The Rad6/18 ubiquitin complex interacts with the Epstein-Barr virus deubiquitinating enzyme, BPLF1, and contributes to virus infectivity

Journal of Virology

Volumn 88, Issue 11, 2014, Pages 6411-6422

  Kumar, Ravindra ^a   Whitehurst, Christopher B ^a   Pagano, Joseph S ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BPLF1 PROTEIN; CYCLINE; DEUBIQUITINASE; RAD18 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING COMPETITION; CELL CYCLE S PHASE; CONTROLLED STUDY; EPSTEIN BARR VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; VIRUS INFECTIVITY; VIRUS REACTIVATION; VIRUS REPLICATION;

DNA-BINDING PROTEINS; ESCHERICHIA COLI; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; HEK293 CELLS; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MULTIPROTEIN COMPLEXES; PROLIFERATING CELL NUCLEAR ANTIGEN; REAL-TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, SMALL INTERFERING; UBIQUITIN-CONJUGATING ENZYMES; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRUS REPLICATION;

EID: 84899793272     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00536-14     Document Type: Article

References (83)

1. Anagnostopoulos I, Hummel M, Kreschel C, Stein H. 1995. Morphology, immunophenotype, and distribution of latently and/or productively Epstein-Barr virus-infected cells in acute infectious mononucleosis: implications for the interindividual infection route of Epstein-Barr virus. Blood 85:744-750.
2. Lemon SM, Hutt LM, Shaw JE, Li JL, Pagano JS. 1977. Replication of EBV in epithelial cells during infectious mononucleosis. Nature 268:268-270. http://dx. doi. org/10. 1038/268268a0.
3. Niederman JC, Miller G, Pearson HA, Pagano JS, Dowaliby JM. 1976. Infectious mononucleosis. Epstein-Barr-virus shedding in saliva and the oropharynx. N. Engl. J. Med. 294:1355-1359.
4. Babcock GJ, Decker LL, Volk M, Thorley-Lawson DA. 1998. EBV persistence in memory B cells in vivo. Immunity 9:395-404. http://dx. doi. org/10. 1016/S1074-7613(00)80622-6.
5. Pagano J. 2009. EBV diseases, p 794. In Damania B, Pipas J (ed), DNA tumor viruses. Springer, New York, NY.
6. Raab-Traub N. 2007. EBV-induced oncogenesis. In Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K (ed), Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, United Kingdom.
7. Saha A, Robertson ES. 2011. Epstein-Barr virus-associated B-cell lymphomas: pathogenesis and clinical outcomes. Clin. Cancer Res. 17:3056-3063. http://dx. doi. org/10. 1158/1078-0432. CCR-10-2578.
8. Niederman JC, McCollum RW, Henle G, Henle W. 1968. Infectious mononucleosis. Clinical manifestations in relation to EB virus antibodies. JAMA 203:205-209.
9. Yuan J, Cahir-McFarland E, Zhao B, Kieff E. 2006. Virus and cell RNAs expressed during Epstein-Barr virus replication. J. Virol. 80:2548-2565. http://dx. doi. org/10. 1128/JVI. 80. 5. 2548-2565. 2006.
10. Abaitua F, Daikoku T, Crump CM, Bolstad M, O'Hare P. 2011. A single mutation responsible for temperature-sensitive entry and assembly defects in the VP1-2 protein of herpes simplex virus. J. Virol. 85:2024-2036. http://dx. doi. org/10. 1128/JVI. 01895-10.
11. Batterson W, Furlong D, Roizman B. 1983. Molecular genetics of herpes simplex virus. VIII. Further characterization of a temperature-sensitive mutant defective in release of viral DNA and in other stages of the viral reproductive cycle. J. Virol. 45:397-407.
12. Bottcher S, Granzow H, Maresch C, Mohl B, Klupp BG, Mettenleiter TC. 2007. Identification of functional domains within the essential large tegument protein pUL36 of pseudorabies virus. J. Virol. 81:13403-13411. http://dx. doi. org/10. 1128/JVI. 01643-07.
13. Desai PJ. 2000. A null mutation in the UL36 gene of herpes simplex virus type 1 results in accumulation of unenveloped DNA-filled capsids in the cytoplasm of infected cells. J. Virol. 74:11608-11618. http://dx. doi. org/10. 1128/JVI. 74. 24. 11608-11618. 2000.
14. Schlieker C, Korbel GA, Kattenhorn LM, Ploegh HL. 2005. A deubiquitinating activity is conserved in the large tegument protein of the herpesviridae. J. Virol. 79:15582-15585. http://dx. doi. org/10. 1128/JVI. 79. 24. 15582-15585. 2005.
15. Schlieker C, Weihofen WA, Frijns E, Kattenhorn LM, Gaudet R, Ploegh HL. 2007. Structure of a herpesvirus-encoded cysteine protease reveals a unique class of deubiquitinating enzymes. Mol. Cell 25:677-687. http://dx. doi. org/10. 1016/j. molcel. 2007. 01. 033.
16. Gastaldello S, Hildebrand S, Faridani O, Callegari S, Palmkvist M, Di Guglielmo C, Masucci MG. 2010. A deneddylase encoded by Epstein-Barr virus promotes viral DNA replication by regulating the activity of cullin-RING ligases. Nat. Cell Biol. 12:351-361. http://dx. doi. org/10. 1038/ncb2035.
17. Whitehurst CB, Ning S, Bentz GL, Dufour F, Gershburg E, Shackelford J, Langelier Y, Pagano JS. 2009. The Epstein-Barr virus (EBV) deubiquitinating enzyme BPLF1 reduces EBV ribonucleotide reductase activity. J. Virol. 83:4345-4353. http://dx. doi. org/10. 1128/JVI. 02195-08.
18. Gonzalez CM, Wang L, Damania B. 2009. Kaposi's sarcoma-associated herpesvirus encodes a viral deubiquitinase. J. Virol. 83:10224-10233. http://dx. doi. org/10. 1128/JVI. 00589-09.
19. Kattenhorn LM, Korbel GA, Kessler BM, Spooner E, Ploegh HL. 2005. A deubiquitinating enzyme encoded by HSV-1 belongs to a family of cysteine proteases that is conserved across the family Herpesviridae. Mol. Cell 19:547-557. http://dx. doi. org/10. 1016/j. molcel. 2005. 07. 003.
20. Bottcher S, Maresch C, Granzow H, Klupp BG, Teifke JP, Mettenleiter TC. 2008. Mutagenesis of the active-site cysteine in the ubiquitin-specific protease contained in large tegument protein pUL36 of pseudorabies virus impairs viral replication in vitro and neuroinvasion in vivo. J. Virol. 82: 6009-6016. http://dx. doi. org/10. 1128/JVI. 00280-08.
21. Gredmark-Russ S, Isaacson MK, Kattenhorn L, Cheung EJ, Watson N, Ploegh HL. 2009. A gammaherpesvirus ubiquitin-specific protease is involved in the establishment of murine gammaherpesvirus 68 infection. J. Virol. 83:10644-10652. http://dx. doi. org/10. 1128/JVI. 01017-09.
22. Kim ET, Oh SE, Lee YO, Gibson W, Ahn JH. 2009. Cleavage specificity of the UL48 deubiquitinating protease activity of human cytomegalovirus and the growth of an active-site mutant virus in cultured cells. J. Virol. 83:12046-12056. http://dx. doi. org/10. 1128/JVI. 00411-09.
23. Wang J, Loveland AN, Kattenhorn LM, Ploegh HL, Gibson W. 2006. High-molecular-weight protein (pUL48) of human cytomegalovirus is a competent deubiquitinating protease: mutant viruses altered in its activesite cysteine or histidine are viable. J. Virol. 80:6003-6012. http://dx. doi. org/10. 1128/JVI. 00401-06.
24. Saito S, Murata T, Kanda T, Isomura H, Narita Y, Sugimoto A, Kawashima D, Tsurumi T. 2013. Epstein-Barr virus deubiquitinase downregulates TRAF6-mediated NF-kappaB signaling during productive replication. J. Virol. 87:4060-4070. http://dx. doi. org/10. 1128/JVI. 02020-12.
25. Ernst R, Claessen JH, Mueller B, Sanyal S, Spooner E, van der Veen AG, Kirak O, Schlieker CD, Weihofen WA, Ploegh HL. 2011. Enzymatic blockade of the ubiquitin-proteasome pathway. PLoS Biol. 8:e1000605. http://dx. doi. org/10. 1371/journal. pbio. 1000605.
26. Whitehurst CB, Vaziri C, Shackelford J, Pagano JS. 2012. Epstein-Barr virus BPLF1 deubiquitinates PCNA and attenuates polymerase eta recruitment to DNA damage sites. J. Virol. 86:8097-8106. http://dx. doi. org/10. 1128/JVI. 00588-12.
27. Inn KS, Lee SH, Rathbun JY, Wong LY, Toth Z, Machida K, Ou JH, Jung JU. 2011. Inhibition of RIG-I-mediated signaling by Kaposi's sarcoma-associated herpesvirus-encoded deubiquitinase ORF64. J. Virol. 85: 10899-10904. http://dx. doi. org/10. 1128/JVI. 00690-11.
28. Gastaldello S, Callegari S, Coppotelli G, Hildebrand S, Song M, Masucci MG. 2012. Herpes virus deneddylases interrupt the cullin-RING ligase neddylation cycle by inhibiting the binding of CAND1. J. Mol. Cell Biol. 4:242-251. http://dx. doi. org/10. 1093/jmcb/mjs012.
29. Rooney CM, Rowe DT, Ragot T, Farrell PJ. 1989. The spliced BZLF1 gene of Epstein-Barr virus (EBV) transactivates an early EBV promoter and induces the virus productive cycle. J. Virol. 63:3109-3116.
30. Fixman ED, Hayward GS, Hayward SD. 1992. trans-acting requirements for replication of Epstein-Barr virus ori-Lyt. J. Virol. 66:5030-5039.
31. Cho MS, Milman G, Hayward SD. 1985. A second Epstein-Barr virus early antigen gene in BamHI fragment M encodes a 48-to 50-kilodalton nuclear protein. J. Virol. 56:860-866.
32. Li JS, Zhou BS, Dutschman GE, Grill SP, Tan RS, Cheng YC. 1987. Association of Epstein-Barr virus early antigen diffuse component and virus-specified DNA polymerase activity. J. Virol. 61:2947-2949.
33. Tsurumi T, Daikoku T, Kurachi R, Nishiyama Y. 1993. Functional interaction between Epstein-Barr virusDNApolymerase catalytic subunit and its accessory subunit in vitro. J. Virol. 67:7648-7653.
34. Tsurumi T, Daikoku T, Nishiyama Y. 1994. Further characterization of the interaction between the Epstein-Barr virus DNA polymerase catalytic subunit and its accessory subunit with regard to the 3'-to-5' exonucleolytic activity and stability of initiation complex at primer terminus. J. Virol. 68:3354-3363.
35. Daikoku T, Yamashita Y, Tsurumi T, Nishiyama Y. 1995. The US3 protein kinase of herpes simplex virus type 2 is associated with phosphorylation of the UL12 alkaline nuclease in vitro. Arch. Virol. 140:1637-1644. http://dx. doi. org/10. 1007/BF01322537.
36. Fixman ED, Hayward GS, Hayward SD. 1995. Replication of Epstein-Barr virus oriLyt: lack of a dedicated virally encoded origin-binding protein and dependence on Zta in cotransfection assays. J. Virol. 69:2998-3006.
37. Kawashima D, Kanda T, Murata T, Saito S, Sugimoto A, Narita Y, Tsurumi T. 2013. Nuclear transport of Epstein-Barr virus DNA polymerase is dependent on the BMRF1 polymerase processivity factor and molecular chaperone Hsp90. J. Virol. 87:6482-6491. http://dx. doi. org/10. 1128/JVI. 03428-12.
38. Kudoh A, Iwahori S, Sato Y, Nakayama S, Isomura H, Murata T, Tsurumi T. 2009. Homologous recombinational repair factors are recruited and loaded onto the viral DNA genome in Epstein-Barr virus replication compartments. J. Virol. 83:6641-6651. http://dx. doi. org/10. 1128/JVI. 00049-09.
39. Daikoku T, Kudoh A, Sugaya Y, Iwahori S, Shirata N, Isomura H, Tsurumi T. 2006. Postreplicative mismatch repair factors are recruited to Epstein-Barr virus replication compartments. J. Biol. Chem. 281:11422-11430. http://dx. doi. org/10. 1074/jbc. M510314200.
40. 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. USA. 102:5844-5849. http://dx. doi. org/10. 1073/pnas. 0501916102.
41. Luo MH, Rosenke K, Czornak K, Fortunato EA. 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. http://dx. doi. org/10. 1128/JVI. 01670-06.
42. 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. http://dx. doi. org/10. 1074/jbc. M500976200.
43. 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. http://dx. doi. org/10. 1128/JVI. 78. 11. 5856-5866. 2004.
44. 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. http://dx. doi. org/10. 1242/jcs. 02981.
45. Sugimoto A, Kanda T, Yamashita Y, Murata T, Saito S, Kawashima D, Isomura H, Nishiyama Y, Tsurumi T. 2011. Spatiotemporally different DNArepair systems participate in Epstein-Barr virus genome maturation. J. Virol. 85:6127-6135. http://dx. doi. org/10. 1128/JVI. 00258-11.
46. Durando M, Tateishi S, Vaziri C. 2013. A non-catalytic role of DNA polymerase eta in recruiting Rad18 and promoting PCNA monoubiquitination at stalled replication forks. Nucleic Acids Res. 41:3079-3093. http://dx. doi. org/10. 1093/nar/gkt016.
47. Masuda Y, Suzuki M, Kawai H, Hishiki A, Hashimoto H, Masutani C, Hishida T, Suzuki F, Kamiya K. 2012. En bloc transfer of polyubiquitin chains to PCNA in vitro is mediated by two different human E2-E3 pairs. Nucleic Acids Res. 40:10394-10407. http://dx. doi. org/10. 1093/nar/gks763.
48. Hibbert RG, Huang A, Boelens R, Sixma TK. 2011. E3 ligase Rad18 promotes monoubiquitination rather than ubiquitin chain formation by E2 enzyme Rad6. Proc. Natl. Acad. Sci. USA. 108:5590-5595. http://dx. doi. org/10. 1073/pnas. 1017516108.
49. Williams SA, Longerich S, Sung P, Vaziri C, Kupfer GM. 2011. The E3 ubiquitin ligase RAD18 regulates ubiquitylation and chromatin loading of FANCD2 and FANCI. Blood 117:5078-5087. http://dx. doi. org/10. 1182/blood-2010-10-311761.
50. Geng L, Huntoon CJ, Karnitz LM. 2010. RAD18-mediated ubiquitination of PCNA activates the Fanconi anemia DNA repair network. J. Cell Biol. 191:249-257. http://dx. doi. org/10. 1083/jcb. 201005101.
51. Masuda Y, Suzuki M, Kawai H, Suzuki F, Kamiya K. 2012. Asymmetric nature of two subunits of RAD18, a RING-type ubiquitin ligase E3, in the human RAD6A-RAD18 ternary complex. Nucleic Acids Res. 40:1065-1076. http://dx. doi. org/10. 1093/nar/gkr805.
52. Notenboom V, Hibbert RG, van Rossum-Fikkert SE, Olsen JV, Mann M, Sixma TK. 2007. Functional characterization of Rad18 domains for Rad6, ubiquitin, DNA binding and PCNA modification. Nucleic Acids Res. 35:5819-5830. http://dx. doi. org/10. 1093/nar/gkm615.
53. Delecluse HJ, Hilsendegen T, Pich D, Zeidler R, Hammerschmidt W. 1998. Propagation and recovery of intact, infectious Epstein-Barr virus from prokaryotic to human cells. Proc. Natl. Acad. Sci. USA. 95:8245-8250. http://dx. doi. org/10. 1073/pnas. 95. 14. 8245.
54. Yang Y, Durando M, Smith-Roe SL, Sproul C, Greenwalt AM, Kaufmann W, Oh S, Hendrickson EA, Vaziri C. 2013. Cell cycle stage-specific roles of Rad18 in tolerance and repair of oxidative DNA damage. Nucleic Acids Res. 41:2296-2312. http://dx. doi. org/10. 1093/nar/gks1325.
55. Day TA, Palle K, Barkley LR, Kakusho N, Zou Y, Tateishi S, Verreault A, Masai H, Vaziri C. 2010. Phosphorylated Rad18 directs DNA polymerase eta to sites of stalled replication. J. Cell Biol. 191:953-966. http://dx. doi. org/10. 1083/jcb. 201006043.
56. Palle K, Vaziri C. 2011. Rad18 E3 ubiquitin ligase activity mediates Fanconi anemia pathway activation and cell survival following DNA topoisomerase 1 inhibition. Cell Cycle 10:1625-1638. http://dx. doi. org/10. 4161/cc. 10. 10. 15617.
57. Zlatanou A, Despras E, Braz-Petta T, Boubakour-Azzouz I, Pouvelle C, Stewart GS, Nakajima S, Yasui A, Ishchenko AA, Kannouche PL. 2011. The hMsh2-hMsh6 complex acts in concert with monoubiquitinated PCNA and Pol eta in response to oxidative DNA damage in human cells. Mol. Cell 43:649-662. http://dx. doi. org/10. 1016/j. molcel. 2011. 06. 023.
58. Bailly V, Lauder S, Prakash S, Prakash L. 1997. Yeast DNA repair proteins Rad6 and Rad18 form a heterodimer that has ubiquitin conjugating, DNA binding, and ATP hydrolytic activities. J. Biol. Chem. 272: 23360-23365. http://dx. doi. org/10. 1074/jbc. 272. 37. 23360.
59. Inagaki A, van Cappellen WA, van der Laan R, Houtsmuller AB, Hoeijmakers JH, Grootegoed JA, Baarends WM. 2009. Dynamic localization of human RAD18 during the cell cycle and a functional connection with DNA double-strand break repair. DNA Repair (Amst.) 8:190-201. http://dx. doi. org/10. 1016/j. dnarep. 2008. 10. 008.
60. Masuyama S, Tateishi S, Yomogida K, Nishimune Y, Suzuki K, Sakuraba Y, Inoue H, Ogawa M, Yamaizumi M. 2005. Regulated expression and dynamic changes in subnuclear localization of mammalian Rad18 under normal and genotoxic conditions. Genes Cells 10:753-762. http://dx. doi. org/10. 1111/j. 1365-2443. 2005. 00874. x.
61. Miyase S, Tateishi S, Watanabe K, Tomita K, Suzuki K, Inoue H, Yamaizumi M. 2005. Differential regulation of Rad18 through Rad6-dependent mono-and polyubiquitination. J. Biol. Chem. 280:515-524. http://dx. doi. org/10. 1074/jbc. M409219200.
62. Hong GK, Delecluse HJ, Gruffat H, Morrison TE, Feng WH, Sergeant A, Kenney SC. 2004. The BRRF1 early gene of Epstein-Barr virus encodes a transcription factor that enhances induction of lytic infection by BRLF1. J. Virol. 78:4983-4992. http://dx. doi. org/10. 1128/JVI. 78. 10. 4983-4992. 2004.
63. Hagemeier SR, Barlow EA, Meng Q, Kenney SC. 2012. The cellular ataxia telangiectasia-mutated kinase promotes Epstein-Barr virus lytic reactivation in response to multiple different types of lytic reactivationinducing stimuli. J. Virol. 86:13360-13370. http://dx. doi. org/10. 1128/JVI. 01850-12.
64. Kudoh A, Fujita M, Zhang L, Shirata N, Daikoku T, Sugaya Y, Isomura H, Nishiyama Y, Tsurumi T. 2005. Epstein-Barr virus lytic replication elicits ATM checkpoint signal transduction while providing an S-phaselike cellular environment. J. Biol. Chem. 280:8156-8163. http://dx. doi. org/10. 1074/jbc. M411405200.
65. Roest HP, Baarends WM, de Wit J, van Klaveren JW, Wassenaar E, Hoogerbrugge JW, van Cappellen WA, Hoeijmakers JH, Grootegoed JA. 2004. The ubiquitin-conjugating DNA repair enzyme HR6A is a maternal factor essential for early embryonic development in mice. Mol. Cell. Biol. 24:5485-5495. http://dx. doi. org/10. 1128/MCB. 24. 12. 5485-5495. 2004.
66. Shekhar MP, Tait L, Gerard B. 2006. Essential role of T-cell factor/betacatenin in regulation of Rad6B: a potential mechanism for Rad6B overexpression in breast cancer cells. Mol. Cancer Res. 4:729-745. http://dx. doi. org/10. 1158/1541-7786. MCR-06-0136.
67. Jentsch S, McGrath JP, Varshavsky A. 1987. The yeast DNA repair gene RAD6 encodes a ubiquitin-conjugating enzyme. Nature 329:131-134. http://dx. doi. org/10. 1038/329131a0.
68. Sung P, Prakash S, Prakash L. 1988. The RAD6 protein of Saccharomyces cerevisiae polyubiquitinates histones, and its acidic domain mediates this activity. Genes Dev. 2:1476-1485. http://dx. doi. org/10. 1101/gad. 2. 11. 1476.
69. Shekhar MP, Gerard B, Pauley RJ, Williams BO, Tait L. 2008. Rad6B is a positive regulator of beta-catenin stabilization. Cancer Res. 68:1741-1750. http://dx. doi. org/10. 1158/0008-5472. CAN-07-2111.
70. Lyakhovich A, Shekhar MP. 2003. Supramolecular complex formation between Rad6 and proteins of the p53 pathway during DNA damageinduced response. Mol. Cell. Biol. 23:2463-2475. http://dx. doi. org/10. 1128/MCB. 23. 7. 2463-2475. 2003.
71. Varanasi L, Do PM, Goluszko E, Martinez LA. 2012. Rad18 is a transcriptional target of E2F3. Cell Cycle 11:1131-1141. http://dx. doi. org/10. 4161/cc. 11. 6. 19558.
72. Wu X, Yen L, Irwin L, Sweeney C, Carraway KL, III. 2004. Stabilization of the E3 ubiquitin ligase Nrdp1 by the deubiquitinating enzyme USP8. Mol. Cell. Biol. 24:7748-7757. http://dx. doi. org/10. 1128/MCB. 24. 17. 7748-7757. 2004.
73. Di Donato F, Chan EK, Askanase AD, Miranda-Carus M, Buyon JP. 2001. Interaction between 52 kDa SSA/Ro and deubiquitinating enzyme UnpEL: a clue to function. Int. J. Biochem. Cell Biol. 33:924-934. http://dx. doi. org/10. 1016/S1357-2725(01)00055-3.
74. Jensen DE, Proctor M, Marquis ST, Gardner HP, Ha SI, Chodosh LA, Ishov AM, Tommerup N, Vissing H, Sekido Y, Minna J, Borodovsky A, Schultz DC, Wilkinson KD, Maul GG, Barlev N, Berger SL, Prendergast GC, Rauscher FJ, III. 1998. BAP1: a novel ubiquitin hydrolase which binds to the BRCA1 RING finger and enhances BRCA1-mediated cell growth suppression. Oncogene 16:1097-1112. http://dx. doi. org/10. 1038/sj. onc. 1201861.
75. Soares L, Seroogy C, Skrenta H, Anandasabapathy N, Lovelace P, Chung CD, Engleman E, Fathman CG. 2004. Two isoforms of otubain 1 regulate T cell anergy via GRAIL. Nat. Immunol. 5:45-54. http://dx. doi. org/10. 1038/ni1017.
76. Feng WH, Israel B, Raab-Traub N, Busson P, Kenney SC. 2002. Chemotherapy induces lytic EBV replication and confers ganciclovir susceptibility to EBV-positive epithelial cell tumors. Cancer Res. 62:1920-1926. http://cancerres. aacrjournals. org/content/62/6/1920. long.
77. Westphal EM, Blackstock W, Feng W, Israel B, Kenney SC. 2000. Activation of lytic Epstein-Barr virus (EBV) infection by radiation and sodium butyrate in vitro and in vivo: a potential method for treating EBV-positive malignancies. Cancer Res. 60:5781-5788. http://cancerres. aacrjournals. org/content/60/20/5781. long.
78. Smith J, Tho LM, Xu N, Gillespie DA. 2010. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv. Cancer Res. 108:73-112. http://dx. doi. org/10. 1016/B978-0-12-380888-2. 00003-0.
79. Zhang XP, Liu F, Wang W. 2011. Two-phase dynamics of p53 in the DNA damage response. Proc. Natl. Acad. Sci. USA. 108:8990-8995. http://dx. doi. org/10. 1073/pnas. 1100600108.
80. Kulinski JM, Leonardo SM, Mounce BC, Malherbe L, Gauld SB, Tarakanova VL. 2012. Ataxia telangiectasia mutated kinase controls chronic gammaherpesvirus infection. J. Virol. 86:12826-12837. http://dx. doi. org/10. 1128/JVI. 00917-12.
81. Nikitin PA, Yan CM, Forte E, Bocedi A, Tourigny JP, White RE, Allday MJ, Patel A, Dave SS, Kim W, Hu K, Guo J, Tainter D, Rusyn E, Luftig MA. 2010. An ATM/Chk2-mediated DNA damage-responsive signaling pathway suppresses Epstein-Barr virus transformation of primary human B cells. Cell Host Microbe 8:510-522. http://dx. doi. org/10. 1016/j. chom. 2010. 11. 004.
82. Cai Q, Guo Y, Xiao B, Banerjee S, Saha A, Lu J, Glisovic T, Robertson ES. 2011. Epstein-Barr virus nuclear antigen 3C stabilizes Gemin3 to block p53-mediated apoptosis. PLoS Pathog. 7:e1002418. http://dx. doi. org/10. 1371/journal. ppat. 1002418.
83. Gruhne B, Sompallae R, Masucci MG. 2009. Three Epstein-Barr virus latency proteins independently promote genomic instability by inducing DNA damage, inhibiting DNA repair and inactivating cell cycle checkpoints. Oncogene 28:3997-4008. http://dx. doi. org/10. 1038/onc. 2009. 258.