Adeno-associated virus replication induces a DNA damage response coordinated by DNA-dependent protein kinase

Journal of Virology

Volumn 83, Issue 12, 2009, Pages 6269-6278

  Schwartz, Rachel A ^a   Carson, Christian T ^a,b   Schuberth, Christine ^a,c   Weitzman, Matthew D ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b BD Technologies   (United States)

^c UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; DNA DEPENDENT PROTEIN KINASE; HISTONE H2AX; KU ANTIGEN; MRE11 PROTEIN; XRCC4 PROTEIN; ATM PROTEIN; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; PROTEIN SERINE THREONINE KINASE; TUMOR SUPPRESSOR PROTEIN; VIRUS DNA;

ADENO ASSOCIATED VIRUS; ARTICLE; ATAXIA TELANGIECTASIA; AUTOPHOSPHORYLATION; CELL DIVISION; CONTROLLED STUDY; DNA DAMAGE; HOST CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MIXED INFECTION; PRIORITY JOURNAL; VIRUS GENOME; VIRUS REPLICATION; ADENOVIRUS; GENETICS; HELA CELL; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; VIROLOGY; VIRUS INFECTION;

ADENO-ASSOCIATED VIRUS; ADENOVIRIDAE; ATAXIA TELANGIECTASIA; PARVOVIRUS;

ADENOVIRIDAE; CELL CYCLE PROTEINS; DEPENDOVIRUS; DNA DAMAGE; DNA, VIRAL; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; PARVOVIRIDAE INFECTIONS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS; VIRUS REPLICATION;

EID: 66149143110     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00318-09     Document Type: Article

References (93)

1. Alexander, I. E., D. W. Russell, and A. D. Miller. 1994. DNA-damaging agents greatly increase the transduction of nondividing cells by adeno-associated virus vectors. J. Virol. 68:8282-8287. (Pubitemid 24362721)
2. Bakkenist, C. J., and M. B. Kastan. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499-506. (Pubitemid 36168436)
3. Berthet, C., K. Raj, P. Saudan, and P. Beard. 2005. How adeno-associated virus Rep78 protein arrests cells completely in S phase. Proc. Natl. Acad. Sci. USA 102:13634-13639.
4. Boyer, J., K. Rohleder, and G. Ketner. 1999. Adenovirus E4 34k and E4 11k inhibit double strand break repair and are physically associated with the cellular DNA-dependent protein kinase. Virology 263:307-312. (Pubitemid 29521523)
5. Branzei, D., and M. Foiani. 2008. Regulation of DNA repair throughout the cell cycle. Nat. Rev. Mol. Cell Biol. 9:297-308.
6. 2/M checkpoint. EMBO J. 22:6610-6620.
7. Carter, B. J. 2004. Adeno-associated virus and the development of adenoassociated virus vectors: a historical perspective. Mol. Ther. 10:981-989.
8. Cassell, G. D., and M. D. Weitzman. 2004. Characterization of a nuclear localization signal in the C-terminus of the adeno-associated virus Rep68/78 proteins. Virology 327:206-214. (Pubitemid 39209326)
9. Cathomen, T., T. H. Stracker, L. B. Gilbert, and M. D. Weitzman. 2001. A genetic screen identifies a cellular regulator of adeno-associated virus. Proc. Natl. Acad. Sci. USA 98:14991-14996.
10. Cerosaletti, K. M., A. Desai-Mehta, T. C. Yeo, M. Kraakman-Van Der Zwet, M. Z. Zdzienicka, and P. Concannon. 2000. Retroviral expression of the NBS1 gene in cultured Nijmegen breakage syndrome cells restores normal radiation sensitivity and nuclear focus formation. Mutagenesis 15:281-286. (Pubitemid 30312721)
11. Cervelli, T., J. A. Palacios, L. Zentilin, M. Mano, R. A. Schwartz, M. D. Weitzman, and M. Giacca. 2008. Processing of recombinant AAV genomes occurs in specific nuclear structures that overlap with foci of DNA-damage-response proteins. J. Cell Sci. 121:349-357. (Pubitemid 351356706)
12. Chejanovsky, N., and B. J. Carter. 1989. Replication of a human parvovirus nonsense mutant in mammalian cells containing an inducible amber suppressor. Virology 171:239-247. (Pubitemid 19180792)
13. Chen, B. P., D. W. Chan, J. Kobayashi, S. Burma, A. Asaithamby, K. Morotomi-Yano, E. Botvinick, J. Qin, and D. J. Chen. 2005. Cell cycle dependence of DNA-dependent protein kinase phosphorylation in response to DNA double strand breaks. J. Biol. Chem. 280:14709-14715.
14. Choi, V. W., D. M. McCarty, and R. J. Samulski. 2006. Host cell DNA repair pathways in adeno-associated viral genome processing. J. Virol. 80:10346-10356. (Pubitemid 44628882)
15. Collaco, R., K. M. Prasad, and J. P. Trempe. 1997. Phosphorylation of the adeno-associated virus replication proteins. Virology 232:332-336. (Pubitemid 27293576)
16. Collis, S. J., T. L. DeWeese, P. A. Jeggo, and A. R. Parker. 2005. The life and death of DNA-PK. Oncogene 24:949-961. (Pubitemid 40313872)
17. Cortez, D., G. Glick, and S. J. Elledge. 2004. Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. Proc. Natl. Acad. Sci. USA 101:10078-10083.
18. Duan, D., P. Sharma, L. Dudus, Y. Zhang, S. Sanlioglu, Z. Yan, Y. Yue, Y. Ye, R. Lester, J. Yang, K. J. Fisher, and J. F. Engelhardt. 1999. Formation of adeno-associated virus circular genomes is differentially regulated by adenovirus E4 ORF6 and E2a gene expression. J. Virol. 73:161-169. (Pubitemid 28565357)
19. Duan, D., P. Sharma, J. Yang, Y. Yue, L. Dudus, Y. Zhang, K. J. Fisher, and J. F. Engelhardt. 1998. Circular intermediates of recombinant adeno-associated virus have defined structural characteristics responsible for long-term episomal persistence in muscle tissue. J. Virol. 72:8568-8577. (Pubitemid 28471794)
20. Duan, D., Y. Yue, and J. F. Engelhardt. 2003. Consequences of DNA-dependent protein kinase catalytic subunit deficiency on recombinant adenoassociated virus genome circularization and heterodimerization in muscle tissue. J. Virol. 77:4751-4759. (Pubitemid 36402825)
21. Durkin, S. S., X. Guo, K. A. Fryrear, V. T. Mihaylova, S. K. Gupta, S. M. Belgnaoui, A. Haoudi, G. M. Kupfer, and O. J. Semmes. 2008. HTLV-1 Tax oncoprotein subverts the cellular DNA damage response via binding to DNA-dependent protein kinase. J. Biol. Chem. 283:36311-36320.
22. Falck, J., J. Coates, and S. P. Jackson. 2005. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434:605-611. (Pubitemid 40488547)
23. Fanning, E., V. Klimovich, and A. R. Nager. 2006. A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic Acids Res. 34:4126-4137. (Pubitemid 44542191)
24. Fragkos, M., M. Breuleux, N. Clement, and P. Beard. 2008. Recombinant adeno-associated viral vectors are deficient in provoking a DNA damage response. J. Virol. 82:7379-7387. (Pubitemid 352031206)
25. Francon, P., J. M. Lemaitre, C. Dreyer, D. Maiorano, O. Cuvier, and M. Mechali. 2004. A hypophosphorylated form of RPA34 is a specific component of pre-replication centers. J. Cell Sci. 117:4909-4920. (Pubitemid 39517508)
26. Gatei, M., D. Young, K. M. Cerosaletti, A. Desai-Mehta, K. Spring, S. Kozlov, M. F. Lavin, R. A. Gatti, P. Concannon, and K. Khanna. 2000. ATM-dependent phosphorylation of nibrin in response to radiation exposure. Nat. Genet. 25:115-119.
27. Geoffroy, M. C., and A. Salvetti. 2005. Helper functions required for wild type and recombinant adeno-associated virus growth. Curr. Gene Ther. 5:265-271.
28. Glauser, D. L., O. Saydam, N. A. Balsiger, I. Heid, R. M. Linden, M. Ackermann, and C. Fraefel. 2005. Four-dimensional visualization of the simultaneous activity of alternative adeno-associated virus replication origins. J. Virol. 79:12218-12230. (Pubitemid 41346083)
29. Glauser, D. L., R. Strasser, A. S. Laimbacher, O. Saydam, N. Clement, R. M. Linden, M. Ackermann, and C. Fraefel. 2007. Live covisualization of competing adeno-associated virus and herpes simplex virus type 1 DNA replication: molecular mechanisms of interaction. J. Virol. 81:4732-4743. (Pubitemid 46668670)
30. Grifman, M., M. Trepel, P. Speece, L. B. Gilbert, W. Arap, R. Pasqualini, and M. D. Weitzman. 2001. Incorporation of tumor-targeting peptides into recombinant adeno-associated virus capsids. Mol. Ther. 3:964-975.
31. Hart, L. S., D. Ornelles, and C. Koumenis. 2007. The adenoviral E4orf6 protein induces atypical apoptosis in response to DNA damage. J. Biol. Chem. 282:6061-6067.
32. Hart, L. S., S. M. Yannone, C. Naczki, J. S. Orlando, S. B. Waters, S. A. Akman, D. J. Chen, D. Ornelles, and C. Koumenis. 2005. The adenovirus E4orf6 protein inhibits DNA double strand break repair and radiosensitizes human tumor cells in an E1B-55K-independent manner. J. Biol. Chem. 280:1474-1481.
33. Heilbronn, R., M. Engstler, S. Weger, A. Krahn, C. Schetter, and M. Boshart. 2003. ssDNA-dependent colocalization of adeno-associated virus Rep. and herpes simplex virus ICP8 in nuclear replication domains. Nucleic Acids Res. 31:6206-6213. (Pubitemid 37442348)
34. Hoppe, B. S., R. B. Jensen, and C. U. Kirchgessner. 2000. Complementation of the radiosensitive M059J cell line. Radiat. Res. 153:125-130.
35. Hunter, L. A., and R. J. Samulski. 1992. Colocalization of adeno-associated virus Rep and capsid proteins in the nuclei of infected cells. J. Virol. 66:317-324.
36. Inagaki, K., C. Ma, T. A. Storm, M. A. Kay, and H. Nakai. 2007. The role of DNA-PKcs and Artemis in opening viral DNA hairpin termini in various tissues in mice. J. Virol. 81:11304-11321. (Pubitemid 47536102)
37. Ishimi, Y., Y. Komamura-Kohno, H. J. Kwon, K. Yamada, and M. Nakanishi. 2003. Identification of MCM4 as a target of the DNA replication block checkpoint system. J. Biol. Chem. 278:24644-24650.
38. Jing, X. J., V. Kalman-Maltese, X. Cao, Q. Yang, and J. P. Trempe. 2001. Inhibition of adenovirus cytotoxicity, replication, and E2a gene expression by adeno-associated virus. Virology 291:140-151. (Pubitemid 34062207)
39. Jurvansuu, J., K. Raj, A. Stasiak, and P. Beard. 2005. Viral transport of DNA damage that mimics a stalled replication fork. J. Virol. 79:569-580. (Pubitemid 39648409)
40. Kudoh, A., M. Fujita, L. Zhang, N. Shirata, T. Daikoku, Y. Sugaya, H. Isomura, Y. Nishiyama, and T. Tsurumi. 2005. Epstein-Barr virus lytic replication elicits ATM checkpoint signal transduction while providing an S-phase-like cellular environment. J. Biol. Chem. 280:8156-8163.
41. Lavin, M. F. 2007. ATM and the Mre11 complex combine to recognize and signal DNA double-strand breaks. Oncogene 26:7749-7758. (Pubitemid 350242462)
42. Leber, R., T. W. Wise, R. Mizuta, and K. Meek. 1998. The XRCC4 gene product is a target for and interacts with the DNA-dependent protein kinase. J. Biol. Chem. 273:1794-1801.
43. Lee, J. H., and T. T. Paull. 2007. Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 26:7741-7748. (Pubitemid 350242454)
44. Lee, K. Y., and K. Myung. 2008. PCNA modifications for regulation of post-replication repair pathways. Mol. Cells 26:5-11.
45. Lees-Miller, S. P., M. C. Long, M. A. Kilvert, V. Lam, S. A. Rice, and C. A. Spencer. 1996. Attenuation of DNA-dependent protein kinase activity and its catalytic subunit by the herpes simplex virus type 1 transactivator ICP0. J. Virol. 70:7471-7477. (Pubitemid 26339051)
46. Lieber, M. R. 2008. The mechanism of human nonhomologous DNA end joining. J. Biol. Chem. 283:1-5.
47. Lilley, C. E., C. T. Carson, A. R. Muotri, F. H. Gage, and M. D. Weitzman. 2005. DNA repair proteins affect the lifecycle of herpes simplex virus 1. Proc. Natl. Acad. Sci. USA 102:5844-5849.
48. Lilley, C. E., R. A. Schwartz, and M. D. Weitzman. 2007. Using or abusing: viruses and the cellular DNA damage response. Trends Microbiol. 15:119-126. (Pubitemid 46356979)
49. Lim, D. S., S. T. Kim, B. Xu, R. S. Maser, J. Lin, J. H. Petrini, and M. B. Kastan. 2000. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404:613-617. (Pubitemid 30205060)
50. Ma, Y., K. Schwarz, and M. R. Lieber. 2005. The Artemis:DNA-PKcs endonuclease cleaves DNA loops, flaps, and gaps. DNA Repair 4:845-851. (Pubitemid 40835856)
51. McGowan, C. H., and P. Russell. 2004. The DNA damage response: sensing and signaling. Curr. Opin. Cell Biol. 16:629-633.
52. Muzyczka, N., and K. I. Berns. 2001. Parvoviridae: the viruses and their replication, p. 2327-2359. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, vol.2, 4th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
53. Narasimhan, D., R. Collaco, V. Kalman-Maltese, and J. P. Trempe. 2002. Hyper-phosphorylation of the adeno-associated virus Rep78 protein inhibits terminal repeat binding and helicase activity. Biochim. Biophys. Acta 1576:298-305.
54. Nash, K., W. Chen, W. F. McDonald, X. Zhou, and N. Muzyczka. 2007. Purification of host cell enzymes involved in adeno-associated virus DNA replication. J. Virol. 81:5777-5787. (Pubitemid 46847016)
55. Nash, K., W. Chen, and N. Muzyczka. 2008. Complete in vitro reconstitution of adeno-associated virus DNA replication requires the minichromosome maintenance complex proteins. J. Virol. 82:1458-1464.
56. Nash, K., W. Chen, M. Salganik, and N. Muzyczka. 2009. Identification of cellular proteins that interact with the adeno-associated virus Rep. protein. J. Virol. 83:454-469.
57. Nghiem, P., P. K. Park, Y. Kim, C. Vaziri, and S. L. Schreiber. 2001. ATR inhibition selectively sensitizes G1 checkpoint-deficient cells to lethal premature chromatin condensation. Proc. Natl. Acad. Sci. USA 98:9092-9097.
58. Ni, T. H., W. F. McDonald, I. Zolotukhin, T. Melendy, S. Waga, B. Stillman, and N. Muzyczka. 1998. Cellular proteins required for adeno-associated virus DNA replication in the absence of adenovirus coinfection. J. Virol. 72:2777-2787. (Pubitemid 28175514)
59. Pegoraro, G., A. Marcello, M. P. Myers, and M. Giacca. 2006. Regulation of adeno-associated virus DNA replication by the cellular TAF-I/set complex. J. Virol. 80:6855-6864. (Pubitemid 44025185)
60. Raj, K., P. Ogston, and P. Beard. 2001. Virus-mediated killing of cells that lack p53 activity. Nature 412:914-917. (Pubitemid 32821736)
61. Ruis, B. L., K. R. Fattah, and E. A. Hendrickson. 2008. The catalytic subunit of DNA-dependent protein kinase regulates proliferation, telomere length, and genomic stability in human somatic cells. Mol. Cell. Biol. 28:6182-6195.
62. Russell, D. W., I. E. Alexander, and A. D. Miller. 1995. DNA synthesis and topoisomerase inhibitors increase transduction by adeno-associated virus vectors. Proc. Natl. Acad. Sci. USA 92:5719-5723.
63. Sancar, A., L. A. Lindsey-Boltz, K. Unsal-Kacmaz, and S. Linn. 2004. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73:39-85.
64. Sanlioglu, S., P. Benson, and J. F. Engelhardt. 2000. Loss of ATM function enhances recombinant adeno-associated virus transduction and integration through pathways similar to UV irradiation. Virology 268:68-78. (Pubitemid 30131972)
65. Saudan, P., J. Vlach, and P. Beard. 2000. Inhibition of S-phase progression by adeno-associated virus Rep78 protein is mediated by hypophosphorylated pRb. EMBO J. 19:4351-4361. (Pubitemid 30623746)
66. Schnepp, B. C., K. R. Clark, D. L. Klemanski, C. A. Pacak, and P. R. Johnson. 2003. Genetic fate of recombinant adeno-associated virus vector genomes in muscle. J. Virol. 77:3495-3504. (Pubitemid 36297269)
67. Schwartz, R. A., J. A. Palacios, G. D. Cassell, S. Adam, M. Giacca, and M. D. Weitzman. 2007. The Mre11/Rad50/Nbs1 complex limits adeno-associated virus transduction and replication. J. Virol. 81:12936-12945. (Pubitemid 350156931)
68. Shi, Y., G. E. Dodson, P. S. Mukhopadhyay, N. P. Shanware, A. T. Trinh, and R. S. Tibbetts. 2007. Identification of carboxyl-terminal MCM3 phosphorylation sites using polyreactive phosphospecific antibodies. J. Biol. Chem. 282:9236-9243.
69. Shi, Y., G. E. Dodson, S. Shaikh, K. Rundell, and R. S. Tibbetts. 2005. Ataxia-telangiectasia-mutated (ATM) is a T-antigen kinase that controls SV40 viral replication in vivo. J. Biol. Chem. 280:40195-40200.
70. Shirata, N., A. Kudoh, T. Daikoku, Y. Tatsumi, M. Fujita, T. Kiyono, Y. Sugaya, H. Isomura, K. Ishizaki, and T. Tsurumi. 2005. Activation of ataxia telangiectasia-mutated DNA damage checkpoint signal transduction elicited by herpes simplex virus infection. J. Biol. Chem. 280:30336-30341.
71. Shrivastav, M., L. P. De Haro, and J. A. Nickoloff. 2008. Regulation of DNA double-strand break repair pathway choice. Cell Res. 18:134-147.
72. Song, S., P. J. Laipis, K. I. Berns, and T. R. Flotte. 2001. Effect of DNA-dependent protein kinase on the molecular fate of the rAAV2 genome in skeletal muscle. Proc. Natl. Acad. Sci. USA 98:4084-4088.
73. Song, S., Y. Lu, Y. K. Choi, Y. Han, Q. Tang, G. Zhao, K. I. Berns, and T. R. Flotte. 2004. DNA-dependent PK inhibits adeno-associated virus DNA integration. Proc. Natl. Acad. Sci. USA 101:2112-2116.
74. Stiff, T., M. O'Driscoll, N. Rief, K. Iwabuchi, M. Lobrich, and P. A. Jeggo. 2004. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 64:2390-2396. (Pubitemid 38523891)
75. Stracker, T. H., C. T. Carson, and M. D. Weitzman. 2002. Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 418:348-352. (Pubitemid 34790688)
76. Stracker, T. H., G. D. Cassell, P. Ward, Y. M. Loo, B. van Breukelen, S. D. Carrington-Lawrence, R. K. Hamatake, P. C. van der Vliet, S. K. Weller, T. Melendy, and M. D. Weitzman. 2004. The Rep protein of adeno-associated virus type 2 interacts with single-stranded DNA-binding proteins that enhance viral replication. J. Virol. 78:441-453. (Pubitemid 37549754)
77. Taylor, T. J., and D. M. Knipe. 2004. Proteomics of herpes simplex virus replication compartments: association of cellular DNA replication, repair, recombination, and chromatin remodeling proteins with ICP8. J. Virol. 78:5856-5866. (Pubitemid 38661673)
78. Tomida, J., Y. Masuda, H. Hiroaki, T. Ishikawa, I. Song, T. Tsurimoto, S. Tateishi, T. Shiomi, Y. Kamei, J. Kim, K. Kamiya, C. Vaziri, H. Ohmori, and T. Todo. 2008. DNA damage-induced ubiquitylation of RFC2 subunit of replication factor C complex. J. Biol. Chem. 283:9071-9079.
79. Urcelay, E., P. Ward, S. M. Wiener, B. Safer, and R. M. Kotin. 1995. Asymmetric replication in vitro from a human sequence element is dependent on adeno-associated virus Rep protein. J. Virol. 69:2038-2046.
80. Uziel, T., Y. Lerenthal, L. Moyal, Y. Andegeko, L. Mittelman, and Y. Shiloh. 2003. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 22:5612-5621. (Pubitemid 37279970)
81. van Gent, D. C., and M. van der Burg. 2007. Non-homologous end-joining, a sticky affair. Oncogene 26:7731-7740. (Pubitemid 350242453)
82. Vassin, V. M., M. S. Wold, and J. A. Borowiec. 2004. Replication protein A (RPA) phosphorylation prevents RPA association with replication centers. Mol. Cell. Biol. 24:1930-1943.
83. Wang, Y., X. Y. Zhou, H. Wang, M. S. Huq, and G. Iliakis. 1999. Roles of replication protein A and DNA-dependent protein kinase in the regulation of DNA replication following DNA damage. J. Biol. Chem. 274:22060-22064.
84. Weitzman, M. D., K. J. Fisher, and J. M. Wilson. 1996. Recruitment of wild-type and recombinant adeno-associated virus into adenovirus replication centers. J. Virol. 70:1845-1854. (Pubitemid 26062948)
85. Weterings, E., and D. J. Chen. 2007. DNA-dependent protein kinase in nonhomologous end joining: a lock with multiple keys? J. Cell Biol. 179:183-186. (Pubitemid 350004882)
86. Weterings, E., and D. J. Chen. 2008. The endless tale of non-homologous end-joining. Cell Res. 18:114-124.
87. Wilkinson, D. E., and S. K. Weller. 2004. Recruitment of cellular recombination and repair proteins to sites of herpes simplex virus type 1 DNA replication is dependent on the composition of viral proteins within prereplicative sites and correlates with the induction of the DNA damage response. J. Virol. 78:4783-4796. (Pubitemid 38501099)
88. Winocour, E., M. F. Callaham, and E. Huberman. 1988. Perturbation of the cell cycle by adeno-associated virus. Virology 167:393-399. (Pubitemid 19037133)
89. Wistuba, A., A. Kern, S. Weger, D. Grimm, and J. A. Kleinschmidt. 1997. Subcellular compartmentalization of adeno-associated virus type 2 assembly. J. Virol. 71:1341-1352. (Pubitemid 27030308)
90. Xiao, X., J. Li, and R. J. Samulski. 1998. Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J. Virol. 72:2224-2232. (Pubitemid 28100780)
91. Yalkinoglu, A. O., R. Heilbronn, A. Burkle, J. R. Schlehofer, and H. zur Hausen. 1988. DNA amplification of adeno-associated virus as a response to cellular genotoxic stress. Cancer Res. 48:3123-3129.
92. Zentilin, L., A. Marcello, and M. Giacca. 2001. Involvement of cellular double-stranded DNA break binding proteins in processing of the recombinant adeno-associated virus genome. J. Virol. 75:12279-12287. (Pubitemid 33115900)
93. Zhao, X., R. J. Madden-Fuentes, B. X. Lou, J. M. Pipas, J. Gerhardt, C. J. Rigell, and E. Fanning. 2008. Ataxia telangiectasia-mutated damage-signaling kinase- and proteasome-dependent destruction of Mre11-Rad50-Nbs1 subunits in Simian virus 40-infected primate cells. J. Virol. 82:5316-5328. (Pubitemid 351705239)