Uracil DNA glycosylase BKRF3 contributes to Epstein-Barr virus DNA replication through physical interactions with proteins in viral DNA replication complex

Journal of Virology

Volumn 88, Issue 16, 2014, Pages 8883-8899

  Su, Mei Tzu ^a   Liu, I Hua ^a   Wu, Chia Wei ^a   Chang, Shu Ming ^a   Tsai, Ching Hwa ^a   Yang, Pei Wen ^a   Chuang, Yu Chia ^a   Lee, Chung Pei ^b   Chen, Mei Ru ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIPEI UNIVERSITY OF NURSING AND HEALTH SCIENCES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DNA POLYMERASE; GLUTATHIONE TRANSFERASE; LEUCINE; PROTEIN BALF5; PROTEIN BKRF3; PROTEIN BMRF1; PROTEIN RTA; PROTEIN UNG2; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; URACIL DNA GLYCOSIDASE; VIRUS DNA;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; DNA REPLICATION; DNA REPLICATION COMPLEX; DNA STRUCTURE; DNA SYNTHESIS; ENZYME ACTIVITY; EPSTEIN BARR VIRUS; GENETIC COMPLEMENTATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

CELL LINE; CELL LINE, TUMOR; CELL NUCLEUS; CYTOPLASM; DNA REPLICATION; DNA, VIRAL; DNA-BINDING PROTEINS; DNA-DIRECTED DNA POLYMERASE; EPSTEIN-BARR VIRUS INFECTIONS; GENOME, VIRAL; GLUTATHIONE TRANSFERASE; HEK293 CELLS; HELA CELLS; HERPESVIRUS 4, HUMAN; HUMANS; URACIL-DNA GLYCOSIDASE; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84904878498     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00950-14     Document Type: Article

References (69)

1. Longnecker R, Kieff E, Cohen J. 2013. Epstein-Barr virus, p 1898-1959. In Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Racaniello VR, Roizman B (ed), Fields virology, 6th ed, vol 2. Lippincott Williams & Wilkins, Philadelphia, PA.
2. 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.
3. El-Guindy A, Ghiassi-Nejad M, Golden S, Delecluse HJ, Miller G. 2013. Essential role of Rta in lytic DNA replication of Epstein-Barr virus. J. Virol. 87:208-223. http://dx.doi.org/10.1128/JVI.01995-12.
4. Lu CC, Huang HT, Wang JT, Slupphaug G, Li TK, Wu MC, Chen YC, Lee CP, Chen MR. 2007. Characterization of the uracil-DNA glycosylase activity of Epstein-Barr virus BKRF3 and its role in lytic viral DNA replication. J. Virol. 81:1195-1208. http://dx.doi.org/10.1128/JVI.01518-06.
5. Pearl LH. 2000. Structure and function in the uracil-DNA glycosylase superfamily. Mutat. Res. 460:165-181. http://dx.doi.org/10.1016/S0921-8777(00)00025-2.
6. Mi R, Dong L, Kaulgud T, Hackett KW, Dominy BN, Cao W. 2009. Insights from xanthine and uracil DNA glycosylase activities of bacterial and human SMUG1: switching SMUG1 to UDG. J. Mol. Biol. 385:761-778. http://dx.doi.org/10.1016/j.jmb.2008.09.038.
7. Yonekura S, Nakamura N, Yonei S, Zhang-Akiyama QM. 2009. Generation, biological consequences and repair mechanisms of cytosine deamination in DNA. J. Radiat. Res. 50:19-26. http://dx.doi.org/10.1269/jrr.08080.
8. Nilsen H, Otterlei M, Haug T, Solum K, Nagelhus TA, Skorpen F, Krokan HE. 1997. Nuclear and mitochondrial uracil-DNA glycosylases are generated by alternative splicing and transcription from different positions in the UNG gene. Nucleic Acids Res. 25:750-755. http://dx.doi.org/10.1093/nar/25.4.750.
9. Slupphaug G, Eftedal I, Kavli B, Bharati S, Helle NM, Haug T, Levine DW, Krokan HE. 1995. Properties of a recombinant human uracil-DNA glycosylase from the UNG gene and evidence that UNG encodes the major uracil-DNA glycosylase. Biochemistry 34:128-138. http://dx.doi.org/10.1021/bi00001a016.
10. Gadsden MH, McIntosh EM, Game JC, Wilson PJ, Haynes RH. 1993. dUTP pyrophosphatase is an essential enzyme in Saccharomyces cerevisiae. EMBO J. 12:4425-4431.
11. Lindahl T. 1974. An N-glycosidase from Escherichia coli that releases free uracil from DNA containing deaminated cytosine residues. Proc. Natl. Acad. Sci. U. S. A. 71:3649-3653. http://dx.doi.org/10.1073/pnas.71.9.3649.
12. Barnes DE, Lindahl T. 2004. Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu. Rev. Genet. 38:445-476. http://dx.doi.org/10.1146/annurev.genet.38.072902.092448.
13. Krokan HE, Drablos F, Slupphaug G. 2002. Uracil in DNA-occurrence, consequences and repair. Oncogene 21:8935-8948. http://dx.doi.org/10.1038/sj.onc.1205996.
14. Scharer OD, Jiricny J. 2001. Recent progress in the biology, chemistry and structural biology of DNA glycosylases. Bioessays 23:270-281. http://dx.doi.org/10.1002/1521-1878(200103)23:3<270::AID-BIES1037>3.0.CO; 2-J.
15. Pascucci B, Stucki M, Jonsson ZO, Dogliotti E, Hubscher U. 1999. Long patch base excision repair with purified human proteins. DNA ligase I as patch size mediator for DNA polymerases delta and epsilon. J. Biol. Chem. 274:33696-33702.
16. Otterlei M, Haug T, Nagelhus TA, Slupphaug G, Lindmo T, Krokan HE. 1998. Nuclear and mitochondrial splice forms of human uracil-DNA glycosylase contain a complex nuclear localisation signal and a strong classical mitochondrial localisation signal, respectively. Nucleic Acids Res. 26:4611-4617. http://dx.doi.org/10.1093/nar/26.20.4611.
17. Ko R, Bennett SE. 2005. Physical and functional interaction of human nuclear uracil-DNA glycosylase with proliferating cell nuclear antigen. DNA Rep. 4:1421-1431. http://dx.doi.org/10.1016/j.dnarep.2005.08.006.
18. Haug T, Skorpen F, Aas PA, Malm V, Skjelbred C, Krokan HE. 1998. Regulation of expression of nuclear and mitochondrial forms of human uracil-DNA glycosylase. Nucleic Acids Res. 26:1449-1457. http://dx.doi.org/10.1093/nar/26.6.1449.
19. Hagen L, Kavli B, Sousa MM, Torseth K, Liabakk NB, Sundheim O, Pena-Diaz J, Otterlei M, Horning O, Jensen ON, Krokan HE, Slupphaug G. 2008. Cell cycle-specific UNG2 phosphorylations regulate protein turnover, activity and association with RPA. EMBO J. 27:51-61. http://dx.doi.org/10.1038/sj.emboj.7601958.
20. Otterlei M, Warbrick E, Nagelhus TA, Haug T, Slupphaug G, Akbari M, Aas PA, Steinsbekk K, Bakke O, Krokan HE. 1999. Post-replicative base excision repair in replication foci. EMBO J. 18:3834-3844. http://dx.doi.org/10.1093/emboj/18.13.3834.
21. Akbari M, Solvang-Garten K, Hanssen-Bauer A, Lieske NV, Pettersen HS, Pettersen GK, Wilson DM, III, Krokan HE, Otterlei M. 2010. Direct interaction between XRCC1 and UNG2 facilitates rapid repair of uracil in DNA by XRCC1 complexes. DNA Rep. 9:785-795. http://dx.doi.org/10.1016/j.dnarep.2010.04.002.
22. Elder RT, Zhu X, Priet S, Chen M, Yu M, Navarro JM, Sire J, Zhao Y. 2003. A fission yeast homologue of the human uracil-DNA-glycosylase and their roles in causing DNA damage after overexpression. Biochem. Biophys. Res. Commun. 306:693-700. http://dx.doi.org/10.1016/S0006-291X(03)01036-2.
23. 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.
24. 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.
25. 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.
26. Ranneberg-Nilsen T, Bjoras M, Luna L, Slettebakk R, Dale HA, Seeberg E, Rollag H. 2006. Human cytomegalovirus infection modulates DNA base excision repair in fibroblast cells. Virology 348:389-397. http://dx.doi.org/10.1016/j.virol.2006.01.001.
27. Verma SC, Bajaj BG, Cai Q, Si H, Seelhammer T, Robertson ES. 2006. Latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus recruits uracil DNA glycosylase 2 at the terminal repeats and is important for latent persistence of the virus. J. Virol. 80:11178-11190. http://dx.doi.org/10.1128/JVI.01334-06.
28. Bogani F, Chua CN, Boehmer PE. 2009. Reconstitution of uracil DNA glycosylase-initiated base excision repair in herpes simplex virus-1. J. Biol. Chem. 284:16784-16790. http://dx.doi.org/10.1074/jbc.M109.010413.
29. Bogani F, Corredeira I, Fernandez V, Sattler U, Rutvisuttinunt W, Defais M, Boehmer PE. 2010. Association between the herpes simplex virus-1 DNA polymerase and uracil DNA glycosylase. J. Biol. Chem. 285: 27664-27672. http://dx.doi.org/10.1074/jbc.M110.131235.
30. Pyles RB, Thompson RL. 1994. Evidence that the herpes simplex virus type 1 uracil DNA glycosylase is required for efficient viral replication and latency in the murine nervous system. J. Virol. 68:4963-4972.
31. Prichard MN, Lawlor H, Duke GM, Mo C, Wang Z, Dixon M, Kemble G, Kern ER. 2005. Human cytomegalovirus uracil DNA glycosylase associates with ppUL44 and accelerates the accumulation of viral DNA. Virol. J. 2:55. http://dx.doi.org/10.1186/1743-422X-2-55.
32. Strang BL, Coen DM. 2010. Interaction of the human cytomegalovirus uracil DNA glycosylase UL114 with the viral DNA polymerase catalytic subunit UL54. J. Gen. Virol. 91:2029-2033. http://dx.doi.org/10.1099/vir.0.022160-0.
33. Ranneberg-Nilsen T, Dale HA, Luna L, Slettebakk R, Sundheim O, Rollag H, Bjoras M. 2008. Characterization of human cytomegalovirus uracil DNA glycosylase (UL114) and its interaction with polymerase processivity factor (UL44). J. Mol. Biol. 381:276-288. http://dx.doi.org/10.1016/j.jmb.2008.05.028.
34. Prichard MN, Duke GM, Mocarski ES. 1996. Human cytomegalovirus uracil DNA glycosylase is required for the normal temporal regulation of both DNA synthesis and viral replication. J. Virol. 70:3018-3025.
35. Courcelle CT, Courcelle J, Prichard MN, Mocarski ES. 2001. Requirement for uracil-DNA glycosylase during the transition to late-phase cytomegalovirus DNA replication. J. Virol. 75:7592-7601. http://dx.doi.org/10.1128/JVI.75.16.7592-7601.2001.
36. Reddy SM, Williams M, Cohen JI. 1998. Expression of a uracil DNA glycosylase (UNG) inhibitor in mammalian cells: varicella-zoster virus can replicate in vitro in the absence of detectable UNG activity. Virology 251:393-401. http://dx.doi.org/10.1006/viro.1998.9428.
37. Geoui T, Buisson M, Tarbouriech N, Burmeister WP. 2007. New insights on the role of the gamma-herpesvirus uracil-DNA glycosylase leucine loop revealed by the structure of the Epstein-Barr virus enzyme in complex with an inhibitor protein. J. Mol. Biol. 366:117-131. http://dx.doi.org/10.1016/j.jmb.2006.11.007.
38. Makarova O, Kamberov E, Margolis B. 2000. Generation of deletion and point mutations with one primer in a single cloning step. Biotechniques 29:970-972. http://www.biotechniques.com/multimedia/archive/00010/ 00295bm08_10062a.pdf.
39. Yang PW, Chang SS, Tsai CH, Chao YH, Chen MR. 2008. Effect of phosphorylation on the transactivation activity of Epstein-Barr virus BMRF1, a major target of the viral BGLF4 kinase. J. Gen. Virol. 89:884-895. http://dx.doi.org/10.1099/vir.0.83546-0.
40. Ragoczy T, Heston L, Miller G. 1998. The Epstein-Barr virus Rta protein activates lytic cycle genes and can disrupt latency in B lymphocytes. J. Virol. 72:7978-7984.
41. Gao Z, Krithivas A, Finan JE, Semmes OJ, Zhou S, Wang Y, Hayward SD. 1998. The Epstein-Barr virus lytic transactivator Zta interacts with the helicase-primase replication proteins. J. Virol. 72:8559-8567.
42. Chang Y, Tung CH, Huang YT, Lu J, Chen JY, Tsai CH. 1999. Requirement for cell-to-cell contact in Epstein-Barr virus infection of nasopharyngeal carcinoma cells and keratinocytes. J. Virol. 73:8857-8866.
43. Lin CT, Wong CI, Chan WY, Tzung KW, Ho JK, Hsu MM, Chuang SM. 1990. Establishment and characterization of two nasopharyngeal carcinoma cell lines. Lab. Investig. 62:713-724.
44. Chen YL, Chen YJ, Tsai WH, Ko YC, Chen JY, Lin SF. 2009. The Epstein-Barr virus replication and transcription activator, Rta/BRLF1, induces cellular senescence in epithelial cells. Cell Cycle 8:58-65. http://dx.doi.org/10.4161/cc.8.1.7411.
45. Lee CP, Huang YH, Lin SF, Chang Y, Chang YH, Takada K, Chen MR. 2008. Epstein-Barr virus BGLF4 kinase induces disassembly of the nuclear lamina to facilitate virion production. J. Virol. 82:11913-11926. http://dx.doi.org/10.1128/JVI.01100-08.
46. Chen C, Okayama H. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745-2752.
47. Chen MR, Chang SJ, Huang H, Chen JY. 2000. A protein kinase activity associated with Epstein-Barr virus BGLF4 phosphorylates the viral early antigen EA-D in vitro. J. Virol. 74:3093-3104. http://dx.doi.org/10.1128/JVI.74.7.3093-3104.2000.
48. Lee CP, Chen JY, Wang JT, Kimura K, Takemoto A, Lu CC, Chen MR. 2007. Epstein-Barr virus BGLF4 kinase induces premature chromosome condensation through activation of condensin and topoisomerase II. J. Virol. 81:5166-5180. http://dx.doi.org/10.1128/JVI.00120-07.
49. Zeng Y, Middeldorp J, Madjar JJ, Ooka T. 1997. A major DNA binding protein encoded by BALF2 open reading frame of Epstein-Barr virus (EBV) forms a complex with other EBV DNA-binding proteins: DNAase, EA-D, and DNA polymerase. Virology 239:285-295. http://dx.doi.org/10.1006/viro.1997.8891.
50. Evan GI, Lewis GK, Ramsay G, Bishop JM. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610-3616.
51. Lu CC, Wu CW, Chang SC, Chen TY, Hu CR, Yeh MY, Chen JY, Chen MR. 2004. Epstein-Barr virus nuclear antigen 1 is a DNA-binding protein with strong RNA-binding activity. J. Gen. Virol. 85:2755-2765. http://dx.doi.org/10.1099/vir.0.80239-0.
52. Jia Q, Wu TT, Liao HI, Chernishof V, Sun R. 2004. Murine gammaherpesvirus 68 open reading frame 31 is required for viral replication. J. Virol. 78:6610-6620. http://dx.doi.org/10.1128/JVI.78.12.6610-6620.2004.
53. Edelheit O, Hanukoglu A, Hanukoglu I. 2009. Simple and efficient site-directed mutagenesis using two single-primer reactions in parallel to generate mutants for protein structure-function studies. BMC Biotechnol. 9:61. http://dx.doi.org/10.1186/1472-6750-9-61.
54. 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. U. S. A. 95:8245-8250. http://dx.doi.org/10.1073/pnas.95.14.8245.
55. Smith GA, Enquist LW. 2000. A self-recombining bacterial artificial chromosome and its application for analysis of herpesvirus pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 97:4873-4878. http://dx.doi.org/10.1073/pnas.080502497.
56. Daikoku T, Kudoh A, Fujita M, Sugaya Y, Isomura H, Shirata N, Tsurumi T. 2005. Architecture of replication compartments formed during Epstein-Barr virus lytic replication. J. Virol. 79:3409-3418. http://dx.doi.org/10.1128/JVI.79.6.3409-3418.2005.
57. Fixman ED, Hayward GS, Hayward SD. 1992. Trans-acting requirements for replication of Epstein-Barr virus ori-Lyt. J. Virol. 66:5030-5039.
58. Park R, Heston L, Shedd D, Delecluse HJ, Miller G. 2008. Mutations of amino acids in the DNA-recognition domain of Epstein-Barr virus ZEBRA protein alter its sub-nuclear localization and affect formation of replication compartments. Virology 382:145-162. http://dx.doi.org/10.1016/j.virol.2008.09.009.
59. 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.
60. Roberts VA, Pique ME, Hsu S, Li S, Slupphaug G, Rambo RP, Jamison JW, Liu T, Lee JH, Tainer JA, Ten Eyck LF, Woods VL, Jr. 2012. Combining H/D exchange mass spectroscopy and computational docking reveals extended DNA-binding surface on uracil-DNA glycosylase. Nucleic Acids Res. 40:6070-6081. http://dx.doi.org/10.1093/nar/gks291.
61. Hardeland U, Kunz C, Focke F, Szadkowski M, Schar P. 2007. Cell cycle regulation as a mechanism for functional separation of the apparently redundant uracil DNA glycosylases TDG and UNG2. Nucleic Acids Res. 35:3859-3867. http://dx.doi.org/10.1093/nar/gkm337.
62. Guo Q, Qian L, Guo L, Shi M, Chen C, Lv X, Yu M, Hu M, Jiang G, Guo N. 2010. Transactivators Zta and Rta of Epstein-Barr virus promote G0/G1 to S transition in Raji cells: a novel relationship between lytic virus and cell cycle. Mol. Immunol. 47:1783-1792. http://dx.doi.org/10.1016/j.molimm.2010.02.017.
63. Chen YJ, Tsai WH, Chen YL, Ko YC, Chou SP, Chen JY, Lin SF. 2011. Epstein-Barr virus (EBV) Rta-mediated EBV and Kaposi's sarcoma associated herpesvirus lytic reactivations in 293 cells. PLoS One 6:e17809. http://dx.doi.org/10.1371/journal.pone.0017809.
64. Akbari M, Solvang-Garten K, Hanssen-Bauer A, Lieske NV, Pettersen HS, Pettersen GK, Wilson DM, III, Krokan HE, Otterlei M. 2010. Direct interaction between XRCC1 and UNG2 facilitates rapid repair of uracil in DNA by XRCC1 complexes. DNA Repair 9:785-795. http://dx.doi.org/10.1016/j.dnarep.2010.04.002.
65. Liao G, Huang J, Fixman ED, Hayward SD. 2005. The Epstein-Barr virus replication protein BBLF2/3 provides an origin-tethering function through interaction with the zinc finger DNA binding protein ZBRK1 and the KAP-1 corepressor. J. Virol. 79:245-256. http://dx.doi.org/10.1128/JVI.79.1.245-256.2005.
66. Song MJ, Hwang S, Wong WH, Wu TT, Lee S, Liao HI, Sun R. 2005. Identification of viral genes essential for replication of murine gammaherpesvirus 68 using signature-tagged mutagenesis. Proc. Natl. Acad. Sci. U. S. A. 102:3805-3810. http://dx.doi.org/10.1073/pnas.0404521102.
67. Chen CY, Mosbaugh DW, Bennett SE. 2005. Mutations at arginine 276 transform human uracil-DNA glycosylase into a single-stranded DNAspecific uracil-DNA glycosylase. DNA Repair 4:793-805. http://dx.doi.org/10.1016/j.dnarep.2005.04.019.
68. Calderwood MA, Venkatesan K, Xing L, Chase MR, Vazquez A, Holthaus AM, Ewence AE, Li N, Hirozane-Kishikawa T, Hill DE, Vidal M, Kieff E, Johannsen E. 2007. Epstein-Barr virus and virus human protein interaction maps. Proc. Natl. Acad. Sci. U. S. A. 104:7606-7611. http://dx.doi.org/10.1073/pnas.0702332104.
69. Gulbahce N, Yan H, Dricot A, Padi M, Byrdsong D, Franchi R, Lee DS, Rozenblatt-Rosen O, Mar JC, Calderwood MA, Baldwin A, Zhao B, Santhanam B, Braun P, Simonis N, Huh KW, Hellner K, Grace M, Chen A, Rubio R, Marto JA, Christakis NA, Kieff E, Roth FP, Roecklein-Canfield J, Decaprio JA, Cusick ME, Quackenbush J, Hill DE, Munger K, Vidal M, Barabasi AL. 2012. Viral perturbations of host networks reflect disease etiology. PLoS Comput. Biol. 8:e1002531. http://dx.doi.org/10.1371/journal.pcbi.1002531.