Regulation of the pp72(syk) protein tyrosine kinase by platelet integrin α(IIb)β3

EMBO Journal

Volumn 16, Issue 21, 1997, Pages 6414-6425

  Gao, J ^a   Zoller, K E ^a   Ginsberg, M H ^a   Brugge, J S ^a,c   Shattil, S J ^a,b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b ARIAD PHARMACEUTICALS INC   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

CHO cells; Integrin; Platelet; Protein tyrosine kinase; Src; Syk

Indexed keywords

CYTOCHALASIN D; FIBRINOGEN; INTEGRIN; PROTEIN KINASE P60; PROTEIN TYROSINE KINASE; CELL ADHESION MOLECULE; ENZYME PRECURSOR; FIBRINOGEN RECEPTOR; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE 1; HYBRID PROTEIN; IMMUNOGLOBULIN RECEPTOR; PROTEIN KINASE SYK; PTK2 PROTEIN, HUMAN; SIGNAL PEPTIDE;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CHO CELL; CONTROLLED STUDY; CYTOPLASM; DELETION MUTANT; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; THROMBOCYTE; AMINO ACID SEQUENCE; ANIMAL; CELL ADHESION; CHEMISTRY; COMPARATIVE STUDY; CRICETULUS; GENE DELETION; HAMSTER; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PHYSIOLOGY; POINT MUTATION; PROTEIN BINDING; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS;

ANIMALIA;

AMINO ACID SEQUENCE; ANIMALS; BLOOD PLATELETS; CELL ADHESION; CELL ADHESION MOLECULES; CHO CELLS; CRICETINAE; CRICETULUS; ENZYME ACTIVATION; ENZYME PRECURSORS; FIBRINOGEN; FOCAL ADHESION KINASE 1; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; POINT MUTATION; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-TYROSINE KINASES; RECEPTORS, IMMUNOLOGIC; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION; SIGNAL TRANSDUCTION;

EID: 0031551590     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.21.6414     Document Type: Article

References (99)

1. Alig, L., Edenhofer, A., Hadváry, P. Hürzeler, M., Knopp, D., Müller, M., Steiner, B., Trzeciak, A. and Weller, T. (1992) Low molecular weight, non-peptide fibrinogen receptor antagonists. J. Med. Chem., 35, 4393-4407.
2. Aoki, Y. Kim, Y.-T., Stillwell, R., Kim, T.J. and Pillai, S. (1995) The SH2 domains of Src family kinases associate with Syk. J. Biol. Chem., 270, 15658-15663.
3. 1. Blood. 89, 1235-1242.
4. Bauer, J.S., Schreiner, C.L., Giancotti, F.G., Ruoslahti, H. and Juliano, R.L. (1992) Motility of fibronectin receptor-deficient cells on fibronectin and vitronectin: (Collaborative interactions among integrins. J. Cell. Biol., 116, 447-487.
5. Briesewitz, R., Kern, A., Smilenov, L.B., David, F.S. and Marcantonio, E.E. (1996) The membrane-cytoplasm interface of integrin α subunits is critical for receptor latency. Mol. Biol. Cell., 7, 1499-1509.
6. Brown, P.J. and Juliano, R.L. (1988) Monoclonal antibodies to distinctive epitopes on the alpha and beta subunits of the fibronectin receptor. Exp. Cell Res., 177, 303-318.
7. Bu, J., Shaw, A.S. and Chan, A.C. (1995) Analysis of the interaction of ZAP-70 and syk protein-tyrosine kinases with the T-cell antigen receptor by plasmon resonance. Proc. Natl Acad. Sci. USA, 91, 5106-5110.
8. Cambier, J.C. (1995) Antigen and Fc receptor signaling: The awesome power of the immunoreceptor tyrosine-based activation motif (ITAM) J. Imunnol., 155, 3281-3285.
9. Cary, L.A., Chang, J.F. and Guan, J.L. (1996) Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn. J. Cell Sci. 109, 1787-1794.
10. syk. J. Biol. Chem., 269, 32435-32440.
11. syk noncovalently associate with the low affinity Fegamma receptor on human platelets through an immunoreceptor tyrosine-based activation motif - Reconstitution with synthetic phosphopeptides. J. Biol. Chem., 271, 10775-10781.
12. Chan, A.C., Iwashima, M., Turck, C.W. and Weiss, A. (1992) ZAP-70: A 70 kDa protein-tyrosine kinase that associates with the TCR zeta chain. Cell, 71, 649-662.
13. Syk. Assessment of binding parameters and real time binding kinetics. J Biol. Chem., 271, 25308-25315.
14. Chen, Y.-P., O'Toole, T.E., Shipley, T., Forsyth, J., LaFlamme, S.E., Yamada, K.M., Shattil, S.J. and Ginsberg, M.H (1994a) 'Inside-out' signal transduction inhibited by isolated integrin cytoplasmic domains. J. Biol. Chem., 269, 18307-18310.
15. 3 (platelet glscoprotein IIb-IIIa). Blood, 84, 857-1865.
16. Cheng, A.M., Rowley, B., Pao, W., Hayday, A., Bolen, J.B. and Pawson, T. (1995) Syk tyrosine kinase required for mouse viability and B-cell development. Nature, 378, 303-306.
17. Chu, D.H., Spits, H., Peyron, J. F., Rowley, R.B., Bolen, J.B. and Weiss, A. (1996) The Syk protein tyrosine kinase can function independently of CD45 or Lck in T cell antigen receptor signaling. EMBO J., 15, 6251-6261.
18. wk to integrin-dependent cytoskeletal complexes in thrombin-stimulated platelets. Mol. Cell. Biol., 13, 1863-1871.
19. 3. J. Biol. Chem., 46, 28859-28864.
20. Clark, F.A. and Brugge, J.S. (1996) Tyrosine phosphorylation. In Watson, S. and Authi, K. (eds). Platelet Function and Signal Transduction: A Practical Approach. Oxford University Press, Oxford, UK.
21. Clark, E.A. and Brugge, J.S. (1995) Integrins and signal transduction pathways. The road taken. Science, 268, 233-239.
22. Costello, P.S., Turner, M. Walters, A.E., Cunningham, C.N., Bauer, P.H., Downward, J. and Tybulewicz, V.L.J. (1996) Critical role for the tyrosine kinase Syk in signaling through the high affinity IgE receptor of mast cells. Oncogene, 13, 2595-2605.
23. Couture, C., Deckert, M., Williams, S., Russo, F.O., Altman, A. and Mustelin, T. (1996) Identification of the site in the Syk protein tyrosine kinase that binds the SH2 domain of Lck. J. Biol. Chem., 271, 24294-24299.
24. Cox, D., Chang, P., Kurosaki, T. and Greenberg, S. (1996) Syk tyrosine kinase is required for immunoreceptor tyrosine activation motif-dependent actin assembly. J. Biol. Chem., 271, 16597-16602.
25. Crowley, M.T., Harmer, S.L. and DeFranco, A.L. (1996) Activation-induced association of a 145-kDa tyrosine-phosphorylated protein with Shc and Syk in B lymphocytes and macrophages. J. Biol. Chem., 271, 1145-1152.
26. Daeron, M. (1997) Fc receptor biology. Annu. Rev. Immunol., 15, 203-234.
27. Dedhar, S. and Hannigan, G.E. (1996) Integrin cytoplasmic interactions and bidirectional transmembrane signalling. Curr. Opin. Cell. Biol., 8, 657-669.
28. El-Hillal, O., Kurosaki, T., Yamamura, H., Kinet, J.P. and Scharenberg, A.M. (1997) Syk kinase activation by a src kinase-initiated activation loop phosphorylation chain reaction Proc. Natl Acad. Sci. USA. 94, 1919-1924.
29. Engvall, E. and Ruoslahti, E. (1977) Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int. J. Cancer, 20, 1-5.
30. 3 through cytoskeletal reorganization and tyrosine phosphorylation in human platelets. J. Biol. Chem., 270, 11927-11934.
31. ras GTPase-activating protein with the membrane skeleton. J. Biol. Chem., 268, 25973-25984.
32. Frangione, J.V., Oda, A., Smith, M., Salzman, E.W. and Neel, B.G. (1993) Calpain-catalyzed cleavage and subcellular relocation of protein phosphotyrosine phosphatase IB (PTP-1B) in human platelets. EMBO J., 12, 4843-1856.
33. 3 (glycoprotein Ilb-IIIa) alter receptor affinity, specificity and function. J. Biol. Chem., 266, 17106-17111.
34. Gibbins, J., Asselin, J., Farndale, R., Barnes, M., Law, C. L. and Watson, S.P. (1996) Tyrosine phosphorylation of the Fc receptor gamma-chain in collagen-stimulated platelets. J. Biol. Chem., 271, 18095-18099.
35. c-src, phospholipase C, inositol-lipid and diacylglyeerol kinases with the cytoskeletons of thrombin-stimulated platelets. J. Biol. Chem., 266, 15705-15709.
36. Guan, J.I., and Chen, H.C. (1996) Signal transduction in cell-matrix interactions. Int. Rev. Cytol., 168, 81-121.
37. 3. A ternary complex of the integrin alpha and beta subunits and a divalent cation. J. Biol. Chem., 271, 6017-6026.
38. Haimovich, B., Lipfert, L., Brugge, J.S. and Shattil, S.J. (1993) Tyrosine phosphorylation and cytoskelelal reorganization in platelets are triggered by interaction of integrin receptors with their immobilized ligands. J. Biol. Chem., 268, 15868-15877.
39. Hamawy, M.M., Mergenhagen, S.E. and Siraganian, R.P. (1993) Cell adherence to fibronectin and the aggregation of the high affinity immunoglobulin E receptor synergistically regulate tyrosine phosphorylation of 105-115-kDa proteins. J. Biol. Chem., 268, 5227-5233.
40. Huang, M.-M., Bolen, J.B., Barnwell, J.W., Shattil, S.J. and Brugge, J.S. (1991) Membrane glycoprotein IV (CD36) is physically associated with Fyn, Lyn and Yes protein tyrosine kinases in human platelets. Proc. Natl Acad. Sci. USA, 88, 7844-7848.
41. FAK. J. Cell. Biol., 122, 473-483.
42. Hughes, P.E., Renshaw, M.W., Pfaff, M., Forsyth, J., Keivens, V.M., Schwartz, M.A. and Ginsberg, M.H. (1996) Suppression of integrin activation: A novel function of a Ras/Raf-initiated MAP-kinase pathway. Cell, 88, 521-530.
43. Hynes, R.O. (1992) Integrins: versatility, modulation and signaling in cell adhesion. Cell, 69, 11-25.
44. Ichinohe, T., Takayama, H., Ezumi, Y., Arai, M., Yamamoto, N., Takahashi, H. and Okuma, M. (1997) Collagen-stimulated activation of Syk but not c-Src is severely compromised in human platelets lacking membrane glvcoprotein VI. J. Biol. Chem., 272, 63-68.
45. Jabril-Cuenod, B., Zhang, C., Scharenberg, A.M., Paolini, R., Numerof, R., Beaven, M.A. and Kinet, J.P. (1996) Syk-dependent phosphorylation of Shc - A potential link between Fc×RI and the Ras/mitogen-activated protein kinase signaling pathway through Sos and Grb2. J. Biol. Chem., 271, 16268-16272.
46. Juliano, R. (1996) Cooperation between soluble factors and integrin-mediated cell anchorage in the control of cell growth and differentiation. BioEssays, 18, 911-917.
47. Kaplan, K.B., Swedlow, J.R., Morgan, D.O. and Varmus, H.E. (1995) c-Src enhances the spreading of src-/- fibroblasts on fibronectin by a kinase-independent mechanism. Genes Dev., 9, 1505-1517.
48. 1 integrin is a necessary co-receptor for collagen-induced activation of Syk and the subsequent phosphorylation of phospholipase Cgamma2 in platelets. J. Biol. Chem., 271, 26668-26676.
49. svk by tyrosine phosphorylation or by binding of phosphorylated immunoreceptor tyrosine-based activation motif peptides. Mol. Cell. Biol., 16, 1471-1478.
50. Kolanus, W., Romeo, C. and Seed, B. (1993) T cell activation by clustered tyrosine kinases. Cell. 74, 171-183.
51. Kunkel, T.A. (1985) Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl Acad. Sci. USA, 82, 488-492.
52. Kurosaki, T., Takata, M., Yamanashi, Y., Inazu, T., Taniguchi, T., Yamamoto, T. and Yamamura, H. (1994) Syk activation by the Src-family tyrosine kinase in the B cell receptor signaling. J. Exp. Med., 179, 1725-1729.
53. Kurosaki, T., Johnson, S.A., Pao, L., Sada, K., Yamamura, H. and Cambier, J.C. (1995) Role of the Syk autophosphorylation site and SH2 domains in B cell antigen receptor signaling. J. Exp. Med., 182. 1815-1823.
54. LaFlamme, S.E., Thomas, L.A., Yamada, S.S. and Yamada, K.M. (1994) Single subunit chimeric integrins as mimics and inhibitors of endogenous integrin functions in receptor localization, cell spreading and migration and matrix assembly. J. Cell Biol., 126, 1287-1298.
55. Latour, S., Fournel, M. and Veillette, A. (1997) Regulation of T-cell antigen receptor signalling by Syk tyrosine protein kinase. Mol. Cell. Biol., 17, 4434-4441.
56. Law, C.-L., Chandran, K.A., Sidorenko, S.P. and Clark, E.A. (1996a) Phospholipase C-γl interacts with conserved phosphotyroxyl residues in the linker region of Syk and is a substrate for Syk. Mol. Cell. Biol., 16, 1305-1315.
57. 3 (GP IIb-IIIa) tyrosine phosphorylation induced by platelet aggregation. J. Biol. Chem., 271, 10811-10815.
58. FAK. J. Cell Sci., 108, 3817-3825.
59. Lin, T.H., Rosales, C., Mondal, K., Bolen, J.B., Haskill, S. and Juliano, R.L. (1995) Integrin-mediated tyrosine phosphorylation and cytokine message induction in monocytic cells. A possible signaling role for the Syk tyrosine kinase. J. Biol. Chem., 270, 16189-16197.
60. 1 integrin cytoplasmic domain. J. Biol. Chem., 269, 18311-18314.
61. Maruyama, S., Kurosaki, T., Sada, K., Yamanashi, Y., Yamamoto, T. and Yamamura, H. (1997) Physical and functional association of conactin with Syk in human leukemic cell line K562. J. Biol. Chem., 271, 6631-6635.
62. svk is a minor component but the major protein tyrosine kinase of pp72. J. Biol. Chem., 269, 16902-16908.
63. Miyamoto, S., Akiyama, S.K. and Yamada, K.M. (1995) Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science, 267, 883-885.
64. Miyamoto, S., Teramoto, H., Gutkind, J.S. and Yamada, K.M. (1996) Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activation: Roles of integrin aggregation and occupancy of receptors. J. Cell Biol., 135, 1633-1642.
65. 3 (platelet GPIIb-IIIa). Biochemistry, 33, 7701-1108.
66. Müller, B., Cooper, L. and Terhorst, C. (1994) Molecular cloning of the human homologue to the pig protein-tyrosine kinase syk. Immunogenetics, 39, 359-362.
67. Ota, Y., Beitz, L.O., Scharenberg, A.M., Donovan, J.A., Kinet, J.P. and Samelson, L.E. (1996) Characterization of Cbl tyrosine phosphorylation and a Cbl-Syk complex in RBL-2H3 cells. J. Exp. Med., 184, 1713-1723.
68. svk in human platelets. J. Biol. Chem., 270, 15119-15124.
69. cbl 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 subunit of phosphatidylinositol 3-kinase. J. Biol. Chem., 271, 3187-3194.
70. Poole, A., Gibbins, J.M., Turner, M., van Vugt, M.J., van den Winkel, J.G.J., Saito, T., Tybulewicz, V.L.J. and Watson, S.P. (1997) The Fc receptor γ-chain and the tyrosine kinase Syk are essential for activation of mouse platelets by collagen. EMBO J., 16, 2333-2341.
71. Qian, D.P. and Weiss, A. (1997) T cell antigen receptor signal transduction. Curr. Opin. Cell Biol. 9, 205-212.
72. Qin, S.F., Minami, Y., Hibi, M., Kurosaki, T. and Yamamura, H. (1997) Syk-dependent and -independent signaling cascades in B cells elicited by osmotic and oxidative stress. J. Biol. Chem., 111, 2098-2103.
73. 1 Integrin-mediated activation of focal adhesion kinase and its association with Fyn and Zap-70 in human NK cells. J. Immunol., 157, 3860-3868.
74. Reth, M. and Wienands, J. (1997) Initiation and processing of signals from the B cell antigen receptor. Annu. Rev. Immunol., 15, 453-479.
75. Rodriguez-Fernández, J.L. and Rozengurt, E. (1996) Bombesin, bradykinin, vasopressin and phorbol esters rapidly and transiently activate Src family tyrosine kinases in Swiss 3T3 cells-Dissociation from tyrosine phosphorylation of p 125 focal adhesion kinase. J. Biol. Chem. 271, 27895-27901.
76. Rowley, R.B., Burkhardt, A.L., Chao, H.-G., Matsueda, G.R. and Bolen, J.B. (1995) Syk protein-tyrosine kinase is regulated by tyrosine-phosphorylated Ign/Igβ immunoreceptor tyrosine activation motif binding and autophosphorylation. J. Biol Chem., 270, 11590-11594.
77. Sastry, S.K. and Horwitz, A.F. (1993) Integrin cytoplasmic domains: Mediators of cytoskeletal linkages and extra- and intracellular initiated transmembrane signaling. Curr. Opin. Cell Biol., 5, 819-831.
78. Sastry, S.K. and Horwitz, A.F. (1996) Adhesion-growth factor interactions during differentiation: An integrated biological response. Dev: Biol., 180, 455-467.
79. Scarborough, R.M. et al. (1993) Design of potent and specific integrin antagonists. Peptide antagonists with high specificity for glycoprotein IIb-IIIa. J. Biol. Chem., 268, 1066-1073.
80. FAK, a structurally unique protein tyrosine kinase associated with focal adhesions. Proc. Natl Acad. Sci. USA, 89, 5192-5196.
81. Schaller, M.D., Otey, C.A., Hildebrand, J.D. and Parsons, J.T. (1995) Focal adhesion kinase and paxillin bind to peptides mimicking β integrin cytoplasmic domains. J. Cell. Biol., 130, 1181-1187.
82. Scharenberg, A.M., Lin, S., Cuenod, B., Yamamura, H. and Kinet, J.-P. (1995) Reconstitution of interactions between tyrosine kinases and the high affinity IgE receptor which are controlled by receptor clustering. EMBO J., 14, 3385-3394.
83. Schlaepfer, D.D. and Hunter, T. (1997) Focal adhesion kinase overexpression enhances Ras-dependent integrin signaling to ERK2/ mitogen-activated protein kinase through interactions with and activation of c-Src. J. Biol. Chem., 272, 13189-13195.
84. Schwartz, M.A., Schaller, M.D. and Ginsberg, M.H. (1995) Integrins: Emerging paradigms of signal transduction. Annu. Rev. Cell Biol. 11, 549-599.
85. FAK in platelets requires coordinated signaling through integrin and agonist receptors. J. Biol. Chem., 269, 14738-14745.
86. syk with the gamma and β subunits of the high-affinity receptor for immunoglobulin E. Fc∈RI. Mol. Cell. Biol. 15, 272-281.
87. Shiue, L., Zoller, M.J. and Brugge, J.S. (1995b) Syk is activated by phosphotyrosine-containing peptides representing the tyrosine-based activation motifs of the high affinity receptor for IgE. J. Biol. Chem., 270, 10498-10502.
88. Takata, M. and Kurosaki, T. (1995) The catalytic activity of Src-family tyrosine kinase is required for B cell antigen receptor signaling. FEBS Lett., 374, 407-411.
89. Taylor, J.A., Karas, J.L., Ram, M.K., Green, O.M. and Seidel-Dugan, C. (1995) Activation of the high-afhnily immunoglobulin E receptor Fc epsilon RI in RBL-2H3 cells is inhibited by Syk SH2 domain. Mol. Cell. Biol. 15, 4149-4157.
90. Teramoto, H., Salem, P., Robbins, K.C., Bustelo, X.R. and Gutkind, J.S. (1997) Tyrosine phosphorylation of the vav proto-oncogene product links Fc∈RI to the Rac-JNK pathway. J. Biol Chem., 272, 10751-10755.
91. Turner, M. et al. (1995) Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature, 378, 298-302
92. 3 complex. J. Clin. Invest., in press.
93. Williams, S., Couture, C., Gilman, J., Jascur, T. Deckert, M., Altman, A. and Mustelin, T. (1997) Reconstitution of T cell antigen receptor-induced Erk2 kinase activation in Lck-negative JCaM 1 cells by Syk. Eur. J. Biochem., 245, 84-90.
94. Yamada, K.M. and Geiger, B. (1997) Molecular interactions in cell adhesion complexes. Curr. Opin. Cell Biol., 9, 76-85.
95. syk and Src family kinases in neutrophils spreading over fibrinogen. J. Immunol., 158, 1902-1910.
96. svk activation by an anti-glycoprotein Ib monoclonal antibody. Blood. 89, 1590-1598.
97. svk) with phosphatidylinositol 3-kinase are early events during platelet activation. Eur. J. Biochem., 224, 329-333.
98. Ylanne, J., Chen, Y., Toole, T.E., Loftus, J.C., Takada, Y. and Ginsberg. M.H. (1993) Distinct functions of integrin-alpha and integrin-beta subunit cytoplasmic domains in cell spreading and formation of focal adhesions. J. Cell Biol., 122, 223-233.
99. Zoller, K.E., MacNeil, I.A. and Brugge, J.S. (1997) Protein tyrosine kinases Syk and ZAP-70 display distinct requirements for Src family kinases in immune response receptor signal transduction. J. Immunol., 158, 1650-1659.