Factor XII inhibition reduces thrombus formation in a primate thrombosis model

Blood

Volumn 123, Issue 11, 2014, Pages 1739-1746

  Matafonov, Anton ^a,b   Leung, Philberta Y ^c,d   Gailani, Adam E ^a   Grach, Stephanie L ^a   Puy, Cristina ^c   Cheng, Qiufang ^a   Sun, Mao Fu ^a   McCarty, Owen J T ^c   Tucker, Erik I ^c,d   Kataoka, Hiroaki ^e   Renné, Thomas ^f,g   Morrissey, James H ^h   Gruber, Andras ^c,d   Gailani, David ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b NATIONAL RESEARCH TOMSK POLYTECHNIC UNIVERSITY   (Russian Federation)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d Aronora Inc ^*  (United States)

^e UNIVERSITY OF MIYAZAKI   (Japan)

^f KAROLINSKA INSTITUTE   (Sweden)

^g UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^h UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICOAGULANT AGENT; BLOOD CLOTTING FACTOR 11 ANTIBODY; BLOOD CLOTTING FACTOR 12; BLOOD CLOTTING FACTOR 12 ANTIBODY; BLOOD CLOTTING FACTOR 12A; COLLAGEN; FERRIC CHLORIDE; FIBRIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 15H8; MONOCLONAL ANTIBODY 9A2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTICOAGULATION; ARTERIOVENOUS SHUNT; ARTERY THROMBOSIS; ARTICLE; BABOON; BIOTRANSFORMATION; BLOOD; BLOOD CLOTTING; BLOOD VESSEL GRAFT; CONTROLLED STUDY; FIBRIN FORMATION; HEAVY CHAIN; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PARTIAL THROMBOPLASTIN TIME; PLASMA; PRIMATE; PRIORITY JOURNAL; THROMBOCYTE;

ANIMALS; ANTIBODIES, MONOCLONAL; BLOOD COAGULATION; DISEASE MODELS, ANIMAL; FACTOR XI; FACTOR XII; FACTOR XII DEFICIENCY; FACTOR XIIA; FIBRIN; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; PAPIO; RECOMBINANT PROTEINS; THROMBIN; THROMBOPLASTIN; THROMBOSIS;

EID: 84897538637     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-04-499111     Document Type: Article

References (54)

1. Schumacher WA, Luettgen JM, Quan ML, Seiffert DA. Inhibition of factor XIa as a new approach to anticoagulation. Arterioscler Thromb Vasc Biol. 2010;30(3):388-392.
2. Löwenberg EC, Meijers JC, Monia BP, Levi M. Coagulation factor XI as a novel target for antithrombotic treatment. J Thromb Haemost. 2010;8(11):2349-2357.
3. Woodruff RS, Sullenger B, Becker RC. The many faces of the contact pathway and their role in thrombosis. J Thromb Thrombolysis. 2011;32(1):9-20.
4. Stavrou E, Schmaier AH. Factor XII: what does it contribute to our understanding of the physiology and pathophysiology of hemostasis & thrombosis. Thromb Res. 2010;125(3):210-215.
5. Renné T, Schmaier AH, Nickel KF, Blombäck M, Maas C. In vivo roles of factor XII. Blood. 2012;120(22):4296-4303.
6. Wang X, Cheng Q, Xu L, et al. Effects of factor IX or factor XI deficiency on ferric chloride-induced carotid artery occlusion in mice. J Thromb Haemost. 2005;3(4):695-702. (Pubitemid 41647883)
7. Renné T, Pozgajová M, Grüner S, et al. Defective thrombus formation in mice lacking coagulation factor XII. J Exp Med. 2005;202(2):271-281. (Pubitemid 41043823)
8. Cheng Q, Tucker EI, Pine MS, et al. A role for factor XIIa-mediated factor XI activation in thrombus formation in vivo. Blood. 2010;116(19): 3981-3989.
9. Müller F, Mutch NJ, Schenk WA, et al. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell. 2009;139(6):1143-1156.
10. Kleinschnitz C, Stoll G, Bendszus M, et al. Targeting coagulation factor XII provides protection from pathological thrombosis in cerebral ischemia without interfering with hemostasis. J Exp Med. 2006;203(3):513-518.
11. Nickel K, Frantz S, Esmon C, Gailani D, Renné T. Targeting the polyphosphate-coagulation factor XII pathway prevents cardiac ischemia-reperfusion injury without influencing bleeding risk. In: Proceedings from the International Society on Thrombosis and Haemostasis; June 29-July 4, 2013; Amsterdam, The Netherlands. Abstract OC53.5.1.
12. Gruber A, Hanson SR. Factor XI-dependence of surface- and tissue factor-initiated thrombus propagation in primates. Blood. 2003;102(3):953-955. (Pubitemid 36917789)
13. Tucker EI, Marzec UM, White TC, et al. Prevention of vascular graft occlusion and thrombus-associated thrombin generation by inhibition of factor XI. Blood. 2009;113(4):936-944.
14. Gailani D, Neff AT. Rare coagulation factor deficiencies, In: Hoffman RH, Benz EJ, Silberstein LE, Heslop H, Weitz JI, Snastasi J, eds. Hematology, Basic Principles and Practice. 6th ed. Philadelphia, PA: Saunders-Elsevier; 2013: 1971-1986.
15. Seligsohn U. Factor XI deficiency in humans. J Thromb Haemost. 2009;7(suppl 1):84-87.
16. MacFarlane RG. An enzyme cascade in the blood clotting mechanism, and its function as a biochemical amplifier. Nature. 1964;202:498-499.
17. Davie EW, Ratnoff OD. Waterfall sequence for intrinsic blood clotting. Science. 1964;145(3638):1310-1312.
18. van der Meijden PE, Munnix IC, Auger JM, et al. Dual role of collagen in factor XII-dependent thrombus formation. Blood. 2009;114(4):881-890.
19. White-Adams TC, Berny MA, Patel IA, et al. Laminin promotes coagulation and thrombus formation in a factor XII-dependent manner. J Thromb Haemost. 2010;8(6):1295-1301.
20. Kannemeier C, Shibamiya A, Nakazawa F, et al. Extracellular RNA constitutes a natural procoagulant cofactor in blood coagulation. Proc Natl Acad Sci U S A. 2007;104(15):6388-6393. (Pubitemid 47186104)
21. Fuchs TA, Brill A, Duerschmied D, et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA. 2010;107(36):15880-15885.
22. Maas C, Govers-Riemslag JW, Bouma B, et al. Misfolded proteins activate factor XII in humans, leading to kallikrein formation without initiating coagulation. J Clin Invest. 2008;118(9):3208-3218.
23. Shariat-Madar Z, Mahdi F, Schmaier AH. Assembly and activation of the plasma kallikrein/kinin system: a new interpretation. Int Immunopharmacol. 2002;2(13-14):1841-1849. (Pubitemid 35373925)
24. Adams GN, LaRusch GA, Stavrou E, et al. Murine prolylcarboxypeptidase depletion induces vascular dysfunction with hypertension and faster arterial thrombosis. Blood. 2011;117(14):3929-3937.
25. Meijers JC, Tekelenburg WL, Bouma BN, Bertina RM, Rosendaal FR. High levels of coagulation factor XI as a risk factor for venous thrombosis. N Engl J Med. 2000;342(10):696-701. (Pubitemid 30131422)
26. Doggen CJ, Rosendaal FR, Meijers JC. Levels of intrinsic coagulation factors and the risk of myocardial infarction among men: opposite and synergistic effects of factors XI and XII. Blood. 2006;108(13):4045-4051. (Pubitemid 44913273)
27. Salomon O, Steinberg DM, Koren-Morag N, Tanne D, Seligsohn U. Reduced incidence of ischemic stroke in patients with severe factor XI deficiency. Blood. 2008;111(8):4113-4117.
28. Cushman M, O'Meara ES, Folsom AR, Heckbert SR. Coagulation factors IX through XIII and the risk of future venous thrombosis: the Longitudinal Investigation of Thromboembolism Etiology. Blood. 2009;114(14):2878-2883.
29. Suri MF, Yamagishi K, Aleksic N, Hannan PJ, Folsom AR. Novel hemostatic factor levels and risk of ischemic stroke: the Atherosclerosis Risk in Communities (ARIC) Study. Cerebrovasc Dis. 2010;29(5):497-502.
30. Salomon O, Steinberg DM, Zucker M, Varon D, Zivelin A, Seligsohn U. Patients with severe factor XI deficiency have a reduced incidence of deep-vein thrombosis. Thromb Haemost. 2011;105(2):269-273.
31. Endler G, Marsik C, Jilma B, Schickbauer T, Quehenberger P, Mannhalter C. Evidence of a U-shaped association between factor XII activity and overall survival. J Thromb Haemost. 2007;5(6):1143-1148. (Pubitemid 46902114)
32. Geng Y, Verhamme IM, Messer A, et al. A sequential mechanism for exosite-mediated factor IX activation by factor XIa. J Biol Chem. 2012;287(45):38200-38209.
33. Miyazawa K, Shimomura T, Kitamura A, Kondo J, Morimoto Y, Kitamura N. Molecular cloning and sequence analysis of the cDNA for a human serine protease reponsible for activation of hepatocyte growth factor. Structural similarity of the protease precursor to blood coagulation factor XII. J Biol Chem. 1993;268(14):10024-10028. (Pubitemid 23150177)
34. Kravtsov DV, Matafonov A, Tucker EI, et al. Factor XI contributes to thrombin generation in the absence of factor XII. Blood. 2009;114(2):452-458.
35. Puy C, Tucker EI, Wong ZC, et al. Factor XII promotes blood coagulation independent of factor XI in the presence of long-chain polyphosphates. J Thromb Haemost. 2013;11(7):1341-1352.
36. Ponczek MB, Gailani D, Doolittle RF. Evolution of the contact phase of vertebrate blood coagulation. J Thromb Haemost. 2008;6(11):1876-1883.
37. 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(18):3733-3741.
38. Colman RW. Are hemostasis and thrombosis two sides of the same coin? J Exp Med. 2006;203(3): 493-495.
39. Hagedorn I, Schmidbauer S, Pleines I, et al. Factor XIIa inhibitor recombinant human albumin Infestin-4 abolishes occlusive arterial thrombus formation without affecting bleeding. Circulation. 2010;121(13):1510-1517.
40. Chen JW, Figueiredo JL, Wojtkiewicz GR, et al. Selective factor XIIa inhibition attenuates silent brain ischemia: application of molecular imaging targeting coagulation pathway. JACC Cardiovasc Imaging. 2012;5(11):1127-1138.
41. Salomon O, Steinberg DM, Seligshon U. Variable bleeding manifestations characterize different types of surgery in patients with severe factor XI deficiency enabling parsimonious use of replacement therapy. Haemophilia. 2006;12(5):490-493. (Pubitemid 44227591)
42. Salomon O, Steinberg DM, Tamarin I, Zivelin A, Seligsohn U. Plasma replacement therapy during labor is not mandatory for women with severe factor XI deficiency. Blood Coagul Fibrinolysis. 2005;16(1):37-41.
43. Ratnoff OD. The George M. Kober lecture. The legacy of John Hageman: new dividends. Trans Assoc Am Physicians. 1985;98:cli-clxi.
44. Koster T, Rosendaal FR, Briët E, Vandenbroucke JP. John Hageman's factor and deep-vein thrombosis: Leiden thrombophilia Study. Br J Haematol. 1994;87(2):422-424. (Pubitemid 24204755)
45. Zeerleder S, Schloesser M, Redondo M, et al. Reevaluation of the incidence of thromboembolic complications in congenital factor XII deficiency-a study on 73 subjects from 14 Swiss families. Thromb Haemost. 1999;82(4):1240-1246. (Pubitemid 29473785)
46. Girolami A, Randi ML, Gavasso S, Lombardi AM, Spiezia F. The occasional venous thromboses seen in patients with severe (homozygous) FXII deficiency are probably due to associated risk factors: a study of prevalence in 21 patients and review of the literature. J Thromb Thrombolysis. 2004;17(2):139-143. (Pubitemid 39157964)
47. Grundt H, Nilsen DW, Hetland O, Valente E, Fagertun HE. Activated factor 12 (FXIIa) predicts recurrent coronary events after an acute myocardial infarction. Am Heart J. 2004;147(2):260-266. (Pubitemid 38176826)
48. 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(18):1854-1861.
49. Konings J, Govers-Riemslag JW, Philippou H, et al. Factor XIIa regulates the structure of the fibrin clot independently of thrombin generation through direct interaction with fibrin. Blood. 2011; 118(14):3942-3951.
50. Pixley RA, Stumpo LG, Birkmeyer K, Silver L, Colman RW. A monoclonal antibody recognizing an icosapeptide sequence in the heavy chain of human factor XII inhibits surface-catalyzed activation. J Biol Chem. 1987;262(21):10140- 10145. (Pubitemid 17103064)
51. Clarke BJ, Côté HC, Cool DE, et al. Mapping of a putative surface-binding site of human coagulation factor XII. J Biol Chem. 1989;264(19):11497-11502. (Pubitemid 19168890)
52. Citarella F, te Velthuis H, Helmer-Citterich M, Hack CE. Identification of a putative binding site for negatively charged surfaces in the fibronectin type II domain of human factor XII - an immunochemical and homology modeling approach. Thromb Haemost. 2000;84(6):1057-1065. (Pubitemid 32014043)
53. Pixley RA, De La Cadena R, Page JD, et al. The contact system contributes to hypotension but not disseminated intravascular coagulation in lethal bacteremia. In vivo use of a monoclonal antifactor XII antibody to block contact activation in baboons. J Clin Invest. 1993;91(1):61-68. (Pubitemid 23037253)
54. Crosby JR, Marzec U, Revenko AS, et al. Antithrombotic effect of antisense factor XI oligonucleotide treatment in primates. Arterioscler Thromb Vasc Biol. 2013;33(7):1670-1678.