Effect of poly(ADP-ribose) polymerase 1 on integration of the adeno-associated viral vector genome

Journal of Gene Medicine

Volumn 13, Issue 6, 2011, Pages 342-352

  Romanova, Liudmila G ^a   Zacharias, Jeana ^a   Cannon, Mark L ^b   Philpott, Nicola J ^a  

^a Department of Medicine Institute of Human Genetics ^*  (United States)

^b Institute of Human Genetics   (United States)

Author keywords

Adeno associated virus; Integration; Ligase III; Nonhomologous end joining; Poly(ADP ribose) polymerase 1; Rep

Indexed keywords

DNA LIGASE III; ENDONUCLEASE; HELICASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PARVOVIRUS VECTOR; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; SCAFFOLD PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; XRCC1 PROTEIN;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS TYPE 2; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HELA CELL; HUMAN; HUMAN CELL; INHIBITION KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DNA INTERACTION; PROTEIN PROTEIN INTERACTION; VIRAL GENE THERAPY; VIRUS GENOME;

BLOTTING, SOUTHERN; BLOTTING, WESTERN; DEPENDOVIRUS; DNA PRIMERS; DNA-BINDING PROTEINS; GENETIC VECTORS; GENOME, VIRAL; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; POLY(ADP-RIBOSE) POLYMERASES; POLYMERASE CHAIN REACTION; VIRAL PROTEINS; VIRUS INTEGRATION;

ADENO-ASSOCIATED VIRUS; ADENO-ASSOCIATED VIRUS - 2;

EID: 79959699183     PISSN: 1099498X     EISSN: 15212254     Source Type: Journal    
DOI: 10.1002/jgm.1577     Document Type: Article

References (62)

1. Berns KI, Linden RM. The cryptic life style of adeno-associated virus. Bioessays 1995; 17: 237-245.
2. Srivastava A, Lusby EW, Berns KI. Nucleotide sequence and organization of the adeno-associated virus 2 genome. J Virol 1983; 45: 555-564.
3. Srivastava A. Replication of the adeno-associated virus DNA termini in vitro. Intervirology 1987; 27: 138-147.
4. Lusby E, Fife KH, Berns KI. Nucleotide sequence of the inverted terminal repetition in adeno-associated virus DNA. J Virol 1980; 34: 402-409.
5. Senapathy P, Carter BJ. Molecular cloning of adeno-associated virus variant genomes and generation of infectious virus by recombination in mammalian cells. J Biol Chem 1984; 259: 4661-4666.
6. Spear IS, Fife KH, Hauswirth WW, et al. Evidence for two nucleotide sequence orientations within the terminal repetition of adeno-associated virus DNA. J Virol 1977; 24: 627-634.
7. Samulski RJ, Srivastava A, Berns KI, et al. Rescue of adeno-associated virus from recombinant plasmids: gene correction within the terminal repeats of AAV. Cell 1983; 33: 135-143.
8. Kotin RM, Berns KI. Organization of adeno-associated virus DNA in latently infected Detroit 6 cells. Virology 1989; 170: 460-467.
9. Kotin RM, Linden RM, Berns KI. Characterization of a preferred site on human chromosome 19q for integration of adeno-associated virus DNA by non-homologous recombination. EMBO J 1992; 11: 5071-5078.
10. Kotin RM, Menninger JC, Ward DC, et al. Mapping and direct visualization of a region-specific viral DNA integration site on chromosome 19q13-qter. Genomics 1991; 10: 831-834.
11. Kotin RM, Siniscalco M, Samulski RJ, et al. Site-specific integration by adeno-associated virus. Proc Natl Acad Sci USA 1990; 87: 2211-2215.
12. Linden RM, Ward P, Giraud C, et al. Site-specific integration by adeno-associated virus. Proc Natl Acad Sci USA 1996; 93: 11288-11294.
13. Samulski RJ, Zhu X, Xiao X, et al. Targeted integration of adeno-associated virus (AAV) into human chromosome 19. EMBO J 1991; 10: 3941-3950.
14. Giraud C, Winocour E, Berns KI. Site-specific integration by adeno-associated virus is directed by a cellular DNA sequence. Proc Natl Acad Sci USA 1994; 91: 10039-10043.
15. Balague C, Kalla M, Zhang WW. Adeno-associated virus Rep78 protein and terminal repeats enhance integration of DNA sequences into the cellular genome. J Virol 1997; 71: 3299-3306.
16. Trempe JP, Mendelson E, Carter BJ. Characterization of adeno-associated virus rep proteins in human cells by antibodies raised against rep expressed in Escherichia coli. Virology 1987; 161: 18-28.
17. Beaton A, Palumbo P, Berns KI. Expression from the adeno-associated virus p5 and p19 promoters is negatively regulated in trans by the rep protein. J Virol 1989; 63: 4450-4454.
18. Drew HR, Lockett LJ, Both GW. Increased complexity of wild-type adeno-associated virus-chromosomal junctions as determined by analysis of unselected cellular genomes. J Gen Virol 2007; 88: 1722-1732.
19. Huser D, Gogol-Doring A, Lutter T, et al. Integration preferences of wildtype AAV-2 for consensus rep-binding sites at numerous loci in the human genome. PLoS Pathog 2010; 6: e1000985.
20. Linden RM, Winocour E, Berns KI. The recombination signals for adeno-associated virus site-specific integration. Proc Natl Acad Sci USA 1996; 93: 7966-7972.
21. Young SM Jr, Samulski RJ. Adeno-associated virus (AAV) site-specific recombination does not require a Rep-dependent origin of replication within the AAV terminal repeat. Proc Natl Acad Sci USA 2001; 98: 13525-13530.
22. Dyall J, Berns KI Site-specific integration of adeno-associated virus into an episome with the target locus via a deletion-substitution mechanism. J Virol 1998; 72: 6195-6198.
23. Yang CC, Xiao X, Zhu X, et al. Cellular recombination pathways and viral terminal repeat hairpin structures are sufficient for adeno-associated virus integration in vivo and in vitro. J Virol 1997; 71: 9231-9247.
24. Urcelay E, Ward P, Wiener SM, et al. Asymmetric replication in vitro from a human sequence element is dependent on adeno-associated virus Rep protein. J Virol 1995; 69: 2038-2046.
25. Young SM Jr, McCarty DM, Degtyareva N, et al. Roles of adeno-associated virus Rep protein and human chromosome 19 in site-specific recombination. J Virol 2000; 74: 3953-3966.
26. Henckaerts E, Dutheil N, Zeltner N, et al. Site-specific integration of adeno-associated virus involves partial duplication of the target locus. Proc Natl Acad Sci USA 2009; 106: 7571-7576.
27. Daya S, Berns KI. Gene therapy using adeno-associated virus vectors. Clin Microbiol Rev 2008; 21: 583-593.
28. Kay MA, Manno CS, Ragni MV, et al. Evidence for gene transfer and expression of factor IX in haemophilia B patients treated with an AAV vector. Nat Genet 2000; 24: 257-261.
29. Herzog RW. AAV-mediated gene transfer to skeletal muscle. Methods Mol Biol 2004; 246: 179-194.
30. Flotte TR. Adeno-associated virus-mediated gene transfer for lung diseases. Hum Gene Ther 2005; 16: 643-648.
31. Moss RB, Milla C, Colombo J, et al. Repeated aerosolized AAV-CFTR for treatment of cystic fibrosis: a randomized placebo-controlled phase 2B trial. Hum Gene Ther 2007; 18: 726-732.
32. Mingozzi F, High KA. Immune responses to AAV in clinical trials. Curr Gene Ther 2007; 7: 316-324.
33. Kaplitt MG, Feigin A, Tang C, et al. Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial. Lancet 2007; 369: 2097-2105.
34. Nakai H, Iwaki Y, Kay MA, et al. Isolation of recombinant adeno-associated virus vector-cellular DNA junctions from mouse liver. J Virol 1999; 73: 5438-5447.
35. Kohn DB, Sadelain M, Glorioso JC. Occurrence of leukaemia following gene therapy of X-linked SCID. Nat Rev Cancer 2003; 3: 477-488.
36. Song S, Lu Y, Choi YK, et al. DNA-dependent PK inhibits adeno-associated virus DNA integration. Proc Natl Acad Sci USA 2004; 101: 2112-2116.
37. Schwartz RA, Carson CT, Schuberth C, et al. Adeno-associated virus replication induces a DNA damage response coordinated by DNA-dependent protein kinase. J Virol 2009; 83: 6269-6278.
38. Daya S, Cortez N, Berns KI. Adeno-associated virus site-specific integration is mediated by proteins of the nonhomologous end-joining pathway. J Virol 2009; 83: 11655-11664.
39. Audebert M, Salles B, Calsou P. Involvement of poly (ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J Biol Chem 2004; 279: 55117-55126.
40. Wang M, Wu W, Rosidi B, et al. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res 2006; 34: 6170-6182.
41. Caldecott KW. Cell signaling. The BRCT domain: signaling with friends? Science 2003; 302: 579-580.
42. Wang H, Rosidi B, Perrault R, et al. DNA ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res 2005; 65: 4020-4030.
43. Caldecott KW, Aoufouchi S, Johnson P, et al. XRCC1 polypeptide interacts with DNA polymerase beta and possibly poly (ADP-ribose) polymerase, and DNA ligase III is a novel molecular 'nick-sensor' in vitro. Nucleic Acids Res 1996; 24: 4387-4394.
44. Ladiges WC. Mouse models of XRCC1 DNA repair polymorphisms and cancer. Oncogene 2006; 25: 1612-1619.
45. Philpott NJ, Giraud-Wali C, Dupuis C, et al. Efficient integration of recombinant adeno-associated virus DNA vectors requires a p5-rep sequence in cis. J Virol 2002; 76: 5411-5421.
46. Grimm D, Kern A, Rittner K, et al. Novel tools for production and purification of recombinant adenoassociated virus vectors. Hum Gene Ther 1998; 9: 2745-2760.
47. Godon C, Cordelieres FP, Biard D, et al. PARP inhibition vs. PARP-1 silencing: different outcomes in terms of single-strand break repair and radiation susceptibility. Nucleic Acids Res 2008; 36: 4454-4464.
48. Biard DS. Untangling the relationships between DNA repair pathways by silencing more than 20 DNA repair genes in human stable clones. Nucleic Acids Res 2007; 35: 3535-3550.
49. Kim MY, Zhang T, Kraus WL. Poly (ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal. Genes Dev 2005; 19: 1951-1967.
50. Zhang J. Are poly (ADP-ribosyl)ation by PARP-1 and deacetylation by Sir2 linked? Bioessays 2003; 25: 808-814.
51. Lamartina S, Sporeno E, Fattori E, et al. Characteristics of the adeno-associated virus preintegration site in human chromosome 19: open chromatin conformation and transcription-competent environment. J Virol 2000; 74: 7671-7677.
52. Philpott NJ, Gomos J, Berns KI, et al. A p5 integration efficiency element mediates Rep-dependent integration into AAVS1 at chromosome 19. Proc Natl Acad Sci USA 2002; 99: 12381-12385.
53. Philpott NJ, Gomos J, Falck-Pedersen E. Transgene expression after rep-mediated site-specific integration into chromosome 19. Hum Gene Ther 2004; 15: 47-61.
54. Windhofer F, Wu W, Iliakis G. Low levels of DNA ligases III and IV sufficient for effective NHEJ. J Cell Physiol 2007; 213: 475-483.
55. Costello E, Saudan P, Winocour E, et al. High mobility group chromosomal protein 1 binds to the adeno-associated virus replication protein (Rep) and promotes Rep-mediated site-specific cleavage of DNA, ATPase activity and transcriptional repression. EMBO J 1997; 16: 5943-5954.
56. Han SI, Kawano MA, Ishizu K, et al. Rep68 protein of adeno-associated virus type 2 interacts with 14-3-3 proteins depending on phosphorylation at serine 535. Virology 2004; 320: 144-155.
57. Pegoraro G, Marcello A, Myers MP, et al. Regulation of adeno-associated virus DNA replication by the cellular TAF-I/set complex. J Virol 2006; 80: 6855-6864.
58. Bevington JM, Needham PG, Verrill KC, et al. Adeno-associated virus interactions with B23/Nucleophosmin: identification of sub-nucleolar virion regions. Virology 2007; 357: 102-113.
59. Yamamoto N, Suzuki M, Kawano MA, et al. Adeno-associated virus site-specific integration is regulated by TRP-185. J Virol 2007; 81: 1990-2001.
60. Nash K, Chen W, Salganik M, et al. Identification of cellular proteins that interact with the adeno-associated virus rep protein. J Virol 2009; 83: 454-469.
61. Schreiber V, Dantzer F, Ame JC, et al. Poly (ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 2006; 7: 517-528.
62. Miller DG, Petek LM, Russell DW. Adeno-associated virus vectors integrate at chromosome breakage sites. Nat Genet 2004; 36: 767-773.