Glycoprotein VI/Fc receptor γ chain-independent tyrosine phosphorylation and activation of murine platelets by collagen

Biochemical Journal

Volumn 383, Issue 3, 2004, Pages 581-588

  Jarvis, Gavin E ^a,b   Best, Denise ^a   Watson, Steve P ^a,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

2 1 integrin; Collagen; Fc receptor chain; Glycoprotein VI; Knock out model; Protein tyrosine phosphorylation

Indexed keywords

ADHESION; ANTIBODIES; IMMUNOLOGY;

GLYCOPROTEINS; IMMUNOPRECIPITATION; PHOSPHOLIPASE; PHOSPHORYLATION;

COLLAGEN;

15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; ADENOSINE TRIPHOSPHATE; ADHESION AND DEGRANULATION PROMOTING ADAPTER PROTEIN; COLLAGEN; FC RECEPTOR; FC RECEPTOR GAMMA CHAIN; FOCAL ADHESION KINASE; GLYCOPROTEIN; GLYCOPROTEIN VI; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY HA1 29; MONOCLONAL ANTIBODY HMALPHA2; PHOSPHOLIPASE C; PROTEIN; PROTEIN KINASE SYK; SLP 76 PROTEIN; THROMBOXANE DERIVATIVE; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 2;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; THROMBOCYTE ACTIVATION; THROMBOCYTE RELEASE REACTION; THROMBOCYTOPENIA;

15-HYDROXY-11 ALPHA,9 ALPHA-(EPOXYMETHANO)PROSTA-5,13-DIENOIC ACID; ANIMALS; BLOOD PLATELETS; COLLAGEN; INTEGRIN ALPHA2BETA1; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHORYLATION; PLATELET AGGREGATION; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PLATELET MEMBRANE GLYCOPROTEINS; PROTEINS; RECEPTORS, FC; RECEPTORS, IGG; SIGNAL TRANSDUCTION; TYROSINE;

ANIMALIA; MURINAE;

EID: 9144269735     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20040654     Document Type: Article

References (50)

1. Clemetson, K. J. and Clemetson, J. M. (2001) Platelet collagen receptors. Thromb. Haemostasis 86, 189-197
2. Barnes, M. J., Knight, C. G. and Farndale, R. W. (1998) The collagen-platelet interaction, Curr. Opin. Hematol. 5, 314-320
3. Nieswandt, B. and Watson, S. P. (2003) Platelet-collagen interaction: is GPVI the central receptor? Blood 102, 449-461
4. Morai, M., Jung, S. M., Okuma, M. and Shinmyozu, K. (1989) A patient with platelets deficient in glycoprotein VI that lack both collagen-induced aggregation and adhesion. J. Clin. Invest. 84, 1440-1445
5. Nieswandt, B., Bergmeier, W., Schulte, V., Rackebrandt, K., Gessner, J. E. and Zirngibl, H. (2000) Expression and function of the mouse collagen receptor glycoprotein VI is strictly dependent on its association with the FcRgamma chain. J. Biol. Chem. 275, 23998-24002
6. Clemetson, J. M., Polgar, J., Magnenat, E., Wells, T. N. and Clemetson, K. J. (1999) 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. 274, 29019-29024
7. Gibbins, J. M., Okuma, M., Farndale, R., Barnes, M. and Watson, S. P. (1997) Glycoprotein VI is the collagen receptor in platelets which underlies tyrosine phosphorylation of the Fc receptor gamma-chain. FEBS Lett. 413, 255-259
8. Asselin, J., Gibbins, J. M., Achison, M., Lee, Y. H., Morton, L. F., Farndale, R. W., Barnes, M. J. and Watson, S. P. (1997) A collagen-like peptide stimulates tyrosine phosphorylation of syk and phospholipase C gamma2 in platelets independent of the integrin alpha2beta1. Blood 89, 1235-1242
9. Poole, A., Gibbins, J. M., Turner, M., van Vugt, M. J., van de Winkel, J. G., Saito, T., Tybulewicz, V. L. and Watson, S. P. (1997) The Fc receptor gamma-chain and the tyrosine kinase Syk are essential for activation of mouse platelets by collagen. EMBO J. 16, 2333-2341
10. Pasquet, J. M., Gross, B., Quek, L., Asazuma, N., Zhang, W., Sommers, C. L., Schweighoffer, E., Tybulewicz, V., Judd, B., Lee, J. R. et al. (1999) LAT is required for tyrosine phosphorylation of phospholipase cgamma2 and platelet activation by the collagen receptor GPVI. Mol. Cell. Biol. 19, 8326-8334
11. Gross, B. S., Lee, J. R., Clements, J. L., Turner, M., Tybulewicz, V. L., Findell, P. R., Koretzky, G. A. and Watson, S. P. (1999) Tyrosine phosphorylation of SLP-76 is downstream of Syk following stimulation of the collagen receptor in platelets. J. Biol. Chem. 274, 5963-5971
12. Knight, C. G., Morton, L. F., Onley, D. J., Peachey, A. R., Ichinohe, T., Okuma, M., Farndale, R. W. and Barnes, M. J. (1999) Collagen-platelet interaction: Gly-Pro-Hyp is uniquely specific for platelet Gp VI and mediates platelet activation by collagen. Cardiovasc. Res. 41, 450-457
13. Polgar, J., Clemetson, J. M., Kehrel, B. E., Wiedemann, M., Magnenat, E. M., Wells, T. N. and Clemetson, K. J. (1997) Platelet activation and signal transduction byconvulxin, a C-type lectin from Crotalus durissus terrificus (tropical rattlesnake) venom via the P62/GPVI collagen receptor. J. Biol. Chem. 272, 13576-13583
14. Ichinohe, T., Takayama, H., Ezumi, Y., Arai, M., Yamamoto, N., Takahashi, H. and Okuma, M. (1997) Collagen-stimulated activation of Syk but notc-Src is severely compromised in human platelets lacking membrane glycoprotein VI. J. Biol. Chem. 272, 63-68
15. Nieswandt, B., Brakebusch, C., Bergmeier, W., Schulte, V., Bouvard, D., Mokhtari-Nejad, R., Lindhout, T., Heemskerk, J. W., Zirngibl, H. and Fassler, R. (2001) Glycoprotein VI but not alpha2beta1 integrin is essential for platelet interaction with collagen. EMBO J. 20, 2120-2130
16. Santoro, S. A., Rajpara, S. M., Staatz, W. D. and Woods, Jr, V. L. (1988) Isolation and characterization of a platelet surface collagen binding complex related to VLA-2. Biochem. Biophys. Res. Commun. 153, 217-223
17. Shattil, S. J., Kashiwagi, H. and Pampori, N. (1998) Integrin signaling: the platelet paradigm. Blood 91, 2645-2657
18. Jung, S. M. and Moroi, M. (2000) Signal-transducing mechanisms involved in activation of the platelet collagen receptor integrin alpha(2)beta(1). J. Biol. Chem. 275, 8016-8026
19. Saelman, E. U., Nieuwenhuis, H. K., Hese, K. M., de Groot, P. G., Heijnen, H. F., Sage, E. H., Williams, S., McKeown, L., Gralnick, H. R. and Sixma, J. J. (1994) Platelet adhesion to collagen types I through VIII under conditions of stasis and flow is mediated byGPIa/IIa (alpha 2 beta 1-integrin). Blood 83, 1244-1250
20. Atkinson, B. T., Jarvis, G. E. and Watson, S. P. (2003) Activation of GPVI by collagen is regulated byalpha2beta1 and secondary mediators. J. Thromb. Haemostasis 1, 1278-1287
21. Siljander, P. R., Munnix, I. C., Smethurst, P. A., Deckmyn, H., Lindhout, T, Ouwehand, W. H., Farndale, R. W. and Heemskerk, J. W. (2004) Platelet receptor interplay regulates collagen-induced thrombus formation in flowing human blood. Blood 103, 1333-1341
22. Jarvis, G. E., Atkinson, B. T., Snell, D. C. and Watson, S. P. (2002) Distinct roles of GPVI and integrin alpha(2)beta(1) in platelet shape change and aggregation induced by different collagens. Br. J. Pharmacol. 137, 107-117
23. Koyama, H., Raines, E. W., Bornfeldt, K. E., Roberts, J. M. and Ross, R. (1996) Fibrillar collagen inhibits arterial smooth muscle proliferation through regulation of Cdk2 inhibitors. Cell 87, 1069-1078
24. Klekotka, P. A., Santoro, S. A., Wang, H. and Zutter, M. M. (2001) Specific residues within the alpha 2 integrin subunit cytoplasmic domain regulate migration and cell cycle progression via distinct MARK pathways. J. Biol. Chem. 276, 32353-32361
25. Keely, P. J. and Parise, L. V. (1996) The alpha2beta1 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
26. Snell, D. C., Schulte, V., Jarvis, G. E., Arase, K., Sakurai, D., Saito, T., Watson, S. P. and Nieswandt, B. (2002) Differential effects of reduced glycoprotein VI levels on activation of murine platelets by glycoprotein VI ligands. Biochem. J. 368, 293-300
27. Chen, H. and Kahn, M. L. (2003) Reciprocal signaling by integrin and nonintegrin receptors during collagen activation of platelets. Mol. Cell. Biol. 23, 4764-4777
28. Inoue, K., Ozaki, Y., Satoh, K., Wu, Y., Yatomi, Y., Shin, Y. and Morita, T. (1999) Signal transaction pathways mediated by glycoprotein Ia/IIa in human platelets: comparison with those of glycoprotein VI. Biochem. Biophys. Res. Commun. 256, 114-120
29. Suzuki-Inoue, K., Ozaki, Y., Kainoh, M., Shin, Y., Wu, Y., Yatomi, Y., Ohmori, T., Tanaka, T., Satoh, K. and Morita, T. (2001) 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. 276, 1643-1652
30. Bergmeier, W., Bouvard, D., Eble, J. A., Mokhtari-Nejad, R., Schulte, V., Zirngibl, H., Brakebusch, C., Fassler, R. and Nieswandt, B. (2001) Rhodocytin (aggretin) activates platelets lacking alpha(2)beta(1) integrin, glycoprotein VI, and the ligand-binding domain of glycoprotein Ibalpha. J. Biol. Chem. 276, 25121-25126
31. Hers, I., Berlanga, O., Tiekstra, M. J., Kamiguti, A. S., Theakston, R. D. and Watson, S. P. (2000) Evidence against a direct role of the integrin alpha2beta1 in collagen-induce tyrosine phosphorylation in human platelets. Eur J. Biochem. 267, 2088-2097
32. Polanowska-Grabowska, R., Simon, Jr, C. G., Falchetto, R., Shabanowitz, J., Hunt, D. F. and Gear, A. R. (1997) Platelet adhesion to collagen under flow causes dissociation of a phosphoprotein complex of heat-shock proteins and protein phosphatase 1. Blood 90, 1516-1526
33. Inoue, O., Suzuki-Inoue, K., Dean, W. L., Frampton, J. and Watson, S. P. (2003) Integrin {alpha}2{beta}1 mediates outside-in regulation of platelet spreading on collagen through activation of Src kinases and PLC{gamma}2. J. Cell Biol. 160, 769-780
34. Guidetti, G., Bertoni, A., Viola, M., Tira, E., Balduini, C. and Torti, M. (2002) The small proteoglycan decorin supports adhesion and activation of human platelets. Blood 100, 1707-1714
35. Lipfert, L., Haimovich, B., Schaller, M. D., Cobb, B. S., Parsons, J. T. and Brugge, J. S. (1992) Integrin-dependent phosphorylation and activation of the protein tyrosine kinase PP125FAK in platelets. J. Cell Biol. 119, 905-912
36. Leong, L., Hughes, P. E., Schwartz, M. A., Ginsberg, M. H. and Shattil, S. J. (1995) Integrin signaling: roles for the cytoplasmic tails of alpha IIb beta 3 in the tyrosine phosphorylation of pp125FAK. J. Cell Sci. 108, 3817-3825
37. Polanowska-Grabowska, R., Geanacopoulos, M. and Gear, A. R. (1993) Platelet adhesion to collagen via the alpha 2 beta 1 integrin under arterial flow conditions causes rapid tyrosine phosphorylation of pp125FAK. Biochem. J. 296, 543-547
38. 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. et al. (2001) Coupling of the TCR to integrin activation by Slap-130/Fyb. Science 293, 2263-2265
39. 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. et al. (2001) Positive regulation of T cell activation and integrin adhesion by the adapter Fyb/Slap. Science 293, 2260-2263
40. Hunter, A. J., Ottoson, N., Boerth, N., Koretzky, G. A. and Shimizu, Y. (2000) Cutting edge: a novel function for the SLAP-130/FYB adapter protein in beta 1 integrin signaling and T lymphocyte migration. J. Immunol. 164, 1143-1147
41. Obergfell, A., Judd, B. A., del Pozo, M. A., Schwartz, M. A., Koretzky, G. A. and Shattil, S. J. (2001) The molecular adapter SLP-76 relays signals from platelet integrin alphaIIbbeta3 to the actin cytoskeleton. J. Biol. Chem. 276, 5916-5923
42. Park, S. Y., Ueda, S., Ohno, H., Hamano, Y., Tanaka, M., Shiratori, T., Yamazaki, T., Arase, H., Arase, M., Karasawa, A. et al. (1998) Resistance of Fc receptor-deficient mice to fatal glomerulonephritis. J. Clin. Invest. 102, 1229-1238
43. Jarvis, G. E. (2004) Platelet aggregation: turbidimetric measurements. Methods Mol. Biol. 272, 65-76
44. Jarvis, G. E. (2004) Platelet aggregation in whole blood: impedance and particle counting methods. Methods Mol. Biol. 272, 77-88
45. Jarvis, G. E., Atkinson, B. T., Frampton, J. and Watson, S. P. (2003) Thrombin-induced conversion of fibrinogen to fibrin results in rapid platelet trapping which is not dependent on platelet activation or GPIb. Br. J. Pharmacol. 138, 574-583
46. Nieswandt, B., Schulte, V., Zywietz, A., Gratacap, M. P. and Offermanns, S. (2002) Costimulation of Gi- and G12/G13-mediated signaling pathways induces integrin alpha IIbbeta 3 activation in platelets. J. Biol. Chem. 277, 39493-39498
47. Wonerow, P., Pearce, A. C., Vaux, D. J. and Watson, S. P. (2003) A critical role for phospholipase Cgamma2 in alphaIIbbeta3-mediated platelet spreading. J. Biol. Chem. 278, 37520-37529
48. Shattil, S. J., Haimovich, B., Cunningham, M., Lipfert, L., Parsons, J. T., Ginsberg, M. H. and Brugge, J. S. (1994) Tyrosine phosphorylation of pp125FAK in platelets requires coordinated signaling through integrin and agonist receptors. J. Biol. Chem. 269, 14738-14745
49. Kato, K., Kanaji, T., Russell, S., Kunicki, T. J., Furihata, K., Kanaji, S., Marchese, P., Reininger, A., Ruggeri, Z. M., and Ware, J. (2003) The contribution of glycoprotein VI to stable platelet adhesion and thrombus formation illustrated by targeted gene deletion. Blood 102, 1701-1707
50. Achison, M., Elton, C. M., Hargreaves, P. G., Knight, C. G., Barnes, M. J. and Farndale, R. W. (2001) Integrin-independent tyrosine phosphorylation of p125(fak) in human platelets stimulated by collagen. J. Biol. Chem. 276, 3167-3174