Genome-wide analysis of epstein-barr virus Rta DNA binding

Journal of Virology

Volumn 86, Issue 9, 2012, Pages 5151-5164

  Heilmann, Andreas M F ^a   Calderwood, Michael A ^a,c   Portal, Daniel ^a   Lu, Yong ^b   Johannsena, Eric ^a,d  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; LYSINE; MUTANT PROTEIN; PROTEIN BALF5; PROTEIN BFRF3; PROTEIN BLRF2; PROTEIN RTA; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA REPLICATION; EPSTEIN BARR VIRUS; GENE SEQUENCE; GENOME ANALYSIS; HUMAN; HUMAN CELL; MOLECULAR GENETICS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; QUANTITATIVE ANALYSIS; RTA RESPONSE ELEMENT; VIRUS GENE; VIRUS GENOME; VIRUS REPLICATION;

BINDING SITES; CELL LINE; DNA REPLICATION; DNA, VIRAL; DNA-BINDING PROTEINS; DNA-DIRECTED DNA POLYMERASE; GENOME, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; MUTATION; PROMOTER REGIONS, GENETIC; PROTEIN INTERACTION DOMAINS AND MOTIFS; RESPONSE ELEMENTS; TRANS-ACTIVATORS; VIRAL PROTEINS; VIRUS REPLICATION;

HUMAN HERPESVIRUS 4;

EID: 84861322312     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06760-11     Document Type: Article

References (77)

1. Adamson AL, et al. 2000. Epstein-Barr virus immediate-early proteins BZLF1 and BRLF1 activate the ATF2 transcription factor by increasing the levels of phosphorylated p38 and c-Jun N-terminal kinases. J. Virol. 74: 1224-1233.
2. Amon W, et al. 2004. Lytic cycle gene regulation of Epstein-Barr virus. J. Virol. 78:13460-13469.
3. Amon W, White RE, Farrell PJ. 2006. Epstein-Barr virus origin of lytic replication mediates association of replicating episomes with promyelocytic leukaemia protein nuclear bodies and replication compartments. J. Gen. Virol. 87:1133-1137.
4. Arumugaswami V, et al. 2006. ORF18 is a transfactor that is essential for late gene transcription of a gammaherpesvirus. J. Virol. 80:9730-9740.
5. Baer R, et al. 1984. DNA sequence and expression of the B95-8 Epstein-Barr virus genome. Nature 310:207-211.
6. Bhende PM, Seaman WT, Delecluse HJ, Kenney SC. 2004. The EBV lytic switch protein, Z, preferentially binds to and activates the methylated viral genome. Nat. Genet. 36:1099-1104.
7. Buisson M, et al. 1989. The Epstein-Barr virus (EBV) early protein EB2 is a posttranscriptional activator expressed under the control of EBV transcription factors EB1 and R. J. Virol. 63:5276-5284.
8. Calderwood MA, Holthaus AM, Johannsen E. 2008. The Epstein-Barr virus LF2 protein inhibits viral replication. J. Virol. 82:8509-8519.
9. Calderwood MA, et al. 2007. Epstein-Barr virus and virus human protein interaction maps. Proc. Natl. Acad. Sci. U. S. A. 104:7606-7611.
10. Chang LK, et al. 2005. Activation of Sp1-mediated transcription by Rta of Epstein-Barr virus via an interaction with MCAF1. Nucleic Acids Res. 33:6528-6539.
11. Chang LK, et al. 2004. Post-translational modification of Rta of Epstein-Barr virus by SUMO-1. J. Biol. Chem. 279:38803-38812.
12. Chang PJ, Shedd D, Miller G. 2005. Two subclasses of Kaposi's sarcomaassociated herpesvirus lytic cycle promoters distinguished by open reading frame 50 mutant proteins that are deficient in binding to DNA. J. Virol. 79:8750-8763.
13. Chen LW, Chang PJ, Delecluse HJ, Miller G. 2005. Marked variation in response of consensus binding elements for the Rta protein of Epstein-Barr virus. J. Virol. 79:9635-9650.
14. Chen LW, et al. 2009. Two phenylalanines in the C-terminus of Epstein-Barr virus Rta protein reciprocally modulate its DNA binding and transactivation function. Virology 386:448-461.
15. Cox MA, Leahy J, Hardwick JM. 1990. An enhancer within the divergent promoter of Epstein-Barr virus responds synergistically to the R and Z transactivators. J. Virol. 64:313-321.
16. Darr CD, Mauser A, Kenney S. 2001. Epstein-Barr virus immediate-early protein BRLF1 induces the lytic form of viral replication through a mechanism involving phosphatidylinositol-3 kinase activation. J. Virol. 75: 6135-6142.
17. 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.
18. El-Guindy AS, Miller G. 2004. Phosphorylation of Epstein-Barr virus ZEBRA protein at its casein kinase 2 sites mediates its ability to repress activation of a viral lytic cycle late gene by Rta. J. Virol. 78:7634-7644.
19. Farrell PJ. 2001. Epstein-Barr virus. The B95-8 strain map. Methods Mol. Biol. 174:3-12.
20. Farrell PJ, Rowe DT, Rooney CM, Kouzarides T. 1989. Epstein-Barr virus BZLF1 trans-activator specifically binds to a consensus AP-1 site and is related to c-fos. EMBO J. 8:127-132.
21. Feederle R, et al. 2000. The Epstein-Barr virus lytic program is controlled by the co-operative functions of two transactivators. EMBO J. 19:3080-3089.
22. 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.
23. Flemington E, Speck SH. 1990. Autoregulation of Epstein-Barr virus putative lytic switch gene BZLF1. J. Virol. 64:1227-1232.
24. Flemington EK, Borras AM, Lytle JP, Speck SH. 1992. Characterization of the Epstein-Barr virus BZLF1 protein transactivation domain. J. Virol. 66:922-929.
25. Furnari FB, Adams MD, Pagano JS. 1992. Regulation of the Epstein-Barr virus DNA polymerase gene. J. Virol. 66:2837-2845.
26. Granato M, et al. 2006. Regulation of the expression of the Epstein-Barr virus early gene BFRF1. Virology 347:109-116.
27. Gruffat H, et al. 1992. Characterization of an R-binding site mediating the R-induced activation of the Epstein-Barr virus BMLF1 promoter. J. Virol. 66:46-52.
28. Gruffat H, Manet E, Rigolet A, Sergeant A. 1990. The enhancer factor R of Epstein-Barr virus (EBV) is a sequence-specific DNA binding protein. Nucleic Acids Res. 18:6835-6843.
29. Gruffat H, Sergeant A. 1994. Characterization of the DNA-binding site repertoire for the Epstein-Barr virus transcription factor R. Nucleic Acids Res. 22:1172-1178.
30. Hammerschmidt W, Sugden B. 1988. Identification and characterization of oriLyt, a lytic origin of DNA replication of Epstein-Barr virus. Cell 55:427-433.
31. 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.
32. Hardwick JM, Tse L, Applegren N, Nicholas J, Veliuona MA. 1992. The Epstein-Barr virus R transactivator (Rta) contains a complex, potent activation domain with properties different from those of VP16. J. Virol. 66:5500-5508.
33. Heilmann AM, Calderwood MA, Johannsen E. 2010. Epstein-Barr virus LF2 protein regulates viral replication by altering Rta subcellular localization. J. Virol. 84:9920-9931.
34. Holland LE, Anderson KP, Shipman C, Jr, Wagner EK. 1980. Viral DNA synthesis is required for the efficient expression of specific herpes simplex virus type 1 mRNA species. Virology 101:10-24.
35. Holley-Guthrie EA, Quinlivan EB, Mar EC, Kenney S. 1990. The Epstein-Barr virus (EBV) BMRF1 promoter for early antigen (EA-D) is regulated by the EBV transactivators, BRLF1 and BZLF1, in a cell-specific manner. J. Virol. 64:3753-3759.
36. 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.
37. Honess RW, Roizman B. 1975. Regulation of herpesvirus macromolecular synthesis: sequential transition of polypeptide synthesis requires functional viral polypeptides. Proc. Natl. Acad. Sci. U. S. A. 72:1276-1280.
38. Honess RW, Watson DH. 1977. Herpes simplex virus resistance and sensitivity to phosphonoacetic acid. J. Virol. 21:584-600.
39. Hong GK, et al. 2005. Epstein-Barr virus lytic infection contributes to lymphoproliferative disease in a SCID mouse model. J. Virol. 79:13993-14003.
40. Hong Y, Qi J, Gong D, Han C, Deng H. 2011. Replication and transcription activator (RTA) of murine gammaherpesvirus 68 binds to an RTA-responsive element and activates the expression of ORF18. J. Virol. 85:11338-11350.
41. Hung CH, Liu ST. 1999. Characterization of the Epstein-Barr virus BALF2 promoter. J. Gen. Virol. 80:2747-2750.
42. Johannsen E, et al. 2004. Proteins of purified Epstein-Barr virus. Proc. Natl. Acad. Sci. U. S. A. 101:16286-16291.
43. Jones PC, Roizman B. 1979. Regulation of herpesvirus macromolecular synthesis. VIII. The transcription program consists of three phases during which both extent of transcription and accumulation of RNA in the cytoplasm are regulated. J. Virol. 31:299-314.
44. Kalla M, Schmeinck A, Bergbauer M, Pich D, Hammerschmidt W. 2010. AP-1 homolog BZLF1 of Epstein-Barr virus has two essential functions dependent on the epigenetic state of the viral genome. Proc. Natl. Acad. Sci. U. S. A. 107:850-855.
45. Kayhan B, et al. 2007. A replication-deficient murine gamma-herpesvirus blocked in late viral gene expression can establish latency and elicit protective cellular immunity. J. Immunol. 179:8392-8402.
46. Kenney S, Holley-Guthrie E, Mar EC, Smith M. 1989. The Epstein-Barr virus BMLF1 promoter contains an enhancer element that is responsive to the BZLF1 and BRLF1 transactivators. J. Virol. 63:3878-3883.
47. Kenney SC. 2007. Reactivation and lytic replication of EBV, p 403-433. In Arvin A, et al (ed), Human herpesviruses. Cambridge University Press, Cambridge, United Kingdom.
48. Kent WJ, et al. 2002. The human genome browser at UCSC. Genome Res. 12:996-1006.
49. Kharchenko PV, Tolstorukov MY, Park PJ. 2008. Design and analysis of ChIP-seq experiments for DNA-binding proteins. Nat. Biotechnol. 26: 1351-1359.
50. Kieff E, Rickinson AB. 2007. Epstein-Barr virus and its replication, In Knipe DM, et al (ed), Fields virology, 5th ed, vol 2, p 2602-2654. Lippincott Williams and Wilkins, Philadelphia, PA.
51. Kutok JL, Wang F. 2006. Spectrum of Epstein-Barr virus-associated diseases. Annu. Rev. Pathol. 1:375-404.
52. Lee YH, Chiu YF, Wang WH, Chang LK, Liu ST. 2008. Activation of the ERK signal transduction pathway by Epstein-Barr virus immediate-early protein Rta. J. Gen. Virol. 89:2437-2446.
53. Li H, Ruan J, Durbin R. 2008. Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res. 18:1851-1858.
54. 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.
55. Liu C, Sista ND, Pagano JS. 1996. Activation of the Epstein-Barr virus DNA polymerase promoter by the BRLF1 immediate-early protein is mediated through USF and E2F. J. Virol. 70:2545-2555.
56. Liu P, Speck SH. 2003. Synergistic autoactivation of the Epstein-Barr virus immediate-early BRLF1 promoter by Rta and Zta. Virology 310: 199-206.
57. Lu CC, et al. 2006. Genome-wide transcription program and expression of the Rta responsive gene of Epstein-Barr virus. Virology 345:358-372.
58. Ma SD, et al. 2011. A new model of Epstein-Barr virus infection reveals an important role for early lytic viral protein expression in the development of lymphomas. J. Virol. 85:165-177.
59. Manet E, et al. 1993. The acidic activation domain of the Epstein-Barr virus transcription factor R interacts in vitro with both TBP and TFIIB and is cellspecifically potentiated by a proline-rich region. Gene Expr. 3:49-59.
60. Manet E, Rigolet A, Gruffat H, Giot JF, Sergeant A. 1991. Domains of the Epstein-Barr virus (EBV) transcription factor R required for dimerization, DNA binding and activation. Nucleic Acids Res. 19:2661-2667.
61. Miller IG, Jr, El-Guindy A. 2002. Regulation of Epstein-Barr virus lytic cycle activation in malignant and nonmalignant disease. J. Natl. Cancer Inst. 94:1733-1735.
62. Quinlivan EB, et al. 1993. Direct BRLF1 binding is required for cooperative BZLF1/BRLF1 activation of the Epstein-Barr virus early promoter, BMRF1. Nucleic Acids Res. 21:1999-2007.
63. Raab-Traub N, Dambaugh T, Kieff E. 1980. DNA of Epstein-Barr virus VIII: B95-8, the previous prototype, is an unusual deletion derivative. Cell 22:257-267.
64. 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.
65. Ragoczy T, Miller G. 1999. Role of the Epstein-Barr virus RTA protein in activation of distinct classes of viral lytic cycle genes. J. Virol. 73:9858-9866.
66. Rennekamp AJ, Lieberman PM. 2011. Initiation of Epstein-Barr virus lytic replication requires transcription and the formation of a stable RNADNA hybrid molecule at OriLyt. J. Virol. 85:2837-2850.
67. Rickinson AB, Kieff E. 2007. Epstein-Barr virus. In Knipe DM, et al (ed), Fields virology, 5th ed, vol 2, p 2655-2700. Lippincott WilliamsandWilkins, Philadelphia, PA.
68. Robinson AR, Kwek SS, Hagemeier SR, Wille CK, Kenney SC. 2011. Cellular transcription factor Oct-1 interacts with the Epstein-Barr virus BRLF1 protein to promote disruption of viral latency. J. Virol. 85:8940-8953.
69. 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.
70. Severini A, Scraba DG, Tyrrell DL. 1996. Branched structures in the intracellular DNA of herpes simplex virus type 1. J. Virol. 70:3169 - 3175.
71. Speck SH, Chatila T, Flemington E. 1997. Reactivation of Epstein-Barr virus: regulation and function of the BZLF1 gene. Trends Microbiol. 5:399-405.
72. Urier G, Buisson M, Chambard P, Sergeant A. 1989. The Epstein-Barr virus early protein EB1 activates transcription from different responsive elements including AP-1 binding sites. EMBO J. 8:1447-1453.
73. Wang JT, et al. 2010. Characterization of Epstein-Barr virus BGLF4 kinase expression control at the transcriptional and translational levels. J. Gen. Virol. 91:2186-2196.
74. Weir JP. 2001. Regulation of herpes simplex virus gene expression. Gene 271:117-130.
75. 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.
76. Wu TT, et al. 2009. ORF30 and ORF34 are essential for expression of late genes in murine gammaherpesvirus 68. J. Virol. 83:2265-2273.
77. 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.