Characterization of mre11 loss following HSV-1 infection

Virology

Volumn 373, Issue 1, 2008, Pages 124-136

  Gregory, Devon A ^a   Bachenheimer, Steven L ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

DNA damage response; HSV; Mrell; MRN

Indexed keywords

CAMPTOTHECIN; MRE11 PROTEIN; PROTEINASE; VIRUS DNA;

ARTICLE; CONTROLLED STUDY; DNA CLEAVAGE; DNA PACKAGING; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; FIBROBLAST; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; KERATINOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; VIRUS GENE;

CELL LINE; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA REPLICATION; DNA, VIRAL; DNA-BINDING PROTEINS; FIBROBLASTS; HERPESVIRUS 1, HUMAN; HUMANS; KERATINOCYTES; MUTATION; VIRAL PROTEINS;

HUMAN HERPESVIRUS 1; SIMPLEXVIRUS;

EID: 40649125286     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.12.005     Document Type: Article

References (74)

1. Addison C., Rixon F.J., and Preston V.G. Herpes simplex virus type 1 UL28 gene product is important for the formation of mature capsids. J. Gen. Virol. 71 Pt 10 (1990) 2377-2384
2. Adelman K., Salmon B., and Baines J.D. Herpes simplex virus DNA packaging sequences adopt novel structures that are specifically recognized by a component of the cleavage and packaging machinery. Proc. Natl. Acad. Sci. U. S. A. 98 6 (2001) 3086-3091
3. Baines J.D., Poon A.P., Rovnak J., and Roizman B. The herpes simplex virus 1 UL15 gene encodes two proteins and is required for cleavage of genomic viral DNA. J. Virol. 68 12 (1994) 8118-8124
4. Bargonetti J., Reynisdottir I., Friedman P.N., and Prives C. Site-specific binding of wild-type p53 to cellular DNA is inhibited by SV40 T antigen and mutant p53. Genes Dev. 6 10 (1992) 1886-1898
5. Burma S., Chen B.P., Murphy M., Kurimasa A., and Chen D.J. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 276 45 (2001) 42462-42467
6. Cai W.Z., and Schaffer P.A. Herpes simplex virus type 1 ICP0 plays a critical role in the de novo synthesis of infectious virus following transfection of viral DNA. J. Virol. 63 11 (1989) 4579-4589
7. Carson C.T., Schwartz R.A., Stracker T.H., Lilley C.E., Lee D.V., and Weitzman M.D. The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J. 22 24 (2003) 6610-6620
8. Chelbi-Alix M.K., and de The H. Herpes virus induced proteasome-dependent degradation of the nuclear bodies-associated PML and Sp100 proteins. Oncogene 18 4 (1999) 935-941
9. Cheng W.H., Muftuoglu M., and Bohr V.A. Werner syndrome protein: functions in the response to DNA damage and replication stress in S-phase. Exp. Gerontol. 42 9 (2007) 871-878
10. Chou J., Chen J.J., Gross M., and Roizman B. Association of a M(r) 90,000 phosphoprotein with protein kinase PKR in cells exhibiting enhanced phosphorylation of translation initiation factor eIF-2 alpha and premature shutoff of protein synthesis after infection with gamma 134.5-mutants of herpes simplex virus 1. Proc. Natl. Acad. Sci. U. S. A. 92 23 (1995) 10516-10520
11. Ciechanover A. The ubiquitin proteolytic system: from a vague idea, through basic mechanisms, and onto human diseases and drug targeting. Neurology 66 2 Suppl 1 (2006) S7-S19
12. DeLuca N.A., and Schaffer P.A. Physical and functional domains of the herpes simplex virus transcriptional regulatory protein ICP4. J. Virol. 62 3 (1988) 732-743
13. Desai P., Watkins S.C., and Person S. The size and symmetry of B capsids of herpes simplex virus type 1 are determined by the gene products of the UL26 open reading frame. J. Virol. 68 9 (1994) 5365-5374
14. Digweed M., Demuth I., Rothe S., Scholz R., Jordan A., Grotzinger C., Schindler D., Grompe M., and Sperling K. SV40 large T-antigen disturbs the formation of nuclear DNA-repair foci containing MRE11. Oncogene 21 32 (2002) 4873-4878
15. Ehmann, G.L., 2001. University of North Carolina at Chapel Hill. Curriculum in genetics and molecular biology. Microform/xvi, 193 leaves. Effects of Herpes Simplex Virus Type 1 on the Cell Cycle.
16. Everett R.D., Orr A., and Preston C.M. A viral activator of gene expression functions via the ubiquitin-proteasome pathway. EMBO J. 17 24 (1998) 7161-7169
17. Everett R.D., Earnshaw W.C., Findlay J., and Lomonte P. Specific destruction of kinetochore protein CENP-C and disruption of cell division by herpes simplex virus immediate-early protein Vmw110. EMBO J. 18 6 (1999) 1526-1538
18. Everett R.D., Boutell C., and Orr A. Phenotype of a herpes simplex virus type 1 mutant that fails to express immediate-early regulatory protein ICP0. J. Virol. 78 4 (2004) 1763-1774
19. Farwell D.G., Shera K.A., Koop J.I., Bonnet G.A., Matthews C.P., Reuther G.W., Coltrera M.D., McDougall J.K., and Klingelhutz A.J. Genetic and epigenetic changes in human epithelial cells immortalized by telomerase. Am. J. Pathol. 156 5 (2000) 1537-1547
20. Fernet M., Gribaa M., Salih M.A., Seidahmed M.Z., Hall J., and Koenig M. Identification and functional consequences of a novel MRE11 mutation affecting 10 Saudi Arabian patients with the ataxia telangiectasia-like disorder. Hum. Mol. Genet. 14 2 (2005) 307-318
21. Fuertes G., Martin De Llano J.J., Villarroya A., Rivett A.J., and Knecht E. Changes in the proteolytic activities of proteasomes and lysosomes in human fibroblasts produced by serum withdrawal, amino-acid deprivation and confluent conditions. Biochem. J. 375 Pt 1 (2003) 75-86
22. Gao M., and Knipe D.M. Genetic evidence for multiple nuclear functions of the herpes simplex virus ICP8 DNA-binding protein. J. Virol. 63 12 (1989) 5258-5267
23. Gregory D., Hargett D., Holmes D., Money E., and Bachenheimer S.L. Efficient replication by herpes simplex virus type 1 involves activation of the IkappaB kinase-IkappaB-p65 pathway. J. Virol. 78 24 (2004) 13582-13590
24. Hagglund R., and Roizman B. Herpes simplex virus 1 mutant in which the ICP0 HUL-1 E3 ubiquitin ligase site is disrupted stabilizes cdc34 but degrades D-type cyclins and exhibits diminished neurotoxicity. J. Virol. 77 24 (2003) 13194-13202
25. Hickson I., Zhao Y., Richardson C.J., Green S.J., Martin N.M., Orr A.I., Reaper P.M., Jackson S.P., Curtin N.J., and Smith G.C. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 64 24 (2004) 9152-9159
26. Hopfner K.P., Craig L., Moncalian G., Zinkel R.A., Usui T., Owen B.A., Karcher A., Henderson B., Bodmer J.L., McMurray C.T., Carney J.P., Petrini J.H., and Tainer J.A. The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418 6897 (2002) 562-566
27. Kastan M.B., and Lim D.S. The many substrates and functions of ATM. Nat. Rev., Mol. Cell Biol. 1 3 (2000) 179-186
28. Kudoh A., Fujita M., Zhang L., Shirata N., Daikoku T., Sugaya Y., Isomura H., Nishiyama Y., and Tsurumi T. Epstein-Barr virus lytic replication elicits ATM checkpoint signal transduction while providing an S-phase-like cellular environment. J. Biol. Chem. 280 9 (2005) 8156-8163
29. Lamberti C., and Weller S.K. The herpes simplex virus type 1 UL6 protein is essential for cleavage and packaging but not for genomic inversion. Virology 226 2 (1996) 403-407
30. Lamberti C., and Weller S.K. The herpes simplex virus type 1 cleavage/packaging protein, UL32, is involved in efficient localization of capsids to replication compartments. J. Virol. 72 3 (1998) 2463-2473
31. Lanson Jr. N.A., Egeland D.B., Royals B.A., and Claycomb W.C. The MRE11-NBS1-RAD50 pathway is perturbed in SV40 large T antigen-immortalized AT-1, AT-2 and HL-1 cardiomyocytes. Nucleic Acids Res. 28 15 (2000) 2882-2892
32. Lee D.H., and Goldberg A.L. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 8 10 (1998) 397-403
33. Lee J.H., and Paull T.T. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304 5667 (2004) 93-96
34. Lee J.H., and Paull T.T. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308 5721 (2005) 551-554
35. Lees-Miller S.P., Long M.C., Kilvert M.A., Lam V., Rice S.A., and Spencer C.A. Attenuation of DNA-dependent protein kinase activity and its catalytic subunit by the herpes simplex virus type 1 transactivator ICP0. J. Virol. 70 11 (1996) 7471-7477
36. Lilley C.E., Carson C.T., Muotri A.R., Gage F.H., and Weitzman M.D. DNA repair proteins affect the lifecycle of herpes simplex virus 1. Proc. Natl. Acad. Sci. U. S. A. 102 16 (2005) 5844-5849
37. Link M.A., Silva L.A., and Schaffer P.A. Cathepsin B mediates cleavage of herpes simplex virus type 1 origin binding protein (OBP) to yield OBPC-1, and cleavage is dependent upon viral DNA replication. J. Virol. 81 17 (2007) 9175-9182
38. Lomonte P., Sullivan K.F., and Everett R.D. Degradation of nucleosome-associated centromeric histone H3-like protein CENP-A induced by herpes simplex virus type 1 protein ICP0. J. Biol. Chem. 276 8 (2001) 5829-5835
39. Marcy A.I., Yager D.R., and Coen D.M. Isolation and characterization of herpes simplex virus mutants containing engineered mutations at the DNA polymerase locus. J. Virol. 64 5 (1990) 2208-2216
40. Mauser A., Holley-Guthrie E., Zanation A., Yarborough W., Kaufmann W., Klingelhutz A., Seaman W.T., and Kenney S. The Epstein-Barr virus immediate-early protein BZLF1 induces expression of E2F-1 and other proteins involved in cell cycle progression in primary keratinocytes and gastric carcinoma cells. J. Virol. 76 24 (2002) 12543-12552
41. Mauser A., Saito S., Appella E., Anderson C.W., Seaman W.T., and Kenney S. The Epstein-Barr virus immediate-early protein BZLF1 regulates p53 function through multiple mechanisms. J. Virol. 76 24 (2002) 12503-12512
42. McNab A.R., Desai P., Person S., Roof L.L., Thomsen D.R., Newcomb W.W., Brown J.C., and Homa F.L. The product of the herpes simplex virus type 1 UL25 gene is required for encapsidation but not for cleavage of replicated viral DNA. J. Virol. 72 2 (1998) 1060-1070
43. Moore M., Horikoshi N., and Shenk T. Oncogenic potential of the adenovirus E4orf6 protein. Proc. Natl. Acad. Sci. U. S. A. 93 21 (1996) 11295-11301
44. Newcomb W.W., Juhas R.M., Thomsen D.R., Homa F.L., Burch A.D., Weller S.K., and Brown J.C. The UL6 gene product forms the portal for entry of DNA into the herpes simplex virus capsid. J. Virol. 75 22 (2001) 10923-10932
45. Parkinson J., Lees-Miller S.P., and Everett R.D. 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 1 (1999) 650-657
46. Pastwa E., and Blasiak J. Non-homologous DNA end joining. Acta Biochim. Pol. 50 4 (2003) 891-908
47. Paull T.T., and Gellert M. The 3′ to 5′exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell 1 7 (1998) 969-979
48. Paull T.T., and Gellert M. Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev. 13 10 (1999) 1276-1288
49. Paull T.T., and Lee J.H. The Mre11/Rad50/Nbs1 complex and its role as a DNA double-strand break sensor for ATM. Cell Cycle 4 6 (2005) 737-740
50. Poon A.P., and Roizman B. Characterization of a temperature-sensitive mutant of the UL15 open reading frame of herpes simplex virus 1. J. Virol. 67 8 (1993) 4497-4503
51. Querido E., Marcellus R.C., Lai A., Charbonneau R., Teodoro J.G., Ketner G., and Branton P.E. Regulation of p53 levels by the E1B 55-kilodalton protein and E4orf6 in adenovirus-infected cells. J. Virol. 71 5 (1997) 3788-3798
52. Quinlan M.P., Chen L.B., and Knipe D.M. The intranuclear location of a herpes simplex virus DNA-binding protein is determined by the status of viral DNA replication. Cell 36 4 (1984) 857-868
53. Rappold I., Iwabuchi K., Date T., and Chen J. Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J. Cell Biol. 153 3 (2001) 613-620
54. Rock K.L., Gramm C., Rothstein L., Clark K., Stein R., Dick L., Hwang D., and Goldberg A.L. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78 5 (1994) 761-771
55. Roizman B., and Knipe D.M. Herpes simplex viruses and their replication. Fundamental Virology, 4th ed. In: Knipe D.M., and Howley P.M. (Eds) (2001), Lippincott Williams & Wilkins, Philadelphia 1123-1183
56. Salmon B., Cunningham C., Davison A.J., Harris W.J., and Baines J.D. The herpes simplex virus type 1 U(L)17 gene encodes virion tegument proteins that are required for cleavage and packaging of viral DNA. J. Virol. 72 5 (1998) 3779-3788
57. Schaffer P.A., Brunschwig J.P., McCombs R.M., and Benyesh-Melnick M. Electron microscopic studies of temperature-sensitive mutants of herpes simplex virus type 1. Virology 62 2 (1974) 444-457
58. Sherman G., and Bachenheimer S.L. DNA processing in temperature-sensitive morphogenic mutants of HSV-1. Virology 158 2 (1987) 427-430
59. Sherman G., and Bachenheimer S.L. Characterization of intranuclear capsids made by ts morphogenic mutants of HSV-1. Virology 163 2 (1988) 471-480
60. Shirata N., Kudoh A., Daikoku T., Tatsumi Y., Fujita M., Kiyono T., Sugaya Y., Isomura H., Ishizaki K., and Tsurumi T. Activation of ataxia telangiectasia-mutated DNA damage checkpoint signal transduction elicited by herpes simplex virus infection. J. Biol. Chem. 280 34 (2005) 30336-30341
61. Stow N.D. Packaging of genomic and amplicon DNA by the herpes simplex virus type 1 UL25-null mutant KUL25NS. J. Virol. 75 22 (2001) 10755-10765
62. Stracker T.H., Carson C.T., and Weitzman M.D. Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 418 6895 (2002) 348-352
63. Tauchi H., Kobayashi J., Morishima K., van Gent D.C., Shiraishi T., Verkaik N.S., vanHeems D., Ito E., Nakamura A., Sonoda E., Takata M., Takeda S., Matsuura S., and Komatsu K. Nbs1 is essential for DNA repair by homologous recombination in higher vertebrate cells. Nature 420 6911 (2002) 93-98
64. Taus N.S., Salmon B., and Baines J.D. The herpes simplex virus 1 UL 17 gene is required for localization of capsids and major and minor capsid proteins to intranuclear sites where viral DNA is cleaved and packaged. Virology 252 1 (1998) 115-125
65. Taylor T.J., and Knipe D.M. Proteomics of herpes simplex virus replication compartments: association of cellular DNA replication, repair, recombination, and chromatin remodeling proteins with ICP8. J. Virol. 78 11 (2004) 5856-5866
66. Tengelsen L.A., Pederson N.E., Shaver P.R., Wathen M.W., and Homa F.L. Herpes simplex virus type 1 DNA cleavage and encapsidation require the product of the UL28 gene: isolation and characterization of two UL28 deletion mutants. J. Virol. 67 6 (1993) 3470-3480
67. Wilkinson D.E., and Weller S.K. The role of DNA recombination in herpes simplex virus DNA replication. IUBMB Life 55 8 (2003) 451-458
68. Wilkinson D.E., and Weller S.K. 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 9 (2004) 4783-4796
69. Wilkinson D.E., and Weller S.K. Herpes simplex virus type I disrupts the ATR-dependent DNA-damage response during lytic infection. J. Cell Sci. 119 Pt 13 (2006) 2695-2703
70. Wu X., Avni D., Chiba T., Yan F., Zhao Q., Lin Y., Heng H., and Livingston D. SV40 T antigen interacts with Nbs1 to disrupt DNA replication control. Genes Dev. 18 11 (2004) 1305-1316
71. Wyman C., Ristic D., and Kanaar R. Homologous recombination-mediated double-strand break repair. DNA Repair (Amst) 3 8-9 (2004) 827-833
72. Yamaguchi-Iwai Y., Sonoda E., Sasaki M.S., Morrison C., Haraguchi T., Hiraoka Y., Yamashita Y.M., Yagi T., Takata M., Price C., Kakazu N., and Takeda S. Mre11 is essential for the maintenance of chromosomal DNA in vertebrate cells. EMBO J. 18 23 (1999) 6619-6629
73. Yu D., and Weller S.K. Genetic analysis of the UL 15 gene locus for the putative terminase of herpes simplex virus type 1. Virology 243 1 (1998) 32-44
74. Zhong H., Bryson A., Eckersdorff M., and Ferguson D.O. Rad50 depletion impacts upon ATR-dependent DNA damage responses. Hum. Mol. Genet. 14 18 (2005) 2685-2693