Inhibition of herpes simplex virus type 1 replication by adeno-associated virus rep proteins depends on their combined DNA-binding and ATPase/helicase activities

Journal of Virology

Volumn 84, Issue 8, 2010, Pages 3808-3824

  Glauser, Daniel L ^a,b   Seyffert, Michael ^a   Strasser, Regina ^a   Franchini, Marco ^a   Laimbacher, Andrea S ^a   Dresch, Christiane ^a   De Oliveira, Anna Paula ^a   Vogel, Rebecca ^a   Büning, Hildegard ^c   Salvetti, Anna ^d,e,f,g   Ackermann, Mathias ^a   Fraefel, Cornel ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^d CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^e UNIVERSITÉ DE LYON   (France)

^f University Lyon i   (France)

^g UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; HELICASE; REPLICATION FACTOR A; REPLICATION INITIATOR PROTEIN; TRANSACTIVATOR PROTEIN; VIRUS DNA; VIRUS PROTEIN;

ADENO ASSOCIATED VIRUS; ARTICLE; DNA BINDING; ENZYME ACTIVITY; HERPES SIMPLEX VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; VIRUS REPLICATION; ANIMAL; APOPTOSIS; CERCOPITHECUS; DNA DAMAGE; GENE DELETION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; VERO CELL;

ADENO-ASSOCIATED VIRUS; HUMAN HERPESVIRUS 1;

ADENOSINE TRIPHOSPHATASES; ANIMALS; APOPTOSIS; CERCOPITHECUS AETHIOPS; DEPENDOVIRUS; DNA DAMAGE; DNA HELICASES; DNA, VIRAL; HERPESVIRUS 1, HUMAN; PHOSPHORYLATION; SEQUENCE DELETION; TRANS-ACTIVATORS; VERO CELLS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 77950464714     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01503-09     Document Type: Article

References (94)

1. Aboody-Guterman, K. S., P. A. Pechan, N. G. Rainov, M. Sena-Esteves, A. Jacobs, E. Y. Snyder, P. Wild, E. Schraner, K. Tobler, X. O. Breakefield, and C. Fraefel. 1997. Green fluorescent protein as a reporter for retrovirus and helper virus-free HSV-1 amplicon vector-mediated gene transfer into neural cells in culture and in vivo. Neuroreport 8: 3801-3808.
2. Adams, R. L., and J. G. Lindsay. 1967. Hydroxyurea reversal of inhibition and use as a cell-synchronizing agent. J. Biol. Chem. 242: 1314-1317.
3. Alazard-Dany, N., A. Nicolas, A. Ploquin, R. Strasser, A. Greco, A. L. Epstein, C. Fraefel, and A. Salvetti. 2009. Definition of herpes simplex virus type 1 helper activities for adeno-associated virus early replication events. PLoS Pathog. 5: e1000340.
4. Bantel-Schaal, U., and H. zur Hausen. 1988. Adeno-associated viruses inhibit SV40 DNA amplification and replication of herpes simplex virus in SV40-transformed hamster cells. Virology 164: 64-74.
5. 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. U. S. A. 102: 13634-13639.
6. Binz, S. K., A. M. Sheehan, and M. S. Wold. 2004. Replication protein A phosphorylation and the cellular response to DNA damage. DNA Repair 3: 1015-1024.
7. Brister, J. R., and N. Muzyczka. 2000. Mechanism of Rep-mediated adenoassociated virus origin nicking. J. Virol. 74: 7762-7771.
8. Brister, J. R., and N. Muzyczka. 1999. Rep-mediated nicking of the adenoassociated virus origin requires two biochemical activities, DNA helicase activity and transesterification. J. Virol. 73: 9325-9336.
9. Buller, R. M., J. E. Janik, E. D. Sebring, and J. A. Rose. 1981. Herpes simplex virus types 1 and 2 completely help adenovirus-associated virus replication. J. Virol. 40: 241-247.
10. Carter, B. J., C. A. Laughlin, L. M. de la Maza, and M. Myers. 1979. Adeno-associated virus autointerference. Virology 92: 449-462.
11. Casto, B. C., J. A. Armstrong, R. W. Atchison, and W. M. Hammon. 1967. Studies on the relationship between adeno-associated virus type 1 (AAV-1) and adenoviruses. II. Inhibition of adenovirus plaques by AAV; its nature and specificity. Virology 33: 452-458.
12. Casto, B. C., R. W. Atchison, and W. M. Hammon. 1967. Studies on the relationship between adeno-associated virus type I (AAV-1) and adenoviruses. I. Replication of AAV-1 in certain cell cultures and its effect on helper adenovirus. Virology 32: 52-59.
13. Chejanovsky, N., and B. J. Carter. 1990. Mutation of a consensus purine nucleotide binding site in the adeno-associated virus rep gene generates a dominant negative phenotype for DNA replication. J. Virol. 64: 1764-1770.
14. Chiorini, J. A., S. M. Wiener, R. A. Owens, S. R. Kyostio, R. M. Kotin, and B. Safer. 1994. Sequence requirements for stable binding and function of Rep68 on the adeno-associated virus type 2 inverted terminal repeats. J. Virol. 68: 7448-7457.
15. Chiorini, J. A., L. Yang, B. Safer, and R. M. Kotin. 1995. Determination of adeno-associated virus Rep68 and Rep78 binding sites by random sequence oligonucleotide selection. J. Virol. 69: 7334-7338.
16. Chiorini, J. A., B. Zimmermann, L. Yang, R. H. Smith, A. Ahearn, F. Herberg, and R. M. Kotin. 1998. Inhibition of PrKX, a novel protein kinase, and the cyclic AMP-dependent protein kinase PKA by the regulatory proteins of adeno-associated virus type 2. Mol. Cell. Biol. 18: 5921-5929.
17. Cohen, G. H., D. Long, and R. J. Eisenberg. 1980. Synthesis and processing of glycoproteins gD and gC of herpes simplex virus type 1. J. Virol. 36: 429-439.
18. Collaco, R. F., V. Kalman-Maltese, A. D. Smith, J. D. Dignam, and J. P. Trempe. 2003. A biochemical characterization of the adeno-associated virus Rep40 helicase. J. Biol. Chem. 278: 34011-34017.
19. Cortez, D. 2005. Unwind and slow down: checkpoint activation by helicase and polymerase uncoupling. Genes Dev. 19: 1007-1012.
20. Davis, M. D., J. Wu, and R. A. Owens. 2000. Mutational analysis of adenoassociated virus type 2 Rep68 protein endonuclease activity on partially single-stranded substrates. J. Virol. 74: 2936-2942.
21. de Oliveira, A. P., D. L. Glauser, A. S. Laimbacher, R. Strasser, E. M. Schraner, P. Wild, U. Ziegler, X. O. Breakefield, M. Ackermann, and C. Fraefel. 2008. Live visualization of herpes simplex virus type 1 compartment dynamics. J. Virol. 82: 4974-4990.
22. Di Pasquale, G., and J. A. Chiorini. 2003. PKA/PrKX activity is a modulator of AAV/adenovirus interaction. EMBO J. 22: 1716-1724.
23. Di Pasquale, G., and S. N. Stacey. 1998. Adeno-associated virus Rep78 protein interacts with protein kinase A and its homolog PRKX and inhibits CREB-dependent transcriptional activation. J. Virol. 72: 7916-7925.
24. Fernandez-Capetillo, O., A. Lee, M. Nussenzweig, and A. Nussenzweig. 2004. H2AX: the histone guardian of the genome. DNA Repair 3: 959-967.
25. Fraefel, C., A. G. Bittermann, H. Bueler, I. Heid, T. Bachi, and M. Ackermann. 2004. Spatial and temporal organization of adeno-associated virus DNA replication in live cells. J. Virol. 78: 389-398.
26. 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.
27. Francois, A., M. Guilbaud, R. Awedikian, G. Chadeuf, P. Moullier, and A. Salvetti. 2005. The cellular TATA binding protein is required for rep-dependent replication of a minimal adeno-associated virus type 2 p5 element. J. Virol. 79: 11082-11094.
28. Geoffroy, M. C., A. L. Epstein, E. Toublanc, P. Moullier, and A. Salvetti. 2004. Herpes simplexvirus type 1 ICP0 proteinmediates activationofadenoassociated virus type 2 rep gene expression from a latent integrated form. J. Virol. 78: 10977-10986.
29. Glauser, D. L., M. Ackermann, O. Saydam, and C. Fraefel. 2006. Chimeric herpes simplex virus/adeno-associated virus amplicon vectors. Curr. Gene Ther. 6: 315-324.
30. 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.
31. 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.
32. Heilbronn, R., A. Burkle, S. Stephan, and H. zur Hausen. 1990. The adenoassociated virus rep gene suppresses herpes simplex virus-induced DNA amplification. J. Virol. 64: 3012-3018.
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.
34. Heilbronn, R., and H. zur Hausen. 1989. A subset of herpes simplex virus replication genes induces DNA amplification within the host cell genome. J. Virol. 63: 3683-3692.
35. Heister, T., I. Heid, M. Ackermann, and C. Fraefel. 2002. Herpes simplex virus type 1/adeno-associated virus hybrid vectors mediate site-specific integration at the adeno-associated virus preintegration site, AAVS1, on human chromosome 19. J. Virol. 76: 7163-7173.
36. Hirt, B. 1969. Replicating molecules of polyoma virus DNA. J. Mol. Biol. 40: 141-144.
37. Horer, M., S. Weger, K. Butz, F. Hoppe-Seyler, C. Geisen, and J. A. Kleinschmidt. 1995. Mutational analysis of adeno-associated virus Rep proteinmediated inhibition of heterologous and homologous promoters. J. Virol. 69: 5485-5496.
38. Im, D. S., and N. Muzyczka. 1990. The AAV origin binding protein Rep68 is an ATP-dependent site-specific endonuclease with DNA helicase activity. Cell 61: 447-457.
39. Im, D. S., and N. Muzyczka. 1989. Factors that bind to adeno-associated virus terminal repeats. J. Virol. 63: 3095-3104.
40. 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.
41. Knipe, D. M., D. Senechek, S. A. Rice, and J. L. Smith. 1987. Stages in the nuclear association of the herpes simplex virus transcriptional activator protein ICP4. J. Virol. 61: 276-284.
42. Kurz, E. U., and S. P. Lees-Miller. 2004. DNAdamage-induced activationof ATM and ATM-dependent signaling pathways. DNA Repair 3: 889-900.
43. Kyostio, S. R., and R. A. Owens. 1996. Identification of mutant adenoassociated virus Rep proteins which are dominant-negative for DNA helicase activity. Biochem. Biophys. Res. Commun. 220: 294-299.
44. 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. U. S. A. 102: 5844-5849.
45. Linden, R. M., E. Winocour, and K. I. Berns. 1996. The recombination signals for adeno-associated virus site-specific integration. Proc. Natl. Acad. Sci. U. S. A. 93: 7966-7972.
46. Lux, K., N. Goerlitz, S. Schlemminger, L. Perabo, D. Goldnau, J. Endell, K. Leike, D. M. Kofler, S. Finke, M. Hallek, and H. Buning. 2005. Green fluorescent protein-tagged adeno-associated virus particles allow the study of cytosolic and nuclear trafficking. J. Virol. 79: 11776-11787.
47. Manthey, K. C., S. Opiyo, J. G. Glanzer, D. Dimitrova, J. Elliott, and G. G. Oakley. 2007. NBS1 mediates ATR-dependent RPA hyperphosphorylation following replication-fork stall and collapse. J. Cell Sci. 120: 4221-4229.
48. Marsden, H. S., A. M. Cross, G. J. Francis, A. H. Patel, K. MacEachran, M. Murphy, G. McVey, D. Haydon, A. Abbotts, and N. D. Stow. 1996. The herpes simplex virus type 1 UL8 protein influences the intracellular localization of the UL52 but not the ICP8 or POL replication proteins in virusinfected cells. J. Gen. Virol. 77: 2241-2249.
49. Marsden, H. S., G. W. McLean, E. C. Barnard, G. J. Francis, K. Mac- Eachran, M. Murphy, G. McVey, A. Cross, A. P. Abbotts, and N. D. Stow. 1997. The catalytic subunit of the DNA polymerase of herpes simplex virus type 1 interacts specifically with the C terminus of the UL8 component of the viral helicase-primase complex. J. Virol. 71: 6390-6397.
50. McCarty, D. M., T. H. Ni, and N. Muzyczka. 1992. Analysis of mutations in adeno-associated virus Rep protein in vivo and in vitro. J. Virol. 66: 4050-4057.
51. McCarty, D. M., D. J. Pereira, I. Zolotukhin, X. Zhou, J. H. Ryan, and N. Muzyczka. 1994. Identification of linear DNA sequences that specifically bind the adeno-associated virus Rep protein. J. Virol. 68: 4988-4997.
52. McCarty, D. M., J. H. Ryan, S. Zolotukhin, X. Zhou, and N. Muzyczka. 1994. Interaction of the adeno-associated virus Rep protein with a sequence within the A palindrome of the viral terminal repeat. J. Virol. 68: 4998-5006.
53. McCarty, D. M., S. M. Young, Jr., and R. J. Samulski. 2004. Integration of adeno-associated virus (AAV) and recombinant AAV vectors. Annu. Rev. Genet. 38: 819-845.
54. McLean, C., A. Buckmaster, D. Hancock, A. Buchan, A. Fuller, and A. Minson. 1982. Monoclonal antibodies to three non-glycosylated antigens of herpes simplex virus type 2. J. Gen. Virol. 63: 297-305.
55. McLean, G. W., A. P. Abbotts, M. E. Parry, H. S. Marsden, and N. D. Stow. 1994. The herpes simplex virus type 1 origin-binding protein interacts specifically with the viral UL8 protein. J. Gen. Virol. 75: 2699-2706.
56. Muzyczka, N., and K. I. Berns. 2001. Parvoviridae: the viruses and their replication, p. 2327-2346. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, PA.
57. 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.
58. Nguyen, M. L., and J. A. Blaho. 2007. Apoptosis during herpes simplex virus infection. Adv. Virus Res. 69: 67-97.
59. Oehmig, A., C. Fraefel, and X. O. Breakefield. 2004. Update on herpesvirus amplicon vectors. Mol. Ther. 10: 630-643.
60. Owens, R. A., M. D. Weitzman, S. R. Kyostio, and B. J. Carter. 1993. Identification of a DNA-binding domain in the amino terminus of adenoassociated virus Rep proteins. J. Virol. 67: 997-1005.
61. Raj, K., P. Ogston, and P. Beard. 2001. Virus-mediated killing of cells that lack p53 activity. Nature 412: 914-917.
62. (Erratum, 416: 202, 2002.)
63. Ryan, J. H., S. Zolotukhin, and N. Muzyczka. 1996. Sequence requirements for binding of Rep68 to the adeno-associated virus terminal repeats. J. Virol. 70: 1542-1553.
64. Sacks, W. R., C. C. Greene, D. P. Aschman, and P. A. Schaffer. 1985. Herpes simplex virus type 1 ICP27 is an essential regulatory protein. J. Virol. 55: 796-805.
65. Saeki, Y., C. Fraefel, T. Ichikawa, X. O. Breakefield, and E. A. Chiocca. 2001. Improved helper virus-free packaging system for HSV amplicon vectors using an ICP27-deleted, oversized HSV-1 DNA in a bacterial artificial chromosome. Mol. Ther. 3: 591-601.
66. 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.
67. Schmidt, M., S. Afione, and R. M. Kotin. 2000. Adeno-associated virus type 2 Rep78 induces apoptosis through caspase activation independently of p53. J. Virol. 74: 9441-9450.
68. Schmidt, M., J. A. Chiorini, S. Afione, and R. Kotin. 2002. Adeno-associated virus type 2 Rep78 inhibition of PKA and PRKX: fine mapping and analysis of mechanism. J. Virol. 76: 1033-1042.
69. Schwartz, R. A., C. T. Carson, C. Schuberth, and M. D. Weitzman. 2009. Adeno-associated virus replication induces a DNA damage response coordinated by DNA-dependent protein kinase. J. Virol. 83: 6269-6278.
70. Shao, R. G., C. X. Cao, H. Zhang, K. W. Kohn, M. S. Wold, and Y. Pommier. 1999. Replication-mediated DNA damage by camptothecin induces phosphorylation of RPA by DNA-dependent protein kinase and dissociates RPA: DNA-PK complexes. EMBO J. 18: 1397-1406.
71. 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.
72. Slanina, H., S. Weger, N. D. Stow, A. Kuhrs, and R. Heilbronn. 2006. Role of the herpes simplex virus helicase-primase complex during adeno-associated virus DNA replication. J. Virol. 80: 5241-5250.
73. Smith, I. L., M. A. Hardwicke, and R. M. Sandri-Goldin. 1992. Evidence that the herpes simplex virus immediate early protein ICP27 acts post-transcriptionally during infection to regulate gene expression. Virology 186: 74-86.
74. Smith, R. H., and R. M. Kotin. 2000. An adeno-associated virus (AAV) initiator protein, Rep78, catalyzes the cleavage and ligation of singlestranded AAV ori DNA. J. Virol. 74: 3122-3129.
75. Smith, R. H., and R. M. Kotin. 1998. The Rep52 gene product of adenoassociated virus is a DNA helicase with 3'-to-5' polarity. J. Virol. 72: 4874-4881.
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.
77. Taylor, T. J., M. A. Brockman, E. E. McNamee, and D. M. Knipe. 2002. Herpes simplex virus. Front. Biosci. 7: d752-d764.
78. Timpe, J. M., K. C. Verrill, and J. P. Trempe. 2006. Effects of adenoassociated virus on adenovirus replication and gene expression during coinfection. J. Virol. 80: 7807-7815.
79. Trempe, J. P., E. Mendelson, and B. J. Carter. 1987. Characterization of adeno-associated virus rep proteins in human cells by antibodies raised against rep expressed in Escherichia coli. Virology 161: 18-28.
80. Tsukamoto, T., N. Hashiguchi, S. M. Janicki, T. Tumbar, A. S. Belmont, and D. L. Spector. 2000. Visualization of gene activity in living cells. Nat. Cell Biol. 2: 871-878.
81. Ward, P., M. Falkenberg, P. Elias, M. Weitzman, and R. M. Linden. 2001. Rep-dependent initiation of adeno-associated virus type 2 DNA replication by a herpes simplex virus type 1 replication complex in a reconstituted system. J. Virol. 75: 10250-10258.
82. Ward, P. L., and B. Roizman. 1994. Herpes simplex genes: the blueprint of a successful human pathogen. Trends Genet. 10: 267-274.
83. (Erratum, 10: 380.)
84. Weindler, F. W., and R. Heilbronn. 1991. A subset of herpes simplex virus replication genes provides helper functions for productive adeno-associated virus replication. J. Virol. 65: 2476-2483.
85. 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.
86. Wilkinson, D. E., and S. K. Weller. 2006. Herpes simplexvirus type I disrupts the ATR-dependent DNA-damage response during lytic infection. J. Cell Sci. 119: 2695-2703.
87. Wilkinson, D. E., and S. K. Weller. 2005. Inhibition of the herpes simplex virus type 1 DNA polymerase induces hyperphosphorylation of replication protein A and its accumulation at S-phase-specific sites of DNA damage during infection. J. Virol. 79: 7162-7171.
88. 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.
89. Wonderling, R. S., and R. A. Owens. 1997. Binding sites for adeno-associated virus Rep proteins within the human genome. J. Virol. 71: 2528-2534.
90. Wu, J., M. D. Davis, and R. A. Owens. 1999. Factors affecting the terminal resolution site endonuclease, helicase, and ATPase activities of adeno-associated virus type 2 Rep proteins. J. Virol. 73: 8235-8244.
91. Yang, Q., F. Chen, J. Ross, and J. P. Trempe. 1995. Inhibition of cellular and SV40 DNA replication by the adeno-associated virus Rep proteins. Virology 207: 246-250.
92. Young, S. M., Jr., D. M. McCarty, N. Degtyareva, and R. J. Samulski. 2000. Roles of adeno-associated virus Rep protein and human chromosome 19 in site-specific recombination. J. Virol. 74: 3953-3966.
93. Zhou, X., I. Zolotukhin, D. S. Im, and N. Muzyczka. 1999. Biochemical characterization of adeno-associated virus rep68 DNA helicase and ATPase activities. J. Virol. 73: 1580-1590.
94. Zou, Y., Y. Liu, X. Wu, and S. M. Shell. 2006. Functions ofhumanreplication protein A (RPA) : from DNA replication to DNA damage and stress responses. J. Cell. Physiol. 208: 267-273.