Integration frequency and intermolecular recombination of rAAV vectors in non-human primate skeletal muscle and liver

Molecular Therapy

Volumn 20, Issue 6, 2012, Pages 1177-1186

  Nowrouzi, Ali ^a   Penaud Budloo, Magalie ^b   Kaeppel, Christine ^a   Appelt, Uwe ^a   Le Guiner, Caroline ^b,c   Moullier, Philippe ^b,c,d   Kalle, Christof Von ^a   Snyder, Richard O ^b,d,e   Schmidt, Manfred ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b INSERM   (France)

^c GÉNÉTHON   (France)

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

^e UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS VECTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; COPY NUMBER VARIATION; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE LOCUS; GENE MAPPING; GENOTOXICITY; HUMAN; HUMAN CELL; INVERTED TERMINAL REPEAT; LIVER; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN SECONDARY STRUCTURE; SKELETAL MUSCLE; VIRUS GENOME; VIRUS RECOMBINANT; VIRUS RECOMBINATION;

PRIMATES;

EID: 84861912888     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2012.47     Document Type: Article

References (39)

1. Hacein-Bey-Abina, S, Von Kalle, C, Schmidt, M, McCormack, MP, Wulffraat, N, Leboulch, P et al. (2003). LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302: 415-419. (Pubitemid 37296260)
2. Ott, MG, Schmidt, M, Schwarzwaelder, K, Stein, S, Siler, U, Koehl, U et al. (2006). Correction of X-linked chronic granulomatous disease by gene therapy, augmented by insertional activation of MDS1-EVI1, PRDM16 or SETBP1. Nat Med 12: 401-409.
3. Schwarzwaelder, K, Howe, SJ, Schmidt, M, Brugman, MH, Deichmann, A, Glimm, H et al. (2007). Gammaretrovirus-mediated correction of SCID-X1 is associated with skewed vector integration site distribution in vivo. J Clin Invest 117: 2241-2249. (Pubitemid 47219569)
4. Nienhuis, AW, Dunbar, CE and Sorrentino, BP (2006). Genotoxicity of retroviral integration in hematopoietic cells. Mol Ther 13: 1031-1049. (Pubitemid 43779188)
5. Donsante, A, Miller, DG, Li, Y, Vogler, C, Brunt, EM, Russell, DW et al. (2007). AAV vector integration sites in mouse hepatocellular carcinoma. Science 317: 477. (Pubitemid 47196106)
6. Russell, DW (2007). AAV vectors, insertional mutagenesis, and cancer. Mol Ther 15: 1740-1743.
7. Bell, P, Wang, L, Lebherz, C, Flieder, DB, Bove, MS, Wu, D et al. (2005). No evidence for tumorigenesis of AAV vectors in a large-scale study in mice. Mol Ther 12: 299-306. (Pubitemid 41025100)
8. Li, H, Malani, N, Hamilton, SR, Schlachterman, A, Bussadori, G, Edmonson, SE et al. (2011). Assessing the potential for AAV vector genotoxicity in a murine model. Blood 117: 3311-3319.
9. Schultz, BR and Chamberlain, JS (2008). Recombinant adeno-associated virus transduction and integration. Mol Ther 16: 1189-1199. (Pubitemid 351866049)
10. Yang, J, Zhou, W, Zhang, Y, Zidon, T, Ritchie, T and Engelhardt, JF (1999). Concatamerization of adeno-associated virus circular genomes occurs through intermolecular recombination. J Virol 73: 9468-9477. (Pubitemid 29487102)
11. Miao, CH, Nakai, H, Thompson, AR, Storm, TA, Chiu, W, Snyder, RO et al. (2000). Nonrandom transduction of recombinant adeno-associated virus vectors in mouse hepatocytes in vivo: cell cycling does not influence hepatocyte transduction. J Virol 74: 3793-3803. (Pubitemid 30180322)
12. Nakai, H, Storm, TA and Kay, MA (2000). Recruitment of single-stranded recombinant adeno-associated virus vector genomes and intermolecular recombination are responsible for stable transduction of liver in vivo. J Virol 74: 9451-9463.
13. Choi, VW, McCarty, DM and Samulski, RJ (2006). Host cell DNA repair pathways in adeno-associated viral genome processing. J Virol 80: 10346-10356. (Pubitemid 44628882)
14. Penaud-Budloo, M, Le Guiner, C, Nowrouzi, A, Toromanoff, A, Chérel, Y, Chenuaud, P et al. (2008). Adeno-associated virus vector genomes persist as episomal chromatin in primate muscle. J Virol 82: 7875-7885.
15. Nakai, H, Montini, E, Fuess, S, Storm, TA, Grompe, M and Kay, MA (2003). AAV serotype 2 vectors preferentially integrate into active genes in mice. Nat Genet 34: 297-302. (Pubitemid 36792862)
16. Miller, DG, Trobridge, GD, Petek, LM, Jacobs, MA, Kaul, R and Russell, DW (2005). Large-scale analysis of adeno-associated virus vector integration sites in normal human cells. J Virol 79: 11434-11442. (Pubitemid 41170684)
17. Miller, DG, Rutledge, EA and Russell, DW (2002). Chromosomal effects of adenoassociated virus vector integration. Nat Genet 30: 147-148.
18. Miller, DG, Petek, LM and Russell, DW (2004). Adeno-associated virus vectors integrate at chromosome breakage sites. Nat Genet 36: 767-773. (Pubitemid 38886641)
19. 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-specific human factor IX expression cassette enable highly efficient transduction of murine and nonhuman primate liver. Blood 107: 2653-2661.
20. Sun, X, Lu, Y, Bish, LT, Calcedo, R, Wilson, JM and Gao, G (2010). Molecular analysis of vector genome structures after liver transduction by conventional and selfcomplementary adeno-associated viral serotype vectors in murine and nonhuman primate models. Hum Gene Ther 21: 750-761.
21. Flageul, M, Aubert, D, Pichard, V, Nguyen, TH, Nowrouzi, A, Schmidt, M et al. (2009). Transient expression of genes delivered to newborn rat liver using recombinant adeno-associated virus 2/8 vectors. J Gene Med 11: 689-696.
22. Mattar, CN, Nathwani, AC, Waddington, SN, Dighe, N, Kaeppel, C, Nowrouzi, A et al. (2011). Stable human FIX expression after 0.9G intrauterine gene transfer of self-complementary adeno-associated viral vector 5 and 8 in macaques. Mol Ther 19: 1950-1960.
23. Niemeyer, GP, Herzog, RW, Mount, J, Arruda, VR, Tillson, DM, Hathcock, J et al. (2009). Long-term correction of inhibitor-prone hemophilia B dogs treated with liverdirected AAV2-mediated factor IX gene therapy. Blood 113: 797-806.
24. Gabriel, R, Eckenberg, R, Paruzynski, A, Bartholomae, CC, Nowrouzi, A, Arens, A et al. (2009). Comprehensive genomic access to vector integration in clinical gene therapy. Nat Med 15: 1431-1436.
25. Paruzynski, A, Arens, A, Gabriel, R, Bartholomae, CC, Scholz, S, Wang, W et al. (2010). Genome-wide high-throughput integrome analyses by nrLAM-PCR and nextgeneration sequencing. Nat Protoc 5: 1379-1395.
26. Schmidt, M, Schwarzwaelder, K, Bartholomae, C, Zaoui, K, Ball, C, Pilz, I et al. (2007). High-resolution insertion-site analysis by linear amplification-mediated PCR (LAMPCR). Nat Methods 4: 1051-1057. (Pubitemid 350201778)
27. Inagaki, K, Piao, C, Kotchey, NM, Wu, X and Nakai, H (2008). Frequency and spectrum of genomic integration of recombinant adeno-associated virus serotype 8 vector in neonatal mouse liver. J Virol 82: 9513-9524.
28. Toromanoff, A, Chérel, Y, Guilbaud, M, Penaud-Budloo, M, Snyder, RO, Haskins, ME et al. (2008). Safety and efficacy of regional intravenous (r.i.) versus intramuscular (i.m.) delivery of rAAV1 and rAAV8 to nonhuman primate skeletal muscle. Mol Ther 16: 1291-1299. (Pubitemid 351866061)
29. Chadeuf, G, Ciron, C, Moullier, P and Salvetti, A (2005). Evidence for encapsidation of prokaryotic sequences during recombinant adeno-associated virus production and their in vivo persistence after vector delivery. Mol Ther 12: 744-753. (Pubitemid 41350156)
30. Inagaki, K, Lewis, SM, Wu, X, Ma, C, Munroe, DJ, Fuess, S et al. (2007). DNA palindromes with a modest arm length of greater, similar 20 base pairs are a significant target for recombinant adeno-associated virus vector integration in the liver, muscles, and heart in mice. J Virol 81: 11290-11303. (Pubitemid 47536101)
31. Li, C, Goudy, K, Hirsch, M, Asokan, A, Fan, Y, Alexander, J et al. (2009). Cellular immune response to cryptic epitopes during therapeutic gene transfer. Proc Natl Acad Sci USA 106: 10770-10774.
32. Gao, G, Lu, Y, Calcedo, R, Grant, RL, Bell, P, Wang, L et al. (2006). Biology of AAV serotype vectors in liver-directed gene transfer to nonhuman primates. Mol Ther 13: 77-87. (Pubitemid 41763485)
33. Jiang, H, Couto, LB, Patarroyo-White, S, Liu, T, Nagy, D, Vargas, JA et al. (2006). Effects of transient immunosuppression on adenoassociated, virus-mediated, liverdirected gene transfer in rhesus macaques and implications for human gene therapy. Blood 108: 3321-3328.
34. Nathwani, AC, Rosales, C, McIntosh, J, Rastegarlari, G, Nathwani, D, Raj, D et al. (2011). Long-term Safety and Efficacy Following Systemic Administration of a Selfcomplementary AAV Vector Encoding Human FIX Pseudotyped With Serotype 5 and 8 Capsid Proteins. Mol Ther 19: 876-885.
35. Toromanoff, A, Adjali, O, Larcher, T, Hill, M, Guigand, L, Chenuaud, P et al. (2010). Lack of immunotoxicity after regional intravenous (RI) delivery of rAAV to nonhuman primate skeletal muscle. Mol Ther 18: 151-160.
36. Fougerousse, F, Bartoli, M, Poupiot, J, Arandel, L, Durand, M, Guerchet, N et al. (2007). Phenotypic correction of alpha-sarcoglycan deficiency by intraarterial injection of a muscle-specific serotype 1 rAAV vector. Mol Ther 15: 53-61. (Pubitemid 46043649)
37. Emery, DW (2011). The use of chromatin insulators to improve the expression and safety of integrating gene transfer vectors. Hum Gene Ther 22: 761-774.
38. Cartier, N, Hacein-Bey-Abina, S, Bartholomae, CC, Veres, G, Schmidt, M, Kutschera, I et al. (2009). Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326: 818-823.
39. Camacho, C, Coulouris, G, Avagyan, V, Ma, N, Papadopoulos, J, Bealer, K et al. (2009). BLAST+: architecture and applications. BMC Bioinformatics 10: 421.