Inhibiting the intrinsic pathway of coagulation with a factor XII-targeting RNA aptamer

Journal of Thrombosis and Haemostasis

Volumn 11, Issue 7, 2013, Pages 1364-1373

  Woodruff, R S ^a,b   Xu, Y ^c   Layzer, J ^a   Wu, W ^c   Ogletree, M L ^c   Sullenger, B A ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY   (United States)

^c MERCK RESEARCH LABORATORIES   (United States)

Author keywords

Anticoagulant agents; Blood coagulation; Factor XII; Factor XIIa; RNA aptamers

Indexed keywords

BLOOD CLOTTING FACTOR 12; BLOOD CLOTTING FACTOR 12A; INTRINSIC FACTOR; KALLIKREIN; KININ; NUCLEASE; PEPTIDE APTAMER; RNA APTAMER; UNCLASSIFIED DRUG;

ANTICOAGULATION; ARTICLE; BINDING AFFINITY; BLOOD CLOTTING; CONTROLLED STUDY; DRUG POTENCY; ENZYME INHIBITION; FIBRIN CLOT; HUMAN; IN VITRO STUDY; KALLIKREIN KININ SYSTEM; MEDIATOR; MOLECULAR BIOLOGY; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

ANTICOAGULANT AGENTS; BLOOD COAGULATION; FACTOR XII; FACTOR XIIA; RNA APTAMERS;

ANTICOAGULANTS; APTAMERS, NUCLEOTIDE; BLOOD COAGULATION; BLOOD COAGULATION TESTS; DOSE-RESPONSE RELATIONSHIP, DRUG; FACTOR XII; FACTOR XIIA; FIBRIN; HUMANS; KINETICS; SELEX APTAMER TECHNIQUE; THROMBIN;

EID: 84880447362     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12302     Document Type: Article

References (33)

1. Hoffman M. A cell-based model of coagulation and the role of factor VIIa. Blood Rev 2003; 17 (Suppl. 1): S1-5.
2. Renne T, Pozgajova M, Gruner 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: 271-81.
3. Kleinschnitz C, Stoll G, Bendszus M, Schuh K, Pauer HU, Burfeind P, Renne C, Gailani D, Nieswandt B, Renne T. Targeting coagulation factor XII provides protection from pathological thrombosis in cerebral ischemia without interfering with hemostasis. J Exp Med 2006; 203: 513-8.
4. Cheng Q, Tucker EI, Pine MS, Sisler I, Matafonov A, Sun MF, White-Adams TC, Smith SA, Hanson SR, McCarty OJ, Renne T, Gruber A, Gailani D. A role for factor XIIa-mediated factor XI activation in thrombus formation in vivo. Blood 2010; 116: 3981-9.
5. 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: 210-5.
6. Samuel M, Pixley RA, Villanueva MA, Colman RW, Villanueva GB. Human factor XII (Hageman factor) autoactivation by dextran sulfate. Circular dichroism, fluorescence, and ultraviolet difference spectroscopic studies. J Biol Chem 1992; 267: 19691-7.
7. Muller F, Mutch NJ, Schenk WA, Smith SA, Esterl L, Spronk HM, Schmidbauer S, Gahl WA, Morrissey JH, Renne T. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell 2009; 139: 1143-56.
8. Kannemeier C, Shibamiya A, Nakazawa F, Trusheim H, Ruppert C, Markart P, Song Y, Tzima E, Kennerknecht E, Niepmann M, von Bruehl ML, Sedding D, Massberg S, Gunther A, Engelmann B, Preissner KT. Extracellular RNA constitutes a natural procoagulant cofactor in blood coagulation. Proc Natl Acad Sci U S A 2007; 104: 6388-93.
9. Maas C, Govers-Riemslag JW, Bouma B, Schiks B, Hazenberg BP, Lokhorst HM, Hammarstrom P, ten Cate H, de Groot PG, Bouma BN, Gebbink MF. Misfolded proteins activate factor XII in humans, leading to kallikrein formation without initiating coagulation. J Clin Invest 2008; 118: 3208-18.
10. van der Meijden PE, Munnix IC, Auger JM, Govers-Riemslag JW, Cosemans JM, Kuijpers MJ, Spronk HM, Watson SP, Renne T, Heemskerk JW. Dual role of collagen in factor XII-dependent thrombus formation. Blood 2009; 114: 881-90.
11. Sainz IM, Pixley RA, Colman RW. Fifty years of research on the plasma kallikrein-kinin system: from protein structure and function to cell biology and in-vivo pathophysiology. Thromb Haemost 2007; 98: 77-83.
12. Rusconi CP, Scardino E, Layzer J, Pitoc GA, Ortel TL, Monroe D, Sullenger BA. RNA aptamers as reversible antagonists of coagulation factor IXa. Nature 2002; 419: 90-4.
13. Rusconi CP, Yeh A, Lyerly HK, Lawson JH, Sullenger BA. Blocking the initiation of coagulation by RNA aptamers to factor VIIa. Thromb Haemost 2000; 84: 841-8.
14. Bompiani KM, Monroe DM, Church FC, Sullenger BA. A high affinity, antidote-controllable prothrombin and thrombin-binding RNA aptamer inhibits thrombin generation and thrombin activity. J Thromb Haemost 2012; 10: 870-80.
15. Buddai SK, Layzer JM, Lu G, Rusconi CP, Sullenger BA, Monroe DM, Krishnaswamy S. An anticoagulant RNA aptamer that inhibits proteinase-cofactor interactions within prothrombinase. J Biol Chem 2010; 285: 5212-23.
16. Rusconi CP, Roberts JD, Pitoc GA, Nimjee SM, White RR, Quick G Jr, Scardino E, Fay WP, Sullenger BA. Antidote-mediated control of an anticoagulant aptamer in vivo. Nat Biotechnol 2004; 22: 1423-8.
17. Oney S, Lam RT, Bompiani KM, Blake CM, Quick G, Heidel JD, Liu JY, Mack BC, Davis ME, Leong KW, Sullenger BA. Development of universal antidotes to control aptamer activity. Nat Med 2009; 15: 1224-8.
18. Oney S, Nimjee SM, Layzer J, Que-Gewirth N, Ginsburg D, Becker RC, Arepally G, Sullenger BA. Antidote-controlled platelet inhibition targeting von Willebrand factor with aptamers. Oligonucleotides 2007; 17: 265-74.
19. Layzer JM, Sullenger BA. Simultaneous generation of aptamers to multiple gamma-carboxyglutamic acid proteins from a focused aptamer library using DeSELEX and convergent selection. Oligonucleotides 2007; 17: 1-11.
20. Keefe AD, Cload ST. SELEX with modified nucleotides. Curr Opin Chem Biol 2008; 12: 448-56.
21. Hemker HC, Giesen P, Al Dieri R, Regnault V, de Smedt E, Wagenvoord R, Lecompte T, Beguin S. Calibrated automated thrombin generation measurement in clotting plasma. Pathophysiol Haemost Thromb 2003; 33: 4-15.
22. Long SB, Long MB, White RR, Sullenger BA. Crystal structure of an RNA aptamer bound to thrombin. RNA 2008; 14: 2504-12.
23. Citarella F, Wuillemin WA, Lubbers YT, Hack CE. Initiation of contact system activation in plasma is dependent on factor XII autoactivation and not on enhanced susceptibility of factor XII for kallikrein cleavage. Br J Haematol 1997; 99: 197-205.
24. Cochrane CG, Revak SD, Wuepper KD. Activation of Hageman factor in solid and fluid phases. A critical role of kallikrein. J Exp Med 1973; 138: 1564-83.
25. Citarella F, Ravon DM, Pascucci B, Felici A, Fantoni A, Hack CE. Structure/function analysis of human factor XII using recombinant deletion mutants. Evidence for an additional region involved in the binding to negatively charged surfaces. Eur J Biochem 1996; 238: 240-9.
26. Shariat-Madar Z, Mahdi F, Warnock M, Homeister JW, Srikanth S, Krijanovski Y, Murphey LJ, Jaffa AA, Schmaier AH. Bradykinin B2 receptor knockout mice are protected from thrombosis by increased nitric oxide and prostacyclin. Blood 2006; 108: 192-9.
27. 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: 5302-11.
28. Rosen ED, Gailani D, Castellino FJ. FXI is essential for thrombus formation following FeCl3-induced injury of the carotid artery in the mouse. Thromb Haemost 2002; 87: 774-6.
29. Zhang H, Lowenberg EC, Crosby JR, MacLeod AR, Zhao C, Gao D, Black C, Revenko AS, Meijers JC, Stroes ES, Levi M, Monia BP. Inhibition of the intrinsic coagulation pathway factor XI by antisense oligonucleotides: a novel antithrombotic strategy with lowered bleeding risk. Blood 2010; 116: 4684-92.
30. Keularts IM, Zivelin A, Seligsohn U, Hemker HC, Beguin S. The role of factor XI in thrombin generation induced by low concentrations of tissue factor. Thromb Haemost 2001; 85: 1060-5.
31. Allen GA, Wolberg AS, Oliver JA, Hoffman M, Roberts HR, Monroe DM. Impact of procoagulant concentration on rate, peak and total thrombin generation in a model system. J Thromb Haemost 2004; 2: 402-13.
32. Renne T, Schmaier AH, Nickel KF, Blomback M, Maas C. In vivo roles of factor XII. Blood 2012; 120: 4296-303.
33. Povsic TJ, Wargin WA, Alexander JH, Krasnow J, Krolick M, Cohen MG, Mehran R, Buller CE, Bode C, Zelenkofske SL, Rusconi CP, Becker RC. Pegnivacogin results in near complete FIX inhibition in acute coronary syndrome patients: RADAR pharmacokinetic and pharmacodynamic substudy. Eur Heart J 2011; 32: 2412-9.