Co-opting the Fanconi anemia genomic stability pathway enables herpesvirus DNA synthesis and productive growth

Molecular Cell

Volumn 55, Issue 1, 2014, Pages 111-122

  Karttunen, Heidi ^a   Savas, Jeffrey N ^b   McKinney, Caleb ^a,d   Chen, Yu Hung ^a   Yates, John R ^b   Hukkanen, Veijo ^c   Huang, Tony T ^a   Mohr, Ian ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF TURKU   (Finland)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; DNA DEPENDENT PROTEIN KINASE; DNA POLYMERASE; FANCONI ANEMIA GROUP D2 PROTEIN; FANCONI ANEMIA PROTEIN; INFECTED CELL PROTEIN 8; PROTEIN FANCI; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; VIRUS DNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; DNA DAMAGE; DNA END JOINING REPAIR; DNA SYNTHESIS; DOUBLE STRANDED DNA BREAK; FANCONI ANEMIA; GENOMIC INSTABILITY; HERPES SIMPLEX VIRUS 1; HUMAN; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; VIROGENESIS; VIRUS CELL INTERACTION; VIRUS REPLICATION;

HERPESVIRIDAE; HUMAN HERPESVIRUS 1;

ANIMALS; CERCOPITHECUS AETHIOPS; DNA DAMAGE; DNA END-JOINING REPAIR; DNA, VIRAL; DNA-DIRECTED DNA POLYMERASE; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP D2 PROTEIN; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; GENOMIC INSTABILITY; HERPESVIRUS 1, HUMAN; UBIQUITINATION; VERO CELLS; VIRUS REPLICATION;

EID: 84903769923     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.05.020     Document Type: Article

References (64)

1. Adamo A., Collis S.J., Adelman C.A., Silva N., Horejsi Z., Ward J.D., Martinez-Perez E., Boulton S.J., La Volpe A. Preventing nonhomologous end joining suppresses DNA repair defects of Fanconi anemia. Mol. Cell 2010, 39:25-35.
2. Balasubramanian N., Bai P., Buchek G., Korza G., Weller S.K. Physical interaction between the herpes simplex virus type 1 exonuclease, UL12, and the DNA double-strand break-sensing MRN complex. J.Virol. 2010, 84:12504-12514.
3. Benboudjema L., Mulvey M., Gao Y., Pimplikar S.W., Mohr I. Association of the herpes simplex virus type 1Us11 gene product with the cellular kinesin light-chain-related protein PAT1 results in the redistribution of both polypeptides. J.Virol. 2003, 77:9192-9203.
4. Boichuk S., Hu L., Hein J., Gjoerup O.V. Multiple DNA damage signaling and repair pathways deregulated by simian virus 40 large T antigen. J.Virol. 2010, 84:8007-8020.
5. Chapman J.R., Taylor M.R., Boulton S.J. Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 2012, 47:497-510.
6. Cherubini G., Naim V., Caruso P., Burla R., Bogliolo M., Cundari E., Benihoud K., Saggio I., Rosselli F. The FANC pathway is activated by adenovirus infection and promotes viral replication-dependent recombination. Nucleic Acids Res. 2011, 39:5459-5473.
7. Ciccia A., Elledge S.J. The DNA damage response: making it safe to play with knives. Mol. Cell 2010, 40:179-204.
8. D'Andrea A.D., Grompe M. The Fanconi anaemia/BRCA pathway. Nat. Rev. Cancer 2003, 3:23-34.
9. DeLuca N.A., McCarthy A.M., Schaffer P.A. Isolation and characterization of deletion mutants of herpes simplex virus type 1 in the gene encoding immediate-early regulatory protein ICP4. J.Virol. 1985, 56:558-570.
10. Everett R.D., Murray J. ND10 components relocate to sites associated with herpes simplex virus type 1 nucleoprotein complexes during virus infection. J.Virol. 2005, 79:5078-5089.
11. Ferguson B.J., Mansur D.S., Peters N.E., Ren H., Smith G.L. DNA-PK is a DNA sensor for IRF-3-dependent innate immunity. eLife 2012, 1:e00047.
12. Garcia-Higuera I., Taniguchi T., Ganesan S., Meyn M.S., Timmers C., Hejna J., Grompe M., D'Andrea A.D. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell 2001, 7:249-262.
13. Gulbahce N., Yan H., Dricot A., Padi M., Byrdsong D., Franchi R., Lee D.S., Rozenblatt-Rosen O., Mar J.C., Calderwood M.A., et al. Viral perturbations of host networks reflect disease etiology. PLoS Comput. Biol. 2012, 8:e1002531.
14. Hartlerode A.J., Scully R. Mechanisms of double-strand break repair in somatic mammalian cells. Biochem. J. 2009, 423:157-168.
15. Hoskins E.E., Morreale R.J., Werner S.P., Higginbotham J.M., Laimins L.A., Lambert P.F., Brown D.R., Gillison M.L., Nuovo G.J., Witte D.P., et al. The fanconi anemia pathway limits human papillomavirus replication. J.Virol. 2012, 86:8131-8138.
16. Hyman R.W., Oakes J.E., Kudler L. Invitro repair of the preexisting nicks and gaps in herpes simplex virus DNA. Virology 1977, 76:286-294.
17. Ishiai M., Kitao H., Smogorzewska A., Tomida J., Kinomura A., Uchida E., Saberi A., Kinoshita E., Kinoshita-Kikuta E., Koike T., et al. FANCI phosphorylation functions as a molecular switch to turn on the Fanconi anemia pathway. Nat. Struct. Mol. Biol. 2008, 15:1138-1146.
18. Jackson S.A., DeLuca N.A. Relationship of herpes simplex virus genome configuration to productive and persistent infections. Proc. Natl. Acad. Sci. USA 2003, 100:7871-7876.
19. Jackson S.P., Bartek J. The DNA-damage response in human biology and disease. Nature 2009, 461:1071-1078.
20. Jacob R.J., Roizman B. Anatomy of herpes simplex virus DNA VIII. Properties of the replicating DNA. J.Virol. 1977, 23:394-411.
21. Kennedy R.D., D'Andrea A.D. The Fanconi Anemia/BRCA pathway: new faces in the crowd. Genes Dev. 2005, 19:2925-2940.
22. Knipscheer P., Räschle M., Smogorzewska A., Enoiu M., Ho T.V., Schärer O.D., Elledge S.J., Walter J.C. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 2009, 326:1698-1701.
23. Kottemann M.C., Smogorzewska A. Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature 2013, 493:356-363.
24. Langevin F., Crossan G.P., Rosado I.V., Arends M.J., Patel K.J. Fancd2 counteracts the toxic effects of naturally produced aldehydes in mice. Nature 2011, 475:53-58.
25. Leahy J.J., Golding B.T., Griffin R.J., Hardcastle I.R., Richardson C., Rigoreau L., Smith G.C. Identification of a highly potent and selective DNA-dependent protein kinase (DNA-PK) inhibitor (NU7441) by screening of chromenone libraries. Bioorg. Med. Chem. Lett. 2004, 14:6083-6087.
26. Lee Y., McKinnon P.J. Responding to DNA double strand breaks in the nervous system. Neuroscience 2007, 145:1365-1374.
27. Lees-Miller S.P., Long M.C., Kilvert M.A., Lam V., Rice S.A., 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. 1996, 70:7471-7477.
28. Lieber M.R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Ann. Rev. Biochem. 2010, 79:181-211.
29. Lilley C.E., Carson C.T., Muotri A.R., Gage F.H., Weitzman M.D. DNA repair proteins affect the lifecycle of herpes simplex virus 1. Proc. Natl. Acad. Sci. USA 2005, 102:5844-5849.
30. Lilley C.E., Chaurushiya M.S., Boutell C., Landry S., Suh J., Panier S., Everett R.D., Stewart G.S., Durocher D., Weitzman M.D. A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses. EMBO J. 2010, 29:943-955.
31. Lilley C.E., Chaurushiya M.S., Boutell C., Everett R.D., Weitzman M.D. The intrinsic antiviral defense to incoming HSV-1 genomes includes specific DNA repair proteins and is counteracted by the viral protein ICP0. PLoS Pathog. 2011, 7:e1002084.
32. Lo Piano A., Martínez-Jiménez M.I., Zecchi L., Ayora S. Recombination-dependent concatemeric viral DNA replication. Virus Res. 2011, 160:1-14.
33. Marcy A.I., Yager D.R., Coen D.M. Isolation and characterization of herpes simplex virus mutants containing engineered mutations at the DNA polymerase locus. J.Virol. 1990, 64:2208-2216.
34. Mohni K.N., Livingston C.M., Cortez D., Weller S.K. ATR and ATRIP are recruited to herpes simplex virus type 1 replication compartments even though ATR signaling is disabled. J.Virol. 2010, 84:12152-12164.
35. Mohni K.N., Dee A.R., Smith S., Schumacher A.J., Weller S.K. Efficient herpes simplex virus 1 replication requires cellular ATR pathway proteins. J.Virol. 2013, 87:531-542.
36. Mohni K.N., Smith S., Dee A.R., Schumacher A.J., Weller S.K. Herpes simplex virus type 1 single strand DNA binding protein and helicase/primase complex disable cellular ATR signaling. PLoS Pathog. 2013, 9:e1003652.
37. Mohr I., Sonenberg N. Host translation at the nexus of infection and immunity. Cell Host Microbe 2012, 12:470-483.
38. Moldovan G.L., D'Andrea A.D. How the fanconi anemia pathway guards the genome. Annu. Rev. Genet. 2009, 43:223-249.
39. Nakanishi K., Yang Y.G., Pierce A.J., Taniguchi T., Digweed M., D'Andrea A.D., Wang Z.Q., Jasin M. Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair. Proc. Natl. Acad. Sci. USA 2005, 102:1110-1115.
40. Nakanishi K., Cavallo F., Perrouault L., Giovannangeli C., Moynahan M.E., Barchi M., Brunet E., Jasin M. Homology-directed Fanconi anemia pathway cross-link repair is dependent on DNA replication. Nat. Struct. Mol. Biol. 2011, 18:500-503.
41. Pace P., Mosedale G., Hodskinson M.R., Rosado I.V., Sivasubramaniam M., Patel K.J. Ku70 corrupts DNA repair in the absence of the Fanconi anemia pathway. Science 2010, 329:219-223.
42. Parkinson J., Lees-Miller S.P., 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. 1999, 73:650-657.
43. Roizman B. The structure and isomerization of herpes simplex virus genomes. Cell 1979, 16:481-494.
44. Roizman B., Knipe D., Whitley R. Herpes simplex virus. Fields Virology 2006, 2501-2601. Lippincott-Williams & Wilkins, Philadelphia. Fifth Edition. D. Knipe, P. Howley, D. Griffin, R. Lamb, M. Martin, S. Straus (Eds.).
45. Rosado I.V., Langevin F., Crossan G.P., Takata M., Patel K.J. Formaldehyde catabolism is essential in cells deficient for the Fanconi anemia DNA-repair pathway. Nat. Struct. Mol. Biol. 2011, 18:1432-1434.
46. Sarisky R.T., Weber P.C. Requirement for double-strand breaks but not for specific DNA sequences in herpes simplex virus type 1 genome isomerization events. J.Virol. 1994, 68:34-47.
47. Schumacher A.J., Mohni K.N., Kan Y., Hendrickson E.A., Stark J.M., Weller S.K. The HSV-1 exonuclease, UL12, stimulates recombination by a single strand annealing mechanism. PLoS Pathog. 2012, 8:e1002862.
48. Shen X., Do H., Li Y., Chung W.H., Tomasz M., de Winter J.P., Xia B., Elledge S.J., Wang W., Li L. Recruitment of fanconi anemia and breast cancer proteins to DNA damage sites is differentially governed by replication. Mol. Cell 2009, 35:716-723.
49. Sims A.E., Spiteri E., Sims R.J., Arita A.G., Lach F.P., Landers T., Wurm M., Freund M., Neveling K., Hanenberg H., et al. FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat. Struct. Mol. Biol. 2007, 14:564-567.
50. Smogorzewska A., Matsuoka S., Vinciguerra P., McDonald E.R., Hurov K.E., Luo J., Ballif B.A., Gygi S.P., Hofmann K., D'Andrea A.D., Elledge S.J. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 2007, 129:289-301.
51. Taniguchi T., Garcia-Higuera I., Andreassen P.R., Gregory R.C., Grompe M., D'Andrea A.D. S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 2002, 100:2414-2420.
52. Tarakanova V.L., Leung-Pineda V., Hwang S., Yang C.-W., Matatall K., Basson M., Sun R., Piwnica-Worms H., Sleckman B.P., Virgin H.W. γ-herpesvirus kinase actively initiates a DNA damage response by inducing phosphorylation of H2AX to foster viral replication. Cell Host Microbe 2007, 1:275-286.
53. Taylor T.J., 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. 2004, 78:5856-5866.
54. Thomas M.S., Gao M., Knipe D.M., Powell K.L. Association between the herpes simplex virus major DNA-binding protein and alkaline nuclease. J.Virol. 1992, 66:1152-1161.
55. Wadsworth S., Hayward G.S., Roizman B. Anatomy of herpes simplex virus DNA. V. Terminally repetitive sequences. J.Virol. 1976, 17:503-512.
56. Walsh D., Mohr I. Assembly of an active translation initiation factor complex by a viral protein. Genes Dev. 2006, 20:461-472.
57. Walsh D., Mohr I. Viral subversion of the host protein synthesis machinery. Nat. Rev. Microbiol. 2011, 9:860-875.
58. Washburn M.P., Wolters D., Yates J.R. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 2001, 19:242-247.
59. Weinheimer S.P., McKnight S.L. Transcriptional and post-transcriptional controls establish the cascade of herpes simplex virus protein synthesis. J.Mol. Biol. 1987, 195:819-833.
60. Weitzman M.D., Lilley C.E., Chaurushiya M.S. Genomes in conflict: maintaining genome integrity during virus infection. Annu. Rev. Microbiol. 2010, 64:61-81.
61. Weller S.K. Herpes simplex virus reorganizes the cellular DNA repair and protein quality control machinery. PLoS Pathog. 2010, 6:e1001105.
62. Weller S.K., Coen D.M. Herpes simplex viruses: mechanisms of DNA replication. Cold Spring Harb. Perspect. Biol. 2012, 4:a013011.
63. Wilkinson D.E., Weller S.K. The role of DNA recombination in herpes simplex virus DNA replication. IUBMB Life 2003, 55:451-458.
64. Wilkinson D.E., 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. 2004, 78:4783-4796.