Efficient herpes simplex virus 1 replication requires cellular ATR pathway proteins

Journal of Virology

Volumn 87, Issue 1, 2013, Pages 531-542

  Mohni, Kareem N ^a   Dee, Alexander R ^a   Smith, Samantha ^a   Schumacher, April J ^a   Weller, Sandra K ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATR INTERACTING PROTEIN; ATR PROTEIN; CLASPIN; PROTEIN CINP; PROTEIN RAD9; PROTEIN TOPBP1; REPLICATION PROTEIN A 70; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; GENE SILENCING; GENETIC TRANSFECTION; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HOMOLOGOUS RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

CELL CYCLE PROTEINS; CELL LINE; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

DNA VIRUSES; HUMAN HERPESVIRUS 1; SIMPLEXVIRUS;

EID: 84871956836     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02504-12     Document Type: Article

References (83)

1. Everett RD, Parada C, Gripon P, Sirma H, Orr A. 2008. Replication of ICP0-null mutant herpes simplex virus type 1 is restricted by both PML and Sp100. J. Virol. 82:2661-2672.
2. Lukashchuk V, Everett RD. 2010. Regulation of ICP0-null mutant herpes simplex virus type 1 infection by ND10 components ATRX and hDaxx. J. Virol. 84:4026-4040.
3. Lilley CE, Chaurushiya MS, Boutell C, Everett RD, Weitzman MD. 2011. The intrinsic antiviral defense to incoming HSV-1 genomes includes specificDNArepair proteins and is counteracted by the viral protein ICP0. PLoS Pathog. 7:e1002084. doi:10.1371/journal.ppat.1002084.
4. Mohni KN, Mastrocola AS, Bai P, Weller SK, Heinen CD. 2011. DNA mismatch repair proteins are required for efficient herpes simplex virus 1 replication. J. Virol. 85:12241-12253.
5. Lilley CE, Carson CT, Muotri AR, Gage FH, Weitzman MD. 2005. DNA repair proteins affect the lifecycle of herpes simplex virus 1. Proc. Natl. Acad. Sci. U. S. A. 102:5844-5849.
6. Mohni KN, Livingston CM, Cortez D, Weller SK. 2010. ATR and ATRIP are recruited to herpes simplex virus type 1 replication compartments even though ATR signaling is disabled. J. Virol. 84:12152-12164.
7. Shirata N, Kudoh A, Daikoku T, Tatsumi Y, Fujita M, Kiyono T, Sugaya Y, Isomura H, Ishizaki K, Tsurumi T. 2005. Activation of ataxia telangiectasia-mutated DNA damage checkpoint signal transduction elicited by herpes simplex virus infection. J. Biol. Chem. 280:30336-30341.
8. Taylor TJ, Knipe DM. 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.
9. Wilkinson DE, Weller SK. 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.
10. Abraham RT. 2004. PI 3-kinase related kinases: 'big' players in stressinduced signaling pathways. DNA Repair (Amst.) 3:883-887.
11. Ciccia A, Elledge SJ. 2010. The DNA damage response: making it safe to play with knives. Mol. Cell 40:179-204.
12. Cimprich KA, Cortez D. 2008. ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 9:616-627.
13. Jackson SA, DeLuca NA. 2003. Relationship of herpes simplex virus genome configuration to productive and persistent infections. Proc. Natl. Acad. Sci. U. S. A. 100:7871-7876.
14. Lees-Miller SP, Long MC, Kilvert MA, Lam V, Rice SA, Spencer CA. 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.
15. Parkinson J, Lees-Miller SP, Everett RD. 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.
16. Brown SM, Ritchie DA, Subak-Sharpe JH. 1973. Genetic studies with herpes simplex virus type 1. The isolation of temperature-sensitive mutants, their arrangement into complementation groups and recombination analysis leading to a linkage map. J. Gen. Virol. 18:329-346.
17. Schaffer PA, Tevethia MJ, Benyesh-Melnick M. 1974. Recombination between temperature-sensitive mutants of herpes simplex virus type 1. Virology 58:219-228.
18. Wold MS. 1997. Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem. 66:61-92.
19. Wilkinson DE, Weller SK. 2006. Herpes simplex virus type I disrupts the ATR-dependent DNA-damage response during lytic infection. J. Cell Sci. 119:2695-2703.
20. Samaniego LA, Wu N, DeLuca NA. 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.
21. DeLuca NA, McCarthy AM, Schaffer PA. 1985. Isolation and characterization of deletion mutants of herpes simplex virus type 1 in the gene encoding immediate-early regulatory protein ICP4. J. Virol. 56:558-570.
22. Long MC, Leong V, Schaffer PA, Spencer CA, Rice SA. 1999. ICP22 and the UL13 protein kinase are both required for herpes simplex virusinduced modification of the large subunit of RNA polymerase II. J. Virol. 73:5593-5604.
23. Rice SA, Knipe DM. 1990. Genetic evidence for two distinct transactivation functions of the herpes simplex virus alpha protein ICP27. J. Virol. 64:1704-1715.
24. Gao M, Knipe DM. 1989. Genetic evidence for multiple nuclear functions of the herpes simplex virus ICP8 DNA-binding protein. J. Virol. 63:5258-5267.
25. Zhu L, Weller SK. 1988. UL5, a protein required for HSV DNA synthesis: genetic analysis, overexpression in Escherichia coli, and generation of polyclonal antibodies. Virology 166:366-378.
26. Blumel J, Matz B. 1995. Thermosensitive UL9 gene function is required for early stages of herpes simplex virus type 1DNAsynthesis. J. Gen. Virol. 76:3119-3124.
27. Matz B, Subak-Sharpe JH, Preston VG. 1983. Physical mapping of temperature-sensitive mutations of herpes simplex virus type 1 using cloned restriction endonuclease fragments. J. Gen. Virol. 64:2261-2270.
28. Ball HL, Ehrhardt MR, Mordes DA, Glick GG, Chazin WJ, Cortez D. 2007. Function of a conserved checkpoint recruitment domain in ATRIP proteins. Mol. Cell. Biol. 27:3367-3377.
29. Lovejoy CA, Xu X, Bansbach CE, Glick GG, Zhao R, Ye F, Sirbu BM, Titus LC, Shyr Y, Cortez D. 2009. Functional genomic screens identify CINP as a genome maintenance protein. Proc. Natl. Acad. Sci. U. S. A. 106:19304-19309.
30. Warmerdam DO, Kanaar R, Smits VA. 2010. Differential dynamics of ATR-mediated checkpoint regulators. J. Nucleic Acids 2010:319142. doi: 10.4061/2010/319142.
31. Unsal-Kacmaz K, Chastain PD, Qu PP, Minoo P, Cordeiro-Stone M, Sancar A, Kaufmann WK. 2007. The human Tim/Tipin complex coordinates an intra-S checkpoint response to UV that slows replication fork displacement. Mol. Cell. Biol. 27:3131-3142.
32. Livingston CM, DeLuca NA, Wilkinson DE, Weller SK. 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.
33. Shelton LS, Albright AG, Ruyechan WT, Jenkins FJ. 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.
34. Cortez D, Guntuku S, Qin J, Elledge SJ. 2001. ATR and ATRIP: partners in checkpoint signaling. Science 294:1713-1716.
35. Myers JS, Zhao R, Xu X, Ham AJ, Cortez D. 2007. Cyclin-dependent kinase 2 dependent phosphorylation of ATRIP regulates the G2-M checkpoint response to DNA damage. Cancer Res. 67:6685-6690.
36. Jiang N, Benard CY, Kebir H, Shoubridge EA, Hekimi S. 2003. Human CLK2 links cell cycle progression, apoptosis, and telomere length regulation. J. Biol. Chem. 278:21678-21684.
37. Haring SJ, Mason AC, Binz SK, Wold MS. 2008. Cellular functions of human RPA1. Multiple roles of domains in replication, repair, and checkpoints. J. Biol. Chem. 283:19095-19111.
38. Xu X, Vaithiyalingam S, Glick GG, Mordes DA, Chazin WJ, Cortez D. 2008. The basic cleft of RPA70N binds multiple checkpoint proteins, including RAD9, to regulate ATR signaling. Mol. Cell. Biol. 28:7345-7353.
39. Vassin VM, Wold MS, Borowiec JA. 2004. Replication protein A (RPA) phosphorylation prevents RPA association with replication centers. Mol. Cell. Biol. 24:1930-1943.
40. Hirai I, Wang HG. 2002. A role of the C-terminal region of human Rad9 (hRad9) in nuclear transport of the hRad9 checkpoint complex. J. Biol. Chem. 277:25722-25727.
41. Medhurst AL, Warmerdam DO, Akerman I, Verwayen EH, Kanaar R, Smits VA, Lakin ND. 2008. ATR and Rad17 collaborate in modulating Rad9 localisation at sites of DNA damage. J. Cell Sci. 121:3933-3940.
42. Sorensen CS, Syljuasen RG, Lukas J, Bartek J. 2004. ATR, Claspin and the Rad9-Rad1-Hus1 complex regulate Chk1 and Cdc25A in the absence of DNA damage. Cell Cycle 3:941-945.
43. Zou L, Cortez D, Elledge SJ. 2002. Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev. 16:198-208.
44. Rendtlew Danielsen JM, Larsen DH, Schou KB, Freire R, Falck J, Bartek J, Lukas J. 2009. HCLK2 is required for activity of the DNA damage response kinase ATR. J. Biol. Chem. 284:4140-4147.
45. Yang XH, Shiotani B, Classon M, Zou L. 2008. Chk1 and Claspin potentiate PCNA ubiquitination. Genes Dev. 22:1147-1152.
46. Collis SJ, Barber LJ, Clark AJ, Martin JS, Ward JD, Boulton SJ. 2007. HCLK2 is essential for the mammalian S-phase checkpoint and impacts on Chk1 stability. Nat. Cell Biol. 9:391-401.
47. Ball HL, Myers JS, Cortez D. 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.
48. Cimprich KA, Shin TB, Keith CT, Schreiber SL. 1996. cDNA cloning and gene mapping of a candidate human cell cycle checkpoint protein. Proc. Natl. Acad. Sci. U. S. A. 93:2850-2855.
49. Cliby WA, Roberts CJ, Cimprich KA, Stringer CM, Lamb JR, Schreiber SL, Friend SH. 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.
50. Takai H, Wang RC, Takai KK, Yang H, de Lange T. 2007. Tel2 regulates the stability of PI3K-related protein kinases. Cell 131:1248-1259.
51. Nam EA, Zhao R, Glick GG, Bansbach CE, Friedman DB, Cortez D. 2011. Thr-1989 phosphorylation is a marker of active ataxia telangiectasia-mutated and Rad3-related (ATR) kinase. J. Biol. Chem. 286:28707-28714.
52. Vogel R, Seyffert M, Strasser R, de Oliveira AP, Dresch C, Glauser DL, Jolinon N, Salvetti A, Weitzman MD, Ackermann M, Fraefel C. 2012. Adeno-associated virus type 2 modulates the host DNA damage response induced by herpes simplex virus 1 during coinfection. J. Virol. 86:143-155.
53. Anantha RW, Vassin VM, Borowiec JA. 2007. Sequential and synergistic modification of human RPA stimulates chromosomalDNArepair. J. Biol. Chem. 282:35910-35923.
54. Vassin VM, Anantha RW, Sokolova E, Kanner S, Borowiec JA. 2009. Human RPA phosphorylation by ATR stimulates DNA synthesis and prevents ssDNA accumulation during DNA-replication stress. J. Cell Sci. 122: 4070-4080.
55. Warmerdam DO. 2010. Biological and functional analysis of the ATR checkpoint pathway. Ph.D. thesis. Erasmus University Rotterdam, Rotterdam, The Netherlands.
56. Livingston CM, Ifrim MF, Cowan AE, Weller SK. 2009. Virus-induced chaperone-enriched (VICE) domains function as nuclear protein quality control centers during HSV-1 infection. PLoS Pathog. 5:e1000619. doi: 10.1371/journal.ppat.1000619.
57. Delacroix S Wagner JM, Kobayashi M, Yamamoto K, Karnitz LM. 2007. The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes Dev. 21:1472-1477.
58. Chen MJ, Lin YT, Lieberman HB, Chen G, Lee EY. 2001. ATMdependent phosphorylation of human Rad9 is required for ionizing radiation-induced checkpoint activation. J. Biol. Chem. 276:16580-16586.
59. Eichinger CS, Jentsch S. 2011. 9-1-1: PCNA's specialized cousin. Trends Biochem. Sci. 36:563-568.
60. He W, Ma X, Yang X, Zhao Y, Qiu J, Hang H. 2011. A role for the arginine methylation of Rad9 in checkpoint control and cellular sensitivity to DNA damage. Nucleic Acids Res. 39:4719-4727.
61. Araki H, Leem SH, Phongdara A, Sugino A. 1995. Dpb11, which interacts with DNA polymerase II(epsilon) in Saccharomyces cerevisiae, has a dual role in S-phase progression and at a cell cycle checkpoint. Proc. Natl. Acad. Sci. U. S. A. 92:11791-11795.
62. Fanning E, Klimovich V, Nager AR. 2006. A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic Acids Res. 34:4126-4137.
63. Masumoto H, Sugino A, Araki H. 2000. Dpb11 controls the association between DNA polymerases alpha and epsilon and the autonomously replicating sequence region of budding yeast. Mol. Cell. Biol. 20:2809-2817.
64. He W, Zhao Y, Zhang C, An L, Hu Z, Liu Y, Han L, Bi L, Xie Z, Xue P, Yang F, Hang H. 2008. Rad9 plays an important role in DNA mismatch repair through physical interaction with MLH1. Nucleic Acids Res. 36: 6406-6417.
65. Kumagai A, Lee J, Yoo HY, Dunphy WG. 2006. TopBP1 activates the ATR-ATRIP complex. Cell 124:943-955.
66. Mordes DA, Glick GG, Zhao R, Cortez D. 2008. TopBP1 activates ATR through ATRIP and a PIKK regulatory domain. Genes Dev. 22:1478-1489.
67. Blackford AN, Patel RN, Forrester NA, Theil K, Groitl P, Stewart GS, Taylor AM, Morgan IM, Dobner T, Grand RJ, Turnell AS. 2010. Adenovirus 12 E4orf6 inhibits ATR activation by promoting TOPBP1 degradation. Proc. Natl. Acad. Sci. U. S. A. 107:12251-12256.
68. Carson CT, Orazio NI, Lee DV, Suh J, Bekker-Jensen S, Araujo FD, Lakdawala SS, Lilley CE, Bartek J, Lukas J, Weitzman MD. 2009. Mislocalization of the MRN complex prevents ATR signaling during adenovirus infection. EMBO J. 28:652-662.
69. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, Lukas J, Jackson SP. 2006. ATM-and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8:37-45.
70. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, Baer R, Lukas J, Jackson SP. 2007. Human CtIP promotes DNA end resection. Nature 450:509-514.
71. Warmerdam DO, Freire R, Kanaar R, Smits VA. 2009. Cell cycledependent processing ofDNAlesions controls localization of Rad9 to sites of genotoxic stress. Cell Cycle 8:1765-1774.
72. Balasubramanian N, Bai P, Buchek G, Korza G, Weller SK. 2010. Physical interaction between the herpes simplex virus type 1 exonuclease, UL12, and the DNA double-strand break-sensing MRN complex. J. Virol. 84:12504-12514.
73. Schumacher AJ, Mohni KN, Kan Y, Hendrickson EA, Stark JM, Weller SK. 2012. The HSV-1 exonuclease, UL12, stimulates recombination by a single strand annealing mechanism. PLoS Pathog. 8:e1002862. doi: 10.1371/journal.ppat.1002862.
74. Barlow JH, Lisby M, Rothstein R. 2008. Differential regulation of the cellular response toDNAdouble-strand breaks in G1. Mol. Cell 30:73-85.
75. Kanoh Y, Tamai K, Shirahige K. 2006. Different requirements for the association of ATR-ATRIP and 9-1-1 to the stalled replication forks. Gene 377:88-95.
76. Lee SE, Moore JK, Holmes A, Umezu K, Kolodner RD, Haber JE. 1998. Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94:399-409.
77. Umezu K, Sugawara N, Chen C, Haber JE, Kolodner RD. 1998. Genetic analysis of yeast RPA1 reveals its multiple functions in DNA metabolism. Genetics 148:989-1005.
78. Sirbu BM, Lachmayer SJ, Wulfing V, Marten LM, Clarkson KE, Lee LW, Gheorghiu L, Zou L, Powell SN, Dahm-Daphi J, Willers H. 2011. ATR-p53 restricts homologous recombination in response to replicative stress but does not limit DNA interstrand crosslink repair in lung cancer cells. PLoS One 6:e23053. doi:10.1371/journal.pone.0023053.
79. Peasland A, Wang LZ, Rowling E, Kyle S, Chen T, Hopkins A, Cliby WA, Sarkaria J, Beale G, Edmondson RJ, Curtin NJ. 2011. Identification and evaluation of a potent novel ATR inhibitor, NU6027, in breast and ovarian cancer cell lines. Br. J. Cancer 105:372-381.
80. Prevo R, Fokas E, Reaper PM, Charlton PA, Pollard JR, McKenna WG, Muschel RJ, Brunner TB. 2012. The novel ATR inhibitor VE-821 increases sensitivity of pancreatic cancer cells to radiation and chemotherapy. Cancer Biol. Ther. 13:1072-1081.
81. Wang H, Wang H, Powell SN, Iliakis G, Wang Y. 2004. ATR affecting cell radiosensitivity is dependent on homologous recombination repair but independent of nonhomologous end joining. Cancer Res. 64:7139-7143.
82. Roizman B. 1979. The structure and isomerization of herpes simplex virus genomes. Cell 16:481-494.
83. Wilkinson DE, Weller SK. 2003. The role of DNA recombination in herpes simplex virus DNA replication. IUBMB Life 55:451-458.