Redundancy and interaction of thrombin- and collagen-mediated platelet activation in tail bleeding and carotid thrombosis in mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 12, 2014, Pages 2563-2569

  Bynagari Settipalli, Yamini S ^a   Cornelissen, Ivo ^a,c   Palmer, Daniel ^a,d   Duong, Daniel ^a   Concengco, Cherry ^a   Ware, Jerry ^b   Coughlin, Shaun R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Collagen; Glycoprotein VI; Hemostasis; Mouse Assays; Platelets; Protease activated receptor 3; Protease activated receptor 4; Thrombin; Thrombosis

Indexed keywords

COLLAGEN; GLYCOPROTEIN VI; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4; THROMBIN; FIBRINOGEN RECEPTOR; PLATELET MEMBRANE GLYCOPROTEIN VI; PROTEASE-ACTIVATED RECEPTOR 3, MOUSE; PROTEASE-ACTIVATED RECEPTOR 4; PROTEINASE ACTIVATED RECEPTOR; THROMBIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLEEDING; BLOOD CLOTTING; CAROTID ARTERY THROMBOSIS; CONTROLLED STUDY; EC50; FERRIC CHLORIDE-INDUCED THROMBOSIS; FIBRIN FORMATION; GENOTYPE; HEMOSTASIS; MOUSE; MUTANT; NONHUMAN; PROTEIN DEPLETION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION; ANIMAL; BLOOD; C57BL MOUSE; DEFICIENCY; GENETICS; HEMORRHAGE; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; TAIL; THROMBOCYTE;

ANIMALS; BLOOD PLATELETS; CAROTID ARTERY THROMBOSIS; COLLAGEN; HEMORRHAGE; HEMOSTASIS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLATELET ACTIVATION; PLATELET MEMBRANE GLYCOPROTEINS; RECEPTORS, PROTEINASE-ACTIVATED; RECEPTORS, THROMBIN; TAIL; THROMBIN;

EID: 84918842633     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.304244     Document Type: Article

References (45)

1. Abrams C. Platelet signal transduction. In: Coleman RW Marder VJ Clowes AW, George JN, Goldhaber SZ, eds. Hemostasis and Thrombosis: Basic Principles and Clinical Practice. Philadelphia, P.A.: J.B. Lippincott; 2006.
2. Yusuf S, Zhao F, Mehta SR, Chrolavicius S, Tognoni G, Fox KK; Clopidogrel in Unstable Angina to Prevent Recurrent Events Trial Investigators. Effects of clopidogrel in addition to aspirin in patients with acute coronary syndromes without ST-segment elevation. N Engl J Med. 2001;345:494-502.
3. Mehta SR, Yusuf S; Clopidogrel in Unstable angina to prevent Recurrent Events (CURE) Study Investigators. The clopidogrel in unstable angina to prevent recurrent events (CURE) trial programme; rationale, design and baseline characteristics including a meta-analysis of the effects of thienopyridines in vascular disease. Eur Heart J. 2000;21:2033-2041.
4. Bakhru MR, Bhatt DL. Interpreting the C.H.ARISM.A. study. What is the role of dual antiplatelet therapy with clopidogrel and aspirin? Cleve Clin J Med. 2008;75:289-295.
5. Bhatt DL, Fox KA, Hacke W, et al; Investigators C. Clopidogrel and aspirin versus aspirin alone for the prevention of atherothrombotic events. N Engl J Med. 2006;354:1706-1717
6. Bhatt DL, Topol EJ; Clopidogrel for High Atherothrombotic Risk and Ischemic Stabilization, Management, and Avoidance Executive Committee. Clopidogrel added to aspirin versus aspirin alone in secondary prevention and high-risk primary prevention: rationale and design of the Clopidogrel for High Atherothrombotic Risk and Ischemic Stabilization, Management, and Avoidance (C.H.ARISM.A.) trial. Am Heart J. 2004;148:263-268.
7. Scirica BM, Bonaca MP, Braunwald E, De Ferrari GM, Isaza D, Lewis BS, Mehrhof F, Merlini P.A., Murphy SA, Sabatine MS, Tendera M, Van de Werf F, Wilcox R, Morrow D.A.; TR.A. 2°P-TIMI 50 Steering Committee Investigators. Vorapaxar for secondary prevention of thrombotic events for patients with previous myocardial infarction: a prespecified subgroup analysis of the TR.A. 2°P-TIMI 50 trial. Lancet. 2012;380:1317-1324.
8. Morrow D.A., Scirica BM, Fox KA, Berman G, Strony J, Veltri E, Bonaca MP, Fish P, McCabe C.H., Braunwald E; TR.A. 2(o)P-TIMI 50 Investigators. Evaluation of a novel antiplatelet agent for secondary prevention in patients with a history of atherosclerotic disease: design and rationale for the Thrombin-Receptor Antagonist in Secondary Prevention of Atherothrombotic Ischemic Events (TR.A. 2 degrees P)-TIMI 50 trial. Am Heart J. 2009;158:335-341.e3.
9. Wiviott SD, Braunwald E, McCabe C.H., Montalescot G, Ruzyllo W, Gottlieb S, Neumann FJ, Ardissino D, De Servi S, Murphy SA, Riesmeyer J, Weerakkody G, Gibson CM, Antman EM; TRITON-TIMI 38 Investigators. Prasugrel versus clopidogrel in patients with acute coronary syndromes. N Engl J Med. 2007;357:2001-2015.
10. Nieswandt B, Watson SP. Platelet-collagen interaction: is GPVI the central receptor? Blood. 2003;102:449-461.
11. Coughlin S.R. Protease-activated receptors in hemostasis, thrombosis and vascular biology. J Thromb Haemost. 2005;3:1800-1814.
12. Davey MG, Lüscher EF. Actions of thrombin and other coagulant and proteolytic enzymes on blood platelets. Nature. 1967;216:857-858.
13. Coughlin S.R. Protease-activated receptors in hemostasis, thrombosis and vascular biology. J Thromb Haemost. 2005;3:1800-1814.
14. Kahn ML, Zheng YW, Huang W, Bigornia V, Zeng D, Moff S, Farese RV Jr, Tam C, Coughlin S.R. A dual thrombin receptor system for platelet activation. Nature. 1998;394:690-694.
15. Nakanishi-Matsui M, Zheng YW, Sulciner DJ, Weiss EJ, Ludeman MJ, Coughlin S.R. P.A.R3 is a cofactor for P.A.R4 activation by thrombin. Nature. 2000;404:609-613.
16. Sambrano GR, Weiss EJ, Zheng YW, Huang W, Coughlin S.R. Role of thrombin signalling in platelets in haemostasis and thrombosis. Nature. 2001;413:74-78.
17. Cornelissen I, Palmer D, David T, Wilsbacher L, Concengco C, Conley P, Pandey A, Coughlin S.R. Roles and interactions among protease-activated receptors and P2ry12 in hemostasis and thrombosis. Proc Natl Acad Sci U S A. 2010;107:18605-18610.
18. Kato K, Kanaji T, Russell S, Kunicki TJ, Furihata K, Kanaji S, Marchese P, Reininger A, Ruggeri ZM, Ware J. The contribution of glycoprotein VI to stable platelet adhesion and thrombus formation illustrated by targeted gene deletion. Blood. 2003;102:1701-1707.
19. Nieswandt B, Brakebusch C, Bergmeier W, Schulte V, Bouvard D, Mokhtari-Nejad R, Lindhout T, Heemskerk JW, Zirngibl H, Fässler R. Glycoprotein VI but not alpha2beta1 integrin is essential for platelet interaction with collagen. EMBO J. 2001;20:2120-2130.
20. Nieswandt B, Bergmeier W, Schulte V, Rackebrandt K, Gessner JE, Zirngibl H. Expression and function of the mouse collagen receptor glycoprotein VI is strictly dependent on its association with the FcRgamma chain. J Biol Chem. 2000;275:23998-24002.
21. Nieswandt B, Schulte V, Bergmeier W, Mokhtari-Nejad R, Rackebrandt K, Cazenave JP, Ohlmann P, Gachet C, Zirngibl H. Long-term antithrombotic protection by in vivo depletion of platelet glycoprotein VI in mice. J Exp Med. 2001;193:459-469.
22. Grüner S, Prostredna M, Aktas B, Moers A, Schulte V, Krieg T, Offermanns S, Eckes B, Nieswandt B. Anti-glycoprotein VI treatment severely compromises hemostasis in mice with reduced alpha2beta1 levels or concomitant aspirin therapy. Circulation. 2004;110:2946-2951.
23. Massberg S, Gawaz M, Grüner S, Schulte V, Konrad I, Zohlnhöfer D, Heinzmann U, Nieswandt B. A crucial role of glycoprotein VI for platelet recruitment to the injured arterial wall in vivo. J Exp Med. 2003;197:41-49.
24. Grüner S, Prostredna M, Koch M, Miura Y, Schulte V, Jung SM, Moroi M, Nieswandt B. Relative antithrombotic effect of soluble GPVI dimer compared with anti-GPVI antibodies in mice. Blood. 2005;105:1492-1499.
25. Dubois C, Panicot-Dubois L, Merrill-Skoloff G, Furie B, Furie BC. Glycoprotein VI-dependent and-independent pathways of thrombus formation in vivo. Blood. 2006;107:3902-3906.
26. Cheli Y, Jensen D, Marchese P, Habart D, Wiltshire T, Cooke M, Fernandez JA, Ware J, Ruggeri ZM, Kunicki TJ. The Modifier of hemostasis (Mh) locus on chromosome 4 controls in vivo hemostasis of Gp6-/-mice. Blood. 2008;111:1266-1273.
27. Bender M, May F, Lorenz V, Thielmann I, Hagedorn I, Finney BA, Vögtle T, Remer K, Braun A, Bösl M, Watson SP, Nieswandt B. Combined in vivo depletion of glycoprotein VI and C-type lectin-like receptor 2 severely compromises hemostasis and abrogates arterial thrombosis in mice. Arterioscler Thromb Vasc Biol. 2013;33:926-934.
28. Mangin P, Yap CL, Nonne C, Sturgeon SA, Goncalves I, Yuan Y, Schoenwaelder SM, Wright CE, Lanza F, Jackson SP. Thrombin overcomes the thrombosis defect associated with platelet GPVI/FcRgamma deficiency. Blood. 2006;107:4346-4353.
29. Konstantinides S, Ware J, Marchese P, Almus-Jacobs F, Loskutoff DJ, Ruggeri ZM. Distinct antithrombotic consequences of platelet glycoprotein Ibalpha and VI deficiency in a mouse model of arterial thrombosis. J Thromb Haemost. 2006;4:2014-2021.
30. Zwaal RF, Schroit AJ. Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood. 1997;89:1121-1132.
31. Vandendries ER, Hamilton JR, Coughlin SR, Furie B, Furie BC. Par4 is required for platelet thrombus propagation but not fibrin generation in a mouse model of thrombosis. Proc Natl Acad Sci U S A. 2007; 104:288-292.
32. Cornelissen I, Palmer D, David T, Wilsbacher L, Concengco C, Conley P, Pandey A, Coughlin S.R. Roles and interactions among protease-activated receptors and P2ry12 in hemostasis and thrombosis. Proc Natl Acad Sci U S A. 2010;107:18605-18610.
33. Bender M, Hagedorn I, Nieswandt B. Genetic and antibody-induced glycoprotein VI deficiency equally protects mice from mechanically and FeCl(3)-induced thrombosis. J Thromb Haemost. 2011;9:1423-1426.
34. Wang X, Xu L. An optimized murine model of ferric chloride-induced arterial thrombosis for thrombosis research. Thromb Res. 2005;115:95-100.
35. Camerer E, Duong DN, Hamilton JR, Coughlin S.R. Combined deficiency of protease-activated receptor-4 and fibrinogen recapitulates the hemostatic defect but not the embryonic lethality of prothrombin deficiency. Blood. 2004;103:152-154.
36. Macfarlane SR, Seatter MJ, Kanke T, Hunter GD, Plevin R. Proteinaseactivated receptors. Pharmacol Rev. 2001;53:245-282.
37. Jung SM, Moroi M. Platelet glycoprotein VI. Adv Exp Med Biol. 2008;640:53-63.
38. Barr JD, Chauhan AK, Schaeffer GV, Hansen JK, Motto DG. Red blood cells mediate the onset of thrombosis in the ferric chloride murine model. Blood. 2013;121:3733-3741.
39. Weiss EJ, Hamilton JR, Lease KE, Coughlin S.R. Protection against thrombosis in mice lacking P.A.R3. Blood. 2002;100:3240-3244.
40. Kahn ML, Nakanishi-Matsui M, Shapiro MJ, Ishihara H, Coughlin S.R. Protease-activated receptors 1 and 4 mediate activation of human platelets by thrombin. J Clin Invest. 1999;103:879-887.
41. Andre P, Delaney SM, LaRocca T, Vincent D, DeGuzman F, Jurek M, Koller B, Phillips DR, Conley PB. P2Y12 regulates platelet adhesion/activation, thrombus growth, and thrombus stability in injured arteries. J Clin Invest. 2003;112:398-406.
42. Uzunova A, Ramey E, Ramwell PW. Effect of testosterone, sex and age on experimentally induced arterial thrombosis. Nature. 1976;261:712-713.
43. Lewis HD Jr, Davis JW, Archibald DG, Steinke WE, Smitherman TC, Doherty JE III, Schnaper HW, LeWinter MM, Linares E, Pouget JM, Sabharwal SC, Chesler E, DeMots H. Protective effects of aspirin against acute myocardial infarction and death in men with unstable angina. Results of a Veterans Administration Cooperative Study. N Engl J Med. 1983;309:396-403.
44. Morrow D.A., Braunwald E, Bonaca MP, et al, Committee TPTS, Investigators. Vorapaxar in the secondary prevention of atherothrombotic events. N Engl J Med. 2012;366:1404-1413.
45. 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.