PDF herunterladen
Thromb Haemost 2005; 93(04): 716-723
DOI: 10.1160/TH04-09-0584
Platelets and Blood Cells
Schattauer GmbH

Glycoprotein VI is associated with GPIb-IX-V on the membrane of resting and activated platelets

Jane F. Arthur
1   Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia
,
Elizabeth E. Gardiner
1   Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia
,
Maria Matzaris
1   Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia
,
Simon G. Taylor
1   Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia
,
Lakshmi Wijeyewickrema
1   Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia
,
Yukio Ozaki
2   Department of Clinical and Laboratory Medicine, Faculty of Medicine, University of Yamanashi, Tamaho, Nakakoma, Yamanashi, Japan
,
Mark L. Kahn
3   Department of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
,
Robert K. Andrews
1   Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia
,
Michael C. Berndt
1   Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia
› InstitutsangabenFinancial support: This study was partly supported by the National Health and Medical Research Council of Australia, and the National Heart Foundation of Australia.
Weitere Informationen

Publikationsverlauf

Received 10. September 2004

Accepted after revision 27. Januar 2005

Publikationsdatum:
14. Dezember 2017 (online)

Auch verfügbar auf
    Lizenzen und Reprints

Summary

The platelet collagen receptor, glycoprotein (GP)VI, initiates platelet aggregation at low shear stress while GPIb-IX-V, which binds von Willebrand factor, elicits platelet aggregation under high shear conditions. To investigate the possibility that GPIb-IX-V and GPVI are associated on the platelet surface, we first ascertained that aggregation induced by a GPVI-specific agonist, collagen-related peptide, like collagen, is markedly cross-blocked by a GPIbα-specific monoclonal antibody, SZ2. Immunoprecipitation of GPIb-IX with anti-GPIbα from the 1% (v/v) Triton-soluble fraction of unstimulated platelets and immunoblot-ting with anti-GPVI demonstrated association between GPIb-IX and GPVI. This association was maintained when platelets were activated by thrombin. Pre-treatment of platelets with methyl-β-cyclodextrin to disrupt lipid rafts did not affect association in resting platelets under these conditions of detergent lysis. The association is also independent of cytoskeletal attachment, since it was unaffected by treatment with N-ethylmaleimide or DNaseI, which dissociate GPIb-IX from filamin and the actin-containing cytoskeleton, respectively. Finally, the association involves an interaction between the ectodomains of GPIbα and GPVI, since soluble fragments of GPIbα (glycocalicin) and GPVI are co-precipitated from the platelet supernatant under conditions where GPVI is shed. A contribution of GPIb-IX-V to GPVI-induced platelet responses, and vice versa, therefore warrants further investigation.

Keywords

Platelet physiology - adhesion molecules - protein function/activity
 

  • References

  • 1 Nieswandt B, Watson SP. Platelet-collagen interaction: is GPVI the central receptor?. Blood 2003; 102: 449-61.
    CrossrefPubMedGoogle Scholar
  • 2 Andrews R, Gardiner E, Shen Y, et al. Platelet interactions in thrombosis. IUBMB Life 2004; 56: 13-8.
    CrossrefPubMedGoogle Scholar
  • 3 Andrews RK, Gardiner EE, Shen Y, et al. Glycoprotein Ib-IX-V. Int J Biochem Cell Biol 2003; 35: 1170-4.
    CrossrefPubMedGoogle Scholar
  • 4 Jackson SP, Nesbitt WS, Kulkarni S. Signaling events underlying thrombus formation. J Thromb Haemost 2003; 1: 1602-12.
    CrossrefPubMedGoogle Scholar
  • 5 Goto S, Tamura N, Handa S. et al. Involvement of glycoprotein VI in platelet thrombus formation on both collagen and von Willebrand factor surfaces under flow conditions. Circulation 2002; 106: 266-72.
    CrossrefPubMedGoogle Scholar
  • 6 Massberg S, Gawaz M, Gruner S. et al. A crucial role of GP VI for platelet recruitment to the injured arterial wall in vivo. J Exp Med 2003; 197: 41-9.
    CrossrefPubMedGoogle Scholar
  • 7 Siljander PRM, Munnix ICA, Smethurst PA. et al. Platelet receptor interplay regulates collagen-induced thrombus formation in flowing human blood. Blood 2004; 103: 1333-41.
    CrossrefPubMedGoogle Scholar
  • 8 Clemetson JM, Polgar J, Magnenat E. et al. The platelet collagen receptor glycoprotein VI is a member of the immunoglobulin superfamily closely related to FcaR and the natural killer receptors. J Biol Chem 1999; 274: 29019-24.
    CrossrefPubMedGoogle Scholar
  • 9 Jandrot-Perrus M, Busfield S, Lagrue AH. 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.
    CrossrefPubMedGoogle Scholar
  • 10 Ruan CG, Du XP, Xi XD. et al. A murine antiglycoprotein Ib complex monoclonal antibody, SZ 2, inhibits platelet aggregation induced by both ristocetin and collagen. Blood 1987; 69: 570-7.
    CrossrefPubMedGoogle Scholar
  • 11 Shen Y, Romo GM, Dong JF. et al. Requirement of leucine-rich repeats of glycoprotein (GP) Ibα for sheardependent and static binding of von Willebrand factor to the platelet membrane GP Ib-IX-V complex. Blood 2000; 95: 903-10.
    CrossrefPubMedGoogle Scholar
  • 12 Moog S, Mangin P, Lenain N. et al. Platelet glycoprotein V binds to collagen and participates in platelet adhesion and aggregation. Blood 2001; 98: 1038-46.
    CrossrefPubMedGoogle Scholar
  • 13 Dormann D, Clemetson JM, Navdaev A. et al. Alboaggregin A activates platelets by a mechanism involving glycoprotein VI as well as glycoprotein Ib. Blood 2001; 97: 929-36.
    CrossrefPubMedGoogle Scholar
  • 14 Bergmeier W, Bouvard D, Eble JA. et al. Rhodocytin (aggretin) activates platelets lacking α2 β1 integrin, glycoprotein VI, and the ligand-binding domain of glycoprotein Ib α. J Biol Chem 2001; 276: 25121-6.
    CrossrefPubMedGoogle Scholar
  • 15 Du X-Y, Magnenat E, Wells TN. et al. Alboluxin, a snake C-type lectin from Trimeresurus albolabris venom is a potent platelet agonist acting via GPIb and GPVI. Thromb Haemost 2002; 87: 692-8.
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 16 Kanaji S, Kanaji T, Furihata K. et al. Convulxin binds to native, human glycoprotein Ib α. J Biol Chem 2003; 278: 39452-60.
    CrossrefPubMedGoogle Scholar
  • 17 Baker J, Griggs RK, Falati S. et al. GPIb potentiates GPVI-induced responses in human platelets. Platelets 2004; 15: 207-14.
    CrossrefPubMedGoogle Scholar
  • 18 Mazurov AV, Vinogradov DV, Vlasik TN. et al. Characterization of an antiglycoprotein Ib monoclonal antibody that specifically inhibits platelet-thrombin interaction. Thromb Res 1991; 62: 673-84.
    CrossrefPubMedGoogle Scholar
  • 19 Shen Y, Dong JF, Romo GM. et al. Functional analysis of the C-terminal flanking sequence of platelet glycoprotein Ib α using canine-human chimeras. Blood 2002; 99: 145-50.
    CrossrefPubMedGoogle Scholar
  • 20 Berndt MC, Du XP, Booth WJ. Ristocetin-dependent reconstitution of binding of von Willebrand factor to purified human platelet membrane glycoprotein Ib- IX complex. Biochemistry 1988; 27: 633-40.
    CrossrefPubMedGoogle Scholar
  • 21 Du X, Fox JE, Pei S. Identification of a binding sequence for the 14–3–3 protein within the cytoplasmic domain of the adhesion receptor, platelet glycoprotein Ibα. J Biol Chem 1996; 271: 7362-7.
    CrossrefPubMedGoogle Scholar
  • 22 Chen H, Locke D, Liu Y. et al. The platelet receptor GPVI mediates both adhesion and signaling responses to collagen in a receptor density-dependent fashion. J Biol Chem 2002; 277: 3011-9.
    CrossrefPubMedGoogle Scholar
  • 23 Berndt MC, Gregory C, Kabral A. et al. Purification and preliminary characterization of the glycoprotein Ib complex in the human platelet membrane. Eur J Biochem 1985; 151: 637-49.
    CrossrefPubMedGoogle Scholar
  • 24 Krissansen GW, Lucas CM, Stomski FC. et al. Blood leukocytes bind platelet glycoprotein (IIb-IIIa)' but do not express the vitronectin receptor. Int Immunol 1990; 2: 267-77.
    CrossrefPubMedGoogle Scholar
  • 25 Ward CM, Andrews RK, Smith I A. et al. Mocarhagin, a novel cobra venom metalloproteinase, cleaves the platelet von Willebrand factor receptor glycoprotein Iba. Identification of the sulfated tyrosine/anionic sequence Tyr-276-Glu-282 of glycoprotein Ib α as a binding site for von Willebrand factor and α -thrombin. Biochemistry 1996; 35: 4929-38.
    CrossrefPubMedGoogle Scholar
  • 26 Morton LF, Hargreaves PG, Farndale RW. et al. Integrin α 2 β 1 -independent activation of platelets by simple collagen-like peptides: collagen tertiary (triplehelical) and quaternary (polymeric) structures are sufficient alone for α 2 β 1 -independent platelet reactivity. Biochem J 1995; 306: 337-44.
    CrossrefPubMedGoogle Scholar
  • 27 Romo GM, Dong JF, Schade AJ. et al. The glycoprotein Ib-IX-V complex is a platelet counterreceptor for P-selectin. J Exp Med 1999; 190: 803-14.
    CrossrefPubMedGoogle Scholar
  • 28 Andrews RK, Kroll MH, Ward CM. et al. Binding of a novel 50-kilodalton alboaggregin from Trimeresurus albolabris and related viper venom proteins to the platelet membrane glycoprotein Ib-IX-V complex. Effect on platelet aggregation and glycoprotein Ib-mediated platelet activation. Biochemistry 1996; 35: 12629-39.
    CrossrefPubMedGoogle Scholar
  • 29 Asselin J, Knight CG, Farndale RW. et al. Monomeric (glycine-proline-hydroxyproline)(10) repeat sequence is a partial agonist of the platelet collagen receptor glycoprotein VI. Biochemical Journal 1999; 339: 413-8.
    CrossrefPubMedGoogle Scholar
  • 30 Modderman PW, Admiraal LG, Sonnenberg A. et al. Glycoproteins V and Ib-IX form a noncovalent complex in the platelet membrane. J Biol Chem 1992; 267: 364-9.
    CrossrefPubMedGoogle Scholar
  • 31 Andrews RK, Suzuki-Inoue K, Tulasne D. et al. Interaction of calmodulin with the cytoplasmic domain of the platelet membrane glycoprotein VI. Blood 2002; 99: 4219-21.
    CrossrefPubMedGoogle Scholar
  • 32 Gardiner EE, Arthur JF, Kahn ML. et al. Regulation of platelet membrane levels of glycoprotein VI by a platelet- derived metalloproteinase. Blood 2004; 104: 3611-17.
    CrossrefPubMedGoogle Scholar
  • 33 Dyson JM, Munday AD, Kong AM. et al. SHIP-2 forms a tetrameric complex with filamin, actin, and GPIb-IX-V: localization of SHIP-2 to the activated platelet actin cytoskeleton. Blood 2003; 102: 940-8.
    CrossrefPubMedGoogle Scholar
  • 34 Locke D, Liu C, Peng X. et al. Fc Rγ -independent signaling by the platelet collagen receptor glycoprotein VI. J Biol Chem 2003; 278: 15441-8.
    CrossrefPubMedGoogle Scholar
  • 35 Andrews RK, Munday AD, Mitchell CA. et al. Interaction of calmodulin with the cytoplasmic domain of the platelet membrane GP Ib-IX-V complex. Blood 2001; 98: 681-7.
    CrossrefPubMedGoogle Scholar
  • 36 Shrimpton CN, Borthakur G, Larrucea S. et al. Localization of the adhesion receptor glycoprotein Ib- IX-V complex to lipid rafts is required for platelet adhesion and activation. J Exp Med 2002; 196: 1057-66.
    CrossrefPubMedGoogle Scholar
  • 37 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: 13576-83.
    CrossrefPubMedGoogle Scholar
  • 38 Fox J. Identification of actin-binding protein as the protein linking the membrane skeleton to glycoproteins on platelet plasma membranes. J Biol Chem 1985; 260: 11970-7.
    CrossrefPubMedGoogle Scholar
  • 39 Ezumi Y, Kodama K, Uchiyama T. et al. Constitutive and functional association of the platelet collagen receptor glycoprotein VI-Fc receptor γ -chain complex with membrane rafts. Blood 2002; 99: 3250-5.
    CrossrefPubMedGoogle Scholar
  • 40 Locke D, Chen H, Liu Y. et al. Lipid rafts orchestrate signaling by the platelet receptor glycoprotein VI. J Biol Chem 2002; 277: 18801-9.
    CrossrefPubMedGoogle Scholar
  • 41 Boylan BB, Chen HH, Rathore V. et al. Anti-GPVI-associated ITP: An acquired platelet disorder caused by autoantibody-mediated clearance of the GPVI/FcRgchain complex from the human platelet surface Blood. 2004; 104: 1350-1355
    PubMedGoogle Scholar
  • 42 Bergmeier W, Burger PC, Piffath CL. et al. Metalloproteinase inhibitors improve the recovery and hemostatic function of in vitro-aged or -injured mouse platelets. Blood 2003; 102: 4229-35.
    CrossrefPubMedGoogle Scholar
  • 43 Kuijpers MJE, Schulte V, Oury C. et al. Facilitating roles of murine platelet glycoprotein Ib and α IIbβ 3 in phosphatidylserine exposure during vWF-collagen-induced thrombus formation. J Physiol (Lond) 2004; 558: 403-415.
    CrossrefPubMedGoogle Scholar
  • 44 Nieswandt B, Bergmeier W, Schulte V. et al. Expression and function of the mouse collagen receptor glycoprotein VI is strictly dependent on its association with the FcRγ chain. J Biol Chem 2000; 275: 23998-4002.
    CrossrefPubMedGoogle Scholar
  • 45 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: 1648-56.
    CrossrefPubMedGoogle Scholar
  • 46 Pike LJ. Lipid rafts: bringing order to chaos. J Lipid Res 2003; 44: 655-67.
    CrossrefPubMedGoogle Scholar
  • 47 Gu M, Xi X, Englund GD. et al. Analysis of the roles of 14–3–3 in the platelet glycoprotein Ib-IX-mediated activation of integrin α IIbβ 3 using a reconstituted mammalian cell expression model. J Cell Biol 1999; 147: 1085-96.
    CrossrefPubMedGoogle Scholar