DNA mismatch repair proteins are required for efficient herpes simplex virus 1 replication

Journal of Virology

Volumn 85, Issue 23, 2011, Pages 12241-12253

  Mohni, Kareem N ^a   Mastrocola, Adam S ^a   Bai, Ping ^a   Weller, Sandra K ^a   Heinen, Christopher D ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; INFECTED CELL PROTEIN 8; MISMATCH REPAIR PROTEIN; PROTEIN; PROTEIN MLH1; PROTEIN MSH2; PROTEIN MSH3; PROTEIN MSH6; PROTEIN UL12; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS INCLUSION BODY; CONTROLLED STUDY; DNA VIRUS; GENE EXPRESSION; GENE SILENCING; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LIFE CYCLE; MISMATCH REPAIR; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS REPLICATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOTTING, WESTERN; CELL NUCLEUS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; DNA MISMATCH REPAIR; FLUORESCENT ANTIBODY TECHNIQUE; GENES, IMMEDIATE-EARLY; HELA CELLS; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNOPRECIPITATION; MUTS HOMOLOG 2 PROTEIN; NUCLEAR PROTEINS; VERO CELLS; VIRUS REPLICATION;

DNA VIRUSES; HUMAN HERPESVIRUS 1;

EID: 81255164924     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05487-11     Document Type: Article

References (73)

1. Acharya, S., P. L. Foster, P. Brooks, and R. Fishel. 2003. The coordinated functions of the E. coli MutS and MutL proteins in mismatch repair. Mol. Cell 12:233-246.
2. Balasubramanian, N., P. Bai, G. Buchek, G. Korza, and S. K. Weller. 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.
3. Boden, M., G. Dellaire, K. Burrage, and T. L. Bailey. 2010. A Bayesian network model of proteins' association with promyelocytic leukemia (PML) nuclear bodies. J. Comput. Biol. 17:617-630.
4. Bronstein, J. C., and P. C. Weber. 1996. Purification and characterization of herpes simplex virus type 1 alkaline exonuclease expressed in Escherichia coli. J. Virol. 70:2008-2013.
5. 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.
6. Chaudhuri, M., L. Song, and D. S. Parris. 2003. The herpes simplex virus type 1 DNA polymerase processivity factor increases fidelity without altering pre-steady-state rate constants for polymerization or excision. J. Biol. Chem. 278:8996-9004.
7. Ciccia, A., and S. J. Elledge. 2010. The DNA damage response: making it safe to play with knives. Mol. Cell 40:179-204.
8. Conlan, L. A., C. J. McNees, and J. Heierhorst. 2004. Proteasome-dependent dispersal of PML nuclear bodies in response to alkylating DNA damage. Oncogene 23:307-310.
9. Cyr, J. L., G. D. Brown, J. Stroop, and C. D. Heinen. 2011. The predicted truncation from a cancer-associated variant of the MSH2 initiation codon alters activity of the MSH2-MSH6 mismatch repair complex. Mol. Carcinog. doi:10.1002/mc.20838.
10. Daikoku, T., et al. 2006. Postreplicative mismatch repair factors are recruited to Epstein-Barr virus replication compartments. J. Biol. Chem. 281:11422-11430.
11. de Wind, N., M. Dekker, A. Berns, M. Radman, and H. te Riele. 1995. Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell 82:321-330.
12. Dimitrova, D. S., and D. M. Gilbert. 2000. Stability and nuclear distribution of mammalian replication protein A heterotrimeric complex. Exp. Cell Res. 254:321-327.
13. Everett, R. D., and M. K. Chelbi-Alix. 2007. PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89:819-830.
14. Everett, R. D., and J. Murray. 2005. ND10 components relocate to sites associated with herpes simplex virus type 1 nucleoprotein complexes during virus infection. J. Virol. 79:5078-5089.
15. 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.
16. Everett, R. D., et al. 2006. PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J. Virol. 80:7995-8005.
17. Everett, R. D., G. Sourvinos, C. Leiper, J. B. Clements, and A. Orr. 2004. Formation of nuclear foci of the herpes simplex virus type 1 regulatory protein ICP4 at early times of infection: localization, dynamics, recruitment of ICP27, and evidence for the de novo induction of ND10-like complexes. J. Virol. 78:1903-1917.
18. Everett, R. D., G. Sourvinos, and A. Orr. 2003. Recruitment of herpes simplex virus type 1 transcriptional regulatory protein ICP4 into foci juxtaposed to ND10 in live, infected cells. J. Virol. 77:3680-3689.
19. Hall, M. C., et al. 2003. DNA binding by yeast Mlh1 and Pms1: implications for DNA mismatch repair. Nucleic Acids Res. 31:2025-2034.
20. Hsieh, P., and K. Yamane. 2008. DNA mismatch repair: molecular mechanism, cancer, and ageing. Mech. Ageing Dev. 129:391-407.
21. Hwang, Y. T., B. Y. Liu, D. M. Coen, and C. B. Hwang. 1997. Effects of mutations in the Exo III motif of the herpes simplex virus DNA polymerase gene on enzyme activities, viral replication, and replication fidelity. J. Virol. 71:7791-7798.
22. Ishov, A. M., and G. G. Maul. 1996. The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition. J. Cell Biol. 134:815-826.
23. Jiricny, J. 2006. The multifaceted mismatch-repair system. Nat. Rev. Mol. Cell. Biol. 7:335-346.
24. Kalamvoki, M., and B. Roizman. 2010. Circadian CLOCK histone acetyl transferase localizes at ND10 nuclear bodies and enables herpes simplex virus gene expression. Proc. Natl. Acad. Sci. U. S. A. 107:17721-17726.
25. Kalamvoki, M., and B. Roizman. 2011. The histone acetyltransferase CLOCK is an essential component of the herpes simplex virus 1 transcriptome that includes TFIID, ICP4, ICP27, and ICP22. J. Virol. 85:9472-9477.
26. Knopf, K. W. 1979. Properties of herpes simplex virus DNA polymerase and characterization of its associated exonuclease activity. Eur. J. Biochem. 98: 231-244.
27. Koi, M., et al. 1994. Human chromosome 3 corrects mismatch repair defi- ciency and microsatellite instability and reduces N-methyl-NUniversal-GreekwithMathPi.-1.H11032-nitro-N-nitrosoguanidine tolerance in colon tumor cells with homozygous hMLH1 mutation. Cancer Res. 54:4308-4312.
28. Kratz, K., et al. 2010. Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 142: 77-88.
29. Lallemand-Breitenbach, V., and H. de The. 2010. PML nuclear bodies. Cold Spring Harb. Perspect. Biol. 2:a000661.
30. Langland, G., et al. 2001. The Bloom's syndrome protein (BLM) interacts with MLH1 but is not required for DNA mismatch repair. J. Biol. Chem. 276:30031-30035.
31. Lees-Miller, S. P., et al. 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.
32. Li, G. M. 2008. Mechanisms and functions of DNA mismatch repair. Cell Res. 18:85-98.
33. 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.
34. Lilley, C. E., et al. 2010. A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses. EMBO J. 29: 943-955.
35. 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.
36. Liptak, L. M., S. L. Uprichard, and D. M. Knipe. 1996. Functional order of assembly of herpes simplex virus DNA replication proteins into prereplica- tive site structures. J. Virol. 70:1759-1767.
37. 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.
38. Lomonte, P., and R. D. Everett. 1999. Herpes simplex virus type 1 immediate-early protein Vmw110 inhibits progression of cells through mitosis and from G(1) into S phase of the cell cycle. J. Virol. 73:9456-9467.
39. Lukashchuk, V., and R. D. Everett. 2010. Regulation of ICP0-null mutant herpes simplex virus type 1 infection by ND10 components ATRX and hDaxx. J. Virol. 84:4026-4040.
40. 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.
41. Lynch, H., et al. 2009. Review of the Lynch syndrome: history, molecular genetics, screening, differential diagnosis, and medicolegal ramifications. Clin. Genet. 76:1-18.
42. Marcy, A. I., P. D. Olivo, M. D. Challberg, and D. M. Coen. 1990. Enzymatic activities of overexpressed herpes simplex virus DNA polymerase purified from recombinant baculovirus-infected insect cells. Nucleic Acids Res. 18: 1207-1215.
43. Marra, G., et al. 1998. Mismatch repair deficiency associated with overexpression of the MSH3 gene. Proc. Natl. Acad. Sci. U. S. A. 95:8568-8573.
44. Martinez, R., L. Shao, J. C. Bronstein, P. C. Weber, and S. K. Weller. 1996. The product of a 1.9-kb mRNA which overlaps the HSV-1 alkaline nuclease gene (UL12) cannot relieve the growth defects of a null mutant. Virology 215:152-164.
45. Mastrocola, A. S., and C. D. Heinen. 2010. Lynch syndrome-associated mutations in MSH2 alter DNA repair and checkpoint response functions in vivo. Hum. Mutat. 31:E1699-E1708.
46. Mastrocola, A. S., and C. D. Heinen. 2010. Nuclear reorganization of DNA mismatch repair proteins in response to DNA damage. DNA Repair (Amst.) 9:120-133.
47. Maul, G. G., E. Yu, A. M. Ishov, and A. L. Epstein. 1995. Nuclear domain 10 (ND10) associated proteins are also present in nuclear bodies and redistribute to hundreds of nuclear sites after stress. J. Cell. Biochem. 59:498-513.
48. Mohni, K. N., C. M. Livingston, D. Cortez, and S. K. Weller. 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.
49. Nicolas, A., et al. 2010. Identification of rep-associated factors in herpes simplex virus type 1-induced adeno-associated virus type 2 replication compartments. J. Virol. 84:8871-8887.
50. 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.
51. Pedrazzi, G., et al. 2001. Direct association of Bloom's syndrome gene product with the human mismatch repair protein MLH1. Nucleic Acids Res. 29:4378-4386.
52. 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.
53. Reuven, N. B., S. Antoku, and S. K. Weller. 2004. The UL12.5 gene product of herpes simplex virus type 1 exhibits nuclease and strand exchange activities but does not localize to the nucleus. J. Virol. 78:4599-4608.
54. Reuven, N. B., A. E. Staire, R. S. Myers, and S. K. Weller. 2003. The herpes simplex virus type 1 alkaline nuclease and single-stranded DNA binding protein mediate strand exchange in vitro. J. Virol. 77:7425-7433.
55. Roizman, B. 1979. The structure and isomerization of herpes simplex virus genomes. Cell 16:481-494.
56. Samaniego, L. A., L. Neiderhiser, and N. A. DeLuca. 1998. Persistence and expression of the herpes simplex virus genome in the absence of immediateearly proteins. J. Virol. 72:3307-3320.
57. Samaniego, L. A., A. L. Webb, and N. A. DeLuca. 1995. Functional interac- tions between herpes simplex virus immediate-early proteins during infec- tion: gene expression as a consequence of ICP27 and different domains of ICP4. J. Virol. 69:5705-5715.
58. 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.
59. 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.
60. Shirata, N., et al. 2005. Activation of ataxia telangiectasia-mutated DNA damage checkpoint signal transduction elicited by herpes simplex virus infection. J. Biol. Chem. 280:30336-30341.
61. Smogorzewska, A., et al. 2010. A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol. Cell 39:36-47.
62. Stojic, L., et al. 2004. Mismatch repair-dependent G2 checkpoint induced by low doses of SN1 type methylating agents requires the ATR kinase. Genes Dev. 18:1331-1344.
63. Stow, N. D., and E. C. Stow. 1986. Isolation and characterization of a herpes simplex virus type 1 mutant containing a deletion within the gene encoding the immediate early polypeptide Vmw110. J. Gen. Virol. 67(Pt. 12):2571-2585.
64. Sugimoto, A., et al. 2011. Spatiotemporally different DNA repair systems participate in Epstein-Barr virus genome maturation. J. Virol. 85:6127-6135.
65. Tauchi, H., et al. 2002. Nbs1 is essential for DNA repair by homologous recombination in higher vertebrate cells. Nature 420:93-98.
66. 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.
67. Thomas, M. S., M. Gao, D. M. Knipe, and K. L. Powell. 1992. Association between the herpes simplex virus major DNA-binding protein and alkaline nuclease. J. Virol. 66:1152-1161.
68. Umar, A., et al. 1997. Correction of hypermutability, N-methyl-NUniversal-GreekwithMathPi.-1.H11032-nitro-N-nitrosoguanidine resistance, and defective DNA mismatch repair by intro- ducing chromosome 2 into human tumor cells with mutations in MSH2 and MSH6. Cancer Res. 57:3949-3955.
69. 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.
70. Wilcock, D., and D. P. Lane. 1991. Localization of p53, retinoblastoma and host replication proteins at sites of viral replication in herpes-infected cells. Nature 349:429-431.
71. 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.
72. Wilkinson, D. E., and S. K. Weller. 2003. The role of DNA recombination in herpes simplex virus DNA replication. IUBMB Life 55:451-458.
73. Zhou, B., et al. 2009. Preparation of heteroduplex enhanced green fluorescent protein plasmid for in vivo mismatch repair activity assay. Anal. Biochem. 388:167-169.