The role of adaptor proteins in lymphocyte activation

Molecular Immunology

Volumn 41, Issue 6-7, 2004, Pages 615-630

  Togni, Mauro ^a   Lindquist, Jon ^a   Gerber, Annegret ^a   Kölsch, Uwe ^a   Hamm Baarke, Andrea ^a   Kliche, Stefanie ^a   Schraven, Burkhart ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

activation induced cell death; ADAP SLAP 130 Fyb; adhesion and degranulation promoting adaptor protein SLP 76 associated phosphoprotein of 130 kDa Fyn binding protein; AICD; immunoreceptor tyrosine based activation motifs; ITAMs; ITIM

Indexed keywords

ADAPTOR PROTEIN; ADHESION AND DEGRANULATION PROMOTING ADAPTOR PROTEIN SLP 76 ASSOCIATED PHOSPHOPROTEIN OF 130KDA FYN BINDING PROTEIN; BINDING PROTEIN; LCK INTERACTING MEMBRANE PROTEIN; LINKER FOR ACTIVATION OF X PROTEIN; LINKER OF ACTIVATION OF T CELL PROTEIN; MEMBRANE PROTEIN; NON T CELL ACTIVATION LINKER LINKER FOR ACTIVATION OF B CELL PROTEIN; PHOSPHOLIPASE C; PROTEIN ASSOCIATED WITH GEM CSK BINDING PROTEIN; PROTEIN SH2; PROTEIN SKAP; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; REGULATOR FOR ADHESION AND POLARIZATION ENRICHED IN LYMPHOCYTE PROTEIN; REGULATOR PROTEIN; SHP2 INTERACTING TRANSMEMBRANE ADAPTOR PROTEIN; SRC KINASE ASSOCIATED PHOSPHOPROTEIN OF 55KDA; T CELL RECEPTOR INTERACTING MOLECULE; TRANSMEMBRANE ADAPTOR PROTEIN; UNCLASSIFIED DRUG;

B LYMPHOCYTE; CELL ADHESION; CELL MEMBRANE; CELLULAR DISTRIBUTION; CYTOSOL; HUMAN; IMMUNOREGULATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DIFFERENTIATION; MEDICAL RESEARCH; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; REGULATORY MECHANISM; REVIEW; T LYMPHOCYTE;

EID: 3042567210     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2004.04.009     Document Type: Article

References (118)

1. Abbas A.K., Sen R. The activation of lymphocytes is in their CARMA. Immunity. 18:2003;721-722
2. Abraham R.T. Rap1 redux. Nat. Immunol. 4:2003;725-727
3. Aguado E., Richelme S., Nunez-Cruz S., Miazek A., Mura A.M., Richelme M., Guo X.J., Sainty D., He H.T., Malissen B., Malissen M. Induction of T helper type 2 immunity by a point mutation in the LAT adaptor. Science. 296:2002;2036-2040
4. Bank I., Chess L. Perturbation of the T4 molecule transmits a negative signal to T cells. J. Exp. Med. 162:1985;1294-1303
5. Benjamin R.J., Waldmann H. Induction of tolerance by monoclonal antibody therapy. Nature. 320:1986;449-451
6. Benoit L., Wang X., Pabst H.F., Dutz J., Tan R. Defective NK cell activation in X-linked lymphoproliferative disease. J. Immunol. 165:2000;3549-3553
7. Black D.S., Marie-Cardine A., Schraven B., Bliska J.B. The Yersinia tyrosine phosphatase YopH targets a novel adhesion-regulated signalling complex in macrophages. Cell Microbiol. 2:2000;401-414
8. Boerth N.J., Judd B.A., Koretzky G.A. Functional association between ADAP and SLP-76 in Jurkat T cells. J. Biol. Chem. 275:2000;5143-5152
9. Boussitis V.A., Freeman G.J., Berezovskaya A., Barber D.L., Nadler L.M. Maintainance of human T cell anergy: Blocking of IL-2 gene transcription by activated Rap 1. Science. 278:1997;124-128
10. Brdicka T., Imrich M., Angelisova P., Brdickova N., Horvath O., Spicka J., Hilgert I., Luskova P., Draber P., Novak P., Engels N., Wienands J., Simeoni L., Osterreicher J., Aguado E., Malissen M., Schraven B., Horejsi V. Non-T cell activation linker (NTAL): a transmembrane adaptor protein involved in immunoreceptor signaling. J. Exp. Med. 196:2002;1617-1626
11. Brdicka T., Pavlistova D., Leo A., Bruyns E., Korinek V., Angelisova P., Scherer J., Shevchenko A., Hilgert I., Cerny J., Drbal K., Kuramitsu Y., Kornacker B., Horejsi V., Schraven B. Phosphoprotein associated with glycosphingolipid-enriched microdomains (PAG), a novel ubiquitously expressed transmembrane adaptor protein, binds the protein tyrosine kinase csk and is involved in regulation of T cell activation. J. Exp. Med. 191:2000;1591-1604
12. Brdicková N., Brdicka T., Angelisová P., Horváth O., Špicka J., Hilgert I., Paces J., Simeoni L., Kliche S., Merten C., Schraven C., Horejší V. LIME: a new membrane raft-associated adaptor protein involved in CD4 and CD8 coreceptor signaling. J. Exp. Med. 198:2003;1453-1462
13. Bruyns E., Marie-Cardine A., Kirchgessner H., Sagolla K., Shevchenko A., Mann M., Autschbach F., Bensussan A., Meuer S., Schraven B. T cell receptor (TCR) interacting molecule (TRIM), a novel disulfide-linked dimer associated with the TCR-CD3-zeta complex, recruits intracellular signaling proteins to the plasma membrane. J. Exp. Med. 188:1998;561-575
14. Cary, L.A., Cooper, J.A., 2000. Molecular switches in lipid rafts. Nature 404, 945-947.
15. Chan A.C., Desai D.M., Weiss A. The role of protein tyrosine kinases and protein tyrosine phosphatases in T cell antigen receptor signal transduction. Annu. Rev. Immunol. 12:1994;555-592
16. Chan B., Lanyi A., Song H.K., Griesbach J., Simarro-Grande M., Poy F., Howie D., Sumegi J., Terhorst C., Eck M.J. SAP couples Fyn to SLAM immune receptors. Nat. Cell Biol. 5:2003;155-160
17. Choi Y.B., Kim C.K., Yun Y. Lad, an adaptor protein interacting with the SH2 domain of p56lck, is required for T cell activation. J. Immunol. 163:1999;5242-5249
18. Christian S.L., Lee R.L., McLeod S.J., Burgess A.E., Li A.H., Dang-Lawson M., Lin K.B., Gold M.R. Activation of the Rap GTPases in B lymphocytes modulates B cell antigen receptor-induced activation of Akt but has no effect on MAP kinase activation. J. Biol. Chem. 278:2003;41756-41767
19. da Silva A.J., Li Z., de Vera C., Canto E., Findell P., Rudd C.E. 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. 94:1997;7493-7498
20. Davidson D., Bakinowski M., Thomas M.L., Horejsi V., Veillette A. Phosphorylation-dependent regulation of T-cell activation by PAG/Cbp, a lipid raft-associated transmembrane adaptor. Mol. Cell Biol. 23:2003;2017-2028
21. Dower N.A., Stang S.L., Bottorff D.A., Ebinu J.O., Dickie P., Ostergaard H.L., Stone J.C. rasGRP is essential for mouse thymocyte differentiation and TCR signaling. Nat. Immunol. 1:2000;317-321
22. Downward J., Graves J.D., Warne P.H., Rayter S., Cantrell D.A. Stimulation of p21ras upon T-cell activation. Nature. 346:1990;719-723
23. Drappa J., Kamen L.A., Chan E., Georgiev M., Ashany D., Marti F., King P.D. Impaired T cell death and lupus-like autoimmunity in t cell-specific adaptor protein-deficient mice. J. Exp. Med. 198:2003;809-821
24. Dustin M.L., Springer T.A. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature. 341:1989;619-624
25. Ebinu J.O., Bottorff D.A., Chan E.Y., Stang S.L., Dunn R.J., Stone J.C. rasGRP, a ras guanyl nucleotide-releasing protein with calcium- and diacylglycerol-binding motifs. Science. 280:1998;1082-1086
26. Ebinu J.O., Stang S.L., Teixeira C., Bottorff D.A., Hooton J., Blumberg P.M., Barry M., Bleakley R.C., Ostergaard H.L., Stone J.C. rasGRP links T-cell receptor signaling to ras. Blood. 95:2000;3199-3203
27. Egawa T., Albrecht B., Favier B., Sunshine M.J., Mirchandani K., O'Brien W., Thome M., Littman D.R. Requirement for CARMA1 in antigen receptor-induced NF-kappa B activation and lymphocyte proliferation. Curr. Biol. 13:2003;1252-1258
28. Eichmann K., Jonsson J.I., Falk I., Emmrich F. Effective activation of resting mouse T lymphocytes by cross-linking submitogenic concentrations of the T cell antigen receptor with either Lyt-2 or L3T4. Eur. J. Immunol. 17:1987;643-650
29. Engels N., Wollscheid B., Wienands J. Association of SLP-65/BLNK with the B cell antigen receptor through a non-ITAM tyrosine of Ig-alpha. Eur. J. Immunol. 31:2001;2126-2134
30. Filipp D., Zhang J., Leung B.L., Shaw A., Levin S.D., Veillette A., Julius M. Regulation of Fyn through translocation of activated Lck into lipid rafts. J. Exp. Med. 197:2003;1221-1227
31. Gaide O., Favier B., Legler D.F., Bonnet D., Brissoni B., Valitutti S., Bron C., Tschopp J., Thome M. CARMA1 is a critical lipid raft-associated regulator of TCR-induced NF-kappa B activation. Nat. Immunol. 3:2002;836-843
32. Geng L., Pfister S., Kraeft S.K., Rudd C.E. Adaptor FYB (Fyn-binding protein) regulates integrin-mediated adhesion and mediator release: differential involvement of the FYB SH3 domain. Proc. Natl. Acad. Sci. USA. 98:2001;11527-11532
33. Greene T.A., Powell P., Nzerem C., Shapiro M.J., Shapiro V.S. Cloning and characterization of ALX, an adaptor downstream of CD28. J. Biol. Chem. 278:2003;45128-45134
34. Griffiths E.K., Krawczyk C., Kong Y.Y., Raab M., Hyduk S.J., Bouchard D., Chan V.S., Kozieradzki I., Oliveira-Dos-Santos A.J., Wakeham A., Ohashi P.S., Cybulsky M.I., Rudd C.E., Penninger J.M. Positive regulation of T cell activation and integrin adhesion by the adaptor Fyb/Slap. Science. 293:2001;2260-2263
35. Hara H., Wada T., Bakal C., Kozieradzki I., Suzuki S., Suzuki N., Nghiem M., Griffiths E.K., Krawczyk C., Bauer B., D'Acquisto F., Ghosh S., Yeh W.C., Baier G., Rottapel R., Penninger J.M. The MAGUK family protein CARD11 is essential for lymphocyte activation. Immunity. 18:2003;763-775
36. Harding S., Lipp P., Alexander D.R. A therapeutic CD4 monoclonal antibody inhibits TCR-zeta chain phosphorylation, zeta-associated protein of 70-kDa Tyr319 phosphorylation, and TCR internalization in primary human T cells. J. Immunol. 169:2002;230-238
37. Hogquist K. rasGRP: the missing link for ras activation in thymocytes. Trends Immunol. 22:2001;69
38. Howe L.R., Weiss A. Multiple kinases mediate T-cell receptor signaling. TIBS. 20:1995;59-64
39. Howie D., Sayos J., Terhorst C., Morra M. The gene defective in X-linked lymphoproliferative disease controls T cell dependent immune surveillance against Epstein-Barr virus. Curr. Opin. Immunol. 12:2000;474-478
40. Hunter A.J., Ottoson N., Boerth N., Koretzky G.A., Shimizu Y. Cutting edge: a novel function for the ADAP/FYB adaptor protein in beta 1 integrin signaling and T lymphocyte migration. J. Immunol. 164:2000;1143-1147
41. Hur E.B., Son M., Lee O.-H., Choi Y., Park C., Lee H., Yun Y. LIME, a novel transmembrane adaptor protein, Associates with p56lck and Mediates T Cell Activation. J. Exp. Med. 198:2003;1463-1473
42. Iwashima M., Irving B.A., Van Oers N.S.C., Chan A.C., Weiss A. Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases. Science. 263:1994;1136-1139
43. Janssen E., Zhu M., Zhang W., Koonpaew S. LAB: a new membrane-associated adaptor molecule in B cell activation. Nat. Immunol. 4:2003;117-123
44. Jordan M.S., Singer A.L., Koretzky G.A. Adaptors as central mediators of signal transduction in immune cells. Nat. Immunol. 4:2003;110-116
45. Jumaa H., Mitterer M., Reth M., Nielsen P.J. The absence of SLP65 and Btk blocks B cell development at the preB cell receptor-positive stage. Eur. J. Immunol. 31:2001;2164-2169
46. Jumaa H., Wollscheid B., Mitterer M., Wienands J., Reth M., Nielsen P.J. Abnormal development and function of B lymphocytes in mice deficient for the signaling adaptor protein SLP-65. Immunity. 11:1999;547-554
47. Jun J.E., Wilson L.E., Vinuesa C.G., Lesage S., Blery M., Miosge L.A., Cook M.C., Kucharska E.M., Hara H., Penninger J.M., Domashenz H., Hong N.A., Glynne R.J., Nelms K.A., Goodnow C.C. Identifying the MAGUK protein Carma-1 as a central regulator of humoral immune responses and atopy by genome-wide mouse mutagenesis. Immunity. 18:2003;751-762
48. June C.H., Fletcher M.C., Ledbetter J.A., Samelson L.E. Increases in tyrosine phosphorylation are detectable before phospholipase C activation after T cell receptor stimulation. J. Immunol. 144:1990a;1591-1599
49. June C.H., Fletcher M.C., Ledbetter J.A., Schieven G.L., Siegel J.N., Phillips A.F., Samelson L.E. Inhibition of tyrosine phosphorylation prevents T-cell receptor-mediated signal transduction. Proc. Natl. Acad. Sci. USA. 87:1990b;7722-7726
50. Kabak S., Skaggs B.J., Gold M.R., Affolter M., West K.L., Foster M.S., Siemasko K., Chan A.C., Aebersold R., Clark M.R. The direct recruitment of BLNK to immunoglobulin alpha couples the B-cell antigen receptor to distal signaling pathways. Mol. Cell Biol. 22:2002;2524-2535
51. Kang H., Freund C., Duke-Cohan J.S., Musacchio A., Wagner G., Rudd C.E. SH3 domain recognition of a proline-independent tyrosine-based RKxxYxxY motif in immune cell adaptor SKAP-55. EMBO J. 19:2000;2889-2899
52. Katagiri K., Hattori M., Minato N., Irie S., Takatsu K., Kinashi T. Rap1 is a potent activation signal for leukocyte function-associated antigen 1 distinct from protein kinase C and phosphatidylinositol-3-OH kinase. Mol. Cell Biol. 20:2000;1956-1969
53. Katagiri K., Hattori M., Minato N., Kinashi T. Rap1 functions as a key regulator of T-cell and antigen-presenting cell interactions and modulates T-cell responses. Mol. Cell Biol. 22:2002;1001-1015
54. Katagiri K., Maeda A., Shimonaka M., Kinashi T. RAPL, a Rap1-binding molecule that mediates Rap1-induced adhesion through spatial regulation of LFA-1. Nat. Immunol. 4:2003;741-748
55. Kawabuchi M., Satomi Y., Takao T., Shimonishi Y., Nada S., Nagai K., Tarakhovsky A., Okada M. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature. 404:2000;999-1003
56. Koretzky G.A., Boerth N.J. The role of adaptor proteins in T cell activation. Cell Mol. Life Sci. 56:1999;1048-1060
57. Koretzky G.A., Myung P.S. Positive and negative regulation of T-cell activation by adaptor proteins. Nat. Rev. Immunol. 1:2001;95-107
58. Latour S., Gish G., Helgason C.D., Humphries R.K., Pawson T., Veillette A. Regulation of SLAM-mediated signal transduction by SAP, the X-linked lymphoproliferative gene product. Nat. Immunol. 2:2001;681-690
59. Latour S., Roncagalli R., Chen R., Bakinowski M., Shi X., Schwartzberg P.L., Davidson D., Veillette A. Binding of SAP SH2 domain to FynT SH3 domain reveals a novel mechanism of receptor signalling in immune regulation. Nat. Cell Biol. 5:2003;149-154
60. Latour S., Veillette A. Molecular and immunological basis of X-linked lymphoproliferative disease. Immunol. Rev. 192:2003;212-224
61. Laub R., Brecht R., Dorsch M., Valey U., Wenk K., Emmrich F. Anti-human CD4 induces peripheral tolerance in a human CD4+, murine CD4-, HLA-DR+ advanced transgenic mouse model. J. Immunol. 169:2002;2947-2955
62. Laub R., Dorsch M., Wenk K., Emmrich F. Induction of immunologic tolerance to tetanus toxoid by anti-human CD4 in HLA-DR3(+)/human CD4(+)/murine CD4(-) multiple transgenic mice. Transplant Proc. 33:2001;2182-2183
63. Layer K., Lin G., Nencioni A., Hu W., Schmucker A., Antov A.N., Li X., Takamatsu S., Chevassut T., Dower N.A., Stang S.L., Beier D., Buhlmann J., Bronson R.T., Elkon K.B., Stone J.C., Van Parijs L., Lim B. Autoimmunity as the consequence of a spontaneous mutation in rasgrp1. Immunity. 19:2003;243-255
64. Leo A., Schraven B. Adaptors in lymphocyte signalling. Curr. Opin. Immunol. 13:2001;307-316
65. Leo A., Wienands J., Baier G., Horejsi V., Schraven B. Adaptors in lymphocyte signaling. J. Clin. Invest. 109:2002;301-309
66. Lin J., Weiss A., Finco T.S. Localization of LAT in glycolipid-enriched microdomains is required for T cell activation. J. Biol. Chem. 274:1999;28861-28864
67. Lindquist J.A., Simeoni L., Schraven B. Transmembrane adaptors: attractants for cytoplasmic effectors. Immunol. Rev. 191:2003;165-182
68. Liu J., Kang H., Raab M., da Silva A.J., Kraeft S.K., Rudd C.E. FYB (FYN binding protein) serves as a binding partner for lymphoid protein and FYN kinase substrate SKAP-55 and a SKAP-55-related protein in T cells. Proc. Natl. Acad. Sci. USA. 95:1998;8779-8784
69. Marie-Cardine A., Bruyns E., Eckerskorn C., Kirchgessner H., Meuer S.C., Schraven B. Molecular cloning of SKAP-55, a novel protein that associates with the protein tyrosine kinase p59fyn in human T-lymphocytes. J. Biol. Chem. 272:1997;16077-16080
70. Marie-Cardine A., Hendricks-Taylor L.R., Boerth N.J., Zhao H., Schraven B., Koretzky G.A. Molecular interaction between the Fyn-associated protein SKAP-55 and the SLP-76-associated phosphoprotein ADAP. J. Biol. Chem. 273:1998;25789-25795
71. Marie-Cardine A., Kirchgessner H., Bruyns E., Shevchenko A., Mann M., Autschbach F., Ratnofsky S., Meuer S., Schraven B. SHP2-interacting transmembrane adaptor protein (SIT), a novel disulfide- linked dimer regulating human T cell activation. J. Exp. Med. 189:1999a;1181-1194
72. Marie-Cardine A., Kirchgessner H., Schraven B. Molecular alterations of the Fyn-complex occur as late events of human T cell activation. Eur. J. Immunol. 29:1999b;1175-1187
73. Marinari B., Simeoni L., Schraven B., Piccolella E., Tuosto L. The activation of Csk by CD4 interferes with TCR-mediated activatory signaling. Eur. J. Immunol. 33:2003;2609-2618
74. McLeod S.J., Ingham R.J., Bos J.L., Kurosaki T., Gold M.R. Activation of the Rap1 GTPase by the B cell antigen receptor. J. Biol. Chem. 273:1998;29218-29223
75. McLeod S.J., Li A.H., Lee R.L., Burgess A.E., Gold M.R. The Rap GTPases regulate B cell migration toward the chemokine stromal cell-derived factor-1 (CXCL12): potential role for Rap2 in promoting B cell migration. J. Immunol. 169:2002;1365-1371
76. Morra M., Lu J., Poy F., Martin M., Sayos J., Calpe S., Gullo C., Howie D., Rietdijk S., Thompson A., Coyle A.J., Denny C., Yaffe M.B., Engel P., Eck M.J., Terhorst C. Structural basis for the interaction of the free SH2 domain EAT-2 with SLAM receptors in hematopoietic cells. EMBO J. 20:2001;5840-5852
77. Musci M.A., Hendricks-Taylor L.R., Motto D.G., Paskind M., Kamens J., Turck C.W., Koretzky G.A. Molecular cloning of ADAP, a SLP-76 associated substrate of the TCR stimulated protein tyrosine kinases. J. Biol. Chem. 272:1997;11674-11677
78. Myung P.S., Derimanov G.S., Jordan M.S., Punt J.A., Liu Q.H., Judd B.A., Meyers E.E., Sigmund C.D., Freedman B.D., Koretzky G.A. Differential requirement for SLP-76 domains in T cell development and function. Immunity. 15:2001;1011-1026
79. Nakajima H., Cella M., Bouchon A., Grierson H.L., Lewis J., Duckett C.S., Cohen J.I., Colonna M. Patients with X-linked lymphoproliferative disease have a defect in 2B4 receptor-mediated NK cell cytotoxicity. Eur. J. Immunol. 30:2000;3309-3318
80. Newton K., Dixit V.M. Mice lacking the CARD of CARMA1 exhibit defective B lymphocyte development and impaired proliferation of their B and T lymphocytes. Curr. Biol. 13:2003;1247-1251
81. Nichols K.E., Koretzky G.A., June C.H. SAP: natural inhibitor or grand SLAM of T cell activation? Nat. Immunol. 2:2001;665-666
82. Nunez-Cruz S., Aguado E., Richelme S., Chetaille B., Mura A.M., Richelme M., Pouyet L., Jouvin-Marche E., Xerri L., Malissen B., Malissen M. LAT regulates gammadelta T cell homeostasis and differentiation. Nat. Immunol. 4:2003;999-1008
83. Ohtake H., Ichikawa N., Okada M., Yamashita T. Cutting edge: transmembrane phosphoprotein Csk-binding protein/phosphoprotein associated with glycosphingolipid-enriched microdomains as a negative feedback regulator of mast cell signaling through the FcepsilonRI. J. Immunol. 168:2002;2087-2090
84. Owens T., Fazekas de St Groth B., Miller J.F. Coaggregation of the T-cell receptor with CD4 and other T-cell surface molecules enhances T-cell activation. Proc. Natl. Acad. Sci. USA. 84:1987;9209-9213
85. Peterson E.J., Woods M.L., Dmowski S.A., Derimanov G., Jordan M.S., Wu J.N., Myung P.S., Liu Q.H., Pribila J.T., Freedman B.D., Shimizu Y., Koretzky G.A. Coupling of the TCR to integrin activation by ADAP/Fyb. Science. 293:2001;2263-2265
86. Pfrepper K.I., Marie-Cardine A., Simeoni L., Kuramitsu Y., Leo A., Spicka J., Hilgert I., Scherer J., Schraven B. Structural and functional dissection of the cytoplasmic domain of the transmembrane adaptor protein SIT (SHP2-interacting transmembrane adaptor protein). Eur. J. Immunol. 31:2001;1825-1836
87. Priatel J.J., Teh S.J., Dower N.A., Stone J.C., Teh H.S. rasGRP1 transduces low-grade TCR signals which are critical for T cell development, homeostasis, and differentiation. Immunity. 17:2002;617-627
88. Reth M. Antigen receptor tail clue. Nature. 338:1989;383
89. Samelson L.E. Adaptor proteins and T-cell antigen receptor signaling. Prog. Biophys. Mol. Biol. 71:1999;393-403
90. Sayos J., Wu C., Morra M., Wang N., Zhang X., Allen D., van Schaik S., Notarangelo L., Geha R., Roncarolo M.G., Oettgen H., De Vries J.E., Aversa G., Terhorst C. The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature. 395:1998;462-469
91. Sebzda E., Bracke M., Tugal T., Hogg N., Cantrell D.A. Rap1A positively regulates T cells via integrin activation rather than inhibiting lymphocyte signaling. Nat. Immunol. 3:2002;251-258
92. Shimonaka M., Katagiri K., Nakayama T., Fujita N., Tsuruo T., Yoshie O., Kinashi T. Rap1 translates chemokine signals to integrin activation, cell polarization, and motility across vascular endothelium under flow. J. Cell Biol. 161:2003;417-427
93. Sommers C.L., Menon R.K., Grinberg A., Zhang W., Samelson L.E., Love P.E. Knock-in mutation of the distal four tyrosines of linker for activation of T cells blocks murine T cell development. J. Exp. Med. 194:2001;135-142
94. Sommers C.L., Park C.S., Lee J., Feng C., Fuller C.L., Grinberg A., Hildebrand J.A., Lacana E., Menon R.K., Shores E.W., Samelson L.E., Love P.E. A LAT mutation that inhibits T cell development yet induces lymphoproliferation. Science. 296:2002;2040-2043
95. Spurkland A., Brinchmann J.E., Markussen G., Pedeutour F., Munthe E., Lea T., Vartdal F., Aasheim H.C. Molecular cloning of a T cell-specific adaptor protein (TSAd) containing an Src homology (SH) 2 domain and putative SH3 and phosphotyrosine binding sites. J. Biol. Chem. 273:1998;4539-4546
96. Su Y.W., Jumaa H. LAT links the pre-BCR to calcium signaling. Immunity. 19:2003;295-305
97. Sundvold V., Torgersen K.M., Post N.H., Marti F., King P.D., Rottingen J.A., Spurkland A., Lea T. T cell-specific adaptor protein inhibits T cell activation by modulating Lck activity. J. Immunol. 165:2000;2927-2931
98. Takeuchi S., Takayama Y., Ogawa A., Tamura K., Okada M. Transmembrane phosphoprotein Cbp positively regulates the activity of the carboxyl-terminal Src kinase, Csk. J. Biol. Chem. 275:2000;29183-29186
99. Tangye S.G., Phillips J.H., Lanier L.L., Nichols K.E. Functional requirement for SAP in 2B4-mediated activation of human natural killer cells as revealed by the X-linked lymphoproliferative syndrome. J. Immunol. 165:2000;2932-2936
100. Thome M., Tschopp J. TCR-induced NF-kappaB activation: a crucial role for Carma1, Bcl10 and MALT1. Trends Immunol. 24:2003;419-424
101. Timms J.F., Swanson K.D., Marie-Cardine A., Raab M., Rudd C.E., Schraven B., Neel B.G. SHPS-1 is a scaffold for assembling distinct adhesion-regulated multi-protein complexes in macrophages. Curr. Biol. 9:1999;927-930
102. Torgersen K.M., Vang T., Abrahamsen H., Yaqub S., Horejsi V., Schraven B., Rolstad B., Mustelin T., Tasken K. Release from tonic inhibition of T cell activation through transient displacement of C-terminal Src kinase (Csk) from lipid rafts. J. Biol. Chem. 276:2001;29313-29318
103. Veillette, A., 2002. The SAP family: a new class of adaptor-like molecules that regulates immune cell functions. Sci STKE 2002, PE8.
104. Veillette A. SAP: a molecular switch regulating the immune response through a unique signaling mechanism. Eur. J. Immunol. 33:2003;1141-1144
105. Veillette A., Latour S. The SLAM family of immune-cell receptors. Curr. Opin. Immunol. 15:2003;277-285
106. Wang D., You Y., Case S.M., McAllister-Lucas L.M., Wang L., DiStefano P.S., Nunez G., Bertin J., Lin X. A requirement for CARMA1 in TCR-induced NF-kappa B activation. Nat. Immunol. 3:2002;830-835
107. Wang H., Moon E.Y., Azouz A., Wu X., Smith A., Schneider H., Hogg N., Rudd C.E. SKAP-55 regulates integrin adhesion and formation of T cell-APC conjugates. Nat. Immunol. 4:2003;366-374
108. Weiss A., Koretzky G., Schatzmann R.C., Kadlecek T. Functional activation of the T-cell antigen receptor induces tyrosine phosphorylation of phospholipase Cg1. Proc. Natl. Acad. Sci. USA. 88:1991;5484-5488
109. Wollscheid B., Wienands J., Reth M. The adaptor protein SLP-65/BLNK controls the calcium response in activated B cells. Curr. Top. Microbiol. Immunol. 246:1999;283-288. discussion pp. 288-289
110. Wu C., Nguyen K.B., Pien G.C., Wang N., Gullo C., Howie D., Sosa M.R., Edwards M.J., Borrow P., Satoskar A.R., Sharpe A.H., Biron C.A., Terhorst C. SAP controls T cell responses to virus and terminal differentiation of TH2 cells. Nat. Immunol. 2:2001;410-414
111. Yablonski D., Kadlecek T., Weiss A. Identification of a phospholipase C-gamma1 (PLC-gamma1) SH3 domain- binding site in SLP-76 required for T-cell receptor-mediated activation of PLC-gamma1 and NFAT. Mol. Cell Biol. 21:2001;4208-4218
112. Yasuda K., Nagafuku M., Shima T., Okada M., Yagi T., Yamada T., Minaki Y., Kato A., Tani-Ichi S., Hamaoka T., Kosugi A. 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. 169:2002;2813-2817
113. Zhang W., Samelson L.E. The role of membrane-associated adaptors in T cell receptor signalling. Semin. Immunol. 12:2000;35-41
114. Zhang W., Sloan-Lancaster J., Kitchen J., Trible R.P., Samelson L.E. LAT: The ZAP-70 tyrosine kinase substrate that links T Cell receptor to cellular activation. Cell. 92:1998a;83-92
115. Zhang W., Sommers C.L., Burshtyn D.N., Stebbins C.C., DeJarnette J.B., Trible R.P., Grinberg A., Tsay H.C., Jacobs H.M., Kessler C.M., Long E.O., Love P.E., Samelson L.E. Essential role of LAT in T cell development. Immunity. 10:1999;323-332
116. Zhang W., Trible R., Samelson L.E. LAT palmitoylation: Its essential role in membrane microdomain targeting and tyrosine phosphorylation during T-cell activation. Immunity. 9:1998b;239-246
117. Zhang W., Trible R.P., Zhu M., Liu S.K., McGlade C.J., Samelson L.E. Association of Grb2, Gads, and phospholipase C-gamma 1 with phosphorylated LAT tyrosine residues. Effect of LAT tyrosine mutations on T cell angigen receptor-mediated signaling. J. Biol. Chem. 275:2000;23355-23361
118. 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. 277:2002;46151-46158