Role of ATM in the formation of the replication compartment during lytic replication of Epstein-Barr virus in nasopharyngeal epithelial cells

Journal of Virology

Volumn 89, Issue 1, 2015, Pages 652-668

  Hau, Pok Man ^a,d   Deng, Wen ^a   Jia, Lin ^a   Yang, Jie ^a   Tsurumi, Tatsuya ^b   Chiang, Alan Kwok Shing ^a   Huen, Michael Shing Yan ^c   Tsao, Sai Wah ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b AICHI CANCER CENTER HOSPITAL   (Japan)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d Prince of Wales Hospital   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 6 (1 THIANTHRENYL) 4 PYRANONE; ATM PROTEIN; IMMEDIATE EARLY PROTEIN BZLF1; SERINE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SP1; VIRUS DNA; ATM PROTEIN, HUMAN; DNA LIGASE; SP1 PROTEIN, HUMAN;

ARTICLE; BZLF1 GENE; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; ENZYME INHIBITION; EPITHELIUM CELL; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; GENE SILENCING; NASOPHARYNGEAL EPITHELIUM CELL; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SP1 GENE; VIRION; VIROGENESIS; VIRUS REACTIVATION; VIRUS REPLICATION; ANTAGONISTS AND INHIBITORS; CELL LINE; DNA REPLICATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; VIROLOGY;

HERPESVIRIDAE; HUMAN HERPESVIRUS 4;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL LINE; DNA REPAIR ENZYMES; DNA REPLICATION; EPITHELIAL CELLS; GENE KNOCKDOWN TECHNIQUES; HERPESVIRUS 4, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SP1 TRANSCRIPTION FACTOR; VIRUS REPLICATION;

EID: 84919432512     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01437-14     Document Type: Article

References (68)

1. Damania B. 2004. Oncogenic gamma-herpesviruses: comparison of viral proteins involved in tumorigenesis. Nat Rev Microbiol 2:656-668. http://dx.doi.org/10.1038/nrmicro958.
2. Tsao SW, Tsang CM, To KF, Lo KW. 24 September 2014. The role of Epstein-Barr virus in epithelial malignancies. J Pathol http://dx.doi.org/10.1002/path.4448.
3. Young LS, Rickinson AB. 2004. Epstein-Barr virus: 40 years on. Nat Rev Cancer 4:757-768. http://dx.doi.org/10.1038/nrc1452.
4. Hawkins JB, Delgado-Eckert E, Thorley-Lawson DA, Shapiro M. 2013. The cycle of EBV infection explains persistence, the sizes of the infected cell populations and which come under CTL regulation. PLoS Pathog 9:e1003685. http://dx.doi.org/10.1371/journal.ppat.1003685.
5. Chaudhuri B, Xu H, Todorov I, Dutta A, Yates JL. 2001. Human DNA replication initiation factors, ORC and MCM, associate with oriP of Epstein-Barr virus. Proc Natl Acad Sci USA 98:10085-10089. http://dx.doi.org/10.1073/pnas.181347998.
6. Schepers A, Ritzi M, Bousset K, Kremmer E, Yates JL, Harwood J, Diffley JF, Hammerschmidt W. 2001. Human origin recognition complex binds to the region of the latent origin of DNA replication of Epstein-Barr virus. EMBO J 20:4588-4602. http://dx.doi.org/10.1093/emboj/20.16.4588.
7. Hammerschmidt W, Sugden B. 1988. Identification and characterization of oriLyt, a lytic origin of DNA replication of Epstein-Barr virus. Cell 55:427-433. http://dx.doi.org/10.1016/0092-8674(88)90028-1.
8. Sato H, Takimoto T, Tanaka S, Tanaka J, Raab-Traub N. 1990. Concatameric replication of Epstein-Barr virus: structure of the termini in virus-producer and newly transformed cell lines. J Virol 64:5295-5300.
9. Fixman ED, Hayward GS, Hayward SD. 1992. trans-Acting requirements for replication of Epstein-Barr virus ori-Lyt. J Virol 66:5030-5039.
10. 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.
11. Yokoyama N, Fujii K, Hirata M, Tamai K, Kiyono T, Kuzushima K, Nishiyama Y, Fujita M, Tsurumi T. 1999. Assembly of the Epstein-Barr virus BBLF4, BSLF1 and BBLF2/3 proteins and their interactive properties. J Gen Virol 80:2879-2887.
12. 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 fingerDNAbinding protein ZBRK1 and the KAP-1 corepressor. J Virol 79:245-256. http://dx.doi.org/10.1128/JVI.79.1.245-256.2005.
13. 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.
14. Schepers A, Pich D, Hammerschmidt W. 1993. A transcription factor with homology to the AP-1 family links RNA transcription and DNA replication in the lytic cycle of Epstein-Barr virus. EMBO J 12:3921-3929.
15. El-Guindy A, Heston L, Miller G. 2010. A subset of replication proteins enhances origin recognition and lytic replication by the Epstein-Barr virus ZEBRA protein. PLoS Pathog 6:e1001054. http://dx.doi.org/10.1371/journal.ppat.1001054.
16. Le Roux F, Sergeant A, Corbo L. 1996. Epstein-Barr virus (EBV) EB1/Zta protein provided in trans and competent for the activation of productive cycle genes does not activate the BZLF1 gene in the EBV genome. J Gen Virol 77:501-509. http://dx.doi.org/10.1099/0022-1317-77-3-501.
17. Baumann M, Feederle R, Kremmer E, Hammerschmidt W. 1999. Cellular transcription factors recruit viral replication proteins to activate the Epstein-Barr virus origin of lytic DNA replication, oriLyt. EMBO J 18: 6095-6105. http://dx.doi.org/10.1093/emboj/18.21.6095.
18. Li R, Zhu J, Xie Z, Liao G, Liu J, Chen MR, Hu S, Woodard C, Lin J, Taverna SD, Desai P, Ambinder RF, Hayward GS, Qian J, Zhu H, Hayward SD. 2011. Conserved herpesvirus kinases target the DNA damage response pathway and TIP60 histone acetyltransferase to promote virus replication. Cell Host Microbe 10:390-400. http://dx.doi.org/10.1016/j.chom.2011.08.013.
19. Schwartz RA, Carson CT, Schuberth C, Weitzman MD. 2009. Adenoassociated virus replication induces a DNA damage response coordinated by DNA-dependent protein kinase. J Virol 83:6269-6278. http://dx.doi.org/10.1128/JVI.00318-09.
20. 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.
21. Simoes M, Martins C, Ferreira F. 2013. Host DNA damage response facilitates African swine fever virus infection. Vet Microbiol 165:140-147. http://dx.doi.org/10.1016/j.vetmic.2013.01.007.
22. 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.
23. Shiloh Y, Ziv Y. 2013. The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat Rev Mol Cell Biol 14:197-210. http://dx.doi.org/10.1038/nrm3546.
24. Tsang SH, Wang X, Li J, Buck CB, You J. 2014. Host DNA damage response factors localize to merkel cell polyomavirus DNA replication sites to support efficient viralDNAreplication. J Virol 88:3285-3297. http://dx.doi.org/10.1128/JVI.03656-13.
25. Moody CA, Laimins LA. 2009. Human papillomaviruses activate the ATM DNA damage pathway for viral genome amplification upon differentiation. PLoS Pathog 5:e1000605. http://dx.doi.org/10.1371/journal.ppat.1000605.
26. 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.
27. Sinclair A, Yarranton S, Schelcher C. 2006. DNA-damage response pathways triggered by viral replication. Expert Rev Mol Med 8:1-11. http://dx.doi.org/10.1017/S1462399406010544.
28. Ariumi Y, Turelli P, Masutani M, Trono D. 2005. DNA damage sensors ATM, ATR, DNA-PKcs, and PARP-1 are dispensable for human immunodeficiency virus type 1 integration. J Virol 79:2973-2978. http://dx.doi.org/10.1128/JVI.79.5.2973-2978.2005.
29. 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.
30. 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.
31. Tarakanova VL, Leung-Pineda V, Hwang S, Yang CW, Matatall K, Basson M, Sun R, Piwnica-Worms H, Sleckman BP, Virgin HWT. 2007. Gamma-herpesvirus kinase actively initiates a DNA damage response by inducing phosphorylation of H2AX to foster viral replication. Cell Host Microbe 1:275-286. http://dx.doi.org/10.1016/j.chom.2007.05.008.
32. 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.
33. Kanda T, Yajima M, Ahsan N, Tanaka M, Takada K. 2004. Production of high-titer Epstein-Barr virus recombinants derived from Akata cells by using a bacterial artificial chromosome system. J Virol 78:7004-7015. http://dx.doi.org/10.1128/JVI.78.13.7004-7015.2004.
34. Ma BB, Lui VW, Cheung CS, Lau CP, Ho K, Hui EP, Tsui SK, Ng MH, Cheng SH, Ng PK, Tsao SW, Chan AT. 2013. Activity of the MEK inhibitor selumetinib (AZD6244; ARRY-142886) in nasopharyngeal cancer cell lines. Invest New Drugs 31:30-38. http://dx.doi.org/10.1007/s10637-012-9828-4.
35. Hui KF, Lam BH, Ho DN, Tsao SW, Chiang AK. 2013. Bortezomib and SAHA synergistically induce ROS-driven caspase-dependent apoptosis of nasopharyngeal carcinoma and block replication of Epstein-Barr virus. Mol Cancer Ther 12:747-758. http://dx.doi.org/10.1158/1535-7163.MCT-12-0811.
36. Di Renzo L, Avila-Carino J, Klein E. 1993. Induction of the lytic viral cycle in Epstein Barr virus carrying Burkitt lymphoma lines is accompanied by increased expression of major histocompatibility complex molecules. Immunol Lett 38:207-214. http://dx.doi.org/10.1016/0165-2478(93)90008-P.
37. Countryman JK, Gradoville L, Miller G. 2008. Histone hyperacetylation occurs on promoters of lytic cycle regulatory genes in Epstein-Barr virusinfected cell lines which are refractory to disruption of latency by histone deacetylase inhibitors. J Virol 82:4706-4719. http://dx.doi.org/10.1128/JVI.00116-08.
38. Baumann M, Mischak H, Dammeier S, Kolch W, Gires O, Pich D, Zeidler R, Delecluse HJ, Hammerschmidt W. 1998. Activation of the Epstein-Barr virus transcription factor BZLF1 by 12-O-tetradecanoylphorbol-13-acetate-induced phosphorylation. J Virol 72:8105-8114.
39. Li X, Lee YK, Jeng JC, Yen Y, Schultz DC, Shih HM, Ann DK. 2007. Role for KAP1 serine 824 phosphorylation and sumoylation/desumoylation switch in regulating KAP1-mediated transcriptional repression. J Biol Chem 282:36177-36189. http://dx.doi.org/10.1074/jbc.M706912200.
40. Li X, Lin HH, Chen H, Xu X, Shih HM, Ann DK. 2010. SUMOylation of the transcriptional co-repressor KAP1 is regulated by the serine and threonine phosphatase PP1. Sci Signal 3:ra32. http://dx.doi.org/10.1126/scisignal.2000781.
41. Ziv Y, Bielopolski D, Galanty Y, Lukas C, Taya Y, Schultz DC, Lukas J, Bekker-Jensen S, Bartek J, Shiloh Y. 2006. Chromatin relaxation in response toDNAdouble-strand breaks is modulated by a novel ATM-and KAP-1 dependent pathway. Nat Cell Biol 8:870-876. http://dx.doi.org/10.1038/ncb1446.
42. Burma S, Chen BP, Murphy M, Kurimasa A, Chen DJ. 2001. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 276:42462-42467. http://dx.doi.org/10.1074/jbc.C100466200.
43. Tempera I, Lieberman PM. 2010. Chromatin organization of gammaherpesvirus latent genomes. Biochim Biophys Acta 1799:236-245. http://dx.doi.org/10.1016/j.bbagrm.2009.10.004.
44. Hickson I, Zhao Y, Richardson CJ, Green SJ, Martin NM, Orr AI, Reaper PM, Jackson SP, Curtin NJ, Smith GC. 2004. Identification and characterization of a novel and specific inhibitor of the ataxiatelangiectasia mutated kinase ATM. Cancer Res 64:9152-9159. http://dx.doi.org/10.1158/0008-5472.CAN-04-2727.
45. Gruffat H, Renner O, Pich D, Hammerschmidt W. 1995. Cellular proteins bind to the downstream component of the lytic origin of DNA replication of Epstein-Barr virus. J Virol 69:1878-1886.
46. Lieberman PM, Hardwick JM, Sample J, Hayward GS, Hayward SD. 1990. The zta transactivator involved in induction of lytic cycle gene expression in Epstein-Barr virus-infected lymphocytes binds to both AP-1 and ZRE sites in target promoter and enhancer regions. J Virol 64:1143-1155.
47. Liu P, Liu S, Speck SH. 1998. Identification of a negative cis element within the ZII domain of the Epstein-Barr virus lytic switch BZLF1 gene promoter. J Virol 72:8230-8239.
48. Ragoczy T, Miller G. 2001. Autostimulation of the Epstein-Barr virus BRLF1 promoter is mediated through consensus Sp1 and Sp3 binding sites. J Virol 75:5240-5251. http://dx.doi.org/10.1128/JVI.75.11.5240-5251.2001.
49. Tsai PF, Lin SJ, Weng PL, Tsai SC, Lin JH, Chou YC, Tsai CH. 2011. Interplay between PKCdelta and Sp1 on histone deacetylase inhibitormediated Epstein-Barr virus reactivation. J Virol 85:2373-2385. http://dx.doi.org/10.1128/JVI.01602-10.
50. Chua HH, Chiu HY, Lin SJ, Weng PL, Lin JH, Wu SW, Tsai SC, Tsai CH. 2012. p53 and Sp1 cooperate to regulate the expression of Epstein-Barr viral Zta protein. J Med Virol 84:1279-1288. http://dx.doi.org/10.1002/jmv.23316.
51. Olofsson BA, Kelly CM, Kim J, Hornsby SM, Azizkhan-Clifford J. 2007. Phosphorylation of Sp1 in response to DNA damage by ataxia telangiectasia-mutated kinase. Mol Cancer Res 5:1319-1330. http://dx.doi.org/10.1158/1541-7786.MCR-07-0374.
52. Beishline K, Kelly CM, Olofsson BA, Koduri S, Emrich J, Greenberg RA, Azizkhan-Clifford J. 2012. Sp1 facilitates DNA double-strand break repair through a nontranscriptional mechanism. Mol Cell Biol 32:3790-3799. http://dx.doi.org/10.1128/MCB.00049-12.
53. Bai L, Merchant JL. 2007. ATM phosphorylates ZBP-89 at Ser202 to potentiate p21waf1 induction by butyrate. Biochem Biophys Res Commun 359:817-821. http://dx.doi.org/10.1016/j.bbrc.2007.05.197.
54. Iwahori S, Shirata N, Kawaguchi Y, Weller SK, Sato Y, Kudoh A, Nakayama S, Isomura H, Tsurumi T. 2007. Enhanced phosphorylation of transcription factor sp1 in response to herpes simplex virus type 1 infection is dependent on the ataxia telangiectasia-mutated protein. J Virol 81:9653-9664. http://dx.doi.org/10.1128/JVI.00568-07.
55. Bailey SG, Verrall E, Schelcher C, Rhie A, Doherty AJ, Sinclair AJ. 2009. Functional interaction between Epstein-Barr virus replication protein Zta and host DNA damage response protein 53BP1. J Virol 83:11116-11122. http://dx.doi.org/10.1128/JVI.00512-09.
56. 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.
57. 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.
58. Liu S, Borras AM, Liu P, Suske G, Speck SH. 1997. Binding of the ubiquitous cellular transcription factors Sp1 and Sp3 to the ZI domains in the Epstein-Barr virus lytic switch BZLF1 gene promoter. Virology 228: 11-18. http://dx.doi.org/10.1006/viro.1996.8371.
59. Black AR, Black JD, Azizkhan-Clifford J. 2001. Sp1 and kruppel-like factor family of transcription factors in cell growth regulation and cancer. J Cell Physiol 188:143-160. http://dx.doi.org/10.1002/jcp.1111.
60. Zhang Q, Holley-Guthrie E, Ge JQ, Dorsky D, Kenney S. 1997. The Epstein-Barr virus (EBV) DNA polymerase accessory protein, BMRF1, activates the essential downstream component of the EBV oriLyt. Virology 230:22-34. http://dx.doi.org/10.1006/viro.1997.8470.
61. Liu P, Speck SH. 2003. Synergistic autoactivation of the Epstein-Barr virus immediate-early BRLF1 promoter by Rta and Zta. Virology 310: 199-206. http://dx.doi.org/10.1016/S0042-6822(03)00145-4.
62. Huang SY, Hsieh MJ, Chen CY, Chen YJ, Chen JY, Chen MR, Tsai CH, Lin SF, Hsu TY. 2012. Epstein-Barr virus Rta-mediated transactivation of p21 and 14-3-3sigma arrests cells at the G1/S transition by reducing cyclin E/CDK2 activity. J Gen Virol 93:139-149. http://dx.doi.org/10.1099/vir.0.034405-0.
63. Chua HH, Lee HH, Chang SS, Lu CC, Yeh TH, Hsu TY, Cheng TH, Cheng JT, Chen MR, Tsai CH. 2007. Role of the TSG101 gene in Epstein-Barr virus late gene transcription. J Virol 81:2459-2471. http://dx.doi.org/10.1128/JVI.02289-06.
64. Smith PR, Gao Y, Karran L, Jones MD, Snudden D, Griffin BE. 1993. Complex nature of the major viral polyadenylated transcripts in Epstein-Barr virus-associated tumors. J Virol 67:3217-3225.
65. Chang LK, Chung JY, Hong YR, Ichimura T, Nakao M, Liu ST. 2005. Activation of Sp1-mediated transcription by Rta of Epstein-Barr virus via an interaction with MCAF1. Nucleic Acids Res 33:6528-6539. http://dx.doi.org/10.1093/nar/gki956.
66. Iwahori S, Yasui Y, Kudoh A, Sato Y, Nakayama S, Murata T, Isomura H, Tsurumi T. 2008. Identification of phosphorylation sites on transcription factor Sp1 in response to DNA damage and its accumulation at damaged sites. Cell Signal 20:1795-1803. http://dx.doi.org/10.1016/j.cellsig.2008.06.007.
67. Chun RF, Semmes OJ, Neuveut C, Jeang KT. 1998. Modulation of Sp1 phosphorylation by human immunodeficiency virus type 1 Tat. J Virol 72:2615-2629.
68. Jackson SP, MacDonald JJ, Lees-Miller S, Tjian R. 1990. GC box binding induces phosphorylation of Sp1 by a DNA-dependent protein kinase. Cell 63:155-165. http://dx.doi.org/10.1016/0092-8674(90)90296-Q.