The molecular basis of factor V and VIII procofactor activation

Journal of Thrombosis and Haemostasis

Volumn 7, Issue 12, 2009, Pages 1951-1961

  Camire, R M ^a   Bos, M H A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Factor V; Factor VIII; FX activation; Procofactor; Proteolytic activation; Prothrombin activation

Indexed keywords

BLOOD CLOTTING FACTOR 5; BLOOD CLOTTING FACTOR 8; PROTEIN PRECURSOR;

BLOOD CLOTTING; CHEMISTRY; HUMAN; METABOLISM; REVIEW;

BLOOD COAGULATION; FACTOR V; FACTOR VIII; HUMANS; PROTEIN PRECURSORS;

EID: 77449128728     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2009.03622.x     Document Type: Review

References (143)

1. Mann KG, Jenny RJ, Krishnaswamy S. Cofactor proteins in the assembly and expression of blood clotting enzyme complexes. Annual Rev Biochem 1988; 57: 915-56.
2. Kane WH, Davie EW. Blood Coagulation factors V and VIII: Structural and functional similarities and their relationship to hemorrhagic and thrombotic disorders. Blood 1988; 71: 539-55.
3. Mann KG, Nesheim ME, Church WR, Haley PE, Krishnaswamy S. Surface dependent reactions of the vitamin K-dependent enzyme complexes. Blood 1990; 76: 1-16.
4. Jacquemin M, De Maeyer M, D'Oiron R, Lavern'Homme R, Peerlinck K, Saint-Remy J-M. Molecular mechanisms of mild and moderate hemophilia A. J Thromb Haemost 2003; 1: 456-63.
5. Mannucci PM, Duga S, Peyvandi F. Recessively inherited coagulation disorders. Blood 2004; 104: 1243-52.
6. Fay PJ. Activation of factor VIII and mechanisms of cofactor action. Blood Rev 2004; 18: 1-15.
7. Lollar P. Structure and function of Factor VIII. Adv Exp Med Biol 1995; 386: 3-17.
8. Krishnaswamy S. Exosite-driven substrate specificity and function in coagulation. J Thromb Haemost 2005; 3: 54-67.
9. Bock PE, Panizzi P, Verhamme IM. Exosites in the substrate specificity of blood coagulation reactions. J Thromb Haemost 2007; 5 (Suppl. 1): 81-94.
10. Nesheim ME, Taswell JB, Mann KG. The contribution of bovine factor V and factor Va to the activity of prothrombinase. J Biol Chem 1979; 254: 10952-62.
11. Foster WB, Nesheim ME, Mann KG. The factor Xa-catalyzed activation of factor V. J Biol Chem 1983; 258: 13970-7.
12. Lollar P, Knutson G, Fass D. Activation of porcine FVIII: C by thrombin and FXa. Biochemistry 1985; 24: 8056-64.
13. Ware AG, Guest M, Seegers WH. Plasma accelerator factor and purified prothrombin activation. Science 1947; 106: 41-2.
14. Ware AG, Murphy R, Seegers WH. The function of Ac-globulin in blood clotting. Science 1947; 106: 618-9.
15. Owren PA. Parahaemophila: haemorrhagic diathesis due to absence of a previously unknown clotting factor. Lancet 1947; 249: 446-8.
16. Rapaport SI, Schiffman S, Patch MJ, Ames SB. The importance of activation of anti-haemophilic globulin and proaccelerin by traces of thrombin in the generation of intrinsic prothrombinase activity. Blood 1963; 21: 221-36.
17. Mann KG, Kalafatis M. Factor V: A combination of Dr. Jekyll and Mr. Hyde. Blood 2002; 101: 20-30.
18. Kane WH. Factor V. In: Colman RW, Marder VJ, Clowes AW, George JN, Goldhaber SZ, eds. Hemostasis and Thrombosis, 5th edn. Philadelphia: Lippincott Williams & Wilkins, 2006: p.177-92.
19. Fay PJ, Jenkins PV. Mutating factor VIII: lessons from structure to function. Blood Rev 2005; 19: 15-27.
20. Segers K, Dahlback B, Nicolaes GA. Coagulation factor V and thrombophilia: background and mechanisms. Thromb Haemost 2007; 98: 530-42.
21. Lenting PJ, Van Mourik JA, Mertens K. The life cycle of coagulation factor VIII in view of its structure and function. Blood 1998; 92: 3983-96.
22. Vehar GA, Davie EW. Preparation and properties of bovine factor VIII (antihemophilic factor). Biochemistry 1980; 19: 401-10.
23. Fass DN, Knutson GJ, Katzmann JA. Monoclonal antibodies to porcine factor VIII coagulant and their use in the isolation of active coagulant protein. Blood 1982; 59: 594-600.
24. Fulcher CA, Roberts J, Zimmerman TS. Thrombin proteolysis of purified FVIII procoagulant protein: Correlation of activation with generation of specific polypeptides. Blood 1983; 60: 807.
25. Lollar P, Knutson G, Fass D. Stabilization of thrombin activated porcine Factor VIII: C by Factor IXa and phospholipid. Blood 1984; 63: 1303-8.
26. Toole JJ, Knopf JL, Wozney JM, Sultman LA, Buecker JL, Pittman DD, Kaufman RJ, Brown E, Shoemaker C, Orr EC, Amphlett GW, Foster WB, Coe ML, Knutson GJ, Fass DN, Hewick RM. Molecular cloning of a cDNA encoding human antihaemophilic factor. Nature 1984; 312: 342-7.
27. Wood WI, Capon DJ, Simonsen CC, Eaton DL, Gitschier J, Keyt B, Seeburg PH, Smith DH, Hollingshead P, Wion KL, Delwart E, Tuddenham EGD, Vehar GA, Lawn RM. Expression of active human factor VIII from recombinant DNA clones. Nature 1984; 312: 330-6.
28. Eaton D, Rodriguez H, Vehar G. Proteolytic processing of human FVIII. Correlation of specific cleavages by thrombin FXa and activated protein C with activation and inactivation of Factor VIII coagulant activity. Biochemistry 1986; 25: 505-12.
29. Duffy EJ, Parker ET, Mutucumarana VP, Johnson AE, Lollar P. Binding of factor VIIIa and factor VIII to factor IXa on phospholipid vesicles. J Biol Chem 1992; 267: 17006-11.
30. Vehar G, Keyt B, Eaton D, Rodriguez H, O'Brien DP, Rotblat F, Oppermann H, Keck R, Wood W, Harkins R, Tuddenham EGD, Lawn R, Capon D. Structure of human factor VIII. Nature 1984; 312: 337-42.
31. Nogami K, Wakabayashi H, Schmidt K, Fay PJ. Altered interactions between the A1 and A2 subunits of factor VIIIa following cleavage of A1 subunit by factor Xa. J Biol Chem 2003; 278: 1634-41.
32. Esmon CT, Lollar P. Involvement of thrombin anion-binding exosites 1 and 2 in the activation of factor V and factor VIII. J Biol Chem 1996; 271: 13882-7.
33. Myles T, Yun TH, Leung LL. Structural requirements for the activation of human factor VIII by thrombin. Blood 2002; 100: 2820-6.
34. Newell JL, Fay PJ. Acidic residues C-terminal to the A2 domain facilitate thrombin-catalyzed activation of factor VIII. Biochemistry 2008; 47: 8786-95.
35. Nogami K, Zhou Q, Myles T, Leung LL, Wakabayashi H, Fay PJ. Exosite-interactive regions in the A1 and A2 domains of factor VIII facilitate thrombin-catalyzed cleavage of heavy chain. J Biol Chem 2005; 280: 18476-87.
36. Lollar P, Parker C. pH-dependent denaturation of thrombin-activated porcine factor VIII. J Biol Chem 1990; 265: 1688-92.
37. Fay PJ, Haidari PJ, Smudzin TM. Human factor VIIIa subunit structure. Reconstitution of factor VIIIa from the isolated A1/A3-C1-C2 dimer and A2 subunit. J Biol Chem 1991; 266: 8957-62.
38. Lollar P, Parker ET. Structural basis for the decreased procoagulant activity of human factor VIII compared to the porcine homolog. J Biol Chem 1991; 266: 12481-6.
39. Pittman DD, Kaufman RJ. Proteolytic requirements for thrombin activation of anti-hemophilic factor (factor VIII). Proc Natl Acad Sci USA 1988; 85: 2429-33.
40. Hamer RJ, Koedam JA, Beeser-Visser NH, Bertina RM, Van Mourik JA, Sixma JJ. Factor VIII binds to von Willebrand factor via its Mr-80, 000 light chain. Eur J Biochem 1987; 166: 37-43.
41. Hill-Eubanks DC, Parker CG, Lollar P. Differential proteolytic activation of factor VIII-von Willebrand factor complex by thrombin. Proc Natl Acad Sci USA 1989; 86: 6508-12.
42. Regan LM, Fay PJ. Cleavage of factor VIII light chain is required for maximal generation of factor VIIIa activity. J Biol Chem 1995; 270: 8546-52.
43. Donath M-JSH, Lenting PJ, Van Mourik JA, Mertens K. The role of cleavage of the light chain at positions Arg1689 or Arg1721 in subunit interactions and activation of human blood coagulation factor VIII. J Biol Chem 1995; 270: 3648-55.
44. Pipe SW, Kaufman RJ. Characterization of genetically engineered inactivation-resistant coagulation factor VIIIa. Proc Natl Acad Sci USA 1997; 94: 11851-6.
45. Newell JL, Fay PJ. Cleavage at Arg-1689 influences heavy chain cleavages during thrombin-catalyzed activation of factor VIII. J Biol Chem 2009; 284: 11080-9.
46. Newell JL, Fay PJ. Proteolysis at Arg740 facilitates subsequent bond cleavages during thrombin-catalyzed activation of factor VIII. J Biol Chem 2007; 282: 25367-75.
47. Shima M, Ware J, Yoshioka A, Fukui H, Fulcher CA. An arginine to cysteine amino acid substitution at a critical thrombin cleavage site in dysfunctional factor VIII molecule. Blood 1989; 74: 1612-7.
48. Arai M, Inaba H, Higuchi M, Antonarakis SE, Kazazian HH, Fujimaki M, Hoyer LW. Direct characterization of factor VIII in plasma: Detection of a mutation altering a thrombin cleavage site (arginine-372 to histidine). Proc Natl Acad Sci USA 1989; 86: 4277-81.
49. O'Brien DP, Pattinson JK, Tuddenham EGD. Purification and characterization of factor VIII 372-Cys: A hypofunctional cofactor from a patient with moderately severe haemophilia A. Blood 1990; 75: 1664-72.
50. Nogami K, Zhou Q, Wakabayashi H, Fay PJ. Thrombin-catalyzed activation of factor VIII with His substituted for Arg372 at the P1 site. Blood 2005; 105: 4362-8.
51. Fay PJ, Mastri M, Koszelak ME, Wakabayashi H. Cleavage of factor VIII heavy chain is required for the functional interaction of a2 subunit with factor IXa. J Biol Chem 2001; 276: 12434-9.
52. Gitschier J, Wood WI, Goralka TM, Wion KL, Chen EY, Eaton DH, Vehar GA, Capon DJ, Lawn RM. Characterization of the human factor VIII gene. Nature 1984; 312: 326-30.
53. Cripe LD, Moore D, Kane WH. Structure of the gene for human coagulation factor V. Biochemistry 1992; 31: 3777-85.
54. Shen BW, Spiegel PC, Chang CH, Huh JW, Lee JS, Kim J, Kim YH, Stoddard BL. The tertiary structure and domain organization of coagulation factor VIII. Blood 2008; 111: 1240-7.
55. Ngo JC, Huang M, Roth DA, Furie BC, Furie B. Crystal structure of human factor VIII: implications for the formation of the factor IXa-factor VIIIa complex. Structure 2008; 16: 597-606.
56. Curtis JE, Helgerson SL, Parker ET, Lollar P. Isolation and characterization of thrombin-activated human factor VIII. J Biol Chem 1994; 269: 6246-51.
57. O'Brien LM, Huggins CF, Fay PJ. Interacting regions in the A1 and A2 subunits of factor VIIIa identified by zero-length cross-linking. Blood 1997; 90: 3943-50.
58. Sudhakar K, Fay PJ. Exposed hydrophobic sites in factor VIII and isolated subunits. J Biol Chem 1996; 271: 23015-21.
59. Toole JJ, Pittman DD, Orr EC, Murtha P, Wasley LC, Kaufman RJ. A large region (~95 kDa) of human factor VIII is dispensable for in vitro procoagulant activity. Proc Natl Acad Sci USA 1986; 83: 5939-42.
60. Eaton DL, Wood WI, Eaton D, Hass PE, Hollingshead P, Wion KL, Mather J, Lawn RM, Vehar GA, Gorman C. Construction and characterization of an active factor VIII variant lacking the central one-third of the molecule. Biochemistry 1986; 25: 8343-7.
61. Pittman DD, Alderman EM, Tomkinson KN, Wang JH, Giles AR, Kaufman RJ. Biochemical, immunological, and in vivo functional characterization of B-domain-deleted FVIII. Blood 1993; 81: 2925-35.
62. Lind P, Larsson K, Spira J, Sydow-Backman M, Almstedt A, Gray E, Sandberg H. Novel forms of B-domain deleted recombinant factor VIII molecules. Construction and biochemical characterization. Eur J Biochem 1995; 232: 19-27.
63. Jenny RJ, Mann KG. Factor V: a prototype pro-cofactor for vitamin K-dependent enzyme complexes in blood clotting. Baillieres Clin Haematol 1989; 2: 919-44.
64. Tracy PB, Eide LL, Bowie EJW, Mann KG. Radioimmunoassay of factor V in human plasma and platelets. Blood 1982; 60: 59-63.
65. Gewirtz AM, Keefer M, Doshi K, Anyanayaki A, Hiu C, Colman RW. Biology of human megakaryocyte Factor V. Blood 1986; 67: 1639-42.
66. Chiu HC, Schick P, Colman RW. Biosynthesis of factor V in isolated guinea pig megakaryocytes. J Clin Invest 1985; 75: 339-46.
67. Giampaolo A, Vulcano F, Macioce G, Mattia G, Barca A, Milazzo L, Ciccarelli C, Hassan HJ. Factor-V expression in platelets from human megakaryocytic culture. Br J Haematol 2005; 128: 108-11.
68. Camire RM, Pollak ES, Kaushansky K, Tracy PB. Secretable human platelet-derived factor V originates from the plasma pool. Blood 1998; 92: 3035-41.
69. Christella M, Thomassen LG, Castoldi E, Tans G, Magdeleyns EJ, Delaunoit C, Debusscher L, Van Assche KJ, Rosing J. Endogenous factor V synthesis in megakaryocytes contributes negligibly to the platelet factor V pool. Haematologica 2003; 88: 1150-6.
70. Gould WR, Simioni P, Silveira JR, Tormene D, Kalafatis M, Tracy PB. Megakaryocytes endocytose and subsequently modify human factor V in vivo to form the entire pool of a unique platelet-derived cofactor. J Thromb Haemost 2005; 3: 450-6.
71. Bouchard BA, Williams JL, Meisler NT, Long MW, Tracy PB. Endocytosis of plasma-derived factor V by megakaryocytes occurs via a clathrin-dependent, specific membrane binding event. J Thromb Haemost 2005; 3: 541-51.
72. Bouchard BA, Meisler NT, Nesheim ME, Liu CX, Strickland DK, Tracy PB. A unique function for LRP-1: a component of a two-receptor system mediating specific endocytosis of plasma-derived factor V by megakaryocytes. J Thromb Haemost 2008; 6: 638-44.
73. Gould WR, Silveira JR, Tracy PB. Unique in vivo modifications of coagulation factor V produce a physically and functionally distinct platelet-derived cofactor: characterization of purified platelet-derived factor V/Va. J Biol Chem 2004; 279: 2383-93.
74. Monkovic DD, Tracy PB. Functional characterization of human platelet-released factor V and its activation by factor Xa and thrombin. J Biol Chem 1990; 265: 17132-40.
75. Camire RM, Kalafatis M, Cushman M, Tracy RP, Mann KG, Tracy PB. The mechanism of inactivation of human platelet factor Va from normal and activated protein C-resistant individuals. J Biol Chem 1995; 270: 20794-800.
76. Leiden cofactor activities are sustained on the surface of activated platelets despite the presence of activated protein C. Blood 1998; 91: 2818-29.
77. Suzuki K, Dahlbäck B, Stenflo J. Thrombin-catalyzed activation of human coagulation factor V. J Biol Chem 1982; 257: 6556-64.
78. Esmon CT, Owen WG, Duiguid D, Jackson CM. The action of thrombin on blood clotting factor V: Conversion of factor V to a prothrombin-binding protein. Biochim Biophys Acta 1973; 310: 289-94.
79. Monkovic DD, Tracy PB. Activation of human factor V by factor Xa and thrombin. Biochemistry 1990; 29: 1118-28.
80. Toso R, Camire RM. Removal of B-domain sequences from factor V rather than specific proteolysis underlies the mechanism by which cofactor function is realized. J Biol Chem 2004; 279: 21643-50.
81. Jenny RJ, Pittman DD, Toole JJ, Kriz RW, Aldape RA, Hewick RM, Kaufman RJ, Mann KG. Complete cDNA and derived amino acid sequence of human factor V. Proc Natl Acad Sci USA 1987; 84: 4846-50.
82. Esmon CT. The subunit structure of thrombin-activated factor V. Isolation of activated factor V, separation of subunits and reconstitution of biological activity. J Biol Chem 1979; 254: 964-73.
83. Nesheim ME, Mann KG. Thrombin-catalyzed activation of single chain bovine factor V. J Biol Chem 1979; 254: 1326-34.
84. Krishnaswamy S, Russell GD, Mann KG. The reassociation of factor Va from its isolated subunits. J Biol Chem 1989; 264: 3160-8.
85. Nesheim ME, Foster WB, Hewick R, Mann KG. Characterization of factor V activation intermediates. J Biol Chem 1984; 259: 3187-96.
86. Arocas V, Lemaire C, Bouton MC, Bezeaud A, Bon C, Guillin MC, Perrus MJ. Inhibition of thrombin-catalyzed factor V interaction by bothrojaracin. Thromb Haemost 1998; 79: 1157-61.
87. Bukys MA, Orban T, Kim PY, Beck DO, Nesheim ME, Kalafatis M. The structural integrity of anion binding exosite I of thrombin is required and sufficient for timely cleavage and activation of factor V and factor VIII. J Biol Chem 2006; 281: 18569-80.
88. Henriksen RA, Owen WG, Nesheim ME, Mann KG. Identification of a congenital dysthrombin, thrombin Quick. J Clin Invest 1980; 66: 934-40.
89. Myles T, Yun TH, Hall SW, Leung LL. An extensive interaction interface between thrombin and factor V is required for factor V activation. J Biol Chem 2001; 276: 25143-9.
90. Esmon CT, Esmon NL, Harris KW. Complex formation between thrombin and thrombomodulin inhibits both thrombin-catalyzed fibrin formation and factor V activation. J Biol Chem 1982; 257: 7944.
91. Dharmawardana KR, Bock PE. Demonstration of exosite I-dependent interactions of thrombin with human factor V and factor Va involving the factor Va heavy chain: analysis by affinity chromatography employing a novel method for active-site selective immobilization of serine proteinases. Biochemistry 1998; 37: 13143-52.
92. Segers K, Dahlbäck B, Bock PE, Tans G, Rosing J, Nicolaes GA. The role of thrombin exosites I and II in the activation of human coagulation factor V. J Biol Chem 2007; 282: 33915-24.
93. Dharmawardana KR, Olson ST, Bock PE. Role of regulatory exosite I in binding of thrombin to human factor V, factor Va, factor Va subunits, and activation fragments. J Biol Chem 1999; 274: 18635-43.
94. Marquette KA, Pittman DD, Kaufman RJ. The factor V B-domain provides two functions to facilitate thrombin cleavage and release of the light chain. Blood 1995; 86: 3026-34.
95. Pittman DD, Tomkinson KN, Michnick D, Seligsohn U, Kaufman RJ. Posttranslational sulfation of factor V is required for efficient thrombin cleavage and activation and for full procoagulant activity. Biochemistry 1994; 33: 6952-9.
96. Beck DO, Bukys MA, Singh LS, Szabo K, Kalafatis M. The contribution of amino acid region Asp695-Asp698 of factor V to procofactor activation and factor Va function. J Biol Chem 2004; 279: 3084-95.
97. Nesheim ME, Myrmel KH, Hibbard L, Mann KG. Isolation and characterization of single chain bovine factor V. J Biol Chem 1979; 254: 508-17.
98. Dahlbäck B. Human coagulation factor V purification and thrombin-catalyzed activation. J Clin Invest 1980; 66: 583-91.
99. Kane WH, Majerus PW. Purification and characterization of human coagulation factor V. J Biol Chem 1981; 256: 1002-7.
100. Oates AM, Salem HH. The regulation of human factor V by a neutrophil protease. Blood 1987; 70: 846-51.
101. Bradford HN, Annamalai A, Doshi K, Colman RW. Factor V is activated and cleaved by platelet calpain: comparison with thrombin proteolysis. Blood 1988; 71: 388-94.
102. Lee CD, Mann KG. Activation/inactivation of human factor V by plasmin. Blood 1989; 73: 185-90.
103. Yukelson LY, Tans G, Thomassen MCLGD, Hemker HC, Rosing J. Procoagulant activities in venoms from central Asian snakes. Toxicon 1991; 29: 491-502.
104. Gerads I, Tans G, Yukelson LY, Zwaal RFA, Rosing J. Activation of bovine factor V by an activator purified from the venom of Naja Naja Oxiana. Toxicon 1992; 30: 1065-79.
105. Bakker HM, Tans G, Thomassen MCLGD, Yukelson LY, Ebberink R, Hemker HC, Rosing J. Functional properties of human factor Va lacking the Asp683-Arg709 domain of the heavy chain. J Biol Chem 1994; 269: 20662-7.
106. Tans G, Nicolaes GAF, Christella M, Thomassen LGD, Hemker HC, Van Zonneveld A-J, Pannekoek H, Rosing J. Activation of human factor V by meizothrombin. J Biol Chem 1994; 269: 15969-72.
107. Allen DH, Tracy PB. Human coagulation factor V is activated to the functional cofactor by elastase and cathepsin G expressed at the monocyte surface. J Biol Chem 1995; 270: 1408-15.
108. Samis JA, Garrett M, Manuel RP, Nesheim ME, Giles AR. Human neutrophil elastase activates human factor V but inactivates thrombin-activated human factor V. Blood 1997; 90: 1065-74.
109. 1545 optimizes cofactor function by facilitating factor Xa binding. Biochemistry 1998; 37: 11896-906.
110. Rosing J, Govers-Riemslag JWP, Yukelson LY, Tans G. Factor V activation and inactivation by venom proteases. Haemostasis 2001; 31: 241-6.
111. Kalafatis M, Beck DO, Mann KG. Structural requirements for expression of factor Va activity. J Biol Chem 2004; 278: 33550-61.
112. Pittman DD, Marquette KA, Kaufman RJ. Role of the B domain for factor VIII and factor V expression and function. Blood 1994; 84: 4214-25.
113. Keller FG, Ortel TL, Quinn-Allen MA, Kane WH. Thrombin-catalyzed activation of recombinant human factor V. Biochemistry 1995; 34: 4118-24.
114. Thorelli E, Kaufman RJ, Dahlbäck B. Cleavage requirements for activation of factor V by factor Xa. Eur J Biochem 1997; 247: 12-20.
115. Steen M, Dahlbäck B. Thrombin-mediated proteolysis of factor V resulting in gradual B-domain release and exposure of the factor Xa-binding site. J Biol Chem 2002; 277: 38424-30.
116. Smith CM, Hanahan DJ. The activation of factor V by factor Xa or α-chymotrypsin and comparison with thrombin and RVV-V action. An improved factor V isolation procedure. Biochemistry 1976; 15: 1830-7.
117. Khan AM, James MNG. Molecular mechanisms for the conversion of zymogens to active proteolytic enzymes. Prot Sci 1998; 7: 815-36.
118. Katzmann JA, Nesheim ME, Hibbard LS, Mann KG. Isolation of functional human coagulation Factor V by using a hybridoma antibody. Proc Natl Acad Sci USA 1981; 78: 162-6.
119. Kane WH, Davie EW. Cloning of a cDNA coding for human factor V, a blood coagulation factor homologous to factor VIII and ceruloplasmin. Proc Natl Acad Sci USA 1986; 83: 6800-4.
120. Kane WH, Ichinose A, Hagen FS, Davie EW. Cloning of cDNAs coding for the heavy chain region and connecting region of human Factor V, a blood coagulation factor with four types of internal repeats. Biochemistry 1987; 26: 6508.
121. Dahlbäck B. Ultrastructure of human coagulation factor V. J Biol Chem 1985; 260: 1347-9.
122. Dahlbäck B. Bovine coagulation factor V visualized with electron microscopy. Ultrastructure of the isolated activated forms and of the activtion fragments. J Biol Chem 1986; 261: 9495-501.
123. Lampe PD, Pusey ML, Wei J, Nelsestuen GL. Electron microscopy and hydrodynamic properties of blood clotting factor V and activation fragments of factor V with phospholipid vesicles. J Biol Chem 1984; 259: 9959-64.
124. Mosesson MW, Nesheim ME, DiOrio JP, Hainfeld JF, Wall JS, Mann KG. Studies on the structure of bovine factor V by scanning transmission electron microscopy. Blood 1985; 65: 1158-62.
125. Fowler WE, Fay PJ, Arvan DS, Marder VJ. Electro microscopy of human factor V and factor VIII: Correlation of morphology with domain structure and localization of factor V activation fragments. Proc Natl Acad Sci USA 1990; 87: 7648-52.
126. Mosesson MW, Church WR, DiOrio JP, Krishnaswamy S, Mann KG, Hainfeld JF, Wall JS. Structural model of factors V and Va based on scanning transmission electron microscope images and mass analysis. J Biol Chem 1990; 265: 8863-8.
127. Laue TM, Johnson AE, Esmon CT, Yphantis DA. Structure of bovine blood coagulation factor Va. Determination of the subunit associations, molecular weights, and asymmetries by analytical ultracentrifugation. Biochemistry 1984; 23: 1339-48.
128. Kane WH, Devore-Carter D, Ortel TL. Expression and characterization of recombinant human factor V and a mutant lacking a major portion of the connecting region. Biochemistry 1990; 29: 6762-8.
129. Zhu H, Toso R, Camire RM. Inhibitory sequences within the B-domain stabilize circulating factor V in an inactive state. J Biol Chem 2007; 282: 15033-9.
130. Guinto ER, Esmon CT, Mann KG, MacGillivray RTA. The complete cDNA sequence of bovine coagulation factor V. J Biol Chem 1992; 267: 2971-8.
131. Yang TL, Cui J, Rehumtulla A, Yang A, Moussalli M, Kaufman RJ, Ginsburg D. The structure and function of murine factor V and its inactivation by protein C. Blood 1998; 91: 4593-9.
132. Grimm DR, Colter MB, Braunschweig M, Alexander LJ, Neame PJ, Kim HK. Porcine factor V: cDNA cloning, gene mapping, three-dimensional protein modeling of membrane binding sites and comparative anatomy of domains. Cell Mol Life Sci 2001; 58: 148-59.
133. Jiang Y, Doolittle RF. The evolution of vertebrate blood coagulation as viewed from a comparison of puffer fish and sea squirt genomes. Proc Natl Acad Sci USA 2003; 100: 7527-32.
134. Davidson CJ, Tuddenham EG, McVey JH. 450 million years of hemostasis. J Thromb Haemost 2003; 1: 1487-94.
135. Vos HL. Alignment of factor V sequences in twelve mammalian species shows several strongly conserved motifs in the B-domain. J Thromb Haemost 2005; 3: P0041.
136. Vos HL, Van Wijngaarden A. Variation and conservation of the B-domain of factor V. J Thromb Haemost 2009; 7: PP-MO-151.
137. Rao VS, Swarup S, Kini RM. The nonenzymatic subunit of pseutarin C, a prothrombin activator from eastern brown snake (Pseudonaja textilis) venom, shows structural similarity to mammalian coagulation factor V. Blood 2003; 102: 1347-54.
138. Welton RE, Burnell JN. Full length nucleotide sequence of a factor V-like subunit of oscutarin from Oxyuranus scutellatus scutellatus (coastal Taipan). Toxicon 2005; 46: 328-36.
139. St.Pierre L, Masci PP, Filippovich I, Sorokina N, Marsh N, Miller DJ, Lavin MF. Comparative analysis of prothrombin activators from the venom of Australian elapids. Mol Biol Evol 2005; 22: 1853-64.
140. Walker FJ, Owen WG, Esmon CT. Characterization of the prothrombin activator from the venom of Oxyuranus scutellatus scutellatus (taipan venom). Biochemistry 1980; 19: 1020-3.
141. Speijer H, Govers-Riemslag JW, Zwaal RF, Rosing J. Prothrombin activation by an activator from the venom of Oxyuranus scutellatus (Taipan snake). J Biol Chem 1986; 261: 13258-67.
142. Rao VS, Kini RM. Pseutarin C, a prothrombin activator from Pseudonaja textilis venom: its structural and functional similarity to mammalian coagulation factor Xa-Va complex. Thromb Haemost 2002; 88: 611-9.
143. Bos MH, Boltz M, St PL, Masci PP, De JJ, Lavin MF, Camire RM. Venom factor V from the common brown snake escapes hemostatic regulation through procoagulant adaptations. Blood 2009; 114: 686-92.