Factor XII regulates the pathological process of thrombus formation on ruptured plaques

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 8, 2014, Pages 1674-1680

  Kuijpers, Marijke J E ^a   Van Der Meijden, Paola E J ^a   Feijge, Marion A H ^a   Mattheij, Nadine J A ^a   May, Frauke ^b   Govers Riemslag, José ^a   Meijers, Joost C M ^c,d   Heemskerk, Johan W M ^a   Renné, Thomas ^e,f   Cosemans, Judith M E M ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b CSL BEHRING GMBH   (Germany)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d Department of Plasma Proteins ^*  (Netherlands)

^e KAROLINSKA INSTITUTE   (Sweden)

^f UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Blood coagulation; Blood platelets; Factor XII; Fibrin; Plaque rupture; Thrombus; Tissue factor

Indexed keywords

APOLIPOPROTEIN E; BLOOD CLOTTING FACTOR 12; BLOOD CLOTTING FACTOR 7A; BLOOD CLOTTING FACTOR 7A INHIBITOR; FIBRIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY THROMBOSIS; ARTICLE; ARTIFICIAL EMBOLISM; ATHEROSCLEROTIC PLAQUE; BLOOD CLOTTING; CAROTID ARTERY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EX VIVO STUDY; FIBRIN FORMATION; HUMAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; THROMBUS;

BLOOD COAGULATION; BLOOD PLATELETS; FACTOR XII; FIBRIN; PLAQUE RUPTURE; THROMBUS; TISSUE FACTOR;

ANIMALS; AORTA, THORACIC; AORTIC DISEASES; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BLOOD COAGULATION; BLOOD PLATELETS; CAROTID ARTERIES; CAROTID ARTERY DISEASES; CHOLESTEROL, DIETARY; DISEASE MODELS, ANIMAL; FACTOR VIIA; FACTOR XI; FACTOR XII; FACTOR XII DEFICIENCY; FACTOR XIIA; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLAQUE, ATHEROSCLEROTIC; RUPTURE, SPONTANEOUS; THROMBOPLASTIN; THROMBOSIS; TIME FACTORS;

EID: 84904675375     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.303315     Document Type: Article

References (34)

1. Jackson SP. Arterial thrombosis-insidious, unpredictable and deadly. Nat Med. 2011;17:1423-1436.
2. Heemskerk JW, Mattheij NJ, Cosemans JM. Platelet-based coagulation: different populations, different functions. J Thromb Haemost. 2013;11:2-16.
3. Renné T, Pozgajová M, Grüner S, Schuh K, Pauer HU, Burfeind P, Gailani D, Nieswandt B. Defective thrombus formation in mice lacking coagulation factor XII. J Exp Med. 2005;202:271-281.
4. Cheng Q, Tucker EI, Pine MS, Sisler I, Matafonov A, Sun MF, White- Adams TC, Smith SA, Hanson SR, McCarty OJ, Renné T, Gruber A, Gailani D. A role for factor XIIa-mediated factor XI activation in thrombus formation in vivo. Blood. 2010;116:3981-3989.
5. Müller F, Mutch NJ, Schenk WA, Smith SA, Esterl L, Spronk HM, Schmidbauer S, Gahl WA, Morrissey JH, Renn é T. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell. 2009;139:1143-1156.
6. Cosemans JM, Kuijpers MJ, Lecut C, Loubele ST, Heeneman S, Jandrot- Perrus M , Heemskerk JW. Contribution of platelet glycoprotein VI to the thrombogenic effect of collagens in fibrous atherosclerotic lesions. Atherosclerosis. 2005;181:19-27.
7. Penz S, Reininger AJ, Brandl R, Goyal P, Rabie T, Bernlochner I, Rother E, Goetz C, Engelmann B, Smethurst PA, Ouwehand WH, Farndale R, Nieswandt B, Siess W. Human atheromatous plaques stimulate thrombus formation by activating platelet glyco protein VI. FASEB J. 2005;19:898-909.
8. Reininger AJ, Bernlochner I, Penz SM, Ravanat C, Smethurst P, Farndale RW, Gachet C, Brandl R, Siess W. A 2-step mechanism of arterial thrombus formation induced by human atherosclerotic plaques. J Am Coll Cardiol. 2010;55:1147-1158.
9. van der Meijden PE, Munnix IC, Auger JM, Govers-Riemslag JW, Cosemans JM, Kuijpers MJ, Spronk HM, Wat son SP, Renné T, Heemskerk JW. Dual role of collagen in factor XII-dependent thrombus formation. Blood. 2009;114:881-890.
10. Kleinschnitz C, Stoll G, Bendszus M, Schuh K, Pauer HU, B urfeind P, Renné C, Gailani D, Nieswandt B, Renné T. Targeting coagulation factor XII provides protection from pathological thrombosis in cerebral ischemia without interfering with hemostasis. J Exp Med. 2006;203:513-518.
11. Hagedorn I, Schmidbauer S, Pleines I, Kleinschnitz C, Kronthaler U, Stoll G, Dickneite G, Nieswandt B. Factor XIIa inhibitor recombinant human albumin Infestin-4 abolishes occlusive art erial thrombus formation without affecting bleeding. Circulation. 2010;121:1510-1517.
12. Revenko AS, Gao D, Crosby JR, Bhattacharjee G, Zhao C, May C, Gailani D, Monia BP, MacLeod AR. Selective depletion of plasma prekallikrein or coagulation factor XII inhibits thrombosis in mice without increased risk of bleeding. Blood. 2011;118:5302-5311.
13. Matafonov A, Leung PY, Gailani AE, Grach SL, Puy C, Cheng Q, Sun MF, McCarty OJ, Tucker EI, Kataoka H, Renné T, Morrissey JH, Gruber A, Gailani D. Factor XII inhibition reduces throm bus formation in a primate thrombosis model. Blood. 2014;123:1739-1746.
14. Ratnoff OD, Colopy JE. A familial hemorrhagic trait associated with a deficiency of a clot-promoting fraction of plasma. J Clin Invest. 1955;34:602-613.
15. Renné T, Schmaier AH, Nickel KF, Blombäck M, Maas C. In vivo roles of factor XII. Blood. 2012;120:4296-4303.
16. Woodruff RS, Sullenger B, Becker RC. The many faces of the contact pathway and their role in thrombosis. J Thromb Thrombolysis. 2011; 32:9-20.
17. Kuijpers MJ, Gilio K, Reitsma S, Nergiz-U nal R, Prinzen L, Heeneman S, Lutgens E, van Zandvoort MA, Nieswandt B, Egbrink MG, Heemskerk JW. Complementary roles of platelets and coagulation in thrombus formation on plaques acutely ruptured by targeted ultrasound tr eatment: a novel intravital model. J Thromb Haemost. 2009;7:152-161.
18. Kuijpers MJ, Munnix IC, Cosemans JM, Vlijmen BV, Reutelingsperger CP, Egbrink MO, Heemskerk JW. Key role of platelet proco agulant activity in tissue factor-and collagen-dependent thrombus formation in arterioles and venules in vivo differential sensitivity to thrombin inhibition. Microcirculation. 2008;15:269-282.
19. Baglia FA, Walsh PN. Thrombin-mediated feedback activation of factor XI on the activated platelet surface is preferred over contact activation by factor XIIa or factor XIa. J Biol Chem. 2000;275:20514-20519.
20. Choi SH, Smith SA, Morrissey JH. Polyphosphate is a cofactor for the activation of factor XI by thrombin. Blood. 2011;118:6963-6970.
21. Konings J, Govers-Riemslag JW, Philippou H, Mutch NJ, Borissoff JI, Allan P, Mohan S, Tans G, Ten Cate H, Arië ns RA. Factor XIIa regulates the structure of the fibrin clot independently of thrombin generation through direct interaction with fibrin. Blood. 2011;118:3942-3951.
22. Cosemans JM, Angelillo-Scherrer A, Mattheij NJ, Heemskerk JW. The effects of arterial flow on platelet activation, thrombus growth, and stabilization. Cardiovasc Res. 2013;99:342-352.
23. Larsson M, Rayzman V, Nolte MW, et al. A factor XIIa inhibitory antibody provides thromboprotection in extracorporeal circulation without increasing bleeding risk. Sci Transl Med. 2014;6:222ra17.
24. Smith SA, Choi SH, Davis-Harrison R, Huyck J, Boettcher J, Rienstra CM, Reinstra CM, Morrissey JH. Polyphosphate exerts differential effects on blood clotting, depending on polymer size. Blood. 2010;116:4353-4359.
25. Leung PY, Hurst S, Berny-Lang MA, Verbout NG, Gailani D, Tucker EI, Wang RK, McCarty OJ, Gruber A. Inhibition of Factor XII-mediated activation of Factor XI provides protection against experimental acute ischemic stroke in mice. Transl Stroke Res. 2012;3:381?389.
26. Ardissino D, Merlini PA, Bauer KA, Bramucci E, Ferrario M, Coppola R, Fetiveau R, Lucreziotti S, Rosenberg RD, Mannucci PM. Thromb ogenic potential of human coronary atherosclerotic plaques. Blood. 2001;98:2726-2729.
27. Thiruvikraman SV, Guha A, Roboz J, Taubman MB, Nemerson Y, Fallon JT. In situ localization of tissue factor in human atherosclerotic plaques by binding of digoxigenin-labeled factors VIIa and X. Lab Invest. 1996;75:451-461.
28. Niemetz J, Fallon JT, Harrington E, Hathcock J. Rapid generation of thrombin by atheroma and platelets. J Thromb Haemost. 2004;2:321-326.
29. Miller GJ, Esnouf MP, Burgess AI, Cooper JA, Mitchell JP. Risk of coronary heart disease and activation of factor XII in middle-aged men. Arterioscler Thromb Vasc Biol. 1997;17:2103-2106.
30. Zito F, Drummond F, Bujac SR, Esnouf MP, Morrissey JH, Humphries SE, Miller GJ. Epidemiological and genetic associations of activated factor XII concentration with factor VII activity, fibrinopeptide A concentration, and risk of coronary heart disease in men. Circulation. 2000;102:2058-2062.
31. Siegerink B, Govers-Riemslag JW, Rosendaal FR, Ten Cate H, Algra A. Intrinsic coagulation activation and the risk of arterial thrombosis in young women: results from the Risk of Arterial Thrombosis in relation to Oral contraceptives (RATIO) case-control study. Circulation. 2010;122:1854-1861.
32. Markus HS, King A, Shipley M, Topakian R, Cullinane M, Reihill S, Bornstein NM, Schaafsma A. Asymptomatic embolisation for prediction of stroke in the Asymptomatic Carotid Emboli Stud y (ACES): a prospective observational study. Lancet Neurol. 2010;9:663-671.
33. Kruis RW, Vlasveld FA, Van Dijk D. The (un)importance of cerebral microemboli. Semin Cardiothorac Vasc Anesth. 2010;14:111-118.
34. Girolami A, Tezza F, Scandellari R, Vettore S, Girolami B. Associated prothrombotic conditions are probably responsible for the occurrence of thrombosis in almost all patients with congenital FVII d eficiency. Critical review of the literature. J Thromb Thrombolysis. 2010;30:172-178.