Efficacy and safety of long-term prophylaxis in severe hemophilia a dogs following liver gene therapy using AAV vectors

Molecular Therapy

Volumn 19, Issue 3, 2011, Pages 442-449

  Sabatino, Denise E ^a   Lange, Amy M ^a   Altynova, Ekaterina S ^a   Sarkar, Rita ^a   Zhou, Shangzhen ^b   Merricks, Elizabeth P ^c   Franck, Helen G ^c   Nichols, Timothy C ^c   Arruda, Valder R ^a,b   Kazazian Jr Jr , Haig H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 1 ANTITRYPSIN; ALPHA 1 MICROGLOBULIN; BETA GLOBIN; BLOOD CLOTTING FACTOR 8; BLOOD CLOTTING FACTOR 8 INHIBITOR; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; PARVOVIRUS VECTOR; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN BINDING PROTEIN 2; ULINASTATIN;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS 8; ADENO ASSOCIATED VIRUS 9; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLEEDING; CONTROLLED STUDY; DISEASE SEVERITY; DOG; DRUG EFFICACY; DRUG SAFETY; ENHANCER REGION; FEMALE; FOLLOW UP; GENE THERAPY; HEMOPHILIA A; IMMUNE RESPONSE; IMMUNOGENICITY; LIVER TOXICITY; LONG TERM CARE; MALE; NONHUMAN; PORTAL VEIN; PROMOTER REGION; PROPHYLAXIS; PROTEIN EXPRESSION; SEROTYPE; TREATMENT OUTCOME; VIRAL GENE DELIVERY SYSTEM;

CANIS FAMILIARIS;

EID: 79952194475     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2010.240     Document Type: Article

References (39)

1. Kazazian, HH Jr, Tuddenham, EGD and Antonarakis, SE (2001). Hemophilia A: Defciency of coagulation factor VIII. In: Scriver, CR, Beaudet, AL, Sly, WS and Valle, D (eds). The Metabolic Basis of Inherited Disease, McCraw-Hill: New York, pp. 4367-4392.
2. Manco-Johnson, MJ, Abshire, TC, Shapiro, AD, Riske, B, Hacker, MR, Kilcoyne, R et al. (2007). Prophylaxis versus episodic treatment to prevent joint disease in boys with severe hemophilia. N Engl J Med 357: 535-544. (Pubitemid 47236278)
3. Arruda, VR, Stedman, HH, Haurigot, V, Buchlis, G, Baila, S, Favaro, P et al. (2010). Peripheral transvenular delivery of adeno-associated viral vectors to skeletal muscle as a novel therapy for hemophilia B. Blood 115: 4678-4688.
4. Niemeyer, G P, Herzog, RW, Mount, J, Arruda, VR, Tillson, DM, Hathcock, J et al. (2009). Long-term correction of inhibitor-prone hemophilia B dogs treated with liver-directed AAV2-mediated factor IX gene therapy. Blood 113: 797-806.
5. Sarkar, R, Mucci, M, Addya, S, Tetreault, R, Bellinger, DA, Nichols, TC et al. (2006). Long-term effcacy of adeno-associated virus serotypes 8 and 9 in hemophilia a dogs and mice. Hum Gene Ther 17: 427-439.
6. Jiang, H, Lillicrap, D, Patarroyo-White, S, Liu, T, Qian, X, Scallan, CD et al. (2006). Multiyear therapeutic beneft of AAV serotypes 2, 6, and 8 delivering factor VIII to hemophilia A mice and dogs. Blood 108: 107-115. (Pubitemid 43990618)
7. Brinkhous, KM, Davis, PD, Graham, JB and Dodds, WJ (1973). Expression and linkage of genes for X-linked hemophilias A and B in the dog. Blood 41: 577-585.
8. Arruda, VR and Xiao, W. It's all about the clothing: capsid domination in the adeno-associated viral vector world. J Thromb Haemost 5: 12-15 (2007 (Pubitemid 44921061)
9. Pacak, CA, Mah, CS, Thattaliyath, BD, Conlon, TJ, Lewis, MA, Cloutier, DE et al. (2006). Recombinant adeno-associated virus serotype 9 leads to preferential cardiac transduction in vivo. Circ Res 99: e3-e9. (Pubitemid 44255502)
10. Sarkar, R, Tetreault, R, Gao, G, Wang, L, Bell, P, Chandler, R et al. (2004). Total correction of hemophilia A mice with canine FVIII using an AAV 8 serotype. Blood 103: 1253-1260. (Pubitemid 38168635)
11. Vandendriessche, T, Thorrez, L, Acosta-Sanchez, A, Petrus, I, Wang, L, Ma, L et al. (2007). Effcacy and safety of adeno-associated viral vectors based on serotype 8 and 9 vs. lentiviral vectors for hemophilia B gene therapy. J Thromb Haemost 5: 16-24. (Pubitemid 44921062)
12. Malhotra, JD, Miao, H, Zhang, K, Wolfson, A, Pennathur, S, Pipe, SW et al. (2008). Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc Natl Acad Sci USA 105: 18525-18530.
13. Herzog, RW, Yang, EY, Couto, LB, Hagstrom, JN, Elwell, D, Fields, PA et al. (1999). Long-term correction of canine hemophilia B by gene transfer of blood coagulation factor IX mediated by adeno-associated viral vector. Nat Med 5: 56-63. (Pubitemid 29050999)
14. Mount, JD, Herzog, RW, Tillson, DM, Goodman, SA, Robinson, N, McCleland, ML et al. (2002). Sustained phenotypic correction of hemophilia B dogs with a factor IX null mutation by liver-directed gene therapy. Blood 99: 2670-2676. (Pubitemid 34525351)
15. Nathwani, AC, Gray, JT, McIntosh, J, Ng, CY, Zhou, J, Spence, Y et al. (2007). Safe and effcient transduction of the liver after peripheral vein infusion of self-complementary AAV vector results in stable therapeutic expression of human FIX in nonhuman primates. Blood 109: 1414-1421. (Pubitemid 46239572)
16. Manno, CS, Pierce, GF, Arruda, VR, Glader, B, Ragni, M, Rasko, JJ et al. (2006). Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat Med 12: 342-347. (Pubitemid 43355084)
17. Sabatino, DE, Freguia, CF, Toso, R, Santos, A, Merricks, EP, Kazazian, HH Jr et al. (2009). Recombinant canine B-domain-deleted FVIII exhibits high specifc activity and is safe in the canine hemophilia A model. Blood 114: 4562-4565.
18. Scallan, CD, Liu, T, Parker, AE, Patarroyo-White, SL, Chen, H, Jiang, H et al. (2003). Phenotypic correction of a mouse model of hemophilia A using AAV2 vectors encoding the heavy and light chains of FVIII. Blood 102: 3919-3926. (Pubitemid 37486971)
19. McCormack, WM Jr, Seiler, MP, Bertin, TK, Ubhayakar, K, Palmer, DJ, Ng, P et al. (2006). Helper-dependent adenoviral gene therapy mediates long-term correction of the clotting defect in the canine hemophilia A model. J Thromb Haemost 4: 1218-1225.
20. Hamer, RJ, Koedam, JA, Beeser-Visser, NH, Bertina, RM, Van Mourik, JA and Sixma, JJ (1987). Factor VIII binds to von Willebrand factor via its Mr-80,000 light chain. Eur J Biochem 166: 37-43. (Pubitemid 17089108)
21. Lollar, P, Hill-Eubanks, DC and Parker, CG (1988). Association of the factor VIII light chain with von Willebrand factor. J Biol Chem 263: 10451-10455.
22. Finn, JD, Ozelo, MC, Sabatino, DE, Franck, HW, Merricks, EP, Crudele, JM et al. (2010). Eradication of neutralizing antibodies to factor VIII in canine hemophilia A following liver gene therapy. Blood (epub ahead of print
23. Mingozzi, F, Liu, YL, Dobrzynski, E, Kaufhold, A, Liu, JH, Wang, Y et al. (2003). Induction of immune tolerance to coagulation factor IX antigen by in vivo hepatic gene transfer. J Clin Invest 111: 1347-1356. (Pubitemid 36554705)
24. Cao, O, Dobrzynski, E, Wang, L, Nayak, S, Mingle, B, Terhorst, C et al. (2007). Induction and role of regulatory CD4+CD25+ T cells in tolerance to the transgene product following hepatic in vivo gene transfer. Blood 110: 1132-1140. (Pubitemid 47281408)
25. Mingozzi, F, Hasbrouck, NC, Basner-Tschakarjan, E, Edmonson, SA, Hui, DJ, Sabatino, DE et al. (2007). Modulation of tolerance to the transgene product in a nonhuman primate model of AAV-mediated gene transfer to liver. Blood 110: 2334-2341. (Pubitemid 47523153)
26. Deyle, DR and Russell, DW (2009). Adeno-associated virus vector integration. Curr Opin Mol Ther 11: 442-447.
27. Nathwani, AC, Gray, JT, Ng, CY, Zhou, J, Spence, Y, Waddington, SN et al. (2006). Self-complementary adeno-associated virus vectors containing a novel liver-specifc human factor IX expression cassette enable highly effcient transduction of murine and nonhuman primate liver. Blood 107: 2653-2661.
28. Zhong, L, Li, B, Mah, CS, Govindasamy, L, Agbandje-McKenna, M, Cooper, M et al. (2008). Next generation of adeno-associated virus 2 vectors: point mutations in tyrosines lead to high-effciency transduction at lower doses. Proc Natl Acad Sci USA 105: 7827-7832. (Pubitemid 351872723)
29. Matsushita, T, Elliger, S, Elliger, C, Podsakoff, G, Villarreal, L, Kurtzman, GJ et al. (1998). Adeno-associated virus vectors can be effciently produced without helper virus. Gene Ther 5: 938-945. (Pubitemid 28371911)
30. Bi, L, Lawler, AM, Antonarakis, SE, High, KA, Gearhart, JD and Kazazian, HH Jr (1995). Targeted disruption of the mouse factor VIII gene produces a model of haemophilia A. Nat Genet 10: 119-121.
31. Bi, L, Sarkar, R, Naas, T, Lawler, AM, Pain, J, Shumaker, SL et al. (1996). Further characterization of factor VIII-defcient mice created by gene targeting: RNA and protein studies. Blood 88: 3446-3450. (Pubitemid 26365578)
32. Kay, MA, Rothenberg, S, Landen, CN, Bellinger, DA, Leland, F, Toman, C et al. (1993). In vivo gene therapy of hemophilia B: sustained partial correction in factor IX-defcient dogs. Science 262: 117-119.
33. Wiinberg, B, Jensen, AL, Rojkjaer, R, Johansson, P, Kjelgaard-Hansen, M and Kristensen, AT (2005). Validation of human recombinant tissue factor-activated thromboelastography on citrated whole blood from clinically healthy dogs. Vet Clin Pathol 34: 389-393. (Pubitemid 43036133)
34. Herzog, RW, Mount, JD, Arruda, VR, High, KA and Lothrop, CD Jr (2001). Muscle-directed gene transfer and transient immune suppression result in sustained partial correction of canine hemophilia B caused by a null mutation. Mol Ther 4: 192-200. (Pubitemid 32851282)
35. Buchman, AR and Berg, P. Comparison of intron-dependent and intron-independent gene expression. Mol Cell Biol 8, 4395-4405 (1988
36. Kurachi, S, Hitomi, Y, Furukawa, M and Kurachi, K (1995). Role of intron I in expression of the human factor IX gene. J Biol Chem 270: 5276-5281.
37. Grieger, JC and Samulski, RJ (2005). Packaging capacity of adeno-associated virus serotypes: impact of larger genomes on infectivity and postentry steps. J Virol 79: 9933-9944. (Pubitemid 41022335)
38. Al-Dosari, MS, Knapp, JE and Liu, D (2005). Hydrodynamic delivery. Adv Genet 54: 65-82. (Pubitemid 43580693)
39. Crespo, A, Peydró, A, Dasí, F, Benet, M, Calvete, JJ, Revert, F et al. (2005). Hydrodynamic liver gene transfer mechanism involves transient sinusoidal blood stasis and massive hepatocyte endocytic vesicles. Gene Ther 12: 927-935. (Pubitemid 40852211)