The role of cell surfaces and cellular receptors in the mode of action of recombinant factor VIIa

Blood Reviews

Volumn 29, Issue 4, 2015, Pages 223-229

  Lisman, Ton ^a   de Groot, Philip G ^b  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

EPCR; Factor VIIa; Fibrin; Hemophilia; Platelet; Prophylaxis; Tissue factor

Indexed keywords

BLOOD CLOTTING FACTOR 7A; CELL RECEPTOR; ENDOTHELIAL PROTEIN C RECEPTOR; ENZYME PRECURSOR; FIBRIN; PROTEIN VARIANT; PROTEINASE ACTIVATED RECEPTOR 1; PROTHROMBIN; RECOMBINANT BLOOD CLOTTING FACTOR 7A; THROMBIN; THROMBOCYTE RECEPTOR; THROMBOPLASTIN; RECOMBINANT FVIIA; RECOMBINANT PROTEIN;

BINDING AFFINITY; CELL SURFACE; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG RECEPTOR BINDING; DRUG TRANSPORT; ENDOTHELIUM CELL; ENZYME SYNTHESIS; FIBRIN CLOT; FIBRIN FORMATION; FIBRINOLYSIS; HEMOPHILIA; HEMOSTASIS; HUMAN; NONHUMAN; PARTIAL THROMBOPLASTIN TIME; PRIORITY JOURNAL; PROTEIN FUNCTION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; VASCULAR ENDOTHELIUM; WOUND HEALING; METABOLISM;

FACTOR VIIA; FIBRIN; HUMANS; RECOMBINANT PROTEINS; THROMBIN; THROMBOPLASTIN;

EID: 84937107105     PISSN: 0268960X     EISSN: 15321681     Source Type: Journal    
DOI: 10.1016/j.blre.2014.12.004     Document Type: Article

References (70)

1. Key N.S., Aledort L.M., Beardsley D., Cooper H.A., Davignon G., Ewenstein B.M., et al. Home treatment of mild to moderate bleeding episodes using recombinant factor VIIa (Novoseven) in haemophiliacs with inhibitors. Thromb Haemost Dec 1998, 80(6):912-918.
2. Shapiro A.D., Gilchrist G.S., Hoots W.K., Cooper H.A., Gastineau D.A. Prospective, randomised trial of two doses of rFVIIa (NovoSeven) in haemophilia patients with inhibitors undergoing surgery. Thromb Haemost Nov 1998, 80(5):773-778.
3. Logan A.C., Yank V., Stafford R.S. Off-label use of recombinant factor VIIa in U.S. hospitals: analysis of hospital records. Ann Intern Med Apr 19 2011, 154(8):516-522.
4. Mariani G., Napolitano M., Dolce A., Perez Garrido R., Batorova A., Karimi M., et al. Replacement therapy for bleeding episodes in factor VII deficiency. A prospective evaluation. Thromb Haemost Feb 2013, 109(2):238-247.
5. White G.C. Congenital and acquired platelet disorders: current dilemmas and treatment strategies. Semin Hematol Jan 2006, 43(1 Suppl. 1):S37-S41.
6. Hedner U. NovoSeven as a universal haemostatic agent. Blood Coagul Fibrinolysis Apr 2000, 11(Suppl. 1):S107-S111.
7. Simpson E., Lin Y., Stanworth S., Birchall J., Doree C., Hyde C. Recombinant factor VIIa for the prevention and treatment of bleeding in patients without haemophilia. Cochrane Database Syst Rev Mar 14 2012, 3:CD005011.
8. Levi M., Levy J.H., Andersen H.F., Truloff D. Safety of recombinant activated factor VII in randomized clinical trials. N Engl J Med Nov 4 2010, 363(19):1791-1800.
9. Lipworth W., Kerridge I., Little M., Day R. Evidence and desperation in off-label prescribing: recombinant factor VIIa. BMJ Jan 16 2012, 344:d7926.
10. Konkle B.A., Ebbesen L.S., Erhardtsen E., Bianco R.P., Lissitchkov T., Rusen L., et al. Randomized, prospective clinical trial of recombinant factor VIIa for secondary prophylaxis in hemophilia patients with inhibitors. J Thromb Haemost Sep 2007, 5(9):1904-1913.
11. Napolitano M., Giansily-Blaizot M., Dolce A., Schved J.F., Auerswald G., Ingerslev J., et al. Prophylaxis in congenital factor VII deficiency: indications, efficacy and safety. Results from the Seven Treatment Evaluation Registry (STER). Haematologica Apr 2013, 98(4):538-544.
12. Lisman T., Adelmeijer J., Cauwenberghs S., Van Pampus E.C., Heemskerk J.W., De Groot P.G. Recombinant factor VIIa enhances platelet adhesion and activation under flow conditions at normal and reduced platelet count. J Thromb Haemost Apr 2005, 3(4):742-751.
13. Kjalke M., Ezban M., Monroe D.M., Hoffman M., Roberts H.R., Hedner U. High-dose factor VIIa increases initial thrombin generation and mediates faster platelet activation in thrombocytopenia-like conditions in a cell-based model system. Br J Haematol Jul 2001, 114(1):114-120.
14. Torbet J. The thrombin activation pathway modulates the assembly, structure and lysis of human plasma clots in vitro. Thromb Haemost May 1995, 73(5):785-792.
15. Undas A., Ariens R.A. Fibrin clot structure and function: a role in the pathophysiology of arterial and venous thromboembolic diseases. Arterioscler Thromb Vasc Biol Dec 2011, 31(12):e88-e99.
16. Wolberg A.S., Allen G.A., Monroe D.M., Hedner U., Roberts H.R., Hoffman M. High dose factor VIIa improves clot structure and stability in a model of haemophilia B. Br J Haematol Dec 2005, 131(5):645-655.
17. He S., Blomback M., Jacobsson Ekman G., Hedner U. The role of recombinant factor VIIa (FVIIa) in fibrin structure in the absence of FVIII/FIX. J Thromb Haemost Jun 2003, 1(6):1215-1219.
18. Broze G.J., Higuchi D.A. Coagulation-dependent inhibition of fibrinolysis: role of carboxypeptidase-U and the premature lysis of clots from hemophilic plasma. Blood Nov 15 1996, 88(10):3815-3823.
19. Lisman T., Mosnier L.O., Lambert T., Mauser-Bunschoten E.P., Meijers J.C., Nieuwenhuis H.K., et al. Inhibition of fibrinolysis by recombinant factor VIIa in plasma from patients with severe hemophilia A. Blood Jan 1 2002, 99(1):175-179.
20. Mosnier L.O., Lisman T., van den Berg H.M., Nieuwenhuis H.K., Meijers J.C., Bouma B.N. The defective down regulation of fibrinolysis in haemophilia A can be restored by increasing the TAFI plasma concentration. Thromb Haemost Oct 2001, 86(4):1035-1039.
21. Brummel-Ziedins K.E., Branda R.F., Butenas S., Mann K.G. Discordant fibrin formation in hemophilia. J Thromb Haemost May 2009, 7(5):825-832.
22. Lisman T., Moschatsis S., Adelmeijer J., Nieuwenhuis H.K., De Groot P.G. Recombinant factor VIIa enhances deposition of platelets with congenital or acquired alpha IIb beta 3 deficiency to endothelial cell matrix and collagen under conditions of flow via tissue factor-independent thrombin generation. Blood Mar 1 2003, 101(5):1864-1870.
23. Lisman T., Adelmeijer J., Heijnen H.F., de Groot P.G. Recombinant factor VIIa restores aggregation of alphaIIbbeta3-deficient platelets via tissue factor-independent fibrin generation. Blood Mar 1 2004, 103(5):1720-1727.
24. Soslau G., Class R., Morgan D.A., Foster C., Lord S.T., Marchese P., et al. Unique pathway of thrombin-induced platelet aggregation mediated by glycoprotein Ib. J Biol Chem Jun 15 2001, 276(24):21173-21183.
25. Jarvis G.E., Atkinson B.T., Frampton J., Watson S.P. Thrombin-induced conversion of fibrinogen to fibrin results in rapid platelet trapping which is not dependent on platelet activation or GPIb. Br J Pharmacol Feb 2003, 138(4):574-583.
26. Hoffman M., Harger A., Lenkowski A., Hedner U., Roberts H.R., Monroe D.M. Cutaneous wound healing is impaired in hemophilia B. Blood Nov 1 2006, 108(9):3053-3060.
27. McDonald A., Hoffman M., Hedner U., Roberts H.R., Monroe D.M. Restoring hemostatic thrombin generation at the time of cutaneous wounding does not normalize healing in hemophilia B. J Thromb Haemost Aug 2007, 5(8):1577-1583.
28. Monroe D.M., Hoffman M., Roberts H.R., Hedner U. Progressive improvement in wound healing with increased therapy in haemophilia B mice. Haemophilia Nov 2013, 19(6):926-932.
29. van 't Veer C., Golden N.J., Mann K.G. Inhibition of thrombin generation by the zymogen factor VII: implications for the treatment of hemophilia A by factor VIIa. Blood Feb 15 2000, 95(4):1330-1335.
30. Butenas S., Brummel K.E., Branda R.F., Paradis S.G., Mann K.G. Mechanism of factor VIIa-dependent coagulation in hemophilia blood. Blood Feb 1 2002, 99(3):923-930.
31. Shibeko A.M., Woodle S.A., Lee T.K., Ovanesov M.V. Unifying the mechanism of recombinant FVIIa action: dose dependence is regulated differently by tissue factor and phospholipids. Blood Jul 26 2012, 120(4):891-899.
32. Augustsson C., Persson E. In vitro evidence of a tissue factor-independent mode of action of recombinant factor VIIa in hemophilia. Blood Nov 13 2014, 124(20):3172-3174.
33. ten Cate H., Bauer K.A., Levi M., Edgington T.S., Sublett R.D., Barzegar S., et al. The activation of factor X and prothrombin by recombinant factor VIIa in vivo is mediated by tissue factor. J Clin Invest Sep 1993, 92(3):1207-1212.
34. Rao L.V., Rapaport S.I. Factor VIIa-catalyzed activation of factor X independent of tissue factor: its possible significance for control of hemophilic bleeding by infused factor VIIa. Blood Mar 1 1990, 75(5):1069-1073.
35. Hoffman M., Monroe D.M., Roberts H.R. Human monocytes support factor X activation by factor VIIa, independent of tissue factor: implications for the therapeutic mechanism of high-dose factor VIIa in hemophilia. Blood Jan 1 1994, 83(1):38-42.
36. Monroe D.M., Hoffman M., Oliver J.A., Roberts H.R. Platelet activity of high-dose factor VIIa is independent of tissue factor. Br J Haematol Dec 1997, 99(3):542-547.
37. Gabriel D.A., Li X., Monroe D.M., Roberts H.R. Recombinant human factor VIIa (rFVIIa) can activate factor FIX on activated platelets. J Thromb Haemost Oct 2004, 2(10):1816-1822.
38. Persson E., Kjalke M., Olsen O.H. Rational design of coagulation factor VIIa variants with substantially increased intrinsic activity. Proc Natl Acad Sci U S A Nov 20 2001, 98(24):13583-13588.
39. Hoffman M., Volovyk Z., Persson E., Gabriel D.A., Ezban M., Monroe D.M. Platelet binding and activity of a factor VIIa variant with enhanced tissue factor independent activity. J Thromb Haemost Apr 2011, 9(4):759-766.
40. Lisman T., de Groot P.G., Lambert T., Rojkjaer R., Persson E. Enhanced in vitro procoagulant and antifibrinolytic potential of superactive variants of recombinant factor VIIa in severe hemophilia A. J Thromb Haemost Oct 2003, 1(10):2175-2178.
41. Tranholm M., Kristensen K., Kristensen A.T., Pyke C., Rojkjaer R., Persson E. Improved hemostasis with superactive analogs of factor VIIa in a mouse model of hemophilia A. Blood Nov 15 2003, 102(10):3615-3620.
42. Feng D., Whinna H., Monroe D., Stafford D.W. FVIIa as used pharmacologically is not TF dependent in hemophilia B mice. Blood Mar 13 2014, 123(11):1764-1766.
43. de Paula E.V., Kavakli K., Mahlangu J., Ayob Y., Lentz S.R., Morfini M., et al. Recombinant factor VIIa analog (vatreptacog alfa [activated]) for treatment of joint bleeds in hemophilia patients with inhibitors: a randomized controlled trial. J Thromb Haemost Jan 2012, 10(1):81-89.
44. Lentz S.R., Ehrenforth S., Karim F.A., Matsushita T., Weldingh K.N., Windyga J., et al. Recombinant factor VIIa analog in the management of hemophilia with inhibitors: results from a multicenter, randomized, controlled trial of vatreptacog alfa. J Thromb Haemost Aug 2014, 12(8):1244-1253.
45. Mahlangu J.N., Coetzee M.J., Laffan M., Windyga J., Yee T.T., Schroeder J., et al. Phase I, randomized, double-blind, placebo-controlled, single-dose escalation study of the recombinant factor VIIa variant BAY 86-6150 in hemophilia. J Thromb Haemost May 2012, 10(5):773-780.
46. Baglia F.A., Badellino K.O., Li C.Q., Lopez J.A., Walsh P.N. Factor XI binding to the platelet glycoprotein Ib-IX-V complex promotes factor XI activation by thrombin. J Biol Chem Jan 18 2002, 277(3):1662-1668.
47. Bradford H.N., Pixley R.A., Colman R.W. Human factor XII binding to the glycoprotein Ib-IX-V complex inhibits thrombin-induced platelet aggregation. J Biol Chem Jul 28 2000, 275(30):22756-22763.
48. Joseph K., Nakazawa Y., Bahou W.F., Ghebrehiwet B., Kaplan A.P. Platelet glycoprotein Ib: a zinc-dependent binding protein for the heavy chain of high-molecular-weight kininogen. Mol Med Aug 1999, 5(8):555-563.
49. White T.C., Berny M.A., Tucker E.I., Urbanus R.T., de Groot P.G., Fernandez J.A., et al. Protein C supports platelet binding and activation under flow: role of glycoprotein Ib and apolipoprotein E receptor 2. J Thromb Haemost Jun 2008, 6(6):995-1002.
50. De Marco L., Mazzucato M., Masotti A., Fenton J.W., Ruggeri Z.M. Function of glycoprotein Ib alpha in platelet activation induced by alpha-thrombin. J Biol Chem Dec 15 1991, 266(35):23776-23783.
51. Weeterings C., de Groot P.G., Adelmeijer J., Lisman T. The glycoprotein Ib-IX-V complex contributes to tissue factor-independent thrombin generation by recombinant factor VIIa on the activated platelet surface. Blood Oct 15 2008, 112(8):3227-3233.
52. Hoffman M., Monroe D. Endothelial protein C receptor is expressed on activated platelets and contributes to FVIIa binding. J Thromb Haemost 2013, 11(S2):218.
53. White-Adams T.C., Berny M.A., Tucker E.I., Gertz J.M., Gailani D., Urbanus R.T., et al. Identification of coagulation factor XI as a ligand for platelet apolipoprotein E receptor 2 (ApoER2). Arterioscler Thromb Vasc Biol Oct 2009, 29(10):1602-1607.
54. Pennings M.T., Derksen R.H., van Lummel M., Adelmeijer J., VanHoorelbeke K., Urbanus R.T., et al. Platelet adhesion to dimeric beta-glycoprotein I under conditions of flow is mediated by at least two receptors: glycoprotein Ibalpha and apolipoprotein E receptor 2[U+02B9]. J Thromb Haemost Feb 2007, 5(2):369-377.
55. Lopez-Vilchez I., Hedner U., Altisent C., Diaz-Ricart M., Escolar G., Galan A.M. Redistribution and hemostatic action of recombinant activated factor VII associated with platelets. Am J Pathol Jun 2011, 178(6):2938-2948.
56. Schut A.M., Hyseni A., Adelmeijer J., Meijers J.C., De Groot P.G., Lisman T. Sustained pro-haemostatic activity of rFVIIa in plasma and platelets in non-bleeding pigs may explain the efficacy of a once-daily prophylaxis in humans. Thromb Haemost Aug 2014, 112(2):304-310.
57. Ghosh S., Pendurthi U.R., Steinoe A., Esmon C.T., Rao L.V. Endothelial cell protein C receptor acts as a cellular receptor for factor VIIa on endothelium. J Biol Chem Apr 20 2007, 282(16):11849-11857.
58. Lopez-Sagaseta J., Montes R., Puy C., Diez N., Fukudome K., Hermida J. Binding of factor VIIa to the endothelial cell protein C receptor reduces its coagulant activity. J Thromb Haemost Sep 2007, 5(9):1817-1824.
59. Puy C., Lopez-Sagaseta J., Hermida J., Montes R. The endothelial cells downregulate the generation of factor VIIa through EPCR binding. Br J Haematol Apr 2010, 149(1):111-117.
60. Pendurthi U.R., Rao L.V. Factor VIIa interaction with endothelial cells and endothelial cell protein C receptor. Thromb Res Apr 2010, 125(Suppl. 1):S19-S22.
61. Pavani G., Ivanciu L., Faella A., Marcos-Contreras O.A., Margaritis P. The endothelial protein C receptor enhances hemostasis of FVIIa administration in hemophilic mice in vivo. Blood Aug 14 2014, 124(7):1157-1165.
62. Sen P., Gopalakrishnan R., Kothari H., Keshava S., Clark C.A., Esmon C.T., et al. Factor VIIa bound to endothelial cell protein C receptor activates protease activated receptor-1 and mediates cell signaling and barrier protection. Blood Mar 17 2011, 117(11):3199-3208.
63. Sundaram J., Keshava S., Gopalakrishnan R., Esmon C.T., Pendurthi U.R., Rao L.V. Factor VIIa binding to endothelial cell protein C receptor protects vascular barrier integrity in vivo. J Thromb Haemost May 2014, 12(5):690-700.
64. Mohan Rao L.V., Esmon C.T., Pendurthi U.R. Endothelial cell protein C receptor: a multiliganded and multifunctional receptor. Blood Sep 4 2014, 124(10):1553-1562.
65. Clark C.A., Vatsyayan R., Hedner U., Esmon C.T., Pendurthi U.R., Rao L.V. Endothelial cell protein C receptor-mediated redistribution and tissue-level accumulation of factor VIIa. J Thromb Haemost Nov 2012, 10(11):2383-2391.
66. Gopalakrishnan R., Hedner U., Clark C., Pendurthi U.R., Rao L.V. rFVIIa transported from the blood stream into tissues is functionally active. J Thromb Haemost Oct 2010, 8(10):2318-2321.
67. Gopalakrishnan R., Hedner U., Ghosh S., Nayak R.C., Allen T.C., Pendurthi U.R., et al. Bio-distribution of pharmacologically administered recombinant factor VIIa (rFVIIa). J Thromb Haemost Feb 2010, 8(2):301-310.
68. Sen P., Ghosh S., Ezban M., Pendurthi U.R., Rao L.V. Effect of glycoPEGylation on factor VIIa binding and internalization. Haemophilia Mar 2010, 16(2):339-348.
69. Ljung R., Karim F.A., Saxena K., Suzuki T., Arkhammar P., Rosholm A., et al. 40K glycoPEGylated, recombinant FVIIa: 3-month, double-blind, randomized trial of safety, pharmacokinetics and preliminary efficacy in hemophilia patients with inhibitors. J Thromb Haemost Jul 2013, 11(7):1260-1268.
70. Ivanciu L., Krishnaswamy S., Camire R.M. New insights into the spatiotemporal localization of prothrombinase in vivo. Blood Sep 11 2014, 124(11):1705-1714.