Anovel Syk-dependent mechanism of platelet activation by the C-type lectin receptor CLEC-2

Blood

Volumn 107, Issue 2, 2006, Pages 542-549

  Suzuki Inoue, Katsue ^b   Fuller, Gemma L J ^b   García, Ángel ^b   Eble, Johannes A ^b   Pöhlmann, Stefan ^b   Inoue, Osamu ^b   Gartner, T Kent ^b   Hughan, Sascha C ^b   Pearce, Andrew C ^b   Laing, Gavin D ^b   Theakston, R David G ^b   Schweighoffer, Edina ^b   Zitzmann, Nicole ^b   Morita, Takashi ^b   Tybulewicz, Victor L J ^b   Ozaki, Yukio ^a   Watson, Steve P ^b  

^a UNIVERSITY OF YAMANASHI   (Japan)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; C TYPE LECTIN RECEPTOR 2; COLLAGEN; CONVULXIN; LAT PROTEIN; LECTIN RECEPTOR; PROTEIN; PROTEIN KINASE SYK; PROTEIN SLP 76; RECEPTOR ANTIBODY; RECEPTOR SUBUNIT; RHODOCYTIN; SNAKE VENOM; THROMBIN RECEPTOR ACTIVATING PEPTIDE; TYROSINE; UNCLASSIFIED DRUG; VAV PROTEIN; ENZYME PRECURSOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HORMONE RECEPTOR; IMMUNOGLOBULIN RECEPTOR; LAT PROTEIN, MOUSE; LECTIN; MEMBRANE PROTEIN; MONOCLONAL ANTIBODY; NEUROPEPTIDE Y RECEPTOR; NPY6R PROTEIN, MOUSE; PEPTIDE FRAGMENT; PHOSPHOLIPASE C GAMMA; PHOSPHOPROTEIN; PROTEIN TYROSINE KINASE; PYRIMIDINE DERIVATIVE; RHODOCYTIN PROTEIN, CALLOSELASMA RHODOSTOMA; SIGNAL PEPTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SLP 76 SIGNAL TRANSDUCING ADAPTOR PROTEINS; SLP-76 SIGNAL TRANSDUCING ADAPTOR PROTEINS; THROMBIN RECEPTOR; THROMBIN RECEPTOR PEPTIDE (42 55); THROMBIN RECEPTOR PEPTIDE (42-55); THROMBIN RECEPTOR PEPTIDE SFLLRNP; VAV1 PROTEIN, MOUSE; VAV3 PROTEIN, MOUSE; VIPER VENOM;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME MECHANISM; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; RECEPTOR INTRINSIC ACTIVITY; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION; ANIMAL; CYTOSOL; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; IMMUNOPRECIPITATION; METABOLISM; MOUSE MUTANT; PHOSPHORYLATION; PHYSIOLOGY; THROMBOCYTE AGGREGATION; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIBODIES, MONOCLONAL; BLOTTING, WESTERN; COLLAGEN; CROTALID VENOMS; CYTOSOL; ENZYME PRECURSORS; FLOW CYTOMETRY; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LECTINS, C-TYPE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; PEPTIDE FRAGMENTS; PHOSPHOLIPASE C GAMMA; PHOSPHOPROTEINS; PHOSPHORYLATION; PLATELET ACTIVATION; PLATELET AGGREGATION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-VAV; PYRIMIDINES; RECEPTORS, GASTROINTESTINAL HORMONE; RECEPTORS, IMMUNOLOGIC; RECEPTORS, NEUROPEPTIDE Y; RECEPTORS, THROMBIN; SIGNAL TRANSDUCTION; TYROSINE; VIPER VENOMS;

EID: 30444452843     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2005-05-1994     Document Type: Article

References (42)

1. Andrews RK, Kamiguti AS, Berlanga O, Leduc M, Theakston RD, Watson SP. The use of snake venom toxins as tools to study platelet receptors for collagen and von Willebrand factor. Haemostasis. 2001;31:155-172.
2. Morita T. Structures and functions of snake venom CLPs (C-type lectin-like proteins) with anti-coagulant-, procoagulant-, and platelet-modulating activities. Toxicon. 2005;45:1099-1114.
3. Clemetson JM, Polgar J, Magnenat E, Wells TN, Clemetson KJ. The platelet collagen receptor glycoprotein VI is a member of the immunoglobulin superfamily closely related to FcalphaR and the natural killer receptors. J Biol Chem. 1999;274: 29019-29024.
4. 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.
5. Jandrot-Perrus M, Lagrue AH, Okuma M, Bon C. Adhesion and activation of human platelets induced by convulxin involve glycoprotein VI and integrin alpha2beta1. J Biol Chem. 1997;272: 27035-27041.
6. Suzuki-Inoue K, Tulasne D, Shen Y, et al. Association of Fyn and Lyn with the proline-rich domain of glycoprotein VI regulates intracellular signaling. J Biol Chem. 2002;277:21561-21566.
7. Bori-Sanz T, Inoue KS, Berndt MC, Watson SP, Tulasne D. Delineation of the region in the glycoprotein VI tail required for association with the Fc receptor gamma-chain. J Biol Chem. 2003;278: 35914-35922.
8. Lee WH, Du XY, Lu QM, Clemetson KJ, Zhang Y. Stejnulxin, a novel snake C-type lectin-like protein from Trimeresurus stejnegeri venom is a potent platelet agonist acting specifically via GPVI. Thromb Haemost. 2003;90:662-671.
9. Asazuma N, Marshall SJ, Berlanga O, et al. The snake venom toxin alboaggregin-A activates glycoprotein VI. Blood. 2001;97:3989-3991.
10. Andrews RK, Gardiner EE, Asazuma N, et al. A novel viper venom metalloproteinase, alborhagin, is an agonist at the platelet collagen receptor GPVI. J Biol Chem. 2001;276:28092-28097.
11. Shin Y, Morita T. Rhodocytin, a functional novel platelet agonist belonging to the heterodimeric C-type lectin family, induces platelet aggregation independently of glycoprotein Ib. Biochem Biophys Res Commun. 1998;245:741-745.
12. Huang TF, Liu CZ, Yang SH. Aggretin, a novel platelet-aggregation inducer from snake (Calloselasma rhodostoma) venom, activates phospholipase C by acting as a glycoprotein Ia/IIa agonist. Biochem J. 1995;309:1021-1027.
13. Suzuki-Inoue K, Ozaki Y, Kainoh M, et al. Rhodocytin induces platelet aggregation by interacting with glycoprotein Ia/IIa (GPIa/IIa, Integrin alpha 2beta 1): involvement of GPIa/IIa-associated src and protein tyrosine phosphorylation. J Biol Chem. 2001;276:1643-1652.
14. Navdaev A, Clemetson JM, Polgar J, et al. Aggretin, a heterodimeric C-type lectin from Calloselasma rhodostoma (malayan pit viper), stimulates platelets by binding to alpha 2beta 1 integrin and glycoprotein Ib, activating Syk and phospholipase Cgamma 2, but does not involve the glycoprotein VI/Fc receptor gamma chain collagen receptor. J Biol Chem. 2001;276:20882-20889.
15. Bergmeier W, Bouvard D, Eble JA, et al. Rhodocytin (aggretin) activates platelets lacking alpha(2) beta(1) integrin, glycoprotein VI, and the ligandbinding domain of glycoprotein Ibalpha. J Biol Chem. 2001;276:25121-25126.
16. Suzuki-Inoue K, Garcia A, Eble JA, et al. Identification of CLEC-2 as a novel signalling receptor for rhodocytin in platelets [abstract]. J Thromb Haemost. 2005;3(suppl 1):Abstract no. P1494.
17. Suzuki-Inoue K, Inoue O, Frampton J, Watson SP. Murine GPVI stimulates weak integrin activation in PLC{gamma}2 / platelets: involvement of PLC{gamma}1 and PI 3-kinase. Blood. 2003; 102:1367-1373.
18. 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.
19. 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.
20. Clements JL, Lee JR, Gross B, et al. Fetal hemorrhage and platelet dysfunction in SLP-76-deficient mice. J Clin Invest. 1999;103:19-25.
21. Pearce AC, Senis YA, Billadeau DD, Turner M, Watson SP, Vigorito E. Vav1 and vav3 have critical but redundant roles in mediating platelet activation by collagen. J Biol Chem. 2004;279: 53955-53962.
22. Eble JA, Beermann B, Hinz HJ, Schmidt-Hederich A. alpha 2beta 1 integrin is not recognized by rhodocytin but is the specific, high affinity target of rhodocetin, an RGD-independent disintegrin and potent inhibitor of cell adhesion to collagen. J Biol Chem. 2001;276:12274-12284.
23. Shevchenko A, Jensen ON, Podtelejnikov AV, et al. Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc Natl Acad Sci U S A. 1996;93:14440-14445.
24. Garcia A, Prabhakar S, Hughan S, et al. Differential proteome analysis of TRAP-activated platelets: involvement of DOK-2 and phosphorylation of RGS proteins. Blood. 2004;103:2088-2095.
25. Pohlmann S, Zhang J, Baribaud F, et al. Hepatitis C virus glycoproteins interact with DC-SIGN and DC-SIGNR. J Virol. 2003;77:4070-4080.
26. Colonna M, Samaridis J, Angman L. Molecular characterization of two novel C-type lectin-like receptors, one of which is selectively expressed in human dendritic cells. Eur J Immunol. 2000;30: 697-704.
27. 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.
28. Gibbins J, Asselin J, Farndale R, Barnes M, Law CL, Watson SP. Tyrosine phosphorylation of the Fc receptor gamma-chain in collagen-stimulated platelets. J Biol Chem. 1996;271:18095-18099.
29. Judd BA, Myung PS, Obergfell A, et al. Differential requirement for LAT and SLP-76 in GPVI versus T cell receptor signaling. J Exp Med. 2002; 195:705-717.
30. Chung CH, Wu WB, Huang TF. Aggretin, a snake venom-derived endothelial integrin alpha 2 beta 1 agonist, induces angiogenesis via expression of vascular endothelial growth factor. Blood. 2004; 103:2105-2113.
31. Marshall AS, Gordon S. Commentary: C-type lectins on the macrophage cell surface - recent findings. Eur J Immunol. 2004;34:18-24.
32. Cambi A, Figdor CG. Dual function of C-type lectin-like receptors in the immune system. Curr Opin Cell Biol. 2003;15:539-546.
33. Vivier E, Nunes JA, Vely F. Natural killer cell signaling pathways. Science. 2004;306:1517-1519.
34. Rogers NC, Slack EC, Edwards AD, et al. Sykdependent cytokine induction by dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity. 2005;22:507-517.
35. Herre J, Marshall AS, Caron E, et al. Dectin-1 uses novel mechanisms for yeast phagocytosis in macrophages. Blood. 2004;104:4038-4045.
36. Fallon RJ, Danaher M, Saylors RL, Saxena A. Defective asialoglycoprotein receptor endocytosis mediated by tyrosine kinase inhibitors; requirement for a tyrosine in the receptor internalization signal. J Biol Chem. 1994;269:11011-11017.
37. Geffen I, Fuhrer C, Leitinger B, et al. Related signals for endocytosis and basolateral sorting of the asialoglycoprotein receptor. J Biol Chem. 1993; 268:20772-20777.
38. Chen M, Kakutani M, Naruko T, et al. Activationdependent surface expression of LOX-1 in human platelets. Biochem Biophys Res Commun. 2001;282:153-158.
39. Dean YD, McGreal EP, Gasque P. Endothelial cells, megakaryoblasts, platelets and alveolar epithelial cells express abundant levels of the mouse AA4 antigen, a C-type lectin-like receptor involved in homing activities and innate immune host defense. Eur J Immunol. 2001;31:1370-1381.
40. Testi R, Pulcinelli F, Frati L, Gazzaniga PP, Santoni A. CD69 is expressed on platelets and mediates platelet activation and aggregation. J Exp Med. 1990;172:701-707.
41. Joseph M, Capron A, Ameisen JC, et al. The receptor for IgE on blood platelets. Eur J Immunol. 1986;16:306-312.
42. Swiss Institute of Bioinformatics. Swiss-Prot protein knowledgebase. http://www.expasy.org/sprot/. Accessed March 2005.