AAV-mediated gene transfer in the perinatal period results in expression of FVII at levels that protect against fatal spontaneous hemorrhage

Blood

Volumn 119, Issue 4, 2012, Pages 957-966

  Binny, Christopher ^a   McIntosh, Jenny ^a   Della Peruta, Marco ^a   Kymalainen, Hanna ^a   Tuddenham, Edward G D ^a   Buckley, Suzanne M K ^a   Waddington, Simon N ^a   McVey, John H ^b   Spence, Yunyu ^c   Morton, Christopher L ^c   Thrasher, Adrian J ^d   Gray, John T ^c   Castellino, Francis J ^e   Tarantal, Alice F ^f   Davidoff, Andrew M ^c   Nathwani, Amit C ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b THROMBOSIS RESEARCH INSTITUTE   (United Kingdom)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF NOTRE DAME   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 7; COMPLEMENTARY DNA; PARVOVIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEEDING; BLOOD CLOTTING FACTOR DEFICIENCY; FEMALE; GENE EXPRESSION; GENE TRANSFER; HUMAN; HUMAN CELL; IN UTERO STEM CELL TRANSPLANTATION; MACACA; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL PERIOD; PRIORITY JOURNAL; SEROTYPE; SURVIVAL RATE; THIRD TRIMESTER PREGNANCY; TRANSGENE;

EID: 84856296022     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-09-377630     Document Type: Article

References (50)

1. Nathwani AC, Tuddenham EG. Epidemiology of coagulation disorders. Baillieres Clin Haematol. 1992;5(2):383-439.
2. Pehlivanov B, Milchev N, Kroumov G. Factor VII deficiency and its treatment in delivery with recombinant factor VII. Eur J Obstet Gynecol Reprod Biol. 2004;116(2):237-238. (Pubitemid 39195143)
3. Mariani G, Konkle BA, Ingerslev J. Congenital factor VII deficiency: therapy with recombinant activated factor VII-a critical appraisal. Haemophilia. 2006;12(1):19-27.
4. Levi D, Pefkarou A, Fort JA, DeFariaW, Tzakis AG. Liver transplantation for factor VII deficiency. Transplantation. 2001;72(11):1836-1837. (Pubitemid 33144241)
5. Lapecorella M, Mariani G. Factor VII deficiency: defining the clinical picture and optimizing therapeutic options. Haemophilia. 2008;14(6):1170-1175.
6. Margaritis P, High KA. Gene therapy in haemophilia-going for cure? Haemophilia. 2010;16(suppl 3):24-28.
7. Bigger BW, Siapati EK, Mistry A, et al. Permanent partial phenotypic correction and tolerance in a mouse model of hemophilia B by stem cell gene delivery of human factor IX. Gene Ther. 2006;13(2):117-126. (Pubitemid 43039904)
8. Nathwani AC, Davidoff AM, Hanawa H, et al. Sustained high-level expression of human factor IX (hFIX) after liver-targeted delivery of recombinant adeno-associated virus encoding the hFIX gene in rhesus macaques. Blood. 2002;100(5):1662-1669. (Pubitemid 34925143)
9. Nathwani AC, Gray JT, McIntosh J, et al. Safe and efficient 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. 2007;109(4):1414-1421. (Pubitemid 46239572)
10. Nathwani AC, Rosales C, McIntosh J, et al. Long-term safety and efficacy following systemic administration of a self-complementary AAV vector encoding human FIX pseudotyped with serotype 5 and 8 capsid proteins. Mol Ther. 2011;19(5):876-885.
11. Mattar CN, Nathwani AC, Waddington SN, et al. Stable human FIX expression after 0.9G intrauterine gene transfer of self-complementary adeno-associated viral vector 5 and 8 in macaques. Mol Ther. 2011;19(11):1950-1960.
12. Waddington SN, Buckley SM, Nivsarkar M, et al. In utero gene transfer of human factor IX to fetal mice can induce postnatal tolerance of the exogenous clotting factor. Blood. 2003;101(4):1359-1366. (Pubitemid 36182507)
13. Manno CS, Pierce GF, Arruda VR, et al. Successful transduction of liver in hemophilia by AAVfactor IX and limitations imposed by the host immune response. Nat Med. 2006;12(3):342-347. (Pubitemid 43355084)
14. Flotte TR, Brantly ML, Spencer LT, et al. Phase I trial of intramuscular injection of a recombinant adeno-associated virus alpha 1-antitrypsin (rAAV2-CB-hAAT) gene vector to AAT-deficient adults. Hum Gene Ther. 2004;15(1):93-128. (Pubitemid 38147192)
15. Ross CJ, Twisk J, Bakker AC, et al. Correction of feline lipoprotein lipase deficiency with adeno-associated virus serotype 1-mediated gene transfer of the lipoprotein lipase S447X beneficial mutation. Hum Gene Ther. 2006;17(5):487-499. (Pubitemid 43794488)
16. Brantly ML, Chulay JD, Wang L, et al. Sustained transgene expression despite T lymphocyte responses in a clinical trial of rAAV1-AAT gene therapy. Proc Natl Acad Sci U S A. 2009;106(38):16363-16368.
17. Bainbridge JW, Smith AJ, Barker SS, et al. Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med. 2008;358(21):2231-2239. (Pubitemid 351724452)
18. Gaudet D, de Wal J, Tremblay K, et al. Review of the clinical development of alipogene tiparvovec gene therapy for lipoprotein lipase deficiency. Atheroscler Suppl. 2010;11(1):55-60.
19. Nathwani AC, Davidoff A, Hanawa H, Zhou JF, Vanin EF, Nienhuis AW. Factors influencing in vivo transduction by recombinant adeno-associated viral vectors expressing the human factor IX cDNA. Blood. 2001;97(5):1258-1265. (Pubitemid 32183747)
20. Ali RR, Reichel MB, De Alwis M, et al. Adeno-associated virus gene transfer to mouse retina. Hum Gene Ther. 1998;9(1):81-86. (Pubitemid 28050913)
21. Snyder RO, Miao C, Meuse L, et al. Correction of hemophilia B in canine and murine models using recombinant adeno-associated viral vectors. Nat Med. 1999;5(1):64-70. (Pubitemid 29051000)
22. Herzog RW, Yang EY, Couto LB, et al. Long-term correction of canine hemophilia B by gene transfer of blood coagulation factor IX mediated by adeno-associated viral vector. Nat Med. 1999;5(1):56-63. (Pubitemid 29050999)
23. Jiang H, Pierce GF, Ozelo MC, et al. Evidence of multiyear factor IX expression by AAV-mediated gene transfer to skeletal muscle in an individual with severe hemophilia B. Mol Ther. 2006;14(3):452-455. (Pubitemid 44184967)
24. Simonelli F, Maguire AM, Testa F, et al. Gene therapy for Leber's congenital amaurosis is safe and effective through 1.5 years after vector administration. Mol Ther. 2010;18(3):643-650.
25. Nathwani AC, Gray JT, Ng CY, et al. Selfcomplementary adeno-associated virus vectors containing a novel liver-specific human factor IX expression cassette enable highly efficient transduction of murine and nonhuman primate liver. Blood. 2006;107(7):2653-2661.
26. McCarty DM, Fu H, Monahan PE, Toulson CE, Naik P, Samulski RJ. Adeno-associated virus terminal repeat (TR) mutant generates self-complementary vectors to overcome the ratelimiting step to transduction in vivo. Gene Ther. 2003;10(26):2112-2118. (Pubitemid 37536760)
27. Hirata RK, Russell DW. Design and packaging of adeno-associated virus gene targeting vectors. J Virol. 2000;74(10):4612-4620. (Pubitemid 30237886)
28. Streck CJ, Dickson PV, Ng CY, et al. Adeno-associated virus vector-mediated systemic delivery of IFN-beta combined with low-dose cyclophosphamide affects tumor regression in murine neuroblastoma models. Clin Cancer Res. 2005;11(16):6020-6029. (Pubitemid 41170334)
29. Lee CC, Jimenez DF, Kohn DB, Tarantal AF. Fetal gene transfer using lentiviral vectors and the potential for germ cell transduction in rhesus monkeys (Macaca mulatta). Hum Gene Ther. 2005;16(4):417-425. (Pubitemid 40647139)
30. Tarantal AF, Lee CC. Long-term luciferase expression monitored by bioluminescence imaging after adeno-associated virus-mediated fetal gene delivery in rhesus monkeys (Macaca mulatta). Hum Gene Ther. 2010;21(2):143-148.
31. Tarantal AF, McDonald RJ, Jimenez DF, et al. Intrapulmonary and intramyocardial gene transfer in rhesus monkeys (Macaca mulatta): safety and efficiency of HIV-1-derived lentiviral vectors for fetal gene delivery. Mol Ther. 2005;12(1):87-98. (Pubitemid 40862360)
32. Kremer JM, Westhovens R, Leon M, et al. Treatment of rheumatoid arthritis by selective inhibition of T-cell activation with fusion protein CTLA4Ig. N Engl J Med. 2003;349(20):1907-1915. (Pubitemid 37409707)
33. Rosen ED, Xu H, Liang Z, Martin JA, Suckow M, Castellino FJ. Generation of genetically-altered mice producing very low levels of coagulation factorVII. Thromb Haemost. 2005;94(3):493-497. (Pubitemid 41300841)
34. Davidoff AM, Ng CY, Zhou J, Spence Y, Nathwani AC. Sex significantly influences transduction of murine liver by recombinant adenoassociated viral vectors through an androgendependent pathway. Blood. 2003;102(2):480-488. (Pubitemid 36841964)
35. Nathwani AC, Cochrane M, McIntosh J, et al. Enhancing transduction of the liver by adeno-associated viral vectors. Gene Ther. 2009;16(1): 60-69.
36. Dejneka NS, Surace EM, Aleman TS, et al. In utero gene therapy rescues vision in a murine model of congenital blindness. Mol Ther. 2004;9(2):182-188. (Pubitemid 38256544)
37. Rucker M, Fraites TJ Jr, Porvasnik SL, et al. Rescue of enzyme deficiency in embryonic diaphragm in a mouse model of metabolic myopathy: Pompe disease. Development. 2004;131(12):3007-3019. (Pubitemid 38997287)
38. Waddington SN, Nivsarkar MS, Mistry AR, et al. Permanent phenotypic correction of hemophilia B in immunocompetent mice by prenatal gene therapy. Blood. 2004;104(9):2714-2721. (Pubitemid 39434952)
39. Wang L, Bell P, Lin J, Calcedo R, Tarantal AF, Wilson JM. AAV8-mediated hepatic gene transfer in infant rhesus monkeys (Macaca mulatta). Mol Ther. 2011;19(11):2012-2020.
40. Menzella HG. Comparison of two codon optimization strategies to enhance recombinant protein production in Escherichia coli. Microb Cell Fact. 2011;10:15.
41. Fath S, Bauer AP, Liss M, et al. Multiparameter RNA and codon optimization: a standardized tool to assess and enhance autologous mammalian gene expression. PLoS One. 2011;6(3):e17596.
42. Ward NJ, Buckley SM, Waddington SN, et al. Codon optimization of human factor VIII cDNAs leads to high-level expression. Blood. 2011;117(3):798-807.
43. Wang L, Calcedo R, Nichols TC, et al. Sustained correction of disease in naive and AAV2-pretreated hemophilia B dogs: AAV2/8-mediated, liver-directed gene therapy. Blood. 2005;105(8):3079-3086.
44. Voutetakis A, Zheng C, Wang J, et al. Gender differences in serotype 2 adeno-associated virus biodistribution after administration to rodent salivary glands. Hum Gene Ther. 2007;18(11):1109-1118. (Pubitemid 350114688)
45. Berraondo P, Crettaz J, Ochoa L, et al. Intrahepatic injection of recombinant adeno-associated virus serotype 2 overcomes gender-related differences in liver transduction. Hum Gene Ther. 2006;17(6):601-610. (Pubitemid 43967864)
46. Passini MA, Macauley SL, Huff MR, et al. AAV vector-mediated correction of brain pathology in a mouse model of Niemann-Pick A disease. Mol Ther. 2005;11(5):754-762. (Pubitemid 40567980)
47. David AL, McIntosh J, Peebles DM, et al. Recombinant adeno-associated virus-mediated in utero gene transfer gives therapeutic transgene expression in the sheep. Hum Gene Ther. 2011;22(4):419-426.
48. Cunningham SC, DaneAP, Spinoulas A, Logan GJ, Alexander IE. Gene delivery to the juvenile mouse liver using AAV2/8 vectors. Mol Ther. 2008;16(6):1081-1088. (Pubitemid 351737073)
49. DaneAP, Cunningham SC, Graf NS, Alexander IE. Sexually dimorphic patterns of episomal rAAV genome persistence in the adult mouse liver and correlation with hepatocellular proliferation. Mol Ther. 2009;17(9):1548-1554.
50. Mariani G, Bernardi F. Factor VII deficiency. Semin Thromb Hemost. 2009;35(4):400-406.