Optimization of factor VIII replacement therapy: Can structural studies help in evading antibody inhibitors?

British Journal of Haematology

Volumn 119, Issue 2, 2002, Pages 310-322

  Spiegel Jr , P Clint ^a   Stoddard, Barry L ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Antibody; Factor VIII; Haemophilia A; Inhibitor; X ray crystallography

Indexed keywords

ACTIVATED PROTHROMBIN COMPLEX; BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 8 ANTIBODY; EPITOPE; PHOSPHOLIPID; PROTHROMBIN COMPLEX; RECOMBINANT BLOOD CLOTTING FACTOR 7A; RECOMBINANT BLOOD CLOTTING FACTOR 8; SERINE PROTEINASE; VITAMIN K GROUP; VON WILLEBRAND FACTOR;

ALLERGIC REACTION; ANTIBODY TITER; ANTIGENICITY; BLOOD CLOTTING; CHILL; CROSS REACTION; CRYSTAL STRUCTURE; DRUG EFFICACY; DRUG HALF LIFE; FEVER; HEMOPHILIA A; HEMOSTASIS; HUMAN; IMMUNE RESPONSE; MUTATIONAL ANALYSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SIDE EFFECT; THROMBOCYTOPENIA; THROMBOSIS; TREATMENT OUTCOME; X RAY CRYSTALLOGRAPHY;

ANIMALS; BLOOD COAGULATION FACTOR INHIBITORS; CRYSTALLOGRAPHY, X-RAY; DOGS; EPITOPES; FACTOR VIII; HEMOPHILIA A; HUMANS; MALE; MICE; MUTATION; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY; STRUCTURE-ACTIVITY RELATIONSHIP; SWINE;

EID: 0036440602     PISSN: 00071048     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2141.2002.03845.x     Document Type: Review

References (100)

1. Antonarakis, S.E., Rossiter, J.P., Young, M., Horst, J., de Moerloose, P., Sommer, S.S., Ketterling, R.P., Kazazian, H.H., Negrier, Jr, C. & Vinciguerra, C. (1995) Factor VIII gene inversions in severe hemophilia A: Results of an international consortium study. Blood, 86, 2206-2212.
2. Barrow, R.T., Healey, J.F., Jacquemin, M.G., Saint-Remy, J.M. & Lollar, P. (2001) Antigenicity of putative phospholipid membrane-binding residues in factor VIII. Blood, 97, 169-174.
3. Baumgartner, S., Hofmann, K., Chiquet-Ehrismann, R. & Bucher, P. (1998) The discoidin domain family revisited: New members from prokaryotes and a homology-based fold prediction. Protein Science, 7, 1626-1631.
4. Bossi, P., Cabane, J., Ninet, J., Dhote, R., Hanslik, T., Chosidow, O., Jouan-Flahault, C., Horellou, M.H., Leynadier, F., Liozon, E., Pouchot, J., Robin, J.P., Sanderson, F., Schaeffer, A., Sicard, D., Staikowsky, F., Wechsler, B. & Zittoun, R. (1998) Acquired hemophilia due to factor VIII inhibitors in 34 patients. American Journal of Medicine, 105, 400-408.
5. Broze, Jr, G.J. & Miletich, J.P. (1987) Characterization of the inhibition of tissue factor in serum. Blood, 69, 150-155.
6. Broze, Jr, G.J., Leykam, J.E., Schwartz, B.D. & Miletich, J.P. (1985) Purification of human brain tissue factor. Journal of Biological Chemistry, 260, 10917-10920.
7. Broze, Jr, G.J., Girard, T.J., & Novotny, W.F. (1990) Regulation of coagulation by a multivalent Kunitz-type inhibitor. Biochemistry, 29, 7539-7546.
8. Davie, E.W. (1995) Biochemical and molecular aspects of the coagulation cascade. Thrombosis and Haemostasis, 74, 1-6.
9. Davie, E.W., Fujikawa, K. & Kisiel, W. (1991) The coagulation cascade: Initiation, maintenance, and regulation. Biochemistry, 30, 10363-10370.
10. Di Scipio, R.G., Hermodson, M.A. & Davie, E.W. (1977) Activation of human factor X (Stuart factor) by a protease from Russell's viper venom. Biochemistry, 16, 5253-5260.
11. van Dieijen, G., Tans, G., Rosing, J. & Hemker, H.C. (1981) The role of phospholipid and factor VIIIa in the activation of bovine factor X. Journal of Biological Chemistry, 256, 3433-3442.
12. Eaton, D., Rodriguez, H. & Vehar, G.A. (1986) Proteolytic processing of human factor VIII. Correlation of specific cleavages by thrombin, factor Xa, and activated protein C with activation and inactivation of factor VIII coagulant activity. Biochemistry, 25, 505-512.
13. Evatt, B.L., Austin, H., Leon, G., Ruiz-Saez, A. & De Bosch, N. (1999) Haemophilia therapy: Assessing the cumulative risk of HIV exposure by cryoprecipitate. Haemophilia, 5, 295-300.
14. Fay, P.J. (1999) Regulation of factor VIIIa in the intrinsic factor Xase. Thrombosis and Haemostasis, 82, 193-200.
15. Fay, P.J. & Koshibu, K. (1998) The A2 subunit of factor VIIIa modulates the active site of factor IXa. Journal of Biological Chemistry, 273, 19049-19054.
16. Fay, P.J. & Scandella, D. (1999) Human inhibitor antibodies specific for the factor VIII A2 domain disrupt the interaction between the subunit and factor IXa. Journal of Biological Chemistry, 274, 29826-29830.
17. Fay, P.J., Beattie, T., Huggins, C.F. & Regan, L.M. (1994) Factor VIIIa A2 subunit residues 558-565 represent a factor IXa interactive site. Journal of Biological Chemistry, 269, 20522-20527.
18. Fijnvandraat, K., Turenhout, E.A., van den Brink, E.N., ten Cate, J.W., van Mourik, J.A., Peters, M. & Voorberg, J. (1997) The missense mutation Arg593 → Cys is related to antibody formation in a patient with mild hemophilia A. Blood, 89, 4371-4377.
19. Foster, P.A., Fulcher, C.A., Marti, T., Titani, K. & Zimmerman, T.S. (1987) A major factor VIII binding domain resides within the amino-terminal 272 amino acid residues of von Willebrand factor. Journal of Biological Chemistry, 262, 8443-8446.
20. Foster, P.A., Fulcher, C.A., Houghten, R.A., de Graaf Mahoney, S. & Zimmerman, T.S. (1988) Localization of the binding regions of a murine monoclonal anti-factor VIII antibody and a human anti-factor VIII alloantibody, both of which inhibit factor VIII procoagulant activity, to amino acid residues threonine351-serine365 of the factor VIII heavy chain. Journal of Clinical Investigations, 82, 123-128.
21. Fulcher, C.A., de Graaf Mahoney, S. & Zimmerman, T.S. (1987) FVIII inhibitor IgG subclass and FVIII polypeptide specificity determined by immunoblotting. Blood, 69, 1475-1480.
22. Garvey, M.B. (2002) Porcine factor VIII in the treatment of high-titre inhibitor patients. Haemophilia, 8, 5-8.
23. Gilbert, G.E. & Drinkwater, D. (1993) Specific membrane binding of factor VIII is mediated by O-phospho-L- serine, a moiety of phosphatidylserine. Biochemistry, 32, 9577-9585.
24. Gilbert, G.E., Kaufman, R.J., Arena, A.A., Miao, H. & Pipe, S.W. (2002) Four hydrophobic amino acids of the factor VIII C2 domain are constituents of both the membrane-binding and von Willebrand factor-binding motifs. Journal of Biological Chemistry, 277, 6374-6381.
25. Gribble, J. & Garvey, M.B. (2000) Porcine factor VIII provides clinical benefit to patients with high levels of inhibitors to human and porcine factor VIII. Haemophilia, 6, 482-485.
26. Hacker, M.R., Geraghty, S. & Manco-Johnson, M. (2001) Barriers to compliance with prophylaxis therapy in haemophilia. Haemophilia, 7, 392-396.
27. Hay, C.R. (1998) Factor VIII inhibitors in mild and moderate-severity haemophilia A. Haemophilia, 4, 558-563.
28. Hay, C.R. (2002) Porcine factor VIII: Current status and future developments. Haemophilia, 8, 24-27.
29. Hay, C.R., Lozier, J.N., Lee, C.A., Lafan, M., Tradati, H., Santagostino, E., Ciavarella, N., Schiavoni, M., Fukui, H., Yoshioka, A., Teitel, J., Mannucci, P.M. & Kasper, C.K. (1994) Porcine factor VIII therapy in patients with congenital hemophilia and inhibitors: Efficacy, patient selection, and side effects. Seminars in Hematology, 31, 20-25.
30. Hay, C.R., Ludlam, C.A., Colvin, B.T., Hill, F.G., Preston, F.E., Wasseem, N., Bagnall, R., Peake, I.R., Berntorp, E., Mauser Bunschoten, E.P., Fijnvandraat, K., Kasper, C.K., White, G. & Santagostino, E. (1998) Factor VIII inhibitors in mild and moderate-severity haemophilia A. UK Haemophilia Centre Directors Organisation. Thrombosis and Haemostasis, 79, 762-766.
31. Healey, J.F., Lubin, I.M., Nakai, H., Saenko, E.L., Hoyer, L.W., Scandella, D. & Lollar, P. (1995) Residues 484-508 contain a major determinant of the inhibitory epitope in the A2 domain of human factor VIII. Journal of Biological Chemistry, 270, 14505-14509.
32. Healey, J.F., Barrow, R.T., Tamim, H.M., Lubin, I.M., Shima, M., Scandella, D. & Lollar, P. (1998) Residues Glu2181-Val2243 contain a major determinant of the inhibitory epitope in the C2 domain of human factor VIII. Blood, 92, 3701-3709.
33. Hoots, W.K. (2001) The future of plasma-derived clotting factor concentrates. Haemophilia, 7, 4-9.
34. Hoyer, L.W. (1994) Hemophilia A. New England Journal of Medicine, 330, 38-47.
35. Hoyer, L.W. (1995) Why do so many haemophilia A patients develop an inhibitor? British Journal of Haematology, 90, 498-501.
36. Hoyer, L.W. & Scandella, D. (1994) Factor VIII inhibitors: Structure and function in autoantibody and hemophilia A patients. Seminars in Hematology, 31, 1-5.
37. Izumi, T., Kim, S.W., Greist, A., Macedo-Ribeiro, S., Fuentes-Prior, P., Bode, W., Kane, W.H. & Ortel, T.L. (2001) Fine mapping of inhibitory anti-factor V antibodies using factor V C2 domain mutants. Identification of two antigenic epitopes involved in phospholipid binding. Thrombosis and Haemostasis, 85, 1048-1054.
38. Jacquemin, M.G., Desqueper, B.G., Benhida, A., Vander Elst, L., Hoylaerts, M.F., Bakkus, M., Thielemans, K., Arnout, J., Peerlinck, K., Gilles, J.G., Vermylen, J. & Saint-Remy, J.M. (1998) Mechanism and kinetics of factor VIII inactivation: Study with an IgG4 monoclonal antibody derived from a hemophilia A patient with inhibitor. Blood, 92, 496-506.
39. Jacquemin, M., Pratt, K.P., Spiegel, Jr, P.C., Stoddard, B.L., Desqueper, B.G., Lavend'homme, R., Benhida, A., Gilles, J.G., Peerlinck, K., Vermylen, J., d'Oiron, R., Saint-Remy, J.M. & Lavergne, J.M. (2001) Deletion of residue Ala2201 in the factor VIII C2 domain results in mild haemophilia A and destroys a major antigenic determinant recognised by factor VIII inhibitor antibodies. Thrombosis and Haemostasis, July Supplement (in press).
40. Kane, W.H. & Davie, E.W. (1988) Blood coagulation factors V and VIII: Structural and functional similarities and their relationship to hemorrhagic and thrombotic disorders. Blood, 71, 539-555.
41. Komiyama, Y., Pedersen, A.H. & Kisiel, W. (1990) Proteolytic activation of human factors IX and X by recombinant human factor VIIa: Effects of calcium, phospholipids, and tissue factor. Biochemistry, 29, 9418-9425.
42. Koshihara, K., Qian, J., Lollar, P. & Hoyer, L.W. (1995) Immunoblot cross-reactivity of factor VIII inhibitors with porcine factor VIII. Blood, 86, 2183-2190.
43. Kulkarni, R., Aledort, L.M., Berntorp, E., Brackman, H.H., Brown, D., Cohen, A.R., Ewing, N.P., Gringeri, A., Gruppo, R., Hoots, K., Leissenger, C., Peerlinck, K., Poon, M.C. & Wong, W.Y. (2001) Therapeutic choices for patients with hemophilia and high-titer inhibitors. American Journal of Hematology, 67, 240-246.
44. Lapan, K.A. & Fay, P.J. (1997) Localization of a factor X interactive site in the A1 subunit of factor VIIIa. Journal of Biological Chemistry, 272, 2082-2088.
45. Lapan, K.A. & Fay, P.J. (1998) Interaction of the A1 subunit of factor VIIIa and the serine protease domain of factor X identified by zero-length cross-linking. Thrombosis and Haemostasis, 80, 418-422.
46. Lawson, J.H., Kalafatis, M., Stram, S. & Mann, K.G. (1994) A model for the tissue factor pathway to thrombin. I. An empirical study. Journal of Biological Chemistry, 269, 23357-23366.
47. Lenting, P.J., Donath, M.J., van Mourik, J.A. & Mertens, K. (1994) Identification of a binding site for blood coagulation factor IXa on the light chain of human factor VIII. Journal of Biological Chemistry, 269, 7150-7155.
48. Lenting, P.J., van de Loo, J.W., Donath, M.J., van Mourik, J.A. & Mertens, K. (1996) The sequence Glu1811-Lys1818 of human blood coagulation factor VIII comprises a binding site for activated factor IX. Journal of Biological Chemistry, 271, 1935-1940.
49. Lenting, P.J., van Mourik, J.A. & Mertens, K. (1998) The life cycle of coagulation factor VIII in view of its structure and function. Blood, 92, 3983-3996.
50. Levine, P.H. & Brettler, D.B. (1991) Clinical Aspects and Therapy for Hemophilia A. In: Hematology: Basic Principles and Practice (ed. by R. Hoffman, E.J. Benz, S.J. Shattil, B. Furie & H.J. Cohen), pp. 1290-1304. Churchill Livingstone, New York.
51. Liu, M.L., Shen, B.W., Nakaya, S., Pratt, K.P., Fujikawa, K., Davie, E.W., Stoddard, B.L. & Thompson, A.R. (2000) Hemophilic factor VIII C1- and C2-domain missense mutations and their modeling to the 1.5-angstrom human C2-domain crystal structure. Blood, 96, 979-987.
52. Lubin, I.M., Healey, J.F., Barrow, R.T., Scandella, D. & Lollar, P. (1997) Analysis of the human factor VIII A2 inhibitor epitope by alanine scanning mutagenesis. Journal of Biological Chemistry, 272, 30191-30195.
53. Lusher, J.M. (1994) Use of prothrombin complex concentrates in management of bleeding in hemophiliacs with inhibitors - Benefits and limitations. Seminars in Hematology, 31, 49-52.
54. Macedo-Ribeiro, S., Bode, W., Huber, R., Quinn-Allen, M.A., Kim, S.W., Ortel, T.L., Bourenkov, G.P., Bartunik, H.D., Stubbs, M.T., Kane, W.H. & Fuentes-Prior, P. (1999) Crystal structures of the membrane-binding C2 domain of human coagulation factor V. Nature, 402, 434-439.
55. McMillan, C.W., Shapiro, S.S., Whitehurst, D., Hoyer, L.W., Rao, A.V. & Lazerson, J. (1988) The natural history of factor VIII: C inhibitors in patients with hemophilia A: A national cooperative study. II. Observations on the initial development of factor VIII: C inhibitors. Blood, 71, 344-348.
56. Mann, K.G. (1999) Biochemistry and physiology of blood coagulation. Thrombosis and Haemostasis, 82, 165-174.
57. Mann, K.G., Nesheim, M.E., Church, W.R., Haley, P. & Krishnaswamy, S. (1990) Surface-dependent reactions of the vitamin K-dependent enzyme complexes. Blood, 76, 1-16.
58. Mauser-Bunschoten, E.P., van der Bom, J.G., Bongers, M., Twijnstra, M., Roosendaal, G., Fischer, K. & van den Berg, H.M. (2001) Purity of factor VIII product and incidence of inhibitors in previously untreated patients with haemophilia A. Haemophilia, 7, 364-368.
59. Naito, K. & Fujikawa, K. (1991) Activation of human blood coagulation factor XI independent of factor XII. Factor XI is activated by thrombin and factor XIa in the presence of negatively charged surfaces. Journal of Biological Chemistry, 266, 7353-7358.
60. Nogami, K., Shima, M., Hosokawa, K., Suzuki, T., Koide, T., Saenko, E.L., Scandella, D., Shibata, M., Kamisue, S., Tanaka, I. & Yoshioka, A. (1999) Role of factor VIII C2 domain in factor VIII binding to factor Xa. Journal of Biological Chemistry, 274, 31000-31007.
61. Nogami, K., Shima, M., Hosokawa, K., Nagata, M., Koide, T., Saenko, E.L., Tanaka, I., Shibata, M. & Yoshioka, A. (2000) Factor VIII C2 domain contains the thrombin-binding site responsible for thrombin-catalyzed cleavage at Arg1689. Journal of Biological Chemistry, 275, 25774-25780.
62. Pasi, K.J. (2001) Gene therapy for haemophilia. British Journal of Haematology, 115, 744-757.
63. Pellequer, J.L., Gale, A.J., Griffin, J.H. & Getzoff, E.D. (1998) Homology models of the C domains of blood coagulation factors V and VIII: A proposed membrane binding mode for FV and FVIII C2 domains. Blood Cells and Molecular Disease, 24, 448-461.
64. Pemberton, S., Lindley, P., Zaitsev, V., Card, G., Tuddenham, E.G. & Kemball-Cook, G. (1997) A molecular model for the triplicated A domains of human factor VIII based on the crystal structure of human ceruloplasmin. Blood, 89, 2413-2421.
65. Penner, J.A. (2001) Haemophilic patients with inhibitors to factor VIII or IX: Variables affecting treatment response. Haemophilia, 7, 103-108.
66. Philipp, C.S. (2001) Viral safety of a pasteurized, monoclonal antibody-purified factor VIII concentrate in previously untreated haemophilia A patients. Haemophilia, 7, 146-153.
67. Pratt, K.P., Shen, B.W., Takeshima, K., Davie, E.W., Fujikawa, K. & Stoddard, B.L. (1999) Structure of the C2 domain of human factor VIII at 1.5 A resolution. Nature, 402, 439-442.
68. Precup, J.W., Kline, B.C. & Fass, D.N. (1991) A monoclonal antibody to factor VIII inhibits von Willebrand factor binding and thrombin cleavage. Blood, 77, 1929-1936.
69. Rao, L.V. & Rapaport, S.I. (1987) Studies of a mechanism inhibiting the initiation of the extrinsic pathway of coagulation. Blood, 69, 645-651.
70. Rapaport, S.I. (1989) Inhibition of factor VIIa/tissue factor-induced blood coagulation: With particular emphasis upon a factor Xa-dependent inhibitory mechanism. Blood, 73, 359-365.
71. Rizza, C.R. & Biggs, R. (1973) The treatment of patients who have factor-VIII antibodies. British Journal of Haematology, 24, 65-82.
72. Rossi, F. (2001) Regulatory perspective on making a therapeutic choice for anti-haemophilic factors. Haemophilia, 7, 123-126.
73. Saenko, E.L. & Scandella, D. (1995) A mechanism for inhibition of factor VIII binding to phospholipid by von Willebrand factor. Journal of Biological Chemistry, 270, 13826-13833.
74. Saenko, E.L. & Scandella, D. (1997) The acidic region of the factor VIII light chain and the C2 domain together form the high affinity binding site for von Willebrand factor. Journal of Biological Chemistry, 272, 18007-18014.
75. Saenko, E.L., Shima, M., Rajalakshmi, K.J. & Scandella, D. (1994) A role for the C2 domain of factor VIII in binding to von Willebrand factor. Journal of Biological Chemistry, 269, 11601-11605.
76. Saenko, E., Sarafanov, A., Greco, N., Shima, M., Loster, K., Schwinn, H. & Josic, D. (1999) Use of surface plasmon resonance for studies of protein-protein and protein-phospholipid membrane interactions. Application to the binding of factor VIII to von Willebrand factor and to phosphatidylserine-containing membranes. Journal of Chromatography A, 852, 59-71.
77. Saenko, E., Sarafanov, A., Ananyeva, N., Behre, E., Shima, M., Schwinn, H. & Josic, D. (2001) Comparison of the properties of phospholipid surfaces formed on HPA and L1 biosensor chips for the binding of the coagulation factor VIII. Journal of Chromatography, 921, 49-56.
78. Saenko, E.L., Ananyeva, N.M., Kouiavskaia, D.V., Khrenov, A.V., Anderson, J.A., Shima, M., Qian, J. & Scott, D. (2002) Haemophilia A: Effects of inhibitory antibodies on factor VIII functional interactions and approaches to prevent their action. Haemophilia, 8, 1-11.
79. Santagostino, E., Gringeri, A., Tagliavacca, L. & Mannucci, P.M. (1995) Inhibitors to factor VIII in a family with mild hemophilia: Molecular characterization and response to factor VIII and desmopressin. Thrombosis and Haemostasis, 74, 619-621.
80. Scandella, D., DeGraaf Mahoney, S., Mattingly, M., Roeder, D., Timmons, L. & Fulcher, C.A. (1988) Epitope mapping of human factor VIII inhibitor antibodies by deletion analysis of factor VIII fragments expressed in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 85, 6152-6156.
81. Scandella, D., Mattingly, M., de Graaf, S. & Fulcher, C.A. (1989) Localization of epitopes for human factor VIII inhibitor antibodies by immunoblotting and antibody neutralization. Blood, 74, 1618-1626.
82. Scandella, D., Mattingly, M. & Prescott, R. (1993) A recombinant factor VIII A2 domain polypeptide quantitatively neutralizes human inhibitor antibodies that bind to A2. Blood, 82, 1767-1775.
83. Scandella, D., Gilbert, G.E., Shima, M., Nakai, H., Eagleson, C., Felch, M., Prescott, R., Rajalakshmi, K.J., Hoyer, L.W. & Saenko, E. (1995) Some factor VIII inhibitor antibodies recognize a common epitope corresponding to C2 domain amino acids 2248 through 2312, which overlap a phospholipid-binding site. Blood, 86, 1811-1819.
84. Scandella, D.H., Nakai, H., Felch, M., Mondorf, W., Scharrer, I., Hoyer, L.W. & Saenko, E.L. (2001) In hemophilia A and auto-antibody inhibitor patients: The factor VIII A2 domain and light chain are most immunogenic. Thrombosis Research, 101, 377-385.
85. Scharrer, I. (1999) Recombinant factor VIIa for patients with inhibitors to factor VIII or IX or factor VII deficiency. Haemophilia, 5, 253-259.
86. Scharrer, I., Bray, G.L. & Neutzling, O. (1999) Incidence of inhibitors in haemophilia A patients - A review of recent studies of recombinant and plasma-derived factor VIII concentrates. Haemophilia, 5, 145-154.
87. Schwaab, R., Brackmann, H.H., Meyer, C., Seehafer, J., Kirchgesser, M., Haack, A., Olek, K., Tuddenham, E.G. & Oldenburg, J. (1995) Haemophilia A: Mutation type determines risk of inhibitor formation. Thrombosis and Haemostasis, 74, 1402-1406.
88. Shima, M., Yoshioka, A., Nakajima, M., Nakai, H. & Fukui, H. (1992) A monoclonal antibody (NMC-VIII/10) to factor VIII light chain recognizing Glu1675-Glu1684 inhibits factor VIII binding to endogenous von Willebrand factor in human umbilical vein endothelial cells. British Journal of Haematology, 81, 533-538.
89. Shima, M., Scandella, D., Yoshioka, A., Nakai, H., Tanaka, I., Kamisue, S., Terada, S. & Fukui, H. (1993) A factor VIII neutralizing monoclonal antibody and a human inhibitor alloantibody recognizing epitopes in the C2 domain inhibit factor VIII binding to von Willebrand factor and to phosphatidylserine. Thrombosis and Haemostasis, 69, 240-246.
90. Shima, M., Nakai, H., Scandella, D., Tanaka, I., Sawamoto, Y., Kamisue, S., Morichika, S., Murakami, T. & Yoshioka, A. (1995) Common inhibitory effects of human anti-C2 domain inhibitor alloantibodies on factor VIII binding to von Willebrand factor. British Journal of Haematology, 91, 714-721.
91. Spiegel, Jr, P.C., Jacquemin, M., Saint-Remy, J.M., Stoddard, B.L. & Pratt, K.P. (2001) Structure of a factor VIII C2 domain-immunoglobulin G4kappa Fab complex: Identification of an inhibitory antibody epitope on the surface of factor VIII. Blood, 98, 13-19.
92. Srivastava, A. (1999) Factor replacement for haemophilia: Should cryoprecipitate be used? Haemophilia, 5, 301-305.
93. Stoilova-McPhie, S., Villoutreix, B.O., Mertens, K., Kemball-Cook, G. & Holzenburg, A. (2002) 3-Dimensional structure of membrane-bound coagulation factor VIII: Modeling of the factor VIII heterodimer within a 3-dimensional density map derived by electron crystallography. Blood, 99, 1215-1223.
94. Stoylova, S.S., Lenting, P.J., Kemball-Cook, G. & Holzenburg, A. (1999) Electron crystallography of human blood coagulation factor VIII bound to phospholipid monolayers. Journal of Biological Chemistry, 274, 36573-36578.
95. Toole, J.J. Knopf, J.L., Wozney, J.M., Sultzman, L.A., Buecker, J.L., Pittman, D.D., Kaufman, R.J., Brown, E., Shoemaker, C., Orr, E.C., Amphlett, G.W., Foster, W.B., Coe, M.L., Knutson, G.J., Fass, D.N. & Hewick, R.M. (1984) Molecular cloning of a cDNA encoding human antihaemophilic factor. Nature, 312, 342-347.
96. Tracy, P.B., Nesheim, M.E. & Mann, K.G. (1981) Coordinate binding of factor Va and factor Xa to the unstimulated platelet. Journal of Biological Chemistry, 256, 743-751.
97. Tuddenham, E.G., Schwaab, R., Seehafer, J., Millar, D.S., Gitschier, J., Higuchi, M., Bidichandani, S., Connor, J.M., Hoyer, L.W. & Yoshioka, A. (1994) Haemophilia A: Database of Nucleotide Substitutions, Deletions, Insertions and Rearrangements of the Factor VIII Gene, second edition. Nucleic Acids Research, 22, 4851-4868.
98. Vehar, G.A., Keyt, B., Eaton, D., Rodriguez, H., O'Brien, D.P., Rotblat, F., Oppermann, H., Keck, R., Wood, W.I., Harkins, R.N., Tuddenham, E.G.D., Lawn, R.M. & Capon, D.J. (1984) Structure of human factor VIII. Nature, 312, 337-342.
99. Ware, J., Toomey, J.R. & Stafford, D.W. (1988) Localization of a factor VIII-inhibiting antibody epitope to a region between residues 338 and 362 of factor VIII heavy chain. Proceedings of the National Academy of Sciences of the United States of America, 85, 3165-3169.
100. Zhong, D., Saenko, E.L., Shima, M., Felch, M. & Scandella, D. (1998) Some human inhibitor antibodies interfere with factor VIII binding to factor IX. Blood, 92, 136-142.