Rapid ubiquitination of Syk following GPVI activation in platelets

Blood

Volumn 105, Issue 10, 2005, Pages 3918-3924

  Dangelmaier, Carol A ^b   Quinter, Patricia G ^b   Jin, Jianguo ^b   Tsygankov, Alexander Y ^b   Kunapuli, Satya P ^b   Daniel, James L ^a  

^a TEMPLE UNIVERSITY   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CBL PROTEIN; COLLAGEN; CONVULXIN; FC RECEPTOR; GLYCOPROTEIN; GLYCOPROTEIN VI; PROTEASOME; PROTEIN KINASE SYK; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION;

EID: 18544374319     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2004-09-3689     Document Type: Article

References (52)

1. Packham MA. Role of platelets in thrombosis and hemostasis. Can J Physiol Pharmacol. 1994;72:278-284.
2. Santoro SA, Zutter MM. The Alpha2Beta1 integrin: a collagen receptor on platelets and other cells. Thromb Haemost. 1995;74:813-821.
3. Tsuji M, Ezumi Y, Arai M, Takayama H. A novel association of Fc receptor gamma-chain with glycoprotein VI and their co-expression as a collagen receptor in human platelets. J Biol Chem. 1997;272:23528-23531.
4. Berlanga O, Bobe R, Becker M, et al. Expression of the collagen receptor glycoprotein VI during megakaryocyte differentiation. Blood. 2000;96:2740-2745.
5. Smith JB, Selak MA, Dangelmaier C, Daniel JL. Cytosolic calcium as a second messenger for collagen-induced platelet responses. Biochem J. 1992;288:925-929.
6. Blake RA, Schieven GL, Watson SP. Collagen stimulates tyrosine phosphorylation of phospholipase C-gamma2 but not phospholipase C-gamma1 in human platelets. FEBS Lett. 1994;353:212-216.
7. Daniel JL, Dangelmaier C, Smith JB, Evidence for a role for tyrosine phosphorylation of phospholipase Cgamma2 in collagen-induced platelet cytosolic calcium mobilization. Biochem J. 1994;302:617-622.
8. Ozdener F, Dangelmaier C, Ashby B, Kunapuli SP, Daniel JL. Activation of phospholipase Cgamma2 by tyrosine phosphorylation. Mol Pharmacol. 2002;62:672-679.
9. Quek LS, Pasquet JM, Hers I, et al. Fyn and Lyn phosphorylate the Fc receptor gamma chain downstream of glycoprotein VI in murine platelets, and Lyn regulates a novel feedback pathway. Blood. 2000;96:4246-4253.
10. Watson SP, Gibbins J. Collagen receptor signalling in platelets: extending the role of the ITAM. Immunol Today. 1998;19:260-264.
11. Poole A, Gibbins JM, Turner M, et al. The Fc receptor gamma-chain and the tyrosine kinase Syk are essential for activation of mouse platelets by collagen. EMBO J. 1997;16:2333-2341.
12. Asselin J, Gibbins JM, Achison M, et al. A collagen-like peptide stimulates tyrosine phosphorylation of syk and phospholipase C gamma2 in platelets independent of the integrin alpha2beta1. Blood. 1997;89:1235-1242.
13. Pasquet JM, Gross B, Quek L, et al. LAT is required for tyrosine phosphorylation of phospholipase cgamma2 and platelet activation by the collagen receptor GPVI. Mol Cell Biol. 1999;19:8326-8334.
14. Quek LS, Bolen J, Watson SP. A role for Bruton's tyrosine kinase (Btk) in platelet activation by collagen. Curr Biol. 1998;8:1137-1140.
15. Tsygankov AY, Teckchandani AM, Feshchenko EA, Swaminathan G. Beyond the RING: CBL proteins as multivalent adapters. Oncogene. 2001;20:6382-6402.
16. Rao N, Dodge I, Band H. The Cbl family of ubiquitin ligases: critical negative regulators of tyrosine kinase signaling in the immune system. J Leukoc Biol. 2002;71:753-763.
17. Rao N, Lupher ML Jr, Ota S, Reedquist KA, Druker BJ, Band H. The linker phosphorylation site Tyr292 mediates the negative regulatory effect of Cbl on ZAP-70 in T cells. J Immunol. 2000;164:4616-4626.
18. Feshchenko EA, Shore SK, Tsygankov AY. Tyrosine phosphorylation of C-Cbl facilitates adhesion and spreading while suppressing anchor-age-independent growth of V-Abl-transformed NIH3T3 fibroblasts. Oncogene. 1999;18:3703-3715.
19. Lupher ML Jr, Rao N, Lill NL, et al. 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. 1998;273:35273-35281.
20. Feshchenko EA, Langdon WY, Tsygankov AY. Fyn, Yes, and Syk phosphorylation sites in C-Cbl map to the same tyrosine residues that become phosphorylated in activated T cells. J Biol Chem. 1998;273:8323-8331.
21. Kurasaki T, Takata M, Yamanashi Y, et al. Syk activation by the Src-family tyrosine kinase in the B cell receptor signaling. J Exp Med. 1994;179:1725-1729.
22. Joazeiro CA, Wing SS, Huang H, Leverson JD, Hunter T, Liu YC. The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science. 1999;286:309-312.
23. Zheng N, Wang P, Jeffrey PD, Pavletich NP. Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases. Cell. 2000;102:533-539.
24. Yokouchi M, Kondo T, Houghton A, et al. Ligand-induced ubiquitination of the epidermal growth factor receptor involves the interaction of the c-Cbl RING finger and UbcH7. J Biol Chem. 1999;274:31707-31712.
25. Levkowitz G, Waterman H, Ertenberg SA, et al. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol Cell. 1999;4:1029-1040.
26. Ota S, Hazeki K, Rao N, et al. The RING finger domain of Cbl is essential for negative regulation of the Syk tyrosine kinase. J Biol Chem. 2000;275:414-422.
27. Waterman H, Levkowitz G, Alroy I, Yarden Y. The RING finger of c-Cbl mediates desensitization of the epidermal growth factor receptor. J Biol Chem. 1999;274:22151-22154.
28. Fang S, Weissman AM. A field guide to ubiquitylation. Cell Mol Life Sci. 2004;61:1546-1561.
29. Marmor MD, Yarden Y. Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene. 2004;23:2057-2070.
30. Oda A, Ozaki K, Druker BJ, et al. p120c-cbl is present in human blood platelets and is differentially involved in signaling by thrombopoietin and thrombin. Blood. 1996;88:1330-1338.
31. Polgar J, Clemetson JM, Kehrel BE, et al. Platelet activation and signal transduction by convulxin, a C-type lectin from Crotalus durissus terrificus (tropical rattlesnake) venom via the p62/GPVI collagen receptor. J Biol Chem. 1997;272:13576-13583.
32. Saoi A, Rendu F, Bachelot-Loza C. Platelet alpha IIb-beta 3 integrin engagement induces the tyrosine phosphorylation of Cbl and its association with phosphoinositide 3-kinase and Syk. Biochem J. 2000;351(pt 3):669-676.
33. Saci A, Liu WQ, Vidal M, Garbay C, Rendu F, Bachelot-Loza C. Differential effect of the inhibition of Grb2-SH3 interactions in platelet activation induced by thrombin and by Fc receptor engagement. Biochem J. 2002;363:717-725.
34. Auger JM, Best D, Snell DC, Wilde JI, Watson SP. c-Cbl negatively regulates platelet activation by glycoprotein VI. J Thromb Haemost. 2003;1:2419-2426.
35. Rao N, Ghosh AK, Ota S, et al. The non-receptor tyrosine kinase Syk is a target of Cbl-mediated ubiquitylation upon B-cell receptor stimulation. Embo J. 2001;20:7085-7095.
36. Melford SK, Turner M, Briddon SJ, Tybulewicz VL, Watson SP. Syk and Fyn are required by mouse megakaryocytes for the rise in intracellular calcium induced by a collagen-related peptide. J Biol Chem. 1997;272:27539-27542.
37. Wang CC, Badylak JA, Lux SE, Moriyama R, Dixon JE, Low PS. Expression, purification, and characterization of the functional dimeric cytoplasmic domain of human erythrocyte band 3 in Escherichia coli. Protein Sci. 1992;1:1206-1214.
38. Ostrowska H, Ostrowska JK, Worowski K, Radziwon P. Human platelet 20S proteasome: inhibition of its chymotrypsin-like activity and identification of the proteasome activator PA28: a preliminary report. Platelets. 2003;14:151-157.
39. Stein RL, Melandri F, Dick L. Kinetic characterization of the chymotryptic activity of the 20S proteasome. Biochemistry. 1996;35:3899-3908.
40. Paolini R, Molfetta R, Beitz LO, et al. Activation of Syk tyrosine kinase is required for c-Cbl-mediated ubiquitination of Fcepsilon RI and Syk in RBL cells. J Biol Chem. 2002;277:36940-36947.
41. Marinissen MJ, Servitja JM, Offermanns S, Simon MI, Gutkind JS. Thrornbin protease-activated receptor-1 signals through Gq- and CIS-initiated MAPK cascades regulating c-Jun expression to induce cell transformation. J Biol Chem. 2003;278:46814-46825.
42. Coughlin SR, Camerer E. PARticipation in inflammation. J Clin Invest. 2003;111:25-27.
43. Paolini R, Molfetta R, Piccoli M, Frati L, Santoni A. Ubiquitination and degradation of Syk and ZAP-70 protein tyrosine kinases in human NK cells upon CD16 engagement. Proc Natl Acad Sci USA. 2001;98:9611-9616.
44. Isakov N, Wange RL, Watts JD, Aebersold R, Samelson LE. Purification and characterization of human ZAP-70 protein-tyrosine kinase from a baculovirus expression system. J Biol Chem. 1996;271:15753-15761.
45. Tsygankov AY. Non-receptor protein tyrosine kinases. Front Biosci. 2003;8:s595-s635.
46. Suzuki-Inoue K, Wilde JI, Andrews RK, et al. Glycoproteins VI and Ib-IX-V stimulate tyrosine phosphorylation of tyrosine kinase Syk and phospholipase Cgamma2 at distinct sites. Biochem J. 2004;378:1023-1029.
47. O'Neill EE, Brock CJ, von Kriegsheim AF, et al. Towards complete analysis of the platelet proteome. Proteomics. 2002;2:288-305,
48. Melander F, Andersson T, Dib K. Fgr but not Syk tyrosine kinase is a target for beta 2 integrin-induced c-Cbl-mediated ubiquitination in adherent human neutrophils. Biochem J. 2003;370:687-694.
49. Sun L, Chen ZJ. The novel functions of ubiquitination in signaling. Curr Opin Cell Biol. 2004;16:119-126.
50. Fang D, Liu YC. Proteolysis-independent regulation of PI3K by Cbl-b-mediated ubiquitination in T cells. Nat Immunol. 2001;2:870-875.
51. Sattler M, Salgia R, Shrikhande G, et al. The phosphatidylinositol polyphosphate 5-phosphatase SHIP and the protein tyrosine phosphatase SHP-2 form a complex in hematopoietic cells which can be regulated by BCR/ABL and growth factors. Oncogene. 1997;15:2379-2384.
52. Cohen S, Dadi H, Shaoul E, Sharfe N, Roifman CM. Cloning and characterization of a lymphoid-specific, inducible human protein tyrosine phosphatase, Lyp. Blood. 1999;93:2013-2024.