Thromb Haemost 2001; 86(01): 276-288
DOI: 10.1055/s-0037-1616225
Research Article
Schattauer GmbH

The Role of ITAM- and ITIM-coupled Receptors in Platelet Activation by Collagen

Steve P. Watson
1   Departments of Pharmacology, John Radcliffe Hospital, Oxford, UK
,
Naoki Asazuma2
,
Ben Atkinson
,
Oscar Berlanga
,
Denise Best
,
Regis Bobe
,
Gavin Jarvis
,
Stuart Marshall
,
Daniel Snell
,
Margaret Stafford
4   Institute of Molecular Medicine, John Radcliffe Hospital, Oxford, UK
,
David Tulasne
,
Jonathan Wilde
,
Peter Wonerow
,
Jon Frampton
4   Institute of Molecular Medicine, John Radcliffe Hospital, Oxford, UK
› Author Affiliations
Further Information

Publication History

Publication Date:
12 December 2017 (online)

Summary

The major activation-inducing collagen receptor glycoprotein VI (GPVI) has been cloned within the last two years. It is a member of the Ig superfamily of proteins and is constitutively associated with the ITAM-bearing Fc receptor γ-chain (FcR γ-chain). GPVI signals through a pathway that involves several of the proteins used by Fc, B- and T-lymphocyte receptors and which takes place in glycolipid-enriched membrane domains in the plasma membrane known as GEMs. Responses to GPVI are regulated by PECAM-1 (CD31) and possibly other ITIM-bearing receptors. Despite a pivotal role for GPVI, there are important differences between signalling events to collagen and GPVI-specific ligands. This may reflect a role for co-receptors in the response to collagen.

2 Present address: Department of Clinical and Laboratory Medicine, Yamanashi Medical College, Shimokato 1110, Tamaho, Nakakoma, Yamanashi 409-38, Japan


 
  • References

  • 1 Jung SM, Moroi M. Signal-transducing mechanisms involved in activation of the platelet collagen receptor integrin alpha(2)beta(1). J Biol Chem 2000; 275: 8016-26.
  • 2 Watson SP, Berlanga O, Best D, Frampton J. Update on collagen receptors: is the two-site, two-state model still valid?. Platelets 2000; 11: 252-9.
  • 3 Sixma JJ, van Zanten GH, Saelman EUM, Verkleji M, Lankhof H, Nieuwenhuis HK. et al. Platelet adhesion to collagen. Thromb Haemost 1995; 74: 454-9.
  • 4 Sixma JJ, van Zanten GH, Huizinga EG, van der Plas RM, Verkley M, Wu Y-P. et al. Platelet adhesion to collagen: an update. Thromb Haemost 1997; 78: 434-8.
  • 5 Watson SP, Gibbins J. Collagen receptor signalling in platelets: extending the role of the ITAM. Immunol. Today 1998; 19: 260-5.
  • 6 Barnes MJ, Knight CG, Farndale RW. Collagens and atherosclerosis: cell-collagen interaction. Elsevier Science; 1998: 299-306.
  • 7 Barnes MJ, Knight G, Farndale RD. The collagen-platelet interaction. Curr Opin Hemat 1998; 5: 314-20.
  • 8 Alberio L, Dale GL. Platelet-collagen interactions: membrane receptors and intracellular signalling pathways. Eur J Clin Invest 1999; 29: 1066-76.
  • 9 Watson SP. Collagen receptor signalling in platelets and megakaryocytes. Thromb Haemost 1999; 82: 365-76.
  • 10 Verkleji M, Saelman E, Gralnick HR, van Zanten H, Ijsseldijk M, Niewenhuis HK. et al. Glycoprotein Ia/IIa has a role in platelet adhesion to surfaces for which it is not a receptor. Thromb Haemost 1995; 73: 1202a (abstr).
  • 11 Nieswandt B, Bergmeier W, Schulte V, Rackerbrandt K, Gessner JE, Zirngibi H. Expression and function of the mouse collagen receptor GPVI is strictly dependent on its association with the FcRgamma-chain. J Biol Chem 2000; 31: 23998-4002.
  • 12 Tsuji M, Ezumi Y, Arai M, Takayama H. A novel association of Fc receptor γ-chain with glycoprotein VI and their co-expression as a collagen receptor in human platelets. J Biol Chem 1997; 272: 23528-31.
  • 13 Kunicki TJ. Platelet antigen polymorphisms. American Society of Hematology Education Program Book 2000 pp 222-8.
  • 14 Asselin J, Gibbins JM, Achison M, Lee Y-H, Morton LF, Farndale RW. et al. A collagen-like peptide stimulates tyrosine phosphorylation of syk and phospholipase Cγ2 in platelets independent of the integrin 2 1. Blood 1997; 89: 1235-42.
  • 15 Polgar J, Clemetson JM, Kehrel BE, Wiedemann M, Magnenat EM, Well TNC. 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: 13576-83.
  • 16 Jandrot-Perrus M, Lagrue A-H, Okuma M, Bon C. Adhesion and activation of human platelets induced by convulxin involves glycoprotein GI and integrin 2 1. J Biol Chem 1997; 272: 27035-41.
  • 17 Schulte V, Snell D, Bermeier W, Zirngibl H, Watson SP, Nieswandt B. Evidence for two distinct epitopes within collagen for activation of murine platelets. J Biol Chem 2001; 276: 364-8.
  • 18 Clemetson JM, Polgar J, Magnenat E, Wells TNC, Clemetson KJ. The platelet collagen receptor glycoprotein VI is a member of the immunoglobulin superfamily closely related to Fc R and the natural killer receptors. J Biol Chem 1999; 274: 29019-24.
  • 19 Jandrot-Perrus M, Busfield S, Lagrue A-H, Xiong X, Debili N, Chickering T. et al. Cloning, characterization, and functional studies of human and mouse glycoprotein VI: a platelet-specific collagen receptor from the immunoglobulin superfamily. Blood 2000; 96: 1798-807.
  • 20 Ezumi Y, Uchiyama T, Takayama H. Molecular cloning, genomic structure, chromosomal localization and alternative splice forms of the platelet collagen receptor glycoprotein VI. Biochem Biophys Res Commun 2000; 277: 27-36.
  • 21 Berlanga O, Bobe R, Becker M, Murphy G, Leduc M, Bon C. et al. Expression of the collagen receptor glycoprotein VI during megakaryocyte differentiation. Blood 2000; 96: 2740-5.
  • 22 Miura Y, Ohnuma M, Jung SM, Moroi M. Cloning and expression of the platelet-specific collagen receptor glycoprotein VI. Thromb Res 2000; 98: 301-9.
  • 23 Berlanga O, Tulasne D, Snell DC, Leduc M, Bon C, Moroi M. et al. Reconstitution of the GPVI signalling cascade in K562 and COS7 cells. Thromb Haemost. 2001 (Abstr cited in the CDROM of abstracts of the XVIIIth Congress of the ISTH).
  • 24 Myung PS, Boerthe NJ, Koretzky GA. Adapter proteins in lymphocyte antigen-receptor signaling. Curr Opin Immunol 2000; 12: 256-66.
  • 25 Tomlinson MG, Lin J, Weiss A. Lymphocytes with a complex: adapter proteins in antigen signaling. Immunology Today 2000; 21: 584-91.
  • 26 Pasquet JM, Gross B, Quek L, Asazuma N, Zhang W, Sommers CL. et al. LAT is required for tyrosine phosphorylation of phospholipase C gamma2 and platelet activation by the collagen receptor GPVI. Mol Cell Biol 1999; 19: 8326-34.
  • 27 Clements JL, Lee JR, Gross B, Yang B, Olson JD, Sandra A. et al. Fetal hemorrhage and platelet dysfunction in SLP-76-deficient mice. J Clin Invest 1999; 103: 19-25.
  • 28 Gross B, Lee JR, Clements JL, Turner M, Tybulewicz VLJ, Findell PR. et al. Tyrosine phosphorylation of SLP-76 is downstream of Syk following stimulation of the collagen receptor GPVI in platelets. J Biol Chem 1999; 274: 5963-71.
  • 29 Falet H, Barkalow KL, Pivniouk VI, Barnes MJ, Geha RS, Hartwig JH. Roles of SLP-76, phosphoinositide 3-kinase, and gelsolin in the platelet shape changes initiated by the collagen receptor GPVI/FcRgamma-chain complex. Blood 2000; 96: 3786-92.
  • 30 Asazuma N, Wilde JI, Berlanga O, Leduc M, Leo A, Schweighoffer E. et al. Interaction of linker for activation of T cells with multiple adapter proteins in platelets activated by the glycoprotein VI-selective ligand, convulxin. J Biol Chem 2000; 275: 33427-34.
  • 31 Ezumi Y, Shindoh K, Tsuji M, Takayama H. Physical and functional association of the Src family kinases Fyn and Lyn with the collagen receptor Glycoprotein VI-Fc receptorchain complex on human platelets. J Exp Med 1998; 188: 267-76.
  • 32 Quek LS, Pasquet JM, Hers I, Cornall R, Knight CG, Barnes M. et al. Fyn and Lyn are essential for maintaining the balance of activation and inactivation by the collagen receptor glycoprotein VI in platelets. Blood 2000; 96: 4246-53.
  • 33 Briddon SJ, Watson SP. Evidence for the involvement of p59fyn and p53/56lyn in signalling via the collagen receptor in human platelets. Biochem J 1998; 337: 203-9.
  • 34 Gross BS, Melford SK, Watson SP. Evidence that phospholipase C-γ2 interacts with SLP-76, Syk, LAT, Lyn and the FcR γ-chain after stimulation of the collagen receptor glycoprotein VI in human platelets. Eur J Biochem 1999; 263: 612-23.
  • 35 Schaeffer EM, Schwartzberg PL. Tec family kinases in lymphocyte signaling and function. Curr Opin Immunol 2000; 12: 282-8.
  • 36 Quek LS, Bolen J, Watson SP. Regulation of Bruton’s tyrosine kinase and phospholipase Cγ2 in collagen-stimulated platelets. Curr Biol 1998; 8: 1137-40.
  • 37 Oda A, Ikeda Y, Ochs HD, Druker BJ, Ozaki K, Handa M. et al. Rapid tyrosine phosphorylation and activation of Bruton’s tyrosine/Tec kinases in platelets induced by collagen binding or CD32 cross-linking. Blood 2000; 95: 1663-70.
  • 38 Pasquet JM, Quek L, Stevens C, Bobe R, Huber M, Duronio V. et al. Phosphatidylinositol 3,4,5-trisphosphate regulates Ca(2+) entry via Btk in platelets and megakaryocytes without increasing phospholipase C activity. Embo J 2000; 19: 2793-802.
  • 39 Pasquet JM, Bobe R, Gross B, Gratacap MP, Tomlinson MG, Payrastre B. et al. A collagen-related peptide regulates phospholipase Cgamma2 via phosphatidylinositol 3-kinase in human platelets. Biochem J 1999; 342: 171-7.
  • 40 Gratacap M-P, Payrastre B, Viala C, Mauco G, Plantavid M, Chap H. Phosphatidylinositol 3,4,5-trisphosphate-dependent stimulation of phospholipase C- 2 is an early key event in Fc RIIA-mediated activation of human platelets. J Biol Chem 1998; 273: 24314-21.
  • 41 Bobe R, Wilde JI, Maschberger P, Venketeswarlu K, Cullen PJ, Siess W. et al. Phosphatidylinositol 3-kinase-dependent translocation of phospholipase Cγ2 in mouse megakaryocytes is independent of Bruton’s tyrosine kinase translocation. Blood 2001; 97: 678-84.
  • 42 Pasquet JM, Gross BS, Gratacap MP, Quek L, Pasquet S, Payrastre B. et al. Thrombopoietin potentiates collagen receptor signaling in platelets through a phosphatidylinositol 3-kinase-dependent pathway. Blood 2000; 95: 3429-34.
  • 43 Wang D, Feng J, Wen R, Marine JC, Sangster MY, Parganas E. et al. Phospholipase Cgamma2 is essential in the functions of B cell and several Fc receptors. Immunity 2000; 13: 25-35.
  • 44 Blake RA, Schieven GL, Watson SP. Collagen stimulates tyrosine phosphorylation of phospholipase C- 2 but not phospholipase C- 1 in human platelets. FEBS Letts 1994; 353: 212-6.
  • 45 Wilde J, Watson SP. Regulation of phospholipase C isoforms in haematopoietic cells: why one, not the other?. Cellular Signal. 2001 in press.
  • 46 Kim HK, J. W. K Zilberstein A, Margolis B, Kim JG, Schlessinger J. et al. PDGF stimulation of inositol phospholipid hydrolysis requires PLC 1 phosphorylation on tyrosine residues 783 and 1254. Cell 1991; 65: 435-41.
  • 47 Irvin BJ, Williams BL, Nilson AE, Maynor HO, Abraham RT. Pleiotropic contributions of phospholipase C- 1 (PLC- 1) to T-cell antigen receptor-mediated signaling: reconstitution studies of a PLC- 1-deficient Jurkat T-cell line. Mol Cell Biol 2000; 20: 9149-61.
  • 48 Gross BS, Wilde JI, Quek L, Chapel H, Nelson DL, Watson SP. Regulation and function of WASp in platelets by the collagen receptor, glycoprotein VI. Blood 1999; 94: 4166-76.
  • 49 Doody GM, Billadeau DD, Clayton E, Hutichings A, Berland R, McAdam S. et al. Vav-2 controls NFAT-dependent transcription inB- but not Tlymphocytes. EMBO J 2000; 19: 6173-84.
  • 50 Ozaki K, Oda A, Wakao H, Rhodes J, Druker B, Ishida A. et al. Thrombopoietin induces association of Crkl with STAT5 but not STAT3 in human platelets. Blood 1998; 92: 4652-62.
  • 51 Best D, Pasquet S, Littlewood TJ, Brunskill SJ, Pallister CJ, Watson SP. Platelet activation via the collagen receptor GPVI is not altered in platelets from CML patients despite the presence of the constitutively phosphorylated adapter protein CrkL. Br J Haematol 2001; 112: 609-16.
  • 52 Langlet C, Bernard AM, Drevot P, He HT. Membrane rafts and signaling by the multichain immune recognition receptors. Curr Opin Immunol 2000; 12: 250-5.
  • 53 Brdicka T, Pavlistova D, Leo A, Bruyns E, Korinek V, Angelisova P. et al. Phosphoprotein associated with glycosphingolipid-enriched microdomains (PAG), a novel ubiquitously expressed transmembrane adaptor protein, binds the protein tyrosine kinase csk and is involved in regulation of T cell activation. J Exp Med 2000; 191: 1591-604.
  • 54 Kawabuchi M, Satomi Y, Takao T, Shimonishi Y, Nada S, Nagai K. et al. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature 2000; 404: 999-1003.
  • 55 Hirao A, Hamaguchi I, Suda T, Yamaguchi N. Translocation of the csk homologous kinase (Chk/Hyl) controls activity of CD36-anchored Lyn tyrosine kinase in thrombin-stimulated platelets. EMBO J 1997; 16: 2342-51.
  • 56 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: 2088-97.
  • 57 Niedergang F, Alcover A, Knight CG, Farndale RW, Barnes MJ, Francischetti IMB. et al. Convulxin binding to platelet receptor GPVI: competition with collagen related peptides. Biochem Biophys Res Commun 2000; 273: 246-50.
  • 58 Poole A, Gibbins JM, Turner M, van Vugt M, van de Winkel J, Saito T. et al. The Fc receptor γ-chain and the tyrosine kinase Syk are essential for activation of mouse platelets by collagen. EMBO J 1997; 16: 2333-41.
  • 59 Ichinohe T, Takayama H, Ezumi Y, Arai M, Yamamoto N, Takahasi H. et al. Collagen-stimulated activation of Syk but not c-Src is severely compromised in human platelets lacking membrane glycoprotein VI. J Biol Chem 1997; 272: 63-8.
  • 60 Kehrel B, Wierwille S, Clemetson KJ, Anders O, Steiner M, Knight CG. et al. Glycoprotein VI is a major collagen receptor for platelet activation: it recognizes the platelet activating quaternary structure of collagen, whereas CD36, glycoprotein IIb/IIIa, and von Willebrand factor do not. Blood 1998; 91: 491-9.
  • 61 Knight CG, Morton LF, Peachey AR, Tuckwell DS, Farndale RW, Barnes MJ. The collagen-binding A-domains of integrins α1β1 and α2β1 recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. J Biol Chem 2000; 275: 35-40.
  • 62 Hers I, Berlanga O, Tiekstra MJ, Kamiguti AS, Theakston DG, Watson SP. Evidence against a direct role of the integrin α2β1 in collagen-induced tyrosine phosphorylation in human platelets. Eur J Biochem 2000; 267: 2088-97.
  • 63 Jung SM, Moroi M. Platelets interact with soluble and insoluble collagens through characteristically different reactions. J Biol Chem 1998; 273: 14827-37.
  • 64 Inoue K, Ozaki Y, Satoh K, Wu Y, Yatomi Y, Shin Y. et al. Signal transduction pathways mediated by glycoprotein la/lla in human platelets: comparison with those of glycoprotein VI. Biochem Biophys Res Commun 1999; 256: 114-20.
  • 65 Inoue K, Ozaki YTO, Wu Y, Yatomi Y, Satoh K. et al. Rhodocytin induces platelet aggregation, by interacting with glycoprotein Ia/IIa: involvement of GPIa/IIa-associated Src family kinases and protein tyrosine phosphorylation. J Biol Chem 2001; 276: 1643-52.
  • 66 Eble JA, Beermann B, Hinz H-J, Schmidt-Hederich A. α2β1 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 in press.
  • 67 Huang M-M, Bolen JB, Barnwell JW, Shattil SJ, Brugge JS. Membrane glycoprotien IC (CD36) is physically associated with the Fyn, Lyn, and Yes protein-tyrosine kinases in human platelets. Proc Natl Acad Sci USA 1991; 88: 7844-8.
  • 68 Dorahy DJ, Burns GF. Active Lyn protein tyrosine kinase is selectively enriched within membrane microdomains of resting platelets. Biochem J 1998; 333: 373-9.
  • 69 Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Brouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 2000; 6: 41-8.
  • 70 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: 514-21.
  • 71 Chiang TM, Kang AH. A synthetic peptide derived from the sequence of a type I collagen receptor inhibits type I collagen-mediated platelet aggregation. J Clin Invest 1997; 100: 2079-84.
  • 72 Monnet E, Fauvel-Lafeve F. A New Platelet Receptor Specific to Type III Collagen. Type III collagen-binding protein. J Biol Chem 2000; 275: 10912-7.
  • 73 Ravetch JV, Lanier LL. Immune inhibitory receptors. Science 2000; 290: 84-9.
  • 74 Rezaei E, Quek L, Watson SP. A novel inhibitory action of wheat germ agglutinin on phospholipase C in HEL and MEG-01 cells lines. Biochem Biophys Acta 1996; 1356: 101-10.
  • 75 Jackson DE, Kupcho KR, Newman PJ. Characterization of phosphotyro-sine binding motifs in the cytoplasmic domain of platelet/endothelial cell adhesion molecule-1 (PECAM-1) that are required for the cellular association and activation of the protein-tyrosine phosphatase, SHP-2. J Biol Chem 1997; 272: 24868-75.
  • 76 Jackson DE, Ward CM, Wang R, Newman PJ. The protein-tyrosine phosphatase SHP-2 binds PECAM-1 and forms a distinct signaling complex during platelet aggregation. Evidence for a mechanistic link between PECAM-1 and integrin-mediated cellulary signaling. J Biol Chem 1997; 272: 6986-93.
  • 77 Edmead CE. Thrombin-induced association of SHP-2 with multiple tyro-sine-phosphorylated proteins in human platelets. FEBS Letts 1999; 459: 27-32.
  • 78 Cicmil M, Thomas JM, Sage T, Barry FA, Leduc M, Bon C. et al. Collagen, convulxin, and thrombin stimulate aggregation-independent tyrosine phosphorylation of CD31 in tlatelets: evidence for the involvment of Src family kinases. J Biol Chem 2000; 275: 27339-47.
  • 79 Newman PJ. The biology of PECAM-1. J Clin Invest 1997; 99: 3-20.
  • 80 Varon D, Jackson DE, Shenkman B, Dardik R, Tamarin I, Savion N. et al. Platelet/endothelial cell adhesion molecule-1 serves as a costimulatory agonist receptor that modulates integrin-dependent adhesion and aggregation of human platelets. Blood 1998; 91: 500-7.
  • 81 Cicmil M, Thomas JM, Sage T, Barry FA, Gibbins JM. PECAM-1: a negative regulator of platelet activation?. Blood 2000; 96: 1921a (abstr).
  • 82 Vollmar B, Schmits R, Kunz D, Menger MD. Lack of in vivo function of CD31 in vascular thrombosis. Thromb Haemost 2001; 85: 160-4.
  • 83 Patil S, Newman DK, Newman PJ. PECAM-1 serves as an inhibitory receptor that modulates platelet responses to collagen. Blood 2001; 97: 1727-32.
  • 84 Snell D, Pasquet J-M, Watson SP. ITIM-bearing receptors in platelets. In: Cooper MD, Takai T, Ravetch JV. eds. Tokyo: Springer-Verlag; 2001. in Press.
  • 85 Kubagawa H, Burrows PD, Cooper MD. A novel pair of immunoglobulin-like receptors expressed by B cells and myeloid cells. Proc Natl Acad Sci USA 1997; 94: 5261-6.
  • 86 Kubagawa H, Cheng C-C, Ho L-H, Shimada T, Gartland L, Mashburn C. et al. Biochemical nature and cellular distribution of the paired immunoglobulin-like receptors, PIR-A and PIR-B. J Exp Med 1999; 189: 309-17.
  • 87 Pasquet JM, Quek L, Pasquet S, Poole A, Matthews JR, Lowell C. et al. Evidence of a Role for SHP-1 in Platelet Activation by the Collagen Receptor Glycoprotein VI. J Biol Chem 2000; 275: 28526-31.
  • 88 Muraille E, Pesesse X, Kuntz C, Erneux C. Distribution of the Src-homo-logy-2-domain-containing inositol 5-phosphatase SHIP-2 in both nonhaemopoietic and haemopoietic cells and possible involvement of SHIP-2 in negative signalling of B-cells. Biochem J 1999; 342: 697-705.
  • 89 Bruhns P, Vely F, Malbec O, Fridman WH, Vivier E, Daeron M. Molecular Basis of the Recruitment of the SH2 Domain-containing Inositol 5-Phosphatases SHIP1 and SHIP2 by Fcgamma RIIB. J Biol Chem 2000; 275: 37357-64.
  • 90 Falati S, Edmead CE, Poole AW. Glycoprotein Ib-V-IX, a receptor for von Willebrand factor, couples physically and functionally to the Fc receptor γ-chain, Fyn, and Lyn to activate human platelets. Blood 1999; 94: 1-10.
  • 91 Asazuma N, Marshall SJ, Berlanga O, Snell D, Poole AW, Berndt MC. et al. The snake venom toxin alboaggregin A activates GPVI. Blood. 2001 in press.
  • 92 Marshall SJ, Asazuma N, Wonerow P, Andrews R. P. WS. Glycoprotein Ib-IX-V promotes phosphorylation of the Fc receptor gamma-chain, Syk and phospholipase C gamma-2 through activation of tyrosine kinases in human platelets. Thromb Haemost. 2001 (Abstr. cited in the CDROM of abstracts of the VIIIth Congress of the ISTH).
  • 93 Cowan KJ, Law DA, Phillips DR. Identification of Shc as the primary protein binding to the tyrosine-phosphorylated beta 3 Subunit of alpha IIbbeta 3 during outside-in integrin platelet signaling. J Biol Chem 2000; 275: 36423-9.
  • 94 Dorahy DJ, Thorne RF, Fecondo JV, Burns GF. Stimulation of platelet activation and aggregation by a carboxyl-terminal peptide from thrombospondin binding to the integrin-associated protein receptor. J Biol Chem 1997; 272: 1323-30.
  • 95 Alberio L, Dale GL. Flow cytometric analysis of platelet activation by different collagen types present in the vessel wall. Br J Haematol 1998; 103: 1212-8.
  • 96 Zheng YM, Liu C, Chen H, Locke D, Ryan JC, Kahn Ml. Expression of the platelet receptor GPVI confers signaling via the FC receptor gamma chain in response to the snake venom convulxin but not to collagen. J Biol Chem. 2001 in press.