Codon optimization of human factor VIII cDNAs leads to high-level expression

Blood

Volumn 117, Issue 3, 2011, Pages 798-807

  Ward, Natalie J ^a   Buckley, Suzanne M K ^b   Waddington, Simon N ^c   VandenDriessche, Thierry ^d,e   Chuah, Marinee K L ^d,e   Nathwani, Amit C ^c   McIntosh, Jenny ^c   Tuddenham, Edward G D ^b   Kinnon, Christine ^a   Thrasher, Adrian J ^a   McVey, John H ^f  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^f THROMBOSIS RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 8; COMPLEMENTARY DNA; LENTIVIRUS VECTOR;

ANIMAL EXPERIMENT; ARTICLE; CODON; CONTROLLED STUDY; DNA SEQUENCE; HEMOPHILIA A; HUMAN; IN VITRO STUDY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; THERAPY EFFECT; WILD TYPE;

EID: 78751681902     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-05-282707     Document Type: Article

References (48)

1. Hoyer LW. Hemophilia A. N Engl J Med. 1994;330(1):38-47.
2. High KA. Gene transfer as an approach to treating hemophilia. Semin Thromb Hemost. 2003;29(1):107-120.
3. Viiala NO, Larsen SR, Rasko JE. Gene therapy for hemophilia: clinical trials and technical tribulations. Semin Thromb Hemost. 2009;35(1):81-92.
4. Lynch CM, Israel DI, Kaufman RJ, Miller AD. Sequences in the coding region of clotting factor VIII act as dominant inhibitors of RNA accumulation and protein production. Hum Gene Ther. 1993;4(3):259-272.
5. Kaufman RJ, Wasley LC, Davies MV, et al. Effect of von Willebrand factor coexpression on the synthesis and secretion of factor VIII in Chinese hamster ovary cells. Mol Cell Biol. 1989;9(3):1233-1242.
6. Hoeben RC, Fallaux FJ, Cramer SJ, et al. Expression of the blood-clotting factor-VIII cDNA is repressed by a transcriptional silencer located in its coding region. Blood. 1995;85(9):2447-2454.
7. Dorner AJ, Bole DG, Kaufman RJ. The relationship of N-linked glycosylation and heavy chainbinding protein association with the secretion of glycoproteins. J Cell Biol. 1987;105(6):2665-2674.
8. Pipe SW, Kaufman RJ. Factor VIII C2 domain missense mutations exhibit defective trafficking of biologically functional proteins. J Biol Chem. 1996;271(41):25671-25676.
9. Pipe SW. The promise and challenges of bioengineered recombinant clotting factors. J Thromb Haemost. 2005;3(8):1692-1701.
10. Fang H, Wang L, Wang H. The protein structure and effect of factor VIII. Thromb Res. 2007;119(1):1-13. (Pubitemid 44716206)
11. Lenting PJ, van Mourik JA, Mertens K. The life cycle of coagulation factor VIII in view of its structure and function. Blood. 1998;92(11):3983-3996. (Pubitemid 28544310)
12. 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 U S A. 1986;83(18):6800-6804.
13. Jenny RJ, Pittman DD, Toole JJ, et al. Complete cDNA and derived amino acid sequence of human factor V. Proc Natl Acad Sci U S A. 1987;84(14):4846- 4850. (Pubitemid 17095844)
14. Pipe SW. Functional roles of the factor VIII B domain. Haemophilia. 2009;15(6):1187-1196.
15. Toole JJ, Pittman DD, Orr EC, et al. A large region (approximately equal to 95 kDa) of human factor VIII is dispensable for in vitro procoagulant activity. Proc Natl Acad Sci U S A. 1986;83(16):5939-5942.
16. Pittman DD, Marquette KA, Kaufman RJ. Role of the B domain for factor VIII and factor V expression and function. Blood. 1994;84(12):4214-4225. (Pubitemid 24371925)
17. Miao HZ, Sirachainan N, Palmer L, et al. Bioengineering of coagulation factor VIII for improved secretion. Blood. 2004;103(9):3412-3419. (Pubitemid 38525672)
18. Brenner S, Elgar G, Sandford R, et al. Characterization of the pufferfish (Fugu) genome as a compact model vertebrate genome. Nature. 1993;366(6452):265-268. (Pubitemid 23359708)
19. Davidson CJ, Hirt RP, Lal K, et al. Molecular evolution of the vertebrate blood coagulation network. Thromb Haemost. 2003;89(3):420-428. (Pubitemid 36329230)
20. Chuah MK, Vandendriessche T, Morgan RA. Development and analysis of retroviral vectors expressing human factor VIII as a potential gene therapy for hemophilia A. Hum Gene Ther. 1995;6(11):1363-1377.
21. Koeberl DD, Halbert CL, Krumm A, Miller AD. Sequences within the coding regions of clotting factor VIII and CFTR block transcriptional elongation. Hum Gene Ther. 1995;6(4):469-479.
22. Fallaux FJ, Hoeben RC, Cramer SJ, et al. The human clotting factor VIII cDNA contains an autonomously replicating sequence consensus- and matrix attachment region-like sequence that binds a nuclear factor, represses heterologous gene expression, and mediates the transcriptional effects of sodium butyrate. Mol Cell Biol. 1996;16(8):4264-4272.
23. Sandberg H, Almstedt A, Brandt J, et al. Structural and functional characteristics of the B domain-deleted recombinant factor VIII protein, r-VIII SQ. Thromb Haemost. 2001;85(1):93-100. (Pubitemid 32050949)
24. Charrier S, Stockholm D, Seye K, et al. A lentiviral vector encoding the human Wiskott-Aldrich syndrome protein corrects immune and cytoskeletal defects in WASP knockout mice. Gene Ther. 2005;12(7):597-606. (Pubitemid 40468107)
25. Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol. 1997;15(9):871-875. (Pubitemid 27391780)
26. Demaison C, Parsley K, Brouns G, et al. High-level transduction and gene expression in hematopoietic repopulating cells using a human immunodeficiency [correction of imunodeficiency] virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Hum Gene Ther. 2002;13(7):803-813.
27. Chuah MK, Schiedner G, Thorrez L, et al. Therapeutic factor VIII levels and negligible toxicity in mouse and dog models of hemophilia A following gene therapy with high-capacity adenoviral vectors. Blood. 2003;101(5):1734-1743.
28. Marquette KA, Pittman DD, Kaufman RJ. A 110-amino acid region within the A1 domain of coagulation factor VIII inhibits secretion from mammalian cells. J Biol Chem. 1995;270(17):10297-10303.
29. Lind P, Larsson K, Spira J, et al. Novel forms of B domain-deleted recombinant factor VIII molecules: construction and biochemical characterization. Eur J Biochem. 1995;232(1):19-27.
30. Doering CB, Denning G, Dooriss K, et al. Directed engineering of a high-expression chimeric transgene as a strategy for gene therapy of hemophilia A. Mol Ther. 2009;17(7):1145-1154.
31. Doering CB, Healey JF, Parker ET, Barrow RT, Lollar P. High level expression of recombinant porcine coagulation factor VIII. J Biol Chem. 2002;277(41):38345-38349. (Pubitemid 35154689)
32. Ye P, Thompson AR, Sarkar R, et al. Naked DNA transfer of Factor VIII induced transgene-specific, species-independent immune response in hemophilia A mice. Mol Ther. 2004;10(1):117-126. (Pubitemid 38878154)
33. Dooriss KL, Denning G, Gangadharan B, et al. Comparison of factor VIII transgenes bioengineered for improved expression in gene therapy of hemophilia A. Hum Gene Ther. 2009;20(5):465-478.
34. Sinn PL, Goreham-Voss JD, Arias AC, et al. Enhanced gene expression conferred by stepwise modification of a nonprimate lentiviral vector. Hum Gene Ther. 2007;18(12):1244-1252.
35. Ramezani A, Hawley RG. Correction of murine hemophilia A following nonmyeloablative transplantation of hematopoietic stem cells engineered to encode an enhanced human factor VIII variant using a safety-augmented retroviral vector. Blood. 2009;114(3):526-534.
36. Malhotra JD, Miao H, Zhang K, et al. Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc Natl Acad Sci U S A. 2008;105(47):18525-18530.
37. Cerullo V, Seiler MP, Mane V, et al. Correction of murine hemophilia A and immunological differences of factor VIII variants delivered by helperdependent adenoviral vectors. Mol Ther. 2007;15(12):2080-2087. (Pubitemid 350148922)
38. Marin M. Folding at the rhythm of the rare codon beat. Biotechnol J. 2008;3(8):1047-1057.
39. Tsai CJ, Sauna ZE, Kimchi-Sarfaty C, et al. Synonymous mutations and ribosome stalling can lead to altered folding pathways and distinct minima. J Mol Biol. 2008;383(2):281-291.
40. Kootstra NA, Matsumura R, Verma IM. Efficient production of human FVIII in hemophilic mice using lentiviral vectors. Mol Ther. 2003;7(5):623-631. (Pubitemid 36626242)
41. Park F, Ohashi K, Kay MA. Therapeutic levels of human factor VIII and IX using HIV-1-based lentiviral vectors in mouse liver. Blood. 2000;96(3):1173- 1176. (Pubitemid 30616890)
42. Kang Y, Xie L, Tran DT, et al. Persistent expression of factor VIII in vivo following nonprimate lentiviral gene transfer. Blood. 2005;106(5):1552- 1558. (Pubitemid 41208565)
43. Shi Q, Wilcox DA, Fahs SA, et al. Factor VIII ectopically targeted to platelets is therapeutic in hemophilia A with high-titer inhibitory antibodies. J Clin Invest. 2006;116(7):1974-1982.
44. Ohmori T, Mimuro J, Takano K, et al. Efficient expression of a transgene in platelets using simian immunodeficiency virus-based vector harboring glycoprotein Ibalpha promoter: in vivo model for platelet-targeting gene therapy. FASEB J. 2006;20(9):1522-1524.
45. Matsui H, Shibata M, Brown B, et al. Ex vivo gene therapy for hemophilia A that enhances safe delivery and sustained in vivo FVIII expression from lentivirally-engineered endothelial progenitors. Stem Cells. 2007;25(10):2660-2669.
46. VandenDriessche T, Vanslembrouck V, Goovaerts I, et al. Long-term expression of human coagulation factor VIII and correction of hemophilia A after in vivo retroviral gene transfer in factor VIII-deficient mice. Proc Natl Acad Sci U S A. 1999;96(18):10379-10384.
47. Xu L, Mei M, Ma X, et al. High expression reduces an antibody response after neonatal gene therapy with B domain-deleted human factor VIII in mice. J Thromb Haemost. 2007;5(9):1805-1812. (Pubitemid 47288934)
48. Matsui H, Shibata M, Brown B, et al. A murine model for induction of long-term immunological tolerance to factor VIII does not require persistent detectable levels of plasma factor VIII and involves contributions from Foxp3+ T regulatory cells. Blood. 2009;114(3):677-685.