ATR and ATRIP are recruited to herpes simplex virus type 1 replication compartments even though ATR signaling is disabled

Journal of Virology

Volumn 84, Issue 23, 2010, Pages 12152-12164

  Mohni, Kareem N ^a   Livingston, Christine M ^a   Cortez, David ^b   Weller, Sandra K ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; PROTEIN ATRIP; PROTEIN SERINE THREONINE KINASE; REPLICATION FACTOR A; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE; ENZYME INACTIVATION; GENE EXPRESSION; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; VERO CELL; VIRUS REPLICATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOTTING, WESTERN; CELL CYCLE PROTEINS; CERCOPITHECUS AETHIOPS; DNA DAMAGE; DNA PRIMERS; DNA-BINDING PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HERPESVIRUS 1, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; IMMUNOPRECIPITATION; PHOSPHORYLATION; PLASMIDS; PROTEIN-SERINE-THREONINE KINASES; REPLICATION PROTEIN A; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; VERO CELLS; VIRUS REPLICATION;

HUMAN HERPESVIRUS 1;

EID: 78049517168     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01643-10     Document Type: Article

References (58)

1. Abraham, R. T. 2004. PI 3-kinase related kinases: 'big' players in stress-induced signaling pathways. DNA Repair (Amst.) 3:883-887.
2. Ball, H. L., and D. Cortez. 2005. ATRIP oligomerization is required for ATR-dependent checkpoint signaling. J. Biol. Chem. 280:31390-31396.
3. Ball, H. L., M. R. Ehrhardt, D. A. Mordes, G. G. Glick, W. J. Chazin, and D. Cortez. 2007. Function of a conserved checkpoint recruitment domain in ATRIP proteins. Mol. Cell. Biol. 27:3367-3377.
4. Ball, H. L., J. S. Myers, and D. Cortez. 2005. ATRIP binding to replication protein A-single-stranded DNA promotes ATR-ATRIP localization but is dispensable for Chk1 phosphorylation. Mol. Biol. Cell 16:2372-2381.
5. Barr, S. M., C. G. Leung, E. E. Chang, and K. A. Cimprich. 2003. ATR kinase activity regulates the intranuclear translocation of ATR and RPA following ionizing radiation. Curr. Biol. 13:1047-1051.
6. Blackford, A. N., R. N. Patel, N. A. Forrester, K. Theil, P. Groitl, G. S. Stewart, A. M. Taylor, I. M. Morgan, T. Dobner, R. J. Grand, and A. S. Turnell. 2010. Adenovirus 12 E4orf6 inhibits ATR activation by promoting TOPBP1 degradation. Proc. Natl. Acad. Sci. U. S. A. 107:12251-12256.
7. Burkham, J., D. M. Coen, and S. K. Weller. 1998. ND10 protein PML is recruited to herpes simplex virus type 1 prereplicative sites and replication compartments in the presence of viral DNA polymerase. J. Virol. 72:10100-10107.
8. Carson, C. T., N. I. Orazio, D. V. Lee, J. Suh, S. Bekker-Jensen, F. D. Araujo, S. S. Lakdawala, C. E. Lilley, J. Bartek, J. Lukas, and M. D. Weitzman. 2009. Mislocalization of the MRN complex prevents ATR signaling during adenovirus infection. EMBO J. 28:652-662.
9. Cimprich, K. A., and D. Cortez. 2008. ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 9:616-627.
10. Cimprich, K. A., T. B. Shin, C. T. Keith, and S. L. Schreiber. 1996. cDNA cloning and gene mapping of a candidate human cell cycle checkpoint protein. Proc. Natl. Acad. Sci. U. S. A. 93:2850-2855.
11. Cliby, W. A., C. J. Roberts, K. A. Cimprich, C. M. Stringer, J. R. Lamb, S. L. Schreiber, and S. H. Friend. 1998. Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO J. 17:159-169.
12. Cortez, D., S. Guntuku, J. Qin, and S. J. Elledge. 2001. ATR and ATRIP: partners in checkpoint signaling. Science 294:1713-1716.
13. Durocher, F., Y. Labrie, P. Soucy, O. Sinilnikova, D. Labuda, P. Bessette, J. Chiquette, R. Laframboise, J. Lepine, B. Lesperance, G. Ouellette, R. Pichette, M. Plante, S. V. Tavtigian, and J. Simard. 2006. Mutation analysis and characterization of ATR sequence variants in breast cancer cases from high-risk French Canadian breast/ovarian cancer families. BMC Cancer 6:230.
14. Everett, R. D. 2000. ICP0, a regulator of herpes simplex virus during lytic and latent infection. Bioessays 22:761-770. (Pubitemid 30613308)
15. Everett, R. D. 2006. Interactions between DNA viruses, ND10 and the DNA damage response. Cell. Microbiol. 8:365-374.
16. Everett, R. D., and M. K. Chelbi-Alix. 2007. PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89:819-830.
17. Everett, R. D., M. Meredith, and A. Orr. 1999. The ability of herpes simplex virus type 1 immediate-early protein Vmw110 to bind to a ubiquitin-specific protease contributes to its roles in the activation of gene expression and stimulation of virus replication. J. Virol. 73:417-426.
18. Everett, R. D., C. Parada, P. Gripon, H. Sirma, and A. Orr. 2008. Replication of ICP0-null mutant herpes simplex virus type 1 is restricted by both PML and Sp100. J. Virol. 82:2661-2672.
19. Fernandez-Capetillo, O., S. K. Mahadevaiah, A. Celeste, P. J. Romanienko, R. D. Camerini-Otero, W. M. Bonner, K. Manova, P. Burgoyne, and A. Nussenzweig. 2003. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell 4:497-508. (Pubitemid 36437557)
20. Hagglund, R., and B. Roizman. 2004. Role of ICP0 in the strategy of conquest of the host cell by herpes simplex virus 1. J. Virol. 78:2169-2178. (Pubitemid 38228910)
21. Kleymann, G., R. Fischer, U. A. Betz, M. Hendrix, W. Bender, U. Schneider, G. Handke, P. Eckenberg, G. Hewlett, V. Pevzner, J. Baumeister, O. Weber, K. Henninger, J. Keldenich, A. Jensen, J. Kolb, U. Bach, A. Popp, J. Maben, I. Frappa, D. Haebich, O. Lockhoff, and H. Rubsamen-Waigmann. 2002. New helicase-primase inhibitors as drug candidates for the treatment of herpes simplex disease. Nat. Med. 8:392-398.
22. Knipe, D. M., and A. Cliffe. 2008. Chromatin control of herpes simplex virus lytic and latent infection. Nat. Rev. Microbiol. 6:211-221.
23. Kristie, T. M., Y. Liang, and J. L. Vogel. Control of alpha-herpesvirus IE gene expression by HCF-1 coupled chromatin modification activities. Biochim. Biophys. Acta 1799:257-265.
24. Lamberti, C., and S. K. Weller. 1996. The herpes simplex virus type 1 UL6 protein is essential for cleavage and packaging but not for genomic inversion. Virology 226:403-407.
25. 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.
26. 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.
27. Lilley, C. E., M. S. Chaurushiya, C. Boutell, S. Landry, J. Suh, S. Panier, R. D. Everett, G. S. Stewart, D. Durocher, and M. D. Weitzman. 2010. A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses. EMBO J. 29:943-955.
28. 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.
29. Liptak, L. M., S. L. Uprichard, and D. M. Knipe. 1996. Functional order of assembly of herpes simplex virus DNA replication proteins into prereplicative site structures. J. Virol. 70:1759-1767.
30. Livingston, C. M., N. A. DeLuca, D. E. Wilkinson, and S. K. Weller. 2008. Oligomerization of ICP4 and rearrangement of heat shock proteins may be important for herpes simplex virus type 1 prereplicative site formation. J. Virol. 82:6324-6336.
31. Livingston, C. M., M. F. Ifrim, A. E. Cowan, and S. K. Weller. 2009. Virus-induced chaperone-enriched (VICE) domains function as nuclear protein quality control centers during HSV-1 infection. PLoS Pathog. 5:e1000619.
32. Lukonis, C. J., and S. K. Weller. 1997. Formation of herpes simplex virus type 1 replication compartments by transfection: requirements and localization to nuclear domain 10. J. Virol. 71:2390-2399.
33. Luo, M. H., K. Rosenke, K. Czornak, and E. A. Fortunato. 2007. Human cytomegalovirus disrupts both ataxia telangiectasia mutated protein (ATM)- and ATM-Rad3-related kinase-mediated DNA damage responses during lytic infection. J. Virol. 81:1934-1950.
34. Mannino, J. L., W. Kim, M. Wernick, S. V. Nguyen, R. Braquet, A. W. Adamson, Z. Den, M. A. Batzer, C. C. Collins, and K. D. Brown. 2001. Evidence for alternate splicing within the mRNA transcript encoding the DNA damage response kinase ATR. Gene 272:35-43.
35. Moffat, J., D. A. Grueneberg, X. Yang, S. Y. Kim, A. M. Kloepfer, G. Hinkle, B. Piqani, T. M. Eisenhaure, B. Luo, J. K. Grenier, A. E. Carpenter, S. Y. Foo, S. A. Stewart, B. R. Stockwell, N. Hacohen, W. C. Hahn, E. S. Lander, D. M. Sabatini, and D. E. Root. 2006. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124:1283-1298.
36. Paladino, P., and K. L. Mossman. 2009. Mechanisms employed by herpes simplex virus 1 to inhibit the interferon response. J. Interferon Cytokine Res. 29:599-607.
37. Parkinson, J., S. P. Lees-Miller, and R. D. Everett. 1999. Herpes simplex virus type 1 immediate-early protein vmw110 induces the proteasome-dependent degradation of the catalytic subunit of DNA-dependent protein kinase. J. Virol. 73:650-657.
38. Paulsen, R. D., and K. A. Cimprich. 2007. The ATR pathway: fine-tuning the fork. DNA Repair (Amst.) 6:953-966.
39. Phelan, A., J. Dunlop, A. H. Patel, N. D. Stow, and J. B. Clements. 1997. Nuclear sites of herpes simplex virus type 1 DNA replication and transcription colocalize at early times postinfection and are largely distinct from RNA processing factors. J. Virol. 71:1124-1132.
40. Quadt, I., A. K. Gunther, D. Voss, M. Schelhaas, and D. Knebel-Morsdorf. 2006. TATA-binding protein and TBP-associated factors during herpes simplex virus type 1 infection: localization at viral DNA replication sites. Virus Res. 115:207-213. (Pubitemid 43088649)
41. Quinlan, M. P., L. B. Chen, and D. M. Knipe. 1984. The intranuclear location of a herpes simplex virus DNA-binding protein is determined by the status of viral DNA replication. Cell 36:857-868.
42. Roizman, B. 1979. The structure and isomerization of herpes simplex virus genomes. Cell 16:481-494. (Pubitemid 9140453)
43. Samaniego, L. A., L. Neiderhiser, and N. A. DeLuca. 1998. Persistence and expression of the herpes simplex virus genome in the absence of immediate-early proteins. J. Virol. 72:3307-3320.
44. Samaniego, L. A., A. L. Webb, and N. A. DeLuca. 1995. Functional interactions between herpes simplex virus immediate-early proteins during infection: gene expression as a consequence of ICP27 and different domains of ICP4. J. Virol. 69:5705-5715.
45. Samaniego, L. A., N. Wu, and N. A. DeLuca. 1997. The herpes simplex virus immediate-early protein ICP0 affects transcription from the viral genome and infected-cell survival in the absence of ICP4 and ICP27. J. Virol. 71:4614-4625.
46. Shelton, L. S., A. G. Albright, W. T. Ruyechan, and F. J. Jenkins. 1994. Retention of the herpes simplex virus type 1 (HSV-1) UL37 protein on single-stranded DNA columns requires the HSV-1 ICP8 protein. J. Virol. 68:521-525.
47. 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.
48. Strang, B. L., and N. D. Stow. 2007. Blocks to herpes simplex virus type 1 replication in a cell line, tsBN2, encoding a temperature-sensitive RCC1 protein. J. Gen. Virol. 88:376-383.
49. 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.
50. Taylor, T. J., E. E. McNamee, C. Day, and D. M. Knipe. 2003. Herpes simplex virus replication compartments can form by coalescence of smaller compartments. Virology 309:232-247.
51. Turner, J. M. 2007. Meiotic sex chromosome inactivation. Development 134:1823-1831.
52. Turner, J. M., S. K. Mahadevaiah, O. Fernandez-Capetillo, A. Nussenzweig, X. Xu, C. X. Deng, and P. S. Burgoyne. 2005. Silencing of unsynapsed meiotic chromosomes in the mouse. Nat. Genet. 37:41-47.
53. Weller, S. K. 2009. Herpesvirus genome replication, p. 249-265. In C. E. Cameron, M. Gotte, and K. D. Raney (ed.), Viral genome replication. Springer, New York, NY.
54. Wilkinson, D. E., and S. K. Weller. 2006. Herpes simplex virus type I disrupts the ATR-dependent DNA-damage response during lytic infection. J. Cell Sci. 119:2695-2703.
55. 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.
56. 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.
57. Xu, X., S. Vaithiyalingam, G. G. Glick, D. A. Mordes, W. J. Chazin, and D. Cortez. 2008. The basic cleft of RPA70N binds multiple checkpoint proteins, including RAD9, to regulate ATR signaling. Mol. Cell. Biol. 28:7345-7353.
58. Zou, L., and S. J. Elledge. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542-1548.