Oversized AAV transductifon is mediated via a DNA-PKcs-independent, Rad51C-dependent repair pathway

Molecular Therapy

Volumn 21, Issue 12, 2013, Pages 2205-2216

  Hirsch, Matthew L ^a   Li, Chengwen ^a   Bellon, Isabella ^a   Yin, Chaoying ^a   Chavala, Sai ^a,b   Pryadkina, Marina ^c   Richard, Isabelle ^c   Samulski, Richard Jude ^a  

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

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c GÉNÉTHON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROFORM; COMPLEMENTARY DNA; DEOXYRIBONUCLEASE; DNA DEPENDENT PROTEIN KINASE; DYSFERLIN; LUCIFERASE; PROTEIN RAD51C; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA REPAIR; DNA STRAND; ENZYME ACTIVE SITE; FEMALE; FRACTIONATION; GENE EXPRESSION; GENOME ANALYSIS; GENOMIC FRAGMENT; IN VITRO STUDY; IN VIVO STUDY; LUCIFERASE ASSAY; MOUSE; NONHUMAN; PARTICLE SIZE; PROCESS OPTIMIZATION; VIRAL GENE DELIVERY SYSTEM; VIRUS GENOME;

ADENO-ASSOCIATED VIRUS; MIRIDAE;

ANIMALS; CAPSID; CHO CELLS; CRICETULUS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; DNA PACKAGING; DNA, VIRAL; DNA-BINDING PROTEINS; EYE; GENES, REPORTER; GENETIC THERAPY; GENETIC VECTORS; GENOME, VIRAL; HEK293 CELLS; HELA CELLS; HUMANS; LIVER; MICE; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCLES; NUCLEIC ACID CONFORMATION; RAD51 RECOMBINASE; TRANSDUCTION, GENETIC;

EID: 84890119936     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.184     Document Type: Article

References (44)

1. Samulski, RJ, Berns, KI, Tan, M and Muzyczka, N (1982). Cloning of adeno-associated virus into pBR322: Rescue of intact virus from the recombinant plasmid in human cells. Proc Natl Acad Sci USA 79: 2077-2081
2. Mitchell, AM, Nicolson, SC, Warischalk, JK and Samulski, RJ (2010). AAV's anatomy: Roadmap for optimizing vectors for translational success. Curr Gene Ther 10: 319-340
3. Summerford, C and Samulski, RJ (1998). Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J Virol 72: 1438-1445
4. Duan, D, Li, Q, Kao, AW, Yue, Y, Pessin, JE and Engelhardt, JF (1999). Dynamin is required for recombinant adeno-associated virus type 2 infection. J Virol 73: 10371-10376
5. Choi, VW, McCarty, DM and Samulski, RJ (2006). Host cell DNA repair pathways in adeno-associated viral genome processing. J Virol 80: 10346-10356
6. Zentilin, L, Marcello, A and Giacca, M (2001). Involvement of cellular double-stranded DNA break binding proteins in processing of the recombinant adeno-associated virus genome. J Virol 75: 12279-12287
7. Duan, D, Yue, Y and Engelhardt, JF (2003). Consequences of DNA-dependent protein kinase catalytic subunit deficiency on recombinant adeno-associated virus genome circularization and heterodimerization in muscle tissue. J Virol 77: 4751-4759
8. Cataldi, MP and McCarty, DM (2010). Differential effects of DNA double-strand break repair pathways on single-strand and self-complementary adeno-associated virus vector genomes. J Virol 84: 8673-8682
9. Lovric, J, Mano, M, Zentilin, L, Eulalio, A, Zacchigna, S and Giacca, M (2012). Terminal differentiation of cardiac and skeletal myocytes induces permissivity to AAV transduction by relieving inhibition imposed by DNA damage response proteins. Mol Ther 20: 2087-2097
10. Hirsch, ML, Storici, F, Li, C, Choi, VW and Samulski, RJ (2009). AAV recombineering with single strand oligonucleotides. PLoS ONE 4: E7705
11. Inagaki, K, Ma, C, Storm, TA, Kay, MA and Nakai, H (2007). The role of DNA-PKcs and artemis in opening viral DNA hairpin termini in various tissues in mice. J Virol 81: 11304-11321
12. Hirsch, ML, Fagan, BM, Dumitru, R, Bower, JJ, Yadav, S, Porteus, MH et al. (2011). Viral single-strand DNA induces p53-dependent apoptosis in human embryonic stem cells. PLoS ONE 6: E27520
13. Raj, K, Ogston, P and Beard, P (2001). Virus-mediated killing of cells that lack p53 activity. Nature 412: 914-917
14. Duan, D, Yue, Y and Engelhardt, JF (2001). Expanding AAV packaging capacity with trans-splicing or overlapping vectors: A quantitative comparison. Mol Ther 4: 383-391
15. Halbert, CL, Allen, JM and Miller, AD (2002). Efficient mouse airway transduction following recombination between AAV vectors carrying parts of a larger gene. Nat Biotechnol 20: 697-701
16. Ghosh, A, Yue, Y and Duan, D (2011). Efficient transgene reconstitution with hybrid dual AAV vectors carrying the minimized bridging sequences. Hum Gene Ther 22(1): 77-83
17. Allocca, M, Doria, M, Petrillo, M, Colella, P, Garcia-Hoyos, M, Gibbs, D et al. (2008). Serotype-dependent packaging of large genes in adeno-associated viral vectors results in effective gene delivery in mice. J Clin Invest 118: 1955-1964
18. Wu, Z, Yang, H and Colosi, P (2010). Effect of genome size on AAV vector packaging. Mol Ther 18: 80-86
19. Dong, B, Nakai, H and Xiao, W (2010). Characterization of genome integrity for oversized recombinant AAV vector. Mol Ther 18: 87-92
20. Lai, Y, Yue, Y and Duan, D (2010). Evidence for the failure of adeno-associated virus serotype 5 to package a viral genome > or = 8.2 kb. Mol Ther 18: 75-79
21. Kapranov, P, Chen, L, Dederich, D, Dong, B, He, J, Steinmann, KE et al. (2012). Native molecular state of adeno-associated viral vectors revealed by single-molecule sequencing. Hum Gene Ther 23: 46-55
22. Hirsch, ML, Agbandje-McKenna, M and Samulski, RJ (2010) Little vector, big gene transduction: Fragmented genome reassembly of adeno-associated virus. Mol Ther 18(1): 6-8
23. Monahan, PE, Lothrop, CD, Sun, J, Hirsch, ML, Kafri, T, Kantor, B et al. (2010). Proteasome inhibitors enhance gene delivery by AAV virus vectors expressing large genomes in hemophilia mouse and dog models: A strategy for broad clinical application. Mol Ther 18: 1907-1916
24. Grose, WE, Clark, KR, Griffin, D, Malik, V, Shontz, KM, Montgomery, CL et al. (2012). Homologous recombination mediates functional recovery of dysferlin deficiency following AAV5 gene transfer. PLoS ONE 7: E39233
25. Grieger, JC, Choi, VW and Samulski, RJ (2006). Production and characterization of adeno-associated viral vectors. Nat Protoc 1: 1412-1428
26. Zhou, X and Muzyczka, N (1998). In vitro packaging of adeno-associated virus DNA. J Virol 72: 3241-3247
27. 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
28. Lostal, W, Bartoli, M, Bourg, N, Roudaut, C, Bentaïb, A, Miyake, K et al. (2010). Efficient recovery of dysferlin deficiency by dual adeno-associated vector-mediated gene transfer. Hum Mol Genet 19: 1897-1907
29. Peterson, SR, Kurimasa, A, Oshimura, M, Dynan, WS, Bradbury, EM and Chen, DJ (1995). Loss of the catalytic subunit of the DNA-dependent protein kinase in DNA double-strand-break-repair mutant mammalian cells. Proc Natl Acad Sci USA 92: 3171-3174
30. Ding, Q, Reddy, YV, Wang, W, Woods, T, Douglas, P, Ramsden, DA et al. (2003). Autophosphorylation of the catalytic subunit of the DNA-dependent protein kinase is required for efficient end processing during DNA double-strand break repair. Mol Cell Biol 23: 5836-5848
31. Liu, Y, Masson, JY, Shah, R, O'Regan, P and West, SC (2004). RAD51C is required for Holliday junction processing in mammalian cells. Science 303: 243-246
32. Masson, JY, Tarsounas, MC, Stasiak, AZ, Stasiak, A, Shah, R, McIlwraith, MJ et al. (2001). Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev 15: 3296-3307
33. 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
34. Xu, Z, Yue, Y, Lai, Y, Ye, C, Qiu, J, Pintel, DJ et al. (2004). Trans-splicing adenoassociated viral vector-mediated gene therapy is limited by the accumulation of spliced mRNA but not by dual vector coinfection efficiency. Hum Gene Ther 15: 896-905
35. Gildemeister, OS, Sage, JM and Knight, KL (2009). Cellular redistribution of Rad51 in response to DNA damage: Novel role for Rad51C. J Biol Chem 284: 31945- 31952
36. Miller, KA, Yoshikawa, DM, McConnell, IR, Clark, R, Schild, D and Albala, JS (2002). RAD51C interacts with RAD51B and is central to a larger protein complex in vivo exclusive of RAD51. J Biol Chem 277: 8406-8411
37. Masson, JY, Stasiak, AZ, Stasiak, A, Benson, FE and West, SC (2001). Complex formation by the human RAD51C and XRCC3 recombination repair proteins. Proc Natl Acad Sci USA 98: 8440-8446
38. Wiese, C, Collins, DW, Albala, JS, Thompson, LH, Kronenberg, A and Schild, D (2002). Interactions involving the Rad51 paralogs Rad51C and XRCC3 in human cells. Nucleic Acids Res 30: 1001-1008
39. Wu, Z, Sun, J, Zhang, T, Yin, C, Yin, F, Van Dyke, T et al. (2008). Optimization of self-complementary AAV vectors for liver-directed expression results in sustained correction of hemophilia B at low vector dose. Mol Ther 16: 280-289
40. Foster, H, Sharp, PS, Athanasopoulos, T, Trollet, C, Graham, IR, Foster, K et al. (2008). Codon and mRNA sequence optimization of microdystrophin transgenes improves expression and physiological outcome in dystrophic mdx mice following AAV2/8 gene transfer. Mol Ther 16: 1825-1832
41. Millay, DP, Maillet, M, Roche, JA, Sargent, MA, McNally, EM, Bloch, RJ et al. (2009). Genetic manipulation of dysferlin expression in skeletal muscle: Novel insights into muscular dystrophy. Am J Pathol 175: 1817-1823
42. Glover, LE, Newton, K, Krishnan, G, Bronson, R, Boyle, A, Krivickas, LS et al. (2010). Dysferlin overexpression in skeletal muscle produces a progressive myopathy. Ann Neurol 67: 384-393
43. Jones, NJ, Cox, R and Thacker, J (1987). Isolation and cross-sensitivity of X-ray-sensitive mutants of V79-4 hamster cells. Mutat Res 183: 279-286
44. Caldecott, K and Jeggo, P (1991). Cross-sensitivity of gamma-ray-sensitive hamster mutants to cross-linking agents. Mutat Res 255: 111-121