Effects of replacement of factor VIII amino acids Asp519 and Glu665 with val on plasma survival and efficacy in vivo

AAPS Journal

Volumn 16, Issue 5, 2014, Pages 1038-1045

  Kosloski, Matthew P ^a   Shetty, Krithika A ^a   Wakabayashi, Hironao ^b   Fay, Philip J ^b   Balu Iyer, Sathy V ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

efficacy; FVIII; Hemophilia A; immunogenicity; mutant

Indexed keywords

ASPARTIC ACID; BLOOD CLOTTING FACTOR 8; GLUTAMIC ACID; VALINE; F8 PROTEIN, HUMAN; HEMOSTATIC AGENT;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; AREA UNDER THE CURVE; ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; DRUG CLEARANCE; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG HALF LIFE; DRUG STABILITY; DRUG STRUCTURE; FLUORESCENCE; HEMOPHILIA A; HEMOSTASIS; IMMUNE RESPONSE; IMMUNOGENICITY; IN VIVO STUDY; MALE; MAXIMUM PLASMA CONCENTRATION; MOUSE; NONHUMAN; PHARMACODYNAMICS; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; ANIMAL; BIOLOGICAL MODEL; BLOOD; C57BL MOUSE; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; GENETICS; IMMUNOLOGY; INTRAVENOUS DRUG ADMINISTRATION; MUTANT MOUSE STRAIN; MUTATION; PROTEIN ENGINEERING; STRUCTURE ACTIVITY RELATION;

AMINO ACID SUBSTITUTION; ANIMALS; DISEASE MODELS, ANIMAL; DRUG STABILITY; FACTOR VIII; HEMOPHILIA A; HEMOSTASIS; HEMOSTATICS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; INJECTIONS, INTRAVENOUS; MALE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTATION; PROTEIN ENGINEERING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84908356007     PISSN: None     EISSN: 15507416     Source Type: Journal    
DOI: 10.1208/s12248-014-9627-2     Document Type: Article

References (46)

1. Lenting PJ, Schooten CJMV, Denis CV. Clearance mechanisms of von Willebrand factor and factor VIII. J Thromb Haemost. 2007;5(7):1353-60. (Pubitemid 46965358)
2. Fay PJ. Activation of factor VIII and mechanisms of cofactor action. Blood Rev. 2004;18(1):1-15. (Pubitemid 38200498)
3. Kaufman RJ, Wasley LC, Dorner AJ. Synthesis, processing, and secretion of recombinant human factor VIII expressed in mammalian cells. J Biol Chem. 1988;263(13):6352-62.
4. Eaton D, Rodriguez H, Vehar GA. 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. 1986;25(2):505-12. (Pubitemid 16053817)
5. Fay PJ, Haidaris PJ, Smudzin TM. Human factor VIIIa subunit structure. Reconstruction of factor VIIIa from the isolated A1/A3-C1-C2 dimer and A2 subunit. J Biol Chem. 1991;266(14):8957-62. (Pubitemid 21906604)
6. Bevers EM, Tilly RHJ, Senden JMG, Comfurius P, Zwaal RFA. Exposure of endogenous phosphatidylserine at the outer surface of stimulated platelets is reversed by restoration of aminophospholipid translocase activity. Biochemistry. 1989;28(6):2382-7. (Pubitemid 19094351)
7. Ahmad SS, Scandura JM, Walsh PN. Structural and functional characterization of platelet receptor-mediated factor VIII binding. J Biol Chem. 2000;275(17):13071-81. (Pubitemid 30241469)
8. Wakabayashi H, Varfaj F, Deangelis J, Fay PJ. Generation of enhanced stability factor VIII variants by replacement of charged residues at the A2 domain interface. Blood. 2008;112(7):2761-9.
9. Pemberton S, Lindley P, Zaitsev V, Card G, Tuddenham EG, Kemball-Cook G. A molecular model for the triplicated A domains of human factor VIII based on the crystal structure of human ceruloplasmin. Blood. 1997;89(7):2413-21. (Pubitemid 27143288)
10. Wakabayashi H, Fay PJ. Identification of residues contributing to A2 domain-dependent structural stability in factor VIII and factor VIIIa. J Biol Chem. 2008;283(17):11645-51.
11. Wakabayashi H, Griffiths AE, Fay PJ. Combining mutations of charged residues at the A2 domain interface enhances factor VIII stability over single point mutations. J Thromb Haemost: JTH. 2009;7(3):438-44.
12. Shen BW, Spiegel PC, Chang CH, Huh JW, Lee JS, Kim J, et al. The tertiary structure and domain organization of coagulation factor VIII. Blood. 2008;111(3):1240-7. (Pubitemid 351213406)
13. Morfini M. Pharmacokinetics of factor VIII and factor IX. Haemophilia: Off J World Fed Hemophilia. 2003;9 Suppl 1:94-9. discussion 100.
14. Manco-Johnson MJ, Abshire TC, Shapiro AD, Riske B, Hacker MR, Kilcoyne R, et al. Prophylaxis versus episodic treatment to prevent joint disease in boys with severe hemophilia. N Engl J Med. 2007;357(6):535-44. (Pubitemid 47236278)
15. Pipe SW, Kaufman RJ. Characterization of a genetically engineered inactivation-resistant coagulation factor VIIIa. Proc Natl Acad Sci U S A. 1997;94(22):11851-6.
16. Radtke KP, Griffin JH, Riceberg J, Gale AJ. Disulfide bond-stabilized factor VIII has prolonged factor VIIIa activity and improved potency in whole blood clotting assays. J Thromb Haemost. 2007;5(1):102-8. (Pubitemid 44921074)
17. Jenkins PV, Dill JL, Zhou Q, Fay PJ. Clustered basic residues within segment 484-510 of the factor VIIIa A2 subunit contribute to the catalytic efficiency for factor Xa generation. J Thromb Haemost: JTH. 2004;2(3):452-8. (Pubitemid 40185658)
18. Peng A, Straubinger RM, Balu-Iyer SV. Phosphatidylinositol containing lipidic particles reduces immunogenicity and catabolism of factor VIII in hemophilia a mice. AAPS J. 2010;12(3):473-81.
19. Nedelman JR, Jia X. An extension of satterth waite's approximation applied to pharmacokinetics. J Biopharm Stat. 1998;8(2):317-28. (Pubitemid 28239874)
20. Holder DJ. Comments on Nedelman and Jia's extension of Satterthwaite's approximation applied to pharmacokinetics. J Biopharm Stat. 2001;11(1-2):75-9. (Pubitemid 32642830)
21. Shetty KA, Kosloski MP, Mager DE, Balu-Iyer SV. Soy phosphatidylinositol containing nanoparticle prolongs hemostatic activity of B-domain deleted factor VIII in hemophilia A Mice. J Pharma Sci. 2014.
22. Purohit VS, Ramani K, Sarkar R, Kazazian Jr HH, Balasubramanian SV. Lower inhibitor development in hemophilia A mice following administration of recombinant factor VIII-O-phospho-L-serine complex. J Biol Chem. 2005;280(18):17593-600. (Pubitemid 41388993)
23. Grillo AO, Edwards KL, Kashi RS, Shipley KM, Hu L, Besman MJ, et al. Conformational origin of the aggregation of recombinant human factor VIII. Biochemistry. 2001;40(2):586-95. (Pubitemid 32062007)
24. Kosloski MP, Pisal DS, Mager DE, Balu-Iyer SV. Nonlinear pharmacokinetics of factor VIII and its phosphatidylinositol lipidic complex in hemophilia A mice. Biopharm Drug Dispos. 2014;35(3):154-63.
25. Dumont JA, Liu T, Low SC, Zhang X, Kamphaus G, Sakorafas P, et al. Prolonged activity of a recombinant factor VIII-Fc fusion protein in hemophilia A mice and dogs. Blood. 2012;119(13):3024-30.
26. Pan J, Liu T, Kim JY, Zhu D, Patel C, Cui ZH, et al. Enhanced efficacy of recombinant FVIII in noncovalent complex with PEGylated liposome in hemophilia A mice. Blood. 2009;114(13):2802-11.
27. Kosloski MP, Miclea RD, Balu-Iyer SV. Role of glycosylation in conformational stability, activity, macromolecular interaction and immunogenicity of recombinant human factor VIII. AAPS J. 2009;11(3):424-31.
28. Pisal DS, Kosloski MP, Middaugh CR, Bankert RB, Balu-Iyer SV. Native-like aggregates of factor VIII are immunogenic in von Willebrand factor deficient and hemophilia a mice. J Pharm Sci. 2012;101(6):2055-65.
29. Reipert BM, Ahmad RU, Turecek PL, Schwarz HP. Characterization of antibodies induced by human factor VIII in a murine knockout model of hemophilia A. Thromb Haemost. 2000;84(5):826-32.
30. Lenting PJ, Vans CJ, Denis CV. Clearance mechanisms of von Willebrand factor and factor VIII. J Thromb Haemost: JTH. 2007;5(7):1353-60. (Pubitemid 46965358)
31. Wang W, Wang YJ, Kelner DN. Coagulation factor VIII: structure and stability. Int J Pharm. 2003;259(1-2):1-15. (Pubitemid 36638549)
32. Pratt KP. Inhibitory antibodies in hemophilia A. Curr Opin Hematol. 2012;19(5):399-405.
33. Gale AJ, Pellequer JL. An engineered interdomain disulfide bond stabilizes human blood coagulation factor VIIIa. J Thromb Haemost. 2003;1(9):1966-71.
34. Bovenschen N, Boertjes RC, van Stempvoort G, Voorberg J, Lenting PJ, Meijer AB, et al. Low density lipoprotein receptor-related protein and factor IXa share structural requirements for binding to the A3 domain of coagulation factor VIII. J Biol Chem. 2003;278(11):9370-7. (Pubitemid 36800424)
35. Bovenschen N, van Stempvoort G, Voorberg J, Mertens K, Meijer AB. Proteolytic cleavage of factor VIII heavy chain is required to expose the binding-site for low-density lipoprotein receptor-related protein within the A2 domain. J Thromb Haemost. 2006;4(7):1487-93.
36. Lenting PJ, Christophe OD, Gueguen P. The disappearing act of factor VIII. Haemophilia. 2010;16(102):6-15.
37. Leyte A, Verbeet MP, Brodniewicz-Proba T, Van Mourik JA, Mertens K. The interaction between human blood-coagulation factor VIII and vonWillebrand factor. Characterization of a high-affinity binding site on factor VIII. Biochem J. 1989;257(3):679-83. (Pubitemid 19050122)
38. Pisal DS, Balu-Iyer SV. Phospholipid binding improves plasma survival of factor VIII. Thromb Haemost. 2010;104(5):1073-5.
39. Saenko EL, Ananyeva NM, Kouiavskaia DV, Khrenov AV, Anderson JA, Shima M, et al. Haemophilia A: effects of inhibitory antibodies on factor VIII functional interactions and approaches to prevent their action. Haemophilia. 2002;8(1):1-11. (Pubitemid 34257912)
40. Fijnvandraat K, Celie PHN, Turenhout EAM, ten Cate JW, van Mourik JA, Mertens K, et al. A human alloantibody interferes with binding of factor IXa to the factor VIII light chain. Blood. 1998;91(7):2347-52. (Pubitemid 28155508)
41. Pratt KP, Qian J, Ellaban E, Okita DK, Diethelm-Okita BM, Conti-Fine B, et al. Immunodominant T-cell epitopes in the factor VIII C2 domain are located within an inhibitory antibody binding site. Thromb Haemost. 2004;92(3):522-8. (Pubitemid 39255359)
42. Zhong D, Saenko EL, Shima M, Felch M, Scandella D. Some human inhibitor antibodies interfere with factor VIII binding to factor IX. Blood. 1998;92(1):136-42. (Pubitemid 28303185)
43. Griffiths AE, Wang W, Hagen FK, Fay PJ. Use of affinity-directed liquid chromatography-mass spectrometry to map the epitopes of a factor VIII inhibitor antibody fraction. J Thromb Haemost. 2011;9(8):1534-40.
44. Wakabayashi H, Griffiths AE, Fay PJ. Enhancing factor VIII and VIIIa stability by combining mutations at the A2 domain interface and A1-C2 domain interface. J Thromb Haemost. 2012;10(3):492-5.
45. Gaitonde P, Peng A, Straubinger RM, Bankert RB, Balu-Iyer SV. Phosphatidylserine reduces immune response against human recombinant Factor VIII in hemophilia A mice by regulation of dendritic cell function. Clin Immunol. 2011;138(2):135-45.
46. Gaitonde P, Peng A, Straubinger RM, Bankert RB, Balu-Iyer SV. Downregulation of CD40 signal and induction of TGF-beta by phosphatidylinositol mediates reduction in immunogenicity against recombinant human Factor VIII. J Pharm Sci. 2012;101(1):48-55.