med. 191, 1591-1604 (2000).
38. Kawabuchi, M. et al. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature 404, 999-1003 (2000).
39. Nada, S., Okada, M., MacAuley, A., Cooper, J.A. & Nakagawa, H. Cloning of a complementary DNA for a protein-tyrosine kinase that specifically phosphorylates a negative regulatory site of p60-src. Nature 351, 69-72 (1991).
40. Jones, N. & Dumont, D.J. Recruitment of Dok-R to the EGF receptor through its PTB domain is required for attenuation of Erk MAP kinase activation. Curr. Biol. 9, 1057-1060 (1999).
41. Suzu, S. et al. p56(dok-2) as a cytokine-inducible inhibitor of cell proliferation and signal transduction. EMBO J. 19, 5114-5122 (2000).
42. Veilette, A., Latour, S. & Davidson, D. Negative regulation of immunoreceptor signaling. Annu. Rev. Immunol. 20, 669-707 (2002).
43. Yamanashi, Y. et al. Role of the rasGAP-associated docking protein p62(dok) in negative regulation of B cell receptor-mediated signaling. Genes Dev. 14, 11-16 (2000).
44. Carpino, N. et al. p62(dok): a constitutively tyrosine-phosphorylated. GAP-associated protein in chronic myelogenous leukemia progenitor cells. Cell 88, 197-204 (1997).
45. Jones, N. & Dumont, D.J. The Tek/Tie2 receptor signals through a novel Dok-related docking protein, Dok-R. Oncogene 17, 1097-1108 (1998).
46. Lemay, S., Davidson, D., Latour, S. & Veillette, A. Dok-3, a novel adapter molecule involved in the negative regulation of immunoreceptor signaling. Mol. Cell. Biol. 20, 2743-2754 (2000).
47. Rafnar, T. et al. Stimulation of the high-affinity IgE receptor results in the tyrosine phosphorylation of a 60 kD protein which is associated with the protein-tyrosine kinase. Csk. Mol. Immunol. 35, 249-257 (1998).
48. Tamir, I, et al. The RasGAP-binding protein p62dok is a mediator of inhibitory FcγRIIB signals in B cells. Immunity 12, 347-358 (2000).
49. Coffey, A.J. et al. Host response to EBV infection in X-linked lymphoproliferative disease results from mutations in an SH2-domain encoding gene. Nat. Genet. 20, 129-135 (1998).
50. Nichols, K.E. et al. Inactivating mutations in an SH2 domain-encoding gene in X-linked lymphoproliferative syndrome. Proc. Natl. Acad. Sci. USA 95, 13765-13770 (1998).
51. Sayos, J. et al. The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature 395, 462-469 (1998).
52. Czar, M.J. et al. Altered lymphocyte responses and cytokine production in mice deficient in the X-linked lymphoproliferative disease gene SH2DIA/DSHP/SAP. Proc. Natl. Acad. Sci. USA 98, 7449-7454 (2001).
53. Wu, C. et al. SAP controls T cell responses to virus and terminal differentiation of TH2 cells. Nat. Immunol. 2, 410-414 (2001).
54. Morra, M. et al. X-linked lymphoproliferative disease: a progressive immunodeficiency. Annu. Rev. Immunol. 19, 657-682 (2001).
55. Latour, S. et al. Regulation of SLAM-mediated signal transduction by SAP, the X-linked lymphoproliferative gene product. Nat. Immunol. 2, 681-690 (2001).
56. Tangye, S.G., Phillips, J.H. Lanier, L.L. & Nichols, K.E. Functional requirements for SAP in 2B4-mediated activation of human natural killer cells as revealed by the X-linked lymphoproliferative syndrome. J. Immunol. 165, 2932-2936 (2000).
57. Fu, C., Turck, C.W., Kurosaki, T. & Chan, A.C. BLNK: a central linker protein in B cell activation. Immunity 9, 93-103 (1998).
58. Wienands, J. et al. SLP-65: a new signaling component in B lymphocytes which requires expression of the antigen receptor for phosphorylation. J. Exp. Med. 188, 791-795 (1998).
59. Ishia, M. et al. BLNK required for coupling Syk to PLCγ2 and RacI-JNK in B cells. Immunity 10, 117-125 (1999).
60. Chiu, C.W., Dalton, M., Ishia, M., Kurosaki, T. & Chan, A.C. BLNK: molecular scaffolding through 'cis'-mediated organization of signaling protein. EMBO J. 21, 6461-6472 (2002).
61. Hayashi, K. et al. The B cell-restricted adaptor BASH is required for normal development and antigen receptor-mediated activation of B cells. Proc. Natl. Acad. Sci. USA 97, 2755-2760 (2000).
62. Jumaa, H. et al. Abnormal development and function of B lymphocytes in mice deficient for the signaling adaptor protein SLP-65. Immunity II, 547-554 (1999).
63. Pappu, R. et al. Requirements for B cell linker protein (BLNK) in B cell development. Science 286, 1949-1954 (1999).
64. Xu, S. et al. B cell development and activation defects resulting in xid-like immunodeficiency in BLNK/SLP-65-deficient mice. Int. Immunol. 12, 397-404 (2000).
65. + B cells. J. Immunol. 165, 4153-4157 (2000).
66. Minegishi, Y. et al. An essential role for BLNK in human B cell development. Science 286, 1954-1957 (1999).
67. Flemming, A., Brummer, T., Reth, M. & Jumaa, H. The adaptor protein SLP-65 acts as a tumor suppressor that limits pre-B cell expansion. Nat. Immunol. 4, 38-43 (2003).
68. Engels, N., Wollscheid, B. & Wienands, J. Association of SLP-65/BLNK with the B cell antigen receptor through a non-ITAM tyrosine of Ig-α. Eur. J. Immunol. 31, 2126-2134 (2001).
69. Kabak, S. et al. The direct recruitment of BLNK to immunoglobulin α couples the B-cell antigen receptor to distal signaling pathways. Mol. Cell. Biol. 22, 2524-2535 (2002).
70. Cassard, S., Choquet, D., Fridman, W.H. & Bonnerot, C. Regulation of ITAM signaling by specific sequences in Ig-β B cell antigen receptor subunit. J. Biol. Chem. 271, 23786-23791 (1996).
71. Judd, B.A. et al. Differential requirement for LAT and SLP-76 in GPVI versus T cell receptor signaling. J. Exp. Med. 195, 705-717 (2002).
72. Clements, J.L. et al. Fetal hemorrhage and platelet dysfunction in SLP-76-deficient mice. J. Clin. Invest. 103, 19-25 (1999).
73. Judd, B.A. et al. Hematopoietic reconstitution of SLP-76 corrects hemostasis and platelet signaling through α IIb β 3 and collagen receptors. Proc. Natl. Acad. Sci. USA 97, 12056-12061 (2000).
74. Pasquet, J.M. et al. LAT is required for tyrosine phosphorylation of phospholipase cγ2 and platelet activation by the collagen receptor GPVI. Mol. Cell. Biol. 19, 8326-8334 (1999).
75. Burack, W.R., Cheng, A.M. & Shaw, A.S. Scaffolds, adaptors and linkers of TCR signaling: theory and practice. Curr. Opin. Immunol. 14, 312-316 (2002).
76. Geng, L. & Rudd, C.E. Signalling scaffolds and adaptors in T-cell immunity. Br. J. Haematol. 116, 19-27 (2002).
77. Werlen, G. & Palmer, E. The T-cell receptor signalosome: a dynamic structure with expanding complexity. Curr. Opin. Immunol. 14, 299-305 (2002).
78. Dustin, M.L. & Shaw, A.S. Constimulation: building an immunological synapse. Science 283, 649-650 (1999).
79. Grakoui, A. et al. The immunological synapse: a molecular machine controlling T cell activation. Science 285, 221-227 (1999).
80. 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).
81. Lee, K.H. et al. T cell receptor signaling precedes immunological synapse formation. Science 295, 1539-1542 (2002).
82. Freiberg, B.A. et al. Staging and resetting T cell activation in SMACs. Nat. Immunol 3, 911-917 (2002).
83. Bunnell, S.C. et al. T cell receptor ligation the formation of dynamically regulated signaling assemblies. J. Cell. Biol. 158, 1263-1275 (2002).
84. Zhu, M., Janssen, E., Leung, K. & Zhang, W. Molecular cloning of a novel gene encoding a membrane-associated adaptor protein (LAX) in lymphocyte signaling. J. Biol. Chem. 277, 46151-46158 (2002).
85. Brdicka, T. et al. NTAL (non-T cell activation linker): a transmembrane adaptor protein involved in immunoreceptor signaling. J. Exp. Med. 196, 1617-1626 (2002).
86. Janssen, E., Zhu, W., Koonpaew, S. & Zhang, W. LAB: A new membrane-associated adaptor molecule in B cell activation. Nat. Immunol. 4, 117-123 (2003).
87. Abtahian, F. et al. Regulation of blood and lymphatic vascular separation by the signaling proteins SLP-76 and Syk. Science 299, 247-251 (2003).
88. Takaki, S. et al. Control of B cell production by the adaptor protein Ink. Definition of a conserved family of signal-modulating proteins. Immunity 13, 599-609 (2000).
89. Takaki, S., Morita, H. Tezuka, Y. & Takatsu, K. Enhanced hematopoiesis by hematopoietic progenitor cells lacking intracellular adaptor protein, Lnk. J. Exp. Med. 195, 151-160 (2002).