Intracellular adapter molecules

Seminars in Immunology

Volumn 12, Issue 1, 2000, Pages 43-54

  Norian, A ^a   Koretzky, Gary A ^b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

BCR; ITAM; Lymphocyte activation; TCR

Indexed keywords

ADAPTOR PROTEIN; B LYMPHOCYTE RECEPTOR; CELL PROTEIN; LYMPHOCYTE RECEPTOR; PROTEIN TYROSINE KINASE; T LYMPHOCYTE RECEPTOR;

HUMAN; LYMPHOCYTE ACTIVATION; NONHUMAN; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

EID: 0343820065     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1006/smim.2000.0206     Document Type: Article

References (125)

1. Hombach J, Tsubata T, Leclercq L, Stappert H, Reth M. Molecular components of the B-cell antigen receptor complex of the IgM class. Nature. 343:1990;760-762.
2. de la Hera A, Muller U, Olsson C, Isaaz S, Tunnacliffe A. Structure of the T cell antigen receptor (TCR): two CD3 epsilon subunits in a functional TCR/CD3 complex. J Exp Med. 173:1991;7-17.
3. Manolios N, Letourneur F, Bonifacino JS, Klausner RD. Pairwise, cooperative and inhibitory interactions describe the assembly and probable structure of the T-cell antigen receptor. EMBO J. 10:1991;1643-1651.
4. Sanchez M, Misulovin Z, Burkhardt AL, Mahajan S, Costa T, Franke R, Bolen JB, Nussenzweig M. Signal transduction by immunoglobin is mediated through Ig alpha and Ig beta. J Exp Med. 178:1993;1049-1055.
5. Cantrell D. T cell antigen receptor signal transduction pathways. Annu Rev Immunol. 14:1996;259-274.
6. Samelson LE, Phillips AF, Luong ET, Klausner RD. Association of the fyn protein-tyrosine kinase with the T-cell antigen receptor. Proc Nat Acad Sciences USA. 87:1990;4358-4362.
7. Reth M. Antigen receptor tail clue. Nature. 338:1989;383-384.
8. DeFranco AL. The complexity of signaling pathways activated by the BCR. Curr Opin Immunol. 9:1997;296-308.
9. Chan AC, Iwashima M, Turck CW, Weiss A. ZAP-70: a 70 kd protein-tyrosine kinase that associates with the TCR zeta chain. Cell. 71:1992;649-662.
10. Straus DB, Weiss A. The CD3 chains of the T cell antigen receptor associate with the ZAP-70 tyrosine kinase and are tyrosine phosphorylated after receptor stimulation. J Exp Med. 178:1993;1523-1530.
11. Wange RL, Malek SN, Desiderio S, Samelson LE. Tandem SH2 domains of ZAP-70 bind to T cell antigen receptor zeta and CD3 epsilon from activated Jurkat T cells. J Biol Chem. 268:1993;19797-19801.
12. Chan AC, Dalton M, Johnson R, Kong GH, Wang T, Thoma R, Kurosaki T. Activation of ZAP-70 kinase activity by phosphorylation of tyrosine 493 is required for lymphocyte antigen receptor function. EMBO J. 14:1995;2499-2508.
13. Mustelin T, Coggeshall KM, Isakov N, Altman A. T cell antigen receptor-mediated activation of phospholipase C requires tyrosine phosphorylation. Science. 247:1990;1584-1587.
14. Nishibe S, Wahl MI, Hernandez-Sotomayor SM, Tonks NK, Rhee SG, Carpenter G. Increase of the catalytic activity of phospholipase C-gamma 1 by tyrosine phosphorylation. Science. 250:1990;1253-1256.
15. Berridge MJ, Irvine RF. Inositol phosphates and cell signaling. Nature. 341:1989;197-205.
16. Clipstone NA, Crabtree GR. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature. 357:1992;695-697.
17. Jain J, McCaffrey PG, Miner Z, Kerppola TK, Lambert JN, Verdine GL, Curran T, Rao A. The T-cell transcription factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature. 365:1993;352-355.
18. Rao A, Luo C, Hogan PG. Transcription factors of the NFAT family: Regulation and function. Annu Rev Immunol. 15:1997;707-747.
19. Beyers AD, Hanekom C, Rheeder A, Strachan AF, Wooten MW, Nel AE. Characterization of protein kinase C and its isoforms in human T lymphocytes. J Immunol. 141:1988;3463-3470.
20. Sidorenko SP, Law CL, Klaus SJ, Chandran KA, Takata M, Kurosaki T, Clark EA. Protein kinase C mu (PKC mu) associates with the B cell antigen receptor complex and regulates lymphocyte signaling. Immunity. 5:1996;353-363.
21. Monks CR, Kupfer H, Tamir I, Barlow A, Kupfer A. Selective modulation of protein kinase C-theta during T-cell activation. Nature. 385:1997;83-86.
22. Izquierdo M, Leevers SJ, Marshall CJ, Cantrell D. p21ras couples the T cell antigen receptor to extracellular signal-regulated kinase 2 in T lymphocytes. J Exp Med. 178:1993;1199-1208.
23. Avruch J, Zhang XF, Kyriakis JM. Raf meets Ras: completing the framework of a signal transduction pathway. Trends Bioch Sci. 19:1994;279-283.
24. Pawson T, Scott JD. Signaling through scaffold, anchoring, and adaptor proteins. Science. 278:1997;2075-2080.
25. Koch CA, Anderson D, Moran MF, Ellis C, Pawson T. SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins. Science. 252:1991;668-674.
26. Kavanaugh WM, Williams LT. An alternative to SH2 domains for binding tyrosine-phosphorylated proteins. Science. 266:1994;1862-1865.
27. Marengere LE, Songyang Z, Gish GD, Schaller MD, Parsons JT, Stern MJ, Cantley LC, Pawson T. SH2 domain specificity and activity modified by a single residue. Nature. 369:1994;502-505.
28. van der Geer P, Pawson T. The PTB domain: a new protein module implicated in signal transduction. Trends Bioch Sci. 20:1995;277-280.
29. Bar-Sagi D, Rotin D, Batzer A, Mandiyan V, Schlessinger J. SH3 domains direct cellular localization of signaling molecules. Cell. 74:1993;83-91.
30. Feng S, Chen JK, Yu H, Simon JA, Schreiber SL. Two binding orientations for peptides to the Src SH3 domain: development of a general model for SH3-ligand interactions. Science. 266:1994;1241-1247.
31. Goudreau N, Cornille F, Duchesne M, Parker F, Tocque B, Garbay C, Roques BP. NMR structure of the N-terminal SH3 domain of GRB2 and its complex with a proline-rich peptide from Sos. Nat Struct Biol. 1:1994;898-907.
32. Lim WA, Richards FM, Fox RO. Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains. Nature. 372:1994;375-379.
33. Harlan JE, Hajduk PJ, Yoon HS, Fesik SW. Pleckstrin homology domains bind to phosphatidylinositol-4,5-bisphosphate. Nature. 371:1994;168-170.
34. Einbond A, Sudol M. Towards prediction of cognate complexes between the WW domain and proline-rich ligands. FEBS Lett. 384:1996;1-8.
35. Sudol M. Structure and function of the WW domain. Prog Biophys Mol Biol. 65:1996;113-132.
36. Lu PJ, Zhou XZ, Shen M, Lu KP. Function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science. 283:1999;1325-1328.
37. Fanning AS, Anderson JM. Protein-protein interactions: PDZ domain networks. Curr Biol. 6:1996;1385-1388.
38. Songyang Z, Fanning AS, Fu C, Xu J, Marfatia SM, Chishti AH, Crompton A, Chan AC, Anderson JM, Cantley LC. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science. 275:1997;73-77.
39. Lowenstein EJ, Daly RJ, Batzer AG, Li W, Margolis B, Lammers R, Ullri ch A, Skolnik EY, Bar-Sagi D, Schlessinger J. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell. 70:1992;431-442.
40. Li N, Batzer A, Daly R, Yajnik V, Skolnik E, Chardin P, Bar-Sagi D, Ma rgolis B, Schlessinger J. Guanine-nucleotide-releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling. Nature. 363:1993;85-88.
41. Buday L, Downward J. Epidermal growth factor regulates p21ras through the formation of a complex of receptor, Grb2 adapter protein, and Sos nucleotide exchange factor. Cell. 73:1993;611-620.
42. Egan SE, Giddings BW, Brooks MW, Buday L, Sizeland AM, Weinberg RA. Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation. Nature. 363:1993;45-51.
43. Rozakis-Adcock M, Fernley R, Wade J, Pawson T, Bowtell D. The SH2 and SH3 domains of mammalian Grb2 couple the EGF receptor to the Ras activator mSos1. Nature. 363:1993;83-85.
44. Langlois WJ, Sasaoka T, Saltiel AR, Olefsky JM. Negative feedback regulation and desensitization of insulin- and epidermal growth factor-stimulated p21ras activation. J Biol Chem. 270:1995;25320-25323.
45. Waters SB, Holt KH, Ross SE, Syu LJ, Guan KL, Saltiel AR, Koretzky GA, Pessin JE. Desensitization of Ras activation by a feedback disassociation of the SOS-Grb2 complex. J Biol Chem. 270:1995;20883-20886.
46. Holt KH, Kasson BG, Pessin JE. Insulin stimulation of a MEK-dependent but ERK-independent SOS protein kinase. Mol Cell Biol. 16:1996;577-583.
47. Ravichandran KS, Lorenz U, Shoelson SE, Burakoff SJ. Interaction of Shc with Grb2 regulates association of Grb2 with mSOS. Mol Cell Biol. 15:1995;593-600.
48. Pelicci G, Lanfrancone L, Grignani F, McGlade J, Cavallo F, Forni G, Nicoletti I, Grignani F, Pawson T, Pelicci PG. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell. 70:1992;93-104.
49. Blaikie P, Immanuel D, Wu J, Li N, Yajnik V, Margolis B. A region in Shc distinct from the SH2 domain can bind tyrosine-phosphorylated growth factor receptors. J Biol Chem. 269:1994;32031-32034.
50. Ravichandran KS, Lee KK, Songyang Z, Cantley LC, Burn P, Burakoff SJ. Interaction of Shc with the zeta chain of the T cell receptor upon T cell activation. Science. 262:1993;902-905.
51. Osman N, Lucas SC, Turner H, Cantrell D. A comparison of the interaction of Shc and the tyrosine kinase ZAP-70 with the T cell antigen receptor zeta chain tyrosine-based activation motif. J Biol Chem. 270:1995;13981-13986.
52. Baldari CT, Pelicci G, Di Somma MM, Milia E, Giuli S, Pelicci PG, Telford JL. Inhibition of CD4/p56lck signaling by a dominant negative mutant of the Shc adaptor protein. Oncogene. 10:1995;1141-1147.
53. Ravichandran KS, Igras V, Shoelson SE, Fesik SW, Burakoff SJ. Evidence for a role for the phosphotyrosine-binding domain of Shc in interleukin 2 signaling. Proc Nat Acad Sci USA. 93:1996;5275-5280.
54. Zhang W, Sloan-Lancaster J, Kitchen J, Trible RP, Samelson LE. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell. 92:1998;83-92.
55. Buday L, Egan SE, Rodriguez Viciana P, Cantrell DA, 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. 269:1994;9019-9023.
56. Feng GS, Ouyang YB, Hu DP, Shi ZQ, Gentz R, Ni J. Grap is a novel SH3-SH2-SH3 adaptor protein that couples tyrosine kinases to the Ras pathway. J Biol Chem. 271:1996;12129-12132.
57. Trub T, Frantz JD, Miyazaki M, Band H, Shoelson SE. The role of a lymphoid-restricted, Grb2-like SH3-SH2-SH3 protein in T cell receptor signaling. J Biol Chem. 272:1997;894-902.
58. Liu SK, McGlade CJ. Gads is a novel SH2 and SH3 domain-containing adaptor protein that binds to tyrosine-phosphorylated Shc. Oncogene. 17:1998;3073-3082.
59. Qiu M, Hua S, Agrawal M, Li G, Cai J, Chan E, Zhou H, Luo Y, Liu M. Molecular cloning and expression of human grap-2, a novel leukocyte-specific SH2- and SH3-containing adaptor-like protein that binds to gab-1. Bioch Biophys Res Commun. 253:1998;443-447.
60. Bourette RP, Arnaud S, Myles GM, Blanchet JP, Rohrschneider LR, Mouchiroud G. Mona, a novel hematopoietic-specific adaptor interacting with the macrophage colony-stimulating factor receptor, is implicated in monocyte/macrophage development. EMBO J. 17:1998;7273-7281.
61. Law CL, Ewings MK, Chaudhary PM, Solow SA, Yun TJ, Marshall AJ, Hood L, Clark EA. GrpL, a Grb2-related adaptor protein, interacts with SLP-76 to regulate nuclear factor of activated T cell activation. J Exp Med. 189:1999;1243-1253.
62. Asada H, Ishii N, Sasaki Y, Endo K, Kasai H, Tanaka N, Takeshita T, Tsuchiya S, Konno T, Sugamura K. Grf40, A novel Grb2 family member, is involved in T cell signaling through interaction with SLP-76 and LAT. J Exp Med. 189:1999;1383-1390.
63. Jackman J, Motto D, Sun Q, Tanemoto M, Turck C, Peltz G, Koretzky G, Findell P. Molecular cloning of SLP-76, a 76 kDa tyrosine phosphoprotein associated with Grb2 in T cells. J Biol Chem. 270:1995;7029-7032.
64. Motto DG, Ross SE, Wu J, Hendricks-Taylor LR, Koretzky GA. Implication of the GRB2-associated phosphoprotein SLP-76 in T cell receptor-mediated interleukin 2 production. J Exp Med. 183:1996;1937-1943.
65. Clements JL, Ross-Barta SE, Tygrett LT, Waldschmidt TJ, Koretzky GA. SLP-76 expression is restricted to hematopoietic cells of monocyte, granulocyte, and T lymphocyte lineage and is regulated during T cell maturation and activation. J Immunol. 161:1998;3880-3889.
66. Clements JL, Lee JR, Gross B, Yang B, Olson JD, Sandra A, Watson SP, Lentz SR, Koretzky GA. Fetal hemorrhage and platelet dysfunction in SLP-76-deficient mice. J Clin Invest. 103:1999;19-25.
67. Fu C, Turck CW, Kurosaki T, Chan AC. BLNK: a central linker protein in B cell activation. Immunity. 9:1998;93-103.
68. Musci MA, Motto DG, Ross SE, Fang N, Koretzky GA. Three domains of SLP-76 are required for its optimal function in a T cell line. J Immunol. 159:1997;1639-1647.
69. Wardenburg JB, Fu C, Jackman JK, Flotow H, Wilkinson SE, Williams DH, Johnson R, Kong G, Chan AC, Findell PR. Phosphorylation of SLP-76 by the ZAP-70 protein-tyrosine kinase is required for T-cell receptor function. J Biol Chem. 271:1996;19641-19644.
70. Fang N, Motto DG, Ross SE, Koretzky GA. Tyrosines 113, 128, and 145 of SLP-76 are required for optimal augmentation of NFAT promoter activity. J Immunol. 157:1996;3769-3773.
71. Onodera H, Motto DG, Koretzky GA, Rothstein DM. Differential regulation of activation-induced tyrosine phosphorylation and recruitment of SLP-76 to Vav by distinct isoforms of the CD45 protein-tyrosine phosphatase. J Biol Chem. 271:1996;22225-22230.
72. Tuosto L, Michel F, Acuto O. p95vav associates with tyrosine-phosphorylated SLP-76 in antigen-stimulated T cells. J Exp Med. 184:1996;1161-1166.
73. Wu J, Motto DG, Koretzky GA, Weiss A. Vav and SLP-76 interact and functionally cooperate in IL-2 gene activation. Immunity. 4:1996;593-602.
74. Fang N, Koretzky GA. SLP-76 and Vav function in separate, but o verlapping pathways to augment interleukin-2 promoter activity. J Biol Chem. 274:1999;16206-16212.
75. Yablonski D, Kuhne MR, Kadlecek T, Weiss A. Uncoupling of nonre ceptor tyrosine kinases from PLC-gamma1 in an SLP-76 deficient T cell. Science. 281:1998;413-416.
76. Clements JL, Yang B, Ross-Barta SE, Eliason SE, Hrstka RF, Williamson RA, Koretzky GA. Requirement for the leukocyte-specific adapter protein SLP-76 for normal T cell development. Science. 281:1998;416-419.
77. Pivniouk V, Tsitsikov E, Swinton P, Rathbun G, Alt FW, Geha RS. Impaired viability and profound block in thymocyte development in mice lacking the adaptor protein SLP-76. Cell. 94:1998;229-238.
78. Appleby MW, Gross JA, Cooke MP, Levin SD, Qian X, Perlmutter RM. Defective T cell receptor signaling in mice lacking the thymic isoform of p59fyn. Cell. 70:1992;751-763.
79. Molina TJ, Kishihara K, Siderovski DP, van Ewijk W, Narendran A, Timms E, Wakeham A, Paige CJ, Hartmann KU, Veillette A et al. Profound block in thymocyte development in mice lacking p56lck. Nature. 357:1992;161-164.
80. Stein PL, Lee HM, Rich S, Soriano P. pp59fyn mutant mice display differential signaling in thymocytes and peripheral T cells. Cell. 70:1992;741-775.
81. Cheng AM, Negisihi I, Anderson SJ, Chan AC, Bolen J, Loh DY, Pawson T. The Syk and ZAP-70 SH2-containing tyrosine kinases are implicated in pre-T cell receptor signaling. Proc Natl Acad Sci USA. 94:1997;9797-9801.
82. Kadlecek TA, oers NSv, Lefrancois L, Olson S, Finlay D, Chu DH, Connolly K, Killeen N, Weiss A. Differential requirements for ZAP-70 in TCR signaling and T cell development. J Immunol. 161:1998;4688-4694.
83. Gross BS, Lee JR, Clements JL, Turner M, Tybulewicz VL, Findell PR, Koretzky GA, Watson SP. Tyrosine phosphorylation of SLP-76 is downstream of Syk following stimulation of the collagen receptor in platelets. J Biol Chem. 274:1999;5963-5971.
84. Peterson EJ, Clements JL, Ballas ZK, Koretzky GA. NK cytokine secretion and cytotoxicity occur independently of the SLP-76 adaptor protein. Eur J Immunol. 29:1999;2223-2232.
85. Liu SK, Fang N, Bouchard D, Koretzky GA, McGlade CJ. The hemato poietic-specific adaptor protein, Gads functions in T cell receptor signaling through interactions with SLP-76 and LAT. Curr Biol. 9:1999;67-75.
86. Lehmann JM, Riethmueller G, Johnson JP. Nck, a melanoma cDNA encoding a cytoplasmic protein consisting of the src homology units SH2 and SH3. Nucl Acid Res. 18:1990;1048.
87. Wardenburg B, Pappu R, Bu JY, Mayer B, Chernoff J, Straus D, Chan AC. Regulation of PAK activation and the T cell cytoskeleton by the linker protein SLP-76. Immunity. 9:1998;607-616.
88. Wunderlich L, Farago A, Downward J, Buday L. Association of Nck with tyrosine-phosphorylated SLP-76 in activated T lymphocytes. Eur J Immunol. 29:1999;1068-1075.
89. Galisteo ML, Chernoff J, Su YC, Skolnik EY, Schlessinger J. The adaptor protein Nck links receptor tyrosine kinases with the serine-threonine kinase Pak1. J Biol Chem. 271:1996;20997-21000.
90. Rivero-Lezcano OM, Marcilla A, Sameshima JH, Robbins KC. Wiskott-Aldrich syndrome protein physically associates with Nck through Src homology 3 domains. Mol Cell Biol. 15:1995;5725-5731.
91. Wienands J, Schweikert J, Wollscheid B, Jumaa H, Nielsen PJ, Reth M. SLP-65: a new signaling component in B lymphocytes which requires expression of the antigen receptor for phosphorylation. J Exp Med. 188:1998;791-795.
92. Goitsuka R, Fujimura Y, Mamada H, Umeda A, Morimura T, Uetsuka K, Doi K, Tsuji S, Kitamura D. BASH, a novel signaling molecule preferentially expressed in B cells of the bursa of Fabricius. J Immunol. 161:1998;5804-5808.
93. Ishiai M, Kurosaki M, Pappu R, Okawa K, Ronko I, Fu C, Shibata M, Iwamatsu A, Chan AC, Kurosaki T. BLNK required for coupling Syk to PLCgamma2 and Rac1-JNK in B cells. Immunity. 10:1999;117-125.
94. Musci M, Hendricks-Taylor L, Motto D, Paskind M, Kamens J, Turck C, Koretzky G. Molecular cloning of SLAP-130, an SLP-76-associated substrate of the T cell antigen receptor-stimulated protein tyrosine kinases. J Biol Chem. 272:1997;11674-11677.
95. da Silva A, Li Z, De Vera C, Canto E, Findell P, Rudd C. Cloning of a novel T-cell protein FYB that binds FYN and SH2-domain-containing leukocyte protein 76 and modulates interleukin 2 production. Proc Nat Acad Sci USA. 94:1997;7493-7498.
96. da Silva AJ, Rosenfield JM, Mueller I, Bouton A, Hirai H, Rudd CE. Biochemical analysis of p120/130: a protein-tyrosine kinase substrate restricted to T and myeloid cells. J Immunol. 158:1997;2007-2016.
97. Raab M, Kang H, da Silva A, Zhu X, Rudd CE. FYN-T-Fyb-SLP-76 interactions define a T-cell receptor ζ/CD3-mediated tyrosine phosphorylation pathway that up-regulates Interleukin-2 transcription in T-cells. J Biol Chem. 274:1999;21170-21179.
98. Marie-Cardine A, Bruyns E, Eckerskorn C, Kirchgessner H, Meuer SC, Schraven B. Molecular cloning of SKAP55, a novel protein that associates with the protein tyrosine kinase p59fyn in human T-lymphocytes. J Biol Chem. 272:1997;16077-16080.
99. Marie-Cardine A, Verhagen AM, Eckerskorn C, Schraven B. SKAP-HOM, a novel adaptor protein homologous to the FYN-associated protein SKAP55. FEBS Lett. 435:1998;55-60.
100. Liu J, Kang H, Raab M, da Silva AJ, Kraeft SK, Rudd CE. FYB (FYN binding protein) serves as a binding partner for lymphoid protein and FYN kinase substrate SKAP55 and a SKAP55-related protein in T cells. Proc Natl Acad Sci USA. 95:1998;8779-8784.
101. Ley SC, Marsh M, Bebbington CR, Proudfoot K, Jordan P. Distinct intracellular localization of Lck and Fyn protein tyrosine kinases in human T lymphocytes. J Cell Biol. 125:1994;639-649.
102. Yasunga M, Yagi T, Hanzawa N, Yasuda M, Yamanashi Y, Yamamoto T, Aizawa S, Miyauchi Y, Nishikawa S. Involvement of Fyn tyrosine kinase in progression of cytokinesis of B lymphocyte progenitor. J Cell Biol. 132:1996;91-99.
103. fynkinase with the dynein light chain, Tctex-1, and colocalization during cytokinesis. J Immunol. 161:1998;1728-1737.
104. Panchamoorthy G, Fukazawa T, Miyake S, Soltoff S, Reedquist K, Druker B, Shoelson S, Cantley L, Band H. p120cbl is a major substrate of tyrosine phosphorylation upon B cell antigen receptor stimulation and interacts in vivo with Fyn and Syk tyrosine kinases, Grb2 and Shc adaptors, and the p85 subuni t of phosphatidylinositol 3-kinase. J Biol Chem. 271:1996;3187-3194.
105. Lupher ML, Jr., Reedquist KA, Miyake S, Langdon WY, Band H. A novel phosphotyrosine-binding domain in the N-terminal transforming region of Cbl interacts directly and selectively with ZAP-70 in T cells. J Biol Chem. 271:1996;24063-24068.
106. Blake TJ, Shapiro M, Morse HC, Langdon WY. The sequences of the human and mouse c-cbl proto-oncogenes show v-cbl was generated by a large truncation encompassing a proline-rich domain and a leucine zipper-like motif. Oncogene. 6:1991;653-657.
107. Donovan JA, Wange RL, Langdon WY, Samelson LE. The protein prod uct of the c-cbl protooncogene is the 120-kDa tyrosine-phosphorylated protein in Jurkat cells activated via the T cell antigen receptor. J Biol Chem. 269:1994;22921-22924.
108. Meng W, Sawasdikosol S, Burakoff SJ, Eck MJ. Structure of the a mino-terminal domain of Cbl complexed to its binding site on ZAP-70 kinase. Nature. 398:1999;84-90.
109. Meisner H, Conway BR, Hartley D, Czech MP. Interactions of Cbl with Grb2 and phosphatidylinositol 3′-kinase in activated Jurkat cells. Mol Cell Biol. 15:1995;3571-3578.
110. Hoeve Jt, Morris C, Heisterkamp N, Groffen J. Isolation and chromosomal location of CRKL, a human crk-like gene. Oncogene. 8:1993;2469-2474.
111. Reedquist KA, Fukazawa T, Panchamoorthy G, Langdon WY, Shoelson SE, Druker BJ, Band H. Stimulation through the T cell receptor induces Cbl association with Crk proteins and the guanine nucleotide exchange protein C3G. J Biol Chem. 271:1996;8435-8442.
112. Sawasdikosol S, Chang JH, Pratt JC, Wolf G, Shoelson SE, Burakoff SJ. Tyrosine-phosphorylated Cbl binds to Crk after T cell activation. J Immunol. 157:1996;110-116.
113. Boussiotis VA, Freeman GJ, Berezovskaya A, Barber DL, Nadler LM. Maintenance of human T cell anergy: blocking of IL-2 gene transcription by activated Rap1. Science. 278:1997;124-128.
114. Ichiba T, Kuraishi Y, Sakai O, Nagata S, Groffen J, Kurata T, Hattori S, Matsuda M. Enhancement of guanine-nucleotide exchange activity of C3G for Rap1 by the expression of Crk, CrkL, and Grb2. J Biol Chem. 272:1997;22215-22220.
115. Hausser A, Storz P, Link G, Stoll H, Liu YC, Altman A, Pfizenmaier K, Johannes FJ. Protein kinase C mu is negatively regulated by 14-3-3 signal transduction proteins. J Biol Chem. 274:1999;9258-9264.
116. Lupher ML, Rao N, Lill NL, Andoniou CE, Miyake S, Clark EA, Druker B, Band H. Cbl-mediated negative regulation of the Syk tyrosine kinase. A critical role for Cbl phosphotyrosine-binding domain binding to Syk phosphotyrosine 323. J Biol Chem. 273:1998;35273-35281.
117. Ota Y, Samelson LE. The product of the proto-oncogene c-cbl: a negative regulator of the Syk tyrosine kinase. Science. 5311:1997;418-420.
118. Thien CB, Bowtell DD, Langdon WY. Perturbed regulation of ZAP-70 and sustained tyrosine phosphorylation of LAT and SLP-76 in c-Cbl-deficient thymocytes. J Immunol. 162:1999;7133-7139.
119. Miyake S, Lupher ML, Druker B, Band H. The tyrosine kinase regulator Cbl enhances the ubiquitination and degradation of the platelet-derived growth factor receptor α Proc Natl Acad Sci USA. 95:1998;7927-7932.
120. Lee PSW, Wang Y, Dominguez MG, Yeung YG, Murphy MA, Bowtell DDL, Stanley ER. The Cbl protooncoprotein stimulates CSF-1 receptor multiubiquitination and endocytosis, and attenuates macrophage proliferation. EMBO J. 18:1999;3616-3628.
121. Sayos J, Wu C, Morra M, Wang N, Zhang X, Allen D, van Schaik S, Notar angelo L, Geha R, Roncarolo MG, Oettgen H, De Vries JE, 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.
122. Cocks BG, Chang CC, Carballido JM, Yssel H, de Vries JE, Aversa G. A novel receptor involved in T-cell activation. Nature. 376:1995;260-263.
123. Aversa G, Chang CC, Carballido JM, Cocks BG, de Vries JE. Engagement of the signaling lymphocytic activation molecule (SLAM) on activated T cells results in IL-2-independent, cyclosporin A-sensitive T cell proliferation and IFN-gamma production. J Immunol. 158:1997;4036-4044.
124. Punnonen J, Cocks BG, Carballido JM, Bennett B, Peterson D, Aversa G, de Vries JE. Soluble and membrane-bound forms of signaling lymphocytic acti vation molecule (SLAM) induce proliferation and Ig synthesis by activated human B lymphocytes. J Exp Med. 185:1997;993-1004.
125. Tangye SG, Lazetic S, Woollatt E, Sutherland GR, Lanier LL, Phillips JH. Human 2B4, an activating NK cell receptor, recruits the protein tyrosine phosphatase SHP-2 and the adaptor signaling protein SAP. J Immunol. 162:1999;6981-6985.