Potential for cellular stress response to hepatic factor VIII expression from AAV vector

Molecular Therapy Methods and Clinical Development

Volumn 3, Issue , 2016, Pages 16063-

  Zolotukhin, Irene ^a   Markusic, David M ^a   Palaschak, Brett ^a   Hoffman, Brad E ^a   Srikanthan, Meera A ^a   Herzog, Roland W ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; ALANINE AMINOTRANSFERASE; BLOOD CLOTTING FACTOR 8; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; TUNICAMYCIN; VON WILLEBRAND FACTOR;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; APOPTOSIS; ARTICLE; CELL STRESS; CELLULAR STRESS RESPONSE; CODON; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE DELETION; GENE TARGETING; GENE TRANSFER; GENETIC BACKGROUND; HEMOPHILIA A; IMMUNOGENICITY; LIVER CELL; LIVER TOXICITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEROTYPE; TUNEL ASSAY; UNFOLDED PROTEIN RESPONSE; UPREGULATION; WESTERN BLOTTING;

EID: 85015190567     PISSN: None     EISSN: 23290501     Source Type: Journal    
DOI: 10.1038/mtm.2016.63     Document Type: Article

References (49)

1. 1 Furie, B, Furie, BC, The molecular basis of blood coagulation. Cell 53 (1988), 505–518.
2. 2 Tiede, A, Half-life extended factor VIII for the treatment of hemophilia A. J Thromb Haemost 13:Suppl 1 (2015), S176–S179.
3. 3 Nathwani, AC, Reiss, UM, Tuddenham, EG, Rosales, C, Chowdary, P, McIntosh, J, et al. Long-term safety and efficacy of factor IX gene therapy in hemophilia B. N Engl J Med 371 (2014), 1994–2004.
4. 4 Rogers, GL, Herzog, RW, Gene therapy for hemophilia. Front Biosci (Landmark Ed) 20 (2015), 556–603.
5. 5 Sabatino, DE, Lange, AM, Altynova, ES, Sarkar, R, Zhou, S, Merricks, EP, et al. Efficacy and safety of long-term prophylaxis in severe hemophilia A dogs following liver gene therapy using AAV vectors. Mol Ther 19 (2011), 442–449.
6. 6 Jiang, H, Lillicrap, D, Patarroyo-White, S, Liu, T, Qian, X, Scallan, CD, et al. Multiyear therapeutic benefit of AAV serotypes 2, 6, and 8 delivering factor VIII to hemophilia A mice and dogs. Blood 108 (2006), 107–115.
7. 7 Markusic, DM, Herzog, RW, Liver-directed adeno-associated viral gene therapy for hemophilia. J Genet Syndr Gene Ther 1 (2012), 1–9.
8. 8 Nathwani, AC, Tuddenham, EG, Rangarajan, S, Rosales, C, McIntosh, J, Linch, DC, et al. Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N Engl J Med 365 (2011), 2357–2365.
9. 9 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 270 (1995), 10297–10303.
10. 10 Tagliavacca, L, Wang, Q, Kaufman, RJ, ATP-dependent dissociation of non-disulfide-linked aggregates of coagulation factor VIII is a rate-limiting step for secretion. Biochemistry 39 (2000), 1973–1981.
11. 11 Toole, JJ, Pittman, DD, Orr, EC, Murtha, P, Wasley, LC, Kaufman, RJ, A large region (approximately equal to 95 kDa) of human factor VIII is dispensable for in vitro procoagulant activity. Proc Natl Acad Sci USA 83 (1986), 5939–5942.
12. 12 Pittman, DD, Alderman, EM, Tomkinson, KN, Wang, JH, Giles, AR, Kaufman, RJ, Biochemical, immunological, and in vivo functional characterization of B-domain-deleted factor VIII. Blood 81 (1993), 2925–2935.
13. 13 Sack, BK, Merchant, S, Markusic, DM, Nathwani, AC, Davidoff, AM, Byrne, BJ, et al. Transient B cell depletion or improved transgene expression by codon optimization promote tolerance to factor VIII in gene therapy. PLoS One, 7, 2012, e37671.
14. 14 McIntosh, J, Lenting, PJ, Rosales, C, Lee, D, Rabbanian, S, Raj, D, et al. Therapeutic levels of FVIII following a single peripheral vein administration of rAAV vector encoding a novel human factor VIII variant. Blood 121 (2013), 3335–3344.
15. 15 Siner, JI, Iacobelli, NP, Sabatino, DE, Ivanciu, L, Zhou, S, Poncz, M, et al. Minimal modification in the factor VIII B-domain sequence ameliorates the murine hemophilia A phenotype. Blood 121 (2013), 4396–4403.
16. 16 Brown, HC, Gangadharan, B, Doering, CB, Enhanced biosynthesis of coagulation factor VIII through diminished engagement of the unfolded protein response. J Biol Chem 286 (2011), 24451–24457.
17. 17 Sack, BK, Herzog, RW, Terhorst, C, Markusic, DM, Development of gene transfer for induction of antigen-specific tolerance. Mol Ther Methods Clin Dev, 1, 2014, 14013.
18. 18 Finn, JD, Ozelo, MC, Sabatino, DE, Franck, HW, Merricks, EP, Crudele, JM, et al. Eradication of neutralizing antibodies to factor VIII in canine hemophilia A after liver gene therapy. Blood 116 (2010), 5842–5848.
19. 19 Malhotra, JD, Miao, H, Zhang, K, Wolfson, A, Pennathur, S, Pipe, SW, et al. Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc Natl Acad Sci USA 105 (2008), 18525–18530.
20. 20 Harding, HP, Zhang, Y, Zeng, H, Novoa, I, Lu, PD, Calfon, M, et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11 (2003), 619–633.
21. 21 Tu, BP, Weissman, JS, Oxidative protein folding in eukaryotes: mechanisms and consequences. J Cell Biol 164 (2004), 341–346.
22. 22 Schröder, M, Kaufman, RJ, The mammalian unfolded protein response. Annu Rev Biochem 74 (2005), 739–789.
23. 23 Malhotra, JD, Kaufman, RJ, Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword?. Antioxid Redox Signal 9 (2007), 2277–2293.
24. 24 Ron, D, Walter, P, Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8 (2007), 519–529.
25. 25 Dorner, AJ, Bole, DG, Kaufman, RJ, The relationship of N-linked glycosylation and heavy chain-binding protein association with the secretion of glycoproteins. J Cell Biol 105:6 Pt 1 (1987), 2665–2674.
26. 26 Cooper, M, Nayak, S, Hoffman, BE, Terhorst, C, Cao, O, Herzog, RW, Improved induction of immune tolerance to factor IX by hepatic AAV-8 gene transfer. Hum Gene Ther 20 (2009), 767–776.
27. 27 Arruda, VR, Fields, PA, Milner, R, Wainwright, L, De Miguel, MP, Donovan, PJ, et al. Lack of germline transmission of vector sequences following systemic administration of recombinant AAV-2 vector in males. Mol Ther 4 (2001), 586–592.
28. 28 Pratt, RM, Yamada, KM, Olden, K, Ohanian, SH, Hascall, VC, Tunicamycin-induced alterations in the synthesis of sulfated proteoglycans and cell surface morphology in the chick embryo fibroblast. Exp Cell Res 118 (1979), 245–252.
29. 29 Everett, LA, Cleuren, AC, Khoriaty, RN, Ginsburg, D, Murine coagulation factor VIII is synthesized in endothelial cells. Blood 123 (2014), 3697–3705.
30. 30 Shahani, T, Covens, K, Lavend'homme, R, Jazouli, N, Sokal, E, Peerlinck, K, et al. Human liver sinusoidal endothelial cells but not hepatocytes contain factor VIII. J Thromb Haemost 12 (2014), 36–42.
31. 31 Fahs, SA, Hille, MT, Shi, Q, Weiler, H, Montgomery, RR, A conditional knockout mouse model reveals endothelial cells as the principal and possibly exclusive source of plasma factor VIII. Blood 123 (2014), 3706–3713.
32. 32 Zanolini, D, Merlin, S, Feola, M, Ranaldo, G, Amoruso, A, Gaidano, G, et al. Extrahepatic sources of factor VIII potentially contribute to the coagulation cascade correcting the bleeding phenotype of mice with hemophilia A. Haematologica 100 (2015), 881–892.
33. 33 Pipe, SW, Functional roles of the factor VIII B domain. Haemophilia 15 (2009), 1187–1196.
34. 34 Mingozzi, F, Liu, YL, Dobrzynski, E, Kaufhold, A, Liu, JH, Wang, Y, et al. Induction of immune tolerance to coagulation factor IX antigen by in vivo hepatic gene transfer. J Clin Invest 111 (2003), 1347–1356.
35. 35 Lisowski, L, Dane, AP, Chu, K, Zhang, Y, Cunningham, SC, Wilson, EM, et al. Selection and evaluation of clinically relevant AAV variants in a xenograft liver model. Nature 506 (2014), 382–386.
36. 36 Li, S, Ling, C, Zhong, L, Li, M, Su, Q, He, R, et al. Efficient and targeted transduction of nonhuman primate liver with systemically delivered optimized AAV3B vectors. Mol Ther 23 (2015), 1867–1876.
37. 37 Wang, L, Bell, P, Somanathan, S, Wang, Q, He, Z, Yu, H, et al. Comparative study of liver gene transfer with AAV vectors based on natural and engineered AAV capsids. Mol Ther 23 (2015), 1877–1887.
38. 38 Mauro, VP, Chappell, SA, A critical analysis of codon optimization in human therapeutics. Trends Mol Med 20 (2014), 604–613.
39. 39 Rosenblum, G, Chen, C, Kaur, J, Cui, X, Zhang, H, Asahara, H, et al. Quantifying elongation rhythm during full-length protein synthesis. J Am Chem Soc 135 (2013), 11322–11329.
40. 40 Komar, AA, A pause for thought along the co-translational folding pathway. Trends Biochem Sci 34 (2009), 16–24.
41. 41 Suda, T, Gao, X, Stolz, DB, Liu, D, Structural impact of hydrodynamic injection on mouse liver. Gene Ther 14 (2007), 129–137.
42. 42 Suda, T, Liu, D, Hydrodynamic gene delivery: its principles and applications. Mol Ther 15 (2007), 2063–2069.
43. 43 Staber, JM, Pollpeter, MJ, Arensdorf, A, Sinn, PL, Rutkowski, DT, McCray, PB Jr, piggyBac-mediated phenotypic correction of factor VIII deficiency. Mol Ther Methods Clin Dev, 1, 2014, 14042.
44. 44 Vlot, AJ, Koppelman, SJ, van den Berg, MH, Bouma, BN, Sixma, JJ, The affinity and stoichiometry of binding of human factor VIII to von Willebrand factor. Blood 85 (1995), 3150–3157.
45. 45 Terraube, V, O'Donnell, JS, Jenkins, PV, Factor VIII and von Willebrand factor interaction: biological, clinical and therapeutic importance. Haemophilia 16 (2010), 3–13.
46. 46 Lytle, AM, Brown, HC, Paik, NY, Knight, KA, Wright, JF, Spencer, HT, et al. Effects of FVIII immunity on hepatocyte and hematopoietic stem cell-directed gene therapy of murine hemophilia A. Mol Ther Methods Clin Dev, 3, 2016, 15056.
47. 47 Doering, CB, Denning, G, Dooriss, K, Gangadharan, B, Johnston, JM, Kerstann, KW, et al. Directed engineering of a high-expression chimeric transgene as a strategy for gene therapy of hemophilia A. Mol Ther 17 (2009), 1145–1154.
48. 48 Dooriss, KL, Denning, G, Gangadharan, B, Javazon, EH, McCarty, DA, Spencer, HT, et al. Comparison of factor VIII transgenes bioengineered for improved expression in gene therapy of hemophilia A. Hum Gene Ther 20 (2009), 465–478.
49. 49 Zolotukhin, S, Byrne, BJ, Mason, E, Zolotukhin, I, Potter, M, Chesnut, K, et al. Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Ther 6 (1999), 973–985.