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

Jane F. Arthur; Elizabeth E. Gardiner; Maria Matzaris; Simon G. Taylor; Lakshmi Wijeyewickrema; Yukio Ozaki; Mark L. Kahn; Robert K. Andrews; Michael C. Berndt

doi:10.1160/TH04-09-0584

Thrombosis and Haemostasis, Table of Contents

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

Authors

Jane F. Arthur

¹Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia
Elizabeth E. Gardiner

¹Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia
Maria Matzaris

¹Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia
Simon G. Taylor

¹Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia
Lakshmi Wijeyewickrema

¹Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia
Yukio Ozaki

²Department of Clinical and Laboratory Medicine, Faculty of Medicine, University of Yamanashi, Tamaho, Nakakoma, Yamanashi, Japan
Mark L. Kahn

³Department of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
Robert K. Andrews

¹Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia
Michael C. Berndt

¹Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia

Abstract

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

Full Text

References

References
1 Nieswandt B, Watson SP. Platelet-collagen interaction: is GPVI the central receptor?. Blood 2003; 102: 449-61.
2 Andrews R, Gardiner E, Shen Y, et al. Platelet interactions in thrombosis. IUBMB Life 2004; 56: 13-8.
3 Andrews RK, Gardiner EE, Shen Y, et al. Glycoprotein Ib-IX-V. Int J Biochem Cell Biol 2003; 35: 1170-4.
4 Jackson SP, Nesbitt WS, Kulkarni S. Signaling events underlying thrombus formation. J Thromb Haemost 2003; 1: 1602-12.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
16 Kanaji S, Kanaji T, Furihata K. et al. Convulxin binds to native, human glycoprotein Ib α. J Biol Chem 2003; 278: 39452-60.
17 Baker J, Griggs RK, Falati S. et al. GPIb potentiates GPVI-induced responses in human platelets. Platelets 2004; 15: 207-14.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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
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.
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.
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.
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.
46 Pike LJ. Lipid rafts: bringing order to chaos. J Lipid Res 2003; 44: 655-67.
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.