Platelet adhesion to collagen and collagen-related peptide under flow: Roles of the α2β1 integrin, GPVI, and Src tyrosine kinases

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 23, Issue 10, 2003, Pages 1934-1940

  Polanowska Grabowska, Renata ^a   Gibbins, Jonathan M ^b   Gear, Adrian R L ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF READING   (United Kingdom)

Author keywords

Adhesion; Collagen; Collagen related peptide; Flow; Platelets; Protein tyrosine kinase

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; COLLAGEN; COLLAGEN RELATED PEPTIDE; FOCAL ADHESION KINASE; GLYCOPROTEIN; GLYCOPROTEIN VI; GLYCYLARGINYLGLYCYLASPARTYLSERYLPROLINE; INTEGRIN; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA2; PP 125 FOCAL ADHESION KINASE; PROTEIN; PROTEIN KINASE SYK; PROTEIN TYROSINE KINASE; PYRAZOLOPYRIMIDINE; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 2;

ARTICLE; AUTOPHOSPHORYLATION; CONTROLLED STUDY; CROSS LINKING; ENZYME ACTIVATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; THROMBOCYTE ADHESION;

CARRIER PROTEINS; COLLAGEN; HUMANS; INTEGRINS; PEPTIDES; PHOSPHORYLATION; PLATELET ADHESIVENESS; PLATELET MEMBRANE GLYCOPROTEINS; PROTEIN-TYROSINE KINASES; PYRIMIDINES; SRC-FAMILY KINASES;

EID: 0141885324     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000086937.46974.70     Document Type: Article

References (41)

1. Staatz WD, Rajpara SM, Wayner EA, Carter WG, Santoro SA. The membrane glycoprotein Ia-IIa (VLA-2) complex mediates the Mg++-dependent adhesion of platelets to collagen. J Cell Biol. 1989;108: 1917-1924.
2. Tandon NN, Kralisz U, Jamieson GA. Identification of glycoprotein IV (CD36) as a primary receptor for platelet-collagen adhesion. J Biol Chem. 1989;264:7576-7583.
3. Moroi M, Jung SM, Okuma M, Shinmyozu K. A patient with platelets deficient in glycoprotein VI that lack both collagen-induced aggregation and adhesion. J Clin Invest. 1989;84:1440-1445.
4. Chiang TM, Rinaldy A, Kang AH. Cloning, characterization, and functional studies of a nonintegrin platelet receptor for type I collagen. J Clin Invest. 1997;100:514-521.
5. Monnet E, Fauvel-Lafeve F. A new platelet receptor specific to type III collagen: type III collagen-binding protein. J Biol Chem. 2000;275: 10912-10917.
6. Deckmyn H, Van Houtte E, Vermylen J. Disturbed platelet aggregation to collagen associated with an antibody against an 85- to 90-Kd platelet glycoprotein in a patient with prolonged bleeding time. Blood. 1992;79: 1466-1471.
7. Nieuwenhuis HK, Sakariassen KS, Houdijk WP, Nievelstein PF, Sixma JJ. Deficiency of platelet membrane glycoprotein Ia associated with a decreased platelet adhesion to subendothelium: a defect in platelet spreading. Blood. 1986;68:692-695.
8. Saelman EU, Nieuwenhuis HK, Hese KM, de Groot PG, Heijnen HF, Sage EH, Williams S, McKeown L, Gralnick HR, Sixma JJ. Platelet adhesion to collagen types I through VIII under conditions of stasis and flow is mediated by GPIa/ IIa (alpha2 beta1-integrin). Blood. 1994;83: 1244-1250.
9. Henrita van Zanten G, Saelman EU, Schut-Hese KM, Wu YP, Slootweg PJ, Nieuwenhuis HK, de Groot PG, Sixma JJ. Platelet adhesion to collagen type IV under flow conditions. Blood. 1996;88:3862-3871.
10. Nieswandt B, Watson SP. Platelet collagen interaction: is GPVI the central receptor? Blood. 2003;102:449-461.
11. Nieswandt B, Brakebusch C, Bergmeier W, Schulte V, Bouvard D, Mokhtari-Nejad R, Lindhout T, Heemskerk JW, Zirngibl H, Fassler R. Glycoprotein VI but not alpha2beta1 integrin is essential for platelet interaction with collagen. EMBO J. 2001;20:2120-2130.
12. Holtkotter O, Nieswandt B, Smyth N, Muller W, Hafner M, Schulte V, Krieg T, Eckes B. Integrin alpha 2-deficient mice develop normally, are fertile, but display partially defective platelet interaction with collagen. J Biol Chem. 2002;277:10789-10794.
13. Chen J, Diacovo TG, Grenache DG, Santoro SA, Zutter MM. The alpha(2) integrin subunit-deficient mouse: a multifaceted phenotype including defects of branching morphogenesis and hemostasis. Am J Pathol. 2002;161:337-344.
14. Morton LF, Hargreaves PG, Farndale RW, Young RD, Barnes MJ. Integrin alpha 2 beta 1-independent activation of platelets by simple collagen-like peptides: collagen tertiary (triple-helical) and quaternary (polymeric) structures are sufficient alone for alpha 2 beta 1-independent platelet reactivity. Biochem J. 1995;306:337-344.
15. Knight CG, Morton LF, Onley DJ, Peachey AR, Ichinohe T, Okuma M, Farndale RW, Barnes MJ. Collagen-platelet interaction: Gly-Pro-Hyp is uniquely specific for platelet Gp VI and mediates platelet activation by collagen. Cardiovasc Res. 1999;41:450-457.
16. Asselin J, Gibbins JM, Achison M, Lee YH, Morton LF, Farndale RW, Barnes MJ, Watson SP. 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.
17. Barnes MJ, Knight CG, Farndale RW. The use of collagen-based model peptides to investigate platelet-reactive sequences in collagen. Biopolymers. 1996;40:383-397.
18. Verkleij MW, Morton LF, Knight CG, de Groot PG, Barnes MJ, Sixma JJ. Simple collagen-like peptides support platelet adhesion under static but not under flow conditions: interaction via alpha2 beta1 and von Willebrand factor with specific sequences in native collagen is a requirement to resist shear forces. Blood. 1998;91:3808-3816.
19. Moroi M, Jung SM, Shinmyozu K, Tomiyama Y, Ordinas A, Diaz-Ricart M. Analysis of platelet adhesion to a collagen-coated surface under flow conditions: the involvement of glycoprotein VI in the platelet adhesion. Blood. 1996;88:2081-2092.
20. Polanowska-Grabowska R, Gear AR. High-speed platelet adhesion under conditions of rapid flow. Proc Natl Acad Sci U S A. 1992;89:5754-5758.
21. Coller BS, Beer JH, Scudder LE, Steinberg MH. Collagen-platelet interactions: evidence for a direct interaction of collagen with platelet GPIa/IIa and an indirect interaction with platelet GPIIb/IIIa mediated by adhesive proteins. Blood. 1989;74:182-192.
22. Polanowska-Grabowska R, Geanacopoulos M, Gear AR. Platelet adhesion to collagen via the alpha 2 beta 1 integrin under arterial flow conditions causes rapid tyrosine phosphorylation of pp125FAK. Biochem J. 1993;296:543-547.
23. Gear AR. Rapid platelet morphological changes visualized by scanning-electron microscopy: kinetics derived from a quenched-flow approach. Br J Haematol. 1984;56:387-398.
24. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok BA, Connelly PA. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor: study of Lck- and FynT-dependent T cell activation. J Biol Chem. 1996;271:695-701.
25. Achison M, Elton CM, Hargreaves PG, Knight CG, Barnes MJ, Farndale RW. Integrin-independent tyrosine phosphorylation of p125(fak) in human platelets stimulated by collagen. J Biol Chem. 2001;276: 3167-3174.
26. Defilippi P, Olivo C, Venturino M, Dolce L, Silengo L, Tarone G. Actin cytoskeleton organization in response to integrin-mediated adhesion. Microsc Res Tech. 1999;47:67-78.
27. 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.
28. Golden A, Nemeth SP, Brugge JS. Blood platelets express high levels of the pp60c-src-specific tyrosine kinase activity. Proc Natl Acad Sci U S A. 1986;83:852-856.
29. Stenberg PE, Pestina TI, Barrie RJ, Jackson CW. The Src family kinases, Fgr, Fyn, Lck, and Lyn, colocalize with coated membranes in platelets. Blood. 1997;89:2384-2393.
30. Pestina TI, Stenberg PE, Druker BJ, Steward SA, Hutson NK, Barrie RJ, Jackson CW. Identification of the Src family kinases, Lck and Fgr in platelets: their tyrosine phosphorylation status and subcellular distribution compared with other Src family members. Arterioscler Thromb Vasc Biol. 1997;17:3278-3285.
31. Briddon SJ, Watson SP. Evidence for the involvement of p59fyn and p53/561yn in collagen receptor signalling in human platelets. Biochem J. 1999;338:203-209.
32. Kaplan KB, Bibbins KB, Swedlow JR, Arnaud M, Morgan DO, Varmus HE. Association of the amino-terminal half of c-Src with focal adhesions alters their properties and is regulated by phosphorylation of tyrosine 527. EMBO J. 1994;13:4745-4756.
33. Kaplan KB, Swedlow JR, Morgan DO, Varmus HE. c-Src enhances the spreading of src-/- fibroblasts on fibronectin by a kinase-independent mechanism. Genes Dev. 1995;9:1505-1517.
34. Bockholt SM, Burridge K. An examination of focal adhesion formation and tyrosine phosphorylation in fibroblasts isolated from src-, fyn-, and yes- mice. Cell Adhes Commun. 1995;3:91-100.
35. Suzuki-Inoue K, Yatomi Y, Asazuma N, Kainoh M, Tanaka T, Satoh K, Ozaki Y. Rac, a small guanosine triphosphate-binding protein, and p21-activated kinase are activated during platelet spreading on collagen-coated surfaces: roles of integrin alpha(2)beta(1). Blood. 2001;98:3708-3716.
36. Polanowska-Grabowska R, Gear AR. Role of cyclic nucleotides in rapid platelet adhesion to collagen. Blood. 1994;83:2508-2515.
37. Haimovich B, Lipfert L, Brugge JS, Shattil SJ. Tyrosine phosphorylation and cytoskeletal reorganization in platelets are triggered by interaction of integrin receptors with their immobilized ligands. J Biol Chem. 1993; 268:15868-15877.
38. Hers I, Berlanga O, Tiekstra MJ, Kamiguti AS, Theakston RD, Watson SP. Evidence against a direct role of the integrin alpha2beta1 in collagen-induced tyrosine phosphorylation in human platelets. Eur J Biochem. 2000;267:2088-2097.
39. Kamiguti AS, Theakston RD, Watson SP, Bon C, Laing GD, Zuzel M. Distinct contributions of glycoprotein VI and alpha(2)beta(1) integrin to the induction of platelet protein tyrosine phosphorylation and aggregation. Arch Biochem Biophys. 2000;374:356-362.
40. Polanowska-Grabowska R, Gear AR. Activation of protein kinase C is required for the stable attachment of adherent platelets to collagen but is not needed for the initial rapid adhesion under flow conditions. Arterioscler Thromb Vasc Biol. 1999;19:3044-3054.
41. Inoue O, Suzuki-Inoue K, Dean WL, Frampton J, Watson SP. Integrin alpha2beta1 mediates outside-in regulation of platelet spreading on collagen through activation of Src kinases and PLC gamma2. J Cell Biol. 2003;160:769-780.