Epstein-Barr virus late gene transcription depends on the assembly of a virus-specific preinitiation complex

Journal of Virology

Volumn 88, Issue 21, 2014, Pages 12825-12838

  Aubry, Valentin ^a,b,c   Mure, Fabrice ^a,b,c   Mariamé, Bernard ^d   Deschamps, Thibaut ^a,b,c   Wyrwicz, Lucjan S ^e   Manet, Evelyne ^a,b,c   Gruffat, Henri ^a,b,c  

^a CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^b UNIVERSITÉ DE LYON   (France)

^c CNRS   (France)

^d UPS   (France)

^e INSTITUTE OF ONCOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

BCRF1 PROTEIN; PROTEIN; RNA POLYMERASE; TATA BINDING PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN; BCRF1 PROTEIN, HUMAN HERPESVIRUS 4; PROTEIN BINDING; RNA POLYMERASE II;

ALPHAHERPESVIRINAE; ARTICLE; BETAHERPESVIRINAE; CONTROLLED STUDY; DNA REPLICATION; EPSTEIN BARR VIRUS; GAMMAHERPESVIRINAE; GENE EXPRESSION; GENETIC TRANSCRIPTION; LATENT VIRUS INFECTION; NONHUMAN; OPEN READING FRAME; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; STRUCTURAL HOMOLOGY; VIRUS GENE; CELL LINE; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PHYSIOLOGY; TRANSCRIPTION INITIATION;

CELL LINE; HERPESVIRUS 4, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN BINDING; RNA POLYMERASE II; TRANSCRIPTION INITIATION, GENETIC; TRANSCRIPTION, GENETIC; VIRAL PROTEINS;

EID: 84907978881     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02139-14     Document Type: Article

References (45)

1. Rickinson AB, Kieff E. 2001. Epstein-Barr virus, p 2575-2627. In Knipe DM, Howley PM, Griffin DE, Martin MA, Lamb RA, Roizman B, Straus SE (ed), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
2. 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.
3. Laichalk LL, Thorley-Lawson DA. 2005. Terminal differentiation into plasma cells initiates the replicative cycle of Epstein-Barr virus in vivo. J. Virol. 79:1296-1307. http://dx.doi.org/10.1128/JVI.79.2.1296-1307.2005.
4. Chevallier-Greco A, Manet E, Chavrier P, Mosnier C, Daillie J, Sergeant A. 1986. Both Epstein-Barr virus (EBV) encoded trans-acting factors, EB1 and EB2, are required to activate transcription from an EBV early promoter. EMBO J. 5:3243-3249.
5. Hardwick JM, Lieberman PM, Hayward SD. 1988. A new Epstein-Barr virus transactivator, R, induces expression of a cytoplasmic early antigen. J. Virol. 62:2274-2284.
6. Feederle R, Kost M, Baumann M, Janz A, Drouet E, Hammerschmidt W, Delecluse HJ. 2000. The Epstein-Barr virus lytic program is controlled by the co-operative functions of two transactivators. EMBO J. 19:3080-3089 http://dx.doi.org/10.1093/emboj/19.12.3080.
7. Fixman ED, Hayward GS, Hayward SD. 1992. Trans-acting requirements for replication of Epstein-Barr virus ori-Lyt. J. Virol. 66:5030-5039.
8. 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.
9. Israel BF, Kenney SC. 2005. EBV lytic infection, p 571-611. In Robertson ES (ed), Epstein-Barr virus. Caister Academic Press, Norfolk, United Kingdom.
10. Serio TR, Kolman JL, Miller G. 1997. Late gene expression from the Epstein-Barr virus BcLF1 and BFRF3 promoters does not require DNA replication in cis. J. Virol. 71:8726-8734.
11. Amon W, Binne UK, Bryant H, Jenkins PJ, Karstegl CE, Farrell PJ. 2004 Lytic cycle gene regulation of Epstein-Barr virus. J. Virol. 78:13460-13469 http://dx.doi.org/10.1128/JVI.78.24.13460-13469.2004.
12. Chang PJ, Chang YS, Liu ST. 1998. Characterization of the BcLF1 promoter in Epstein-Barr virus. J. Gen. Virol. 79:2003-2006.
13. Homa FL, Otal TM, Glorioso JC, Levine M. 1986. Transcriptional control signals of a herpes simplex virus type 1 late (gamma 2) gene lie within bases-34 to +124 relative to the 5' terminus of the mRNA. Mol. Cell. Biol. 6:3652-3666.
14. Shapira M, Homa FL, Glorioso JC, Levine M. 1987. Regulation of the herpes simplex virus type 1 late (gamma 2) glycoproteinCgene: sequences between base pairs-34 to +29 control transient expression and responsiveness to transactivation by the products of the immediate early (alpha) 4 and 0 genes. Nucleic Acids Res. 15:3097-3111. http://dx.doi.org/10.1093 /nar/15.7.3097.
15. Wong-Ho E, Wu T-T, Davis ZH, Zhang B, Huang J, Gong H, Deng H, Liu F, Glaunsinger B, Sun R. 2014. Unconventional sequence requirement for viral late gene core promoters of murine gammaherpesvirus 68. J. Virol. 88:3411-3422. http://dx.doi.org/10.1128/JVI.01374-13.
16. Serio TR, Cahill N, Prout ME, Miller G. 1998. A functionally distinct TATA box required for late progression through the Epstein-Barr virus life cycle. J. Virol. 72:8338-8343.
17. Wyrwicz LS, Rychlewski L. 2007. Identification of herpes TATT-binding protein. Antiviral Res. 75:167-172. http://dx.doi.org/10.1016/j.antiviral.2007.03.002.
18. Gruffat H, Kadjouf F, Mariamé B, Manet E. 2012. The Epstein-Barr virus BcRF1 gene product is a TBP-like protein with an essential role in late gene expression. J. Virol. 86:6023-6032. http://dx.doi.org/10.1128/JVI.00159-12.
19. Isomura H, Stinski MF, Murata T, Yamashita Y, Kanda T, Toyokuni S, Tsurumi T. 2011. The human cytomegalovirus gene products essential for late viral gene expression assemble into pre-replication complexes before viral DNA replication. J. Virol. 85:6629-6644. http://dx.doi.org/10.1128 /JVI.00384-11.
20. Gruffat H, Manet E, Sergeant A. 2002. MEF2-mediated recruitment of class II HDAC at the EBV immediate early gene BZLF1 links latency and chromatin remodeling. EMBO Rep. 3:141-146. http://dx.doi.org/10.1093 /embo-reports/kvf031.
21. 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.
22. Feederle R, Bartlett EJ, Delecluse HJ. 2010. Epstein-Barr virus genetics: talking about the BAC generation. Herpesviridae 1:6. http://dx.doi.org/10.1186/2042-4280-1-6.
23. Hirt B. 1969. Replicating molecules of polyoma virus DNA. J. Mol. Biol. 40:141-144. http://dx.doi.org/10.1016/0022-2836(69)90302-7.
24. Batisse J, Manet E, Middeldorp J, Sergeant A, Gruffat H. 2005. Epstein-Barr virus mRNA export factor EB2 is essential for intranuclear capsid assembly and production of gp350. J. Virol. 79:14102-14111. http://dx.doi.org/10.1128/JVI.79.22.14102-14111.2005.
25. Juillard F, Bazot Q, Mure F, Tafforeau L, Macri C, Rabourdin-Combe C, Lotteau V, Manet E, Gruffat H. 2012. Epstein-Barr virus protein EB2 stimulates cytoplasmic mRNA accumulation by counteracting the deleterious effects of SRp20 on viral mRNAs. Nucleic Acids Res. 40:6834-6849. http://dx.doi.org/10.1093/nar/gks319.
26. Arumugaswami V, Wu TT, Martinez-Guzman D, Jia Q, Deng H, Reyes N, Sun R. 2006. ORF18 is a transfactor that is essential for late gene transcription of a gammaherpesvirus. J. Virol. 80:9730-9740. http://dx.doi.org/10.1128/JVI.00246-06.
27. Wu T-T, Park T, Kim H, Tran T, Tong L, Martinez-Guzman D, Reyes N, Deng H, Sun R. 2009. ORF30 and ORF34 are essential for expression of late genes in murine gammaherpesvirus 68. J. Virol. 83:2265-2273. http://dx.doi.org/10.1128/JVI.01785-08.
28. Wong E, Wu TT, Reyes N, Deng H, Sun R. 2007. Murine gammaherpesvirus 68 open reading frame 24 is required for late gene expression after DNA replication. J. Virol. 81:6761-6764. http://dx.doi.org/10.1128/JVI.02726-06.
29. 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.
30. Omoto S, Mocarski ES. 2013. Cytomegalovirus UL91 is essential for transcription of viral true late (γ2) genes. J. Virol. 87:8651-8664. http://dx.doi.org/10.1128/JVI.01052-13.
31. Omoto S, Mocarski ES. 2014. Transcription of true late (γ2) cytomegalovirus genes requires UL92 function that is conserved among beta-and gammaherpesviruses. J. Virol. 88:120-130. http://dx.doi.org/10.1128/JVI.02983-13.
32. Chapa TJ, Perng Y-C, French AR, Yu D. 2014. Murine cytomegalovirus protein pM92 is a conserved regulator of viral late gene expression. J. Virol. 88:131-142. http://dx.doi.org/10.1128/JVI.02684-13.
33. Perng YC, Qian Z, Fehr AR, Xuan B, Yu D. 2011. The human cytomegalovirus gene UL79 is required for the accumulation of late viral transcripts. J. Virol. 85:4841-4852. http://dx.doi.org/10.1128/JVI.02344-10.
34. Ohno S, Steer B, Sattler C, Adler H. 2012. ORF23 of murine gammaherpesvirus 68 is non-essential for in vitro and in vivo infection. J. Gen. Virol. 93:1076-1080. http://dx.doi.org/10.1099/vir.0.041129-0.
35. Gruffat H, Batisse J, Pich D, Neuhierl B, Manet E, Hammerschmidt W, Sergeant A. 2002. Epstein-Barr virus mRNA export factor EB2 is essential for production of infectious virus. J. Virol. 76:9635-9644. http://dx.doi.org/10.1128/JVI.76.19.9635-9644.2002.
36. Grondin B, DeLuca N. 2000. Herpes simplex virus type 1 ICP4 promotes transcription preinitiation complex formation by enhancing the binding of TFIID to DNA. J. Virol. 74:11504-11510. http://dx.doi.org/10.1128 /JVI.74.24.11504-11510.2000.
37. Wyrwicz LS, Rychlewski L. 2007. Fold recognition insights into function of herpes ICP4 protein. Acta Biochim. Pol. 54:551-559.
38. Ramasubramanyan S, Kanhere A, Osborn K, Flower K, Jenner RG, Sinclair AJ. 2012. Genome-wide analyses of Zta binding to the Epstein-Barr virus genome reveals interactions in both early and late lytic cycle and an epigenetic switch leading to an altered binding profile. J. Virol. 86: 12494-12502. http://dx.doi.org/10.1128/JVI.01705-12.
39. 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.
40. Sugimoto A, Sato Y, Kanda T, Murata T, Narita Y, Kawashima D, Kimura H, Tsurumi T. 2013. Different distributions of Epstein-Barr virus early and late gene transcripts within viral replication compartments. J. Virol. 87:6693-6699. http://dx.doi.org/10.1128/JVI.00219-13.
41. Cuevas-Bennett C, Shenk T. 2008. Dynamic histone H3 acetylation and methylation at human cytomegalovirus promoters during replication in fibroblasts. J. Virol. 82:9525-9536. http://dx.doi.org/10.1128/JVI.00946-08.
42. Chen H-S, Lu F, Lieberman PM. 2013. Epigenetic regulation of EBV and KSHV latency. Curr. Opin. Virol. 3:251-259. http://dx.doi.org/10.1016/j.coviro.2013.03.004.
43. Lieberman PM. 2013. Keeping it quiet: chromatin control of gammaherpesvirus latency. Nat. Rev. Microbiol. 11:863-875. http://dx.doi.org/10.1038/nrmicro3135.
44. Chiu Y-F, Sugden AU, Sugden B. 2013. Epstein-Barr viral productive amplification reprograms nuclear architecture, DNA replication, and histone deposition. Cell Host Microbe 14:607-618. http://dx.doi.org/10.1016/j.chom.2013.11.009.
45. Mocarski ES, Jr. 2007. Betaherpes viral genes and their functions, p 204-230 In Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, YamanishiK(ed), Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, United Kingdom.