Focusing on plasma glycoprotein VI

Thrombosis and Haemostasis

Volumn 107, Issue 4, 2012, Pages 648-655

  Al Tamimi, Mohammad ^a   Arthur, Jane F ^a   Gardiner, Elizabeth E ^a   Andrews, Robert K ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Glycoprotein VI; Platelets; Shedding; Thrombocytopenia; Thrombosis

Indexed keywords

ADAM10 ENDOPEPTIDASE; AUTOANTIBODY; C REACTIVE PROTEIN; CALMODULIN INHIBITOR; COLLAGEN; GLYCOCALICIN; GLYCOPROTEIN VI; METALLOPROTEINASE; N ETHYLMALEIMIDE; PHOSPHOLIPASE C GAMMA; PROTEIN KINASE C; PROTEIN KINASE C ACTIVATOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; THROMBOCYTE RECEPTOR; VON WILLEBRAND FACTOR;

ATHEROSCLEROSIS; AUTOIMMUNE DISEASE; BLOOD CLOTTING; BLOOD CLOTTING DISORDER; HEMOSTASIS; HUMAN; METASTASIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; STROKE; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE COUNT; THROMBOCYTOPATHY; THROMBOCYTOPENIA; THROMBOGENESIS;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; ARTHRITIS, RHEUMATOID; ATHEROSCLEROSIS; BLOOD COAGULATION; BLOOD PLATELETS; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; LIGANDS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NEOPLASM METASTASIS; PLATELET MEMBRANE GLYCOPROTEINS; PROTEIN BINDING; THROMBOCYTOPENIA; THROMBOSIS;

EID: 84859312878     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/th11-10-0745     Document Type: Review

References (89)

1. Fong KP, Barry C, Tran AN, et al. Deciphering the human platelet sheddome. Blood 2011; 117: 15-26.
2. Gardiner EE, Karunakaran D, Shen Y, et al. Controlled shedding of platelet glycoprotein (GP)VI and GPIb-IX-V by ADAM family metalloproteinases. J Thromb Haemost 2007; 5: 1530-1537.
3. Gardiner EE, Karunakaran D, Arthur JF, et al. Dual ITAM-mediated proteolytic pathways for irreversible inactivation of platelet receptors: de-ITAM-izing FcγRIIa. Blood 2008; 111: 165-174.
4. Al-Tamimi M, Mu FT, Moroi M, et al. Measuring soluble platelet glycoprotein VI in human plasma by ELISA. Platelets 2009; 20: 143-149.
5. Bigalke B, Potz O, Kremmer E, et al. Sandwich immunoassay for soluble glycoprotein VI in patients with symptomatic coronary artery disease. Clin Chem 2011; 57: 898-904.
6. Laske C, Leyhe T, Stransky E, et al. Association of platelet-derived soluble glycoprotein VI in plasma with Alzheimer's disease. J Psychiatr Res 2008; 42: 746-751.
7. Ungerer M, Rosport K, Bultmann A, et al. Novel antiplatelet drug Revacept (dimeric glycoprotein VI-Fc) specifically and efficiently inhibited collagen-induced platelet aggregation without affecting general hemostasis in humans. Circulation 2011; 123: 1891-1899.
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 FcαR and the natural killer receptors. J Biol Chem 1999; 274: 29019-29024.
9. Arthur JF, Gardiner EE, Matzaris M, et al. Glycoprotein VI is associated with GPIb-IX-V on the membrane of resting and activated platelets. Thromb Haemost 2005; 93: 716-723.
10. Andrews R, Berndt M, Lopez J. The glycoprotein Ib-IX-V complex. In: Michelson AD, ed Platelets (ed 2nd edition) San Diego, CA: Academic Press 2006: pp. 145-164.
11. Nieswandt B, Watson SP. Platelet-collagen interaction: is GPVI the central receptor? Blood 2003; 102: 449-461.
12. Bergmeier W, Hynes RO. Extracellular matrix proteins in hemostasis and thrombosis. Cold Spring Harb Perspect Biol 2011.
13. Jung SM, Moroi M. Platelet glycoprotein VI. Adv Exp Med Biol 2008; 640: 53-63.
14. Inoue O, Suzuki-Inoue K, McCarty OJ, et al. Laminin stimulates spreading of platelets through integrin α6β1-dependent activation of GPVI. Blood 2006; 107: 1405-1412.
15. Schmaier AA, Zou Z, Kazlauskas A, et al. Molecular priming of Lyn by GPVI enables an immune receptor to adopt a hemostatic role. Proc Natl Acad Sci USA 2009; 106: 21167-21172.
16. Wu Y, Suzuki-Inoue K, Satoh K, et al. Role of Fc receptor γ-chain in platelet glycoprotein Ib-mediated signaling. Blood 2001; 97: 3836-3845.
17. Canobbio I, Bertoni A, Lova P, et al. Platelet activation by von Willebrand factor requires coordinated signaling through thromboxane A2 and FcγIIA receptor. J Biol Chem 2001; 276: 26022-26029.
18. Gardiner EE, Arthur JF, Shen Y, et al. GPIbα-selective activation of platelets induces platelet signaling events comparable to GPVI activation events. Platelets 2010; 21: 244-252.
19. Arthur JF, Shen Y, Gardiner EE, et al. TNF Receptor-Associated Factor 4 (TRAF4) is a novel binding partner of glycoprotein Ib and glycoprotein VI in human platelets. J Thromb Haemost 2011; 9: 163-172.
20. Arthur JF, Gardiner EE, Kenny D, et al. Platelet receptor redox regulation. Platelets 2008; 19: 1-8.
21. Joutsi-Korhonen L, Smethurst PA, Rankin A, et al. The low-frequency allele of the platelet collagen signaling receptor glycoprotein VI is associated with reduced functional responses and expression. Blood 2003; 101: 4372-4379.
22. Bray PF, Howard TD, Vittinghoff E, et al. Effect of genetic variations in platelet glycoproteins Ibα and VI on the risk for coronary heart disease events in postmenopausal women taking hormone therapy. Blood 2007; 109: 1862-1869.
23. Trifiro E, Williams SA, Cheli Y, et al. The low-frequency isoform of platelet glycoprotein VIb attenuates ligand-mediated signal transduction but not receptor expression or ligand binding. Blood 2009; 114: 1893-1899.
24. Crockett J, Newman DK, Newman PJ. PECAM-1 is a negative regulator of laminin- induced platelet activation. J Thromb Haemost 2010; 8: 1584-1593.
25. Jones CI, Garner SF, Moraes LA, et al. PECAM-1 expression and activity negatively regulate multiple platelet signaling pathways. FEBS Lett 2009; 583: 3618-3624.
26. Rivera J, Lozano ML, Navarro-Nunez L, et al. Platelet receptors and signaling in the dynamics of thrombus formation. Haematologica 2009; 94: 700-711.
27. Bergmeier W, Rabie T, Strehl A, et al. GPVI down-regulation in murine platelets through metalloproteinase-dependent shedding. Thromb Haemost 2004; 91: 951-958.
28. Rabie T, Varga-Szabo D, Bender M, et al. Diverging signaling events control the pathway of GPVI down-regulation in vivo. Blood 2007; 110: 529-535.
29. Takayama H, Hosaka Y, Nakayama K, et al. A novel antiplatelet antibody therapy that induces cAMP-dependent endocytosis of the GPVI/Fc receptor γ-chain complex. J Clin Invest 2008; 118: 1785-1795.
30. Andrews RK, Karunakaran D, Gardiner EE, et al. Platelet receptor proteolysis: a mechanism for downregulating platelet reactivity. Arterioscler Thromb Vasc Biol 2007; 27: 1511-1520.
31. Bigalke B, Elvers M, Schonberger T, et al. Platelet and Soluble Glycoprotein VI - Novel Applications in Diagnosis and Therapy. Curr Drug Targets 2011; 12: 1821-1830.
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: 3611-3617.
33. Stephens G, Yan Y, Jandrot-Perrus M, et al. Platelet activation induces metalloproteinase- dependent GPVI cleavage to down-regulate platelet reactivity to collagen. Blood 2005; 105: 186-191.
34. Dunkley S, Arthur JF, Evans S, et al. A familial platelet function disorder associated with abnormal signalling through the glycoprotein VI pathway. Br J Haematol 2007; 137: 569-577.
35. 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: 4229-4235.
36. Aktas B, Pozgajova M, Bergmeier W, et al. Aspirin induces platelet receptor shedding via ADAM17 (TACE). J Biol Chem 2005; 280: 39716-39722.
37. Al-Tamimi M, Grigoriadis G, Tran H, et al. Coagulation-induced shedding of platelet glycoprotein VI mediated by factor Xa. Blood 2011; 117: 3912-3920.
38. Bender M, Hofmann S, Stegner D, et al. Differentially regulated GPVI ectodomain shedding by multiple platelet-expressed proteinases. Blood 2010; 116: 3347-3355.
39. Black RA, Rauch CT, Kozlosky CJ, et al. A metalloproteinase disintegrin that releases tumour-necrosis factor-α from cells. Nature 1997; 385: 729-733.
40. Scott AJ, O'Dea KP, O'Callaghan D, et al. Reactive oxygen species and p38 mitogen- activated protein kinase mediate tumor necrosis factor α-converting enzyme (TACE/ADAM-17) activation in primary human monocytes. J Biol Chem 2011; 286: 35466-35476.
41. Schoenwaelder SM, Jarman KE, Gardiner EE, et al. Bcl-xL-inhibitory BH3 mimetics can induce a transient thrombocytopathy that undermines the hemostatic function of platelets. Blood 2011; 118: 1663-1674.
42. Gardiner EE, Thom JY, Al-Tamimi M, et al. Restored platelet function after romiplostim treatment in a patient with immune thrombocytopenic purpura. Br J Haematol 2010; 149: 625-628.
43. Gardiner EE, Al-Tamimi M, Mu FT, et al. Compromised ITAM-based platelet receptor function in a patient with immune thrombocytopenic purpura. J Thromb Haemost 2008; 6: 1175-1182.
44. Massberg S, Gawaz M, Gruner S, et al. A crucial role of glycoprotein VI for platelet recruitment to the injured arterial wall in vivo. J Exp Med 2003; 197: 41-49.
45. Nieswandt B, Schulte V, Bergmeier W, et al. Long-term antithrombotic protection by in vivo depletion of platelet glycoprotein VI in mice. J Exp Med 2001; 193: 459-469.
46. Nurden P, Tandon N, Takizawa H, et al. An acquired inhibitor to the GPVI platelet collagen receptor in a patient with lupus nephritis. J Thromb Haemost 2009; 7: 1541-1549.
47. Al-Tamimi M, Mu FT, Arthur JF, et al. Anti-glycoprotein VI monoclonal antibodies directly aggregate platelets independently of FcγRIIa and induce GPVI ectodomain shedding. Platelets 2009; 20: 75-82.
48. Arthur JF, Dunkley S, Andrews RK. Platelet glycoprotein VI-related clinical defects. Br J Haematol 2007; 139: 363-372.
49. Boylan B, Chen H, Rathore V, et al. Anti-GPVI-associated ITP: an acquired platelet disorder caused by autoantibody-mediated clearance of the GPVI/FcRγ- chain complex from the human platelet surface. Blood 2004; 104: 1350-1355.
50. Barsam SJ, Psaila B, Forestier M, et al. Platelet production and platelet destruction: assessing mechanisms of treatment effect in immune thrombocytopenia (ITP). Blood 2011; 117: 5723-5732.
51. Al-Tamimi M, Gardiner EE, Thom JY, et al. Soluble glycoprotein VI is raised in the plasma of patients with acute ischemic stroke. Stroke 2010; 42: 498-500.
52. Bigalke B, Stellos K, Geisler T, et al. Expression of platelet glycoprotein VI is associated with transient ischemic attack and stroke. Eur J Neurol 2010; 17: 111-117.
53. Kleinschnitz C, Pozgajova M, Pham M, et al. Targeting platelets in acute experimental stroke: impact of glycoprotein Ib, VI, and IIb/IIIa blockade on infarct size, functional outcome, and intracranial bleeding. Circulation 2007; 115: 2323-2330.
54. Stoll G, Kleinschnitz C, Nieswandt B. Molecular mechanisms of thrombus formation in ischemic stroke: novel insights and targets for treatment. Blood 2008; 112: 3555-3562.
55. Bigalke B, Stellos K, Stakos D, et al. Influence of platelet count on the expression of platelet collagen receptor glycoprotein VI (GPVI) in patients with acute coronary syndrome. Thromb Haemost 2009; 101: 911-915.
56. Heemskerk JW, Kuijpers MJ, Munnix IC, et al. Platelet collagen receptors and coagulation. A characteristic platelet response as possible target for antithrombotic treatment. Trends Cardiovasc Med 2005; 15: 86-92.
57. Heemskerk JW, Siljander P, Vuist WM, et al. Function of glycoprotein VI and integrin α2β1 in the procoagulant response of single, collagen-adherent platelets. Thromb Haemost 1999; 81: 782-792.
58. Munnix IC, Strehl A, Kuijpers MJ, et al. The glycoprotein VI-phospholipase Cγ2 signaling pathway controls thrombus formation induced by collagen and tissue factor in vitro and in vivo. Arterioscler Thromb Vasc Biol 2005; 25: 2673-2678.
59. Boilard E, Nigrovic PA, Larabee K, et al. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 2010; 327: 580-583.
60. Bigalke B, Stellos K, Weig HJ, et al. Regulation of platelet glycoprotein VI (GPVI) surface expression and of soluble GPVI in patients with atrial fibrillation (AF) and acute coronary syndrome (ACS). Basic Res Cardiol 2009; 104: 352-357.
61. Colciaghi F, Marcello E, Borroni B, et al. Platelet APP, ADAM 10 and BACE alterations in the early stages of Alzheimer disease. Neurology 2004; 62: 498-501.
62. Endres K, Fahrenholz F. Upregulation of the α-secretase ADAM10 - risk or reason for hope? FEBS J 2010; 277: 1585-1596.
63. Kojro E, Gimpl G, Lammich S, et al. Low cholesterol stimulates the nonamyloidogenic pathway by its effect on the α-secretase ADAM10. Proc Natl Acad Sci USA 2001; 98: 5815-5820.
64. Massberg S, Konrad I, Bultmann A, et al. Soluble glycoprotein VI dimer inhibits platelet adhesion and aggregation to the injured vessel wall in vivo. FASEB J 2004; 18: 397-399.
65. Gruner S, Prostredna M, Koch M, et al. Relative antithrombotic effect of soluble GPVI dimer compared with anti-GPVI antibodies in mice. Blood 2005; 105: 1492-1499.
66. Bender M, Hagedorn I, Nieswandt B. Genetic and antibody-induced GPVI deficiency equally protect mice from mechanically and FeCl3-induced thrombosis. J Thromb Haemost 2011; 9: 1423-1426.
67. Li H, Lockyer S, Concepcion A, et al. The Fab fragment of a novel anti-GPVI monoclonal antibody, OM4, reduces in vivo thrombosis without bleeding risk in rats. Arterioscler Thromb Vasc Biol 2007; 27: 1199-1205.
68. Muzard J, Bouabdelli M, Zahid M, et al. Design and humanization of a murine scFv that blocks human platelet glycoprotein VI in vitro. FEBS J 2009; 276: 4207-4222.
69. Zahid M, Loyau S, Bouabdelli M, et al. Design and reshaping of an scFv directed against human platelet glycoprotein VI with diagnostic potential. Anal Biochem 2010; 417: 274-282.
70. Jung SM, Tsuji K, Moroi M. Glycoprotein (GP) VI dimer as a major collagenbinding site of native platelets: direct evidence obtained with dimeric GPVI-specific Fabs. J Thromb Haemost 2009; 7: 1347-1355.
71. Miura Y, Takahashi T, Jung SM, et al. Analysis of the interaction of platelet collagen receptor glycoprotein VI (GPVI) with collagen. A dimeric form of GPVI, but not the monomeric form, shows affinity to fibrous collagen. J Biol Chem 2002; 277: 46197-46204.
72. Bultmann A, Herdeg C, Li Z, et al. Local delivery of soluble platelet collagen receptor glycoprotein VI inhibits thrombus formation in vivo. Thromb Haemost 2006; 95: 763-766.
73. Bigalke B, Lindemann S, Schonberger T, et al. Ex vivo imaging of injured arteries in rabbits using fluorescence-labelled glycoprotein VI-Fc. Platelets 2012; 23: 1-6.
74. Liu J, Gao BB, Clermont AC, et al. Hyperglycemia-induced cerebral hematoma expansion is mediated by plasma kallikrein. Nat Med 2011; 17: 206-210.
75. Nieswandt B, Stoll G. Sugar rush bleeds the brain. Nat Med 2011; 17: 161-162.
76. Herr AB. Direct evidence of a native GPVI dimer at the platelet surface. J Thromb Haemost 2009; 7: 1344-1346.
77. Kato-Takagaki K, Mizukoshi Y, Yoshizawa Y, et al. Structural and interaction analysis of glycoprotein VI-binding peptide selected from a phage display library. J Biol Chem 2009; 284: 10720-10727.
78. Locke D, Liu C, Peng X, et al. FcRγ-independent signaling by the platelet collagen receptor glycoprotein VI. J Biol Chem 2003; 278: 15441-15448.
79. Reilly MP, Sinha U, Andre P, et al. PRT-060318, a novel Syk inhibitor, prevents heparin- induced thrombocytopenia and thrombosis in a transgenic mouse model. Blood 2011; 117: 2241-2246.
80. Lhermusier T, van Rottem J, Garcia C, et al. The Syk-kinase inhibitor R406 impairs platelet activation and monocyte tissue factor expression triggered by heparin- PF4 complex directed antibodies. J Thromb Haemost 2011; 9: 2067-2076.
81. Seizer P, Borst O, Langer HF, et al. EMMPRIN (CD147) is a novel receptor for platelet GPVI and mediates platelet rolling via GPVI-EMMPRIN interaction. Thromb Haemost 2009; 101: 682-686.
82. Pennings GJ, Yong AS, Kritharides L. Expression of EMMPRIN (CD147) on circulating platelets in vivo. J Thromb Haemost 2010; 8: 472-481.
83. Schulz C, von Bruhl ML, Barocke V, et al. EMMPRIN (CD147/basigin) mediates platelet-monocyte interactions in vivo and augments monocyte recruitment to the vascular wall. J Thromb Haemost 2011; 9: 1007-1019.
84. Jain S, Russell S, Ware J. Platelet glycoprotein VI facilitates experimental lung metastasis in syngenic mouse models. J Thromb Haemost 2009; 7: 1713-1717.
85. Farndale RW. Platelet glycoprotein VI as a mediator of metastasis. J Thromb Haemost 2009; 7: 1711-1712.
86. Flaujac C, Boukour S, Cramer-Borde E. Platelets and viruses: an ambivalent relationship. Cell Mol Life Sci 2010; 67: 545-556.
87. Zahn A, Jennings N, Ouwehand WH, et al. Hepatitis C virus interacts with human platelet glycoprotein VI. J Gen Virol 2006; 87: 2243-2251.
88. Hu H, Armstrong PC, Khalil E, et al. GPVI and GPIbα mediate Staphylococcal superantigen-like protein 5 (SSL5) induced platelet activation and direct toward glycans as potential inhibitors. PLoS One 2011; 6: e19190.
89. Devi S, Kuligowski MP, Kwan RY, et al. Platelet recruitment to the inflamed glomerulus occurs via an αIIbβ3/GPVI-dependent pathway. Am J Pathol 2010; 177: 1131-1142.