Phosphoacceptor site S173 in the regulatory domain of Epstein-Barr virus ZEBRA protein is required for lytic DNA replication but not for activation of viral early genes

Journal of Virology

Volumn 81, Issue 7, 2007, Pages 3303-3316

  El Guindy, Ayman ^a,b   Heston, Lee ^a   Delecluse, Henri Jacques ^c   Miller, George ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL RESEARCH CENTRE   (Egypt)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; IMMEDIATE EARLY PROTEIN BZLF1; PHOSPHORUS DERIVATIVE; PROTEIN ORILYT; PROTEIN S173; PROTEIN S173A; PROTEIN S173Z; SERINE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CHROMATIN IMMUNOPRECIPITATION; DNA BINDING; DNA REPLICATION; EPSTEIN BARR VIRUS; GENE ACTIVATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LYSIS; MOLECULAR INTERACTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SOLUBILITY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; VIRUS ACTIVATION; VIRUS GENE; VIRUS REPLICATION; WILD TYPE;

ALANINE; DEOXYRIBONUCLEASE I; DNA REPLICATION; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 4, HUMAN; MOLECULAR MIMICRY; MUTATION; PHENOTYPE; PHOSPHORYLATION; REGULATORY ELEMENTS, TRANSCRIPTIONAL; SERINE; SOLUBILITY; TIME FACTORS; TRANS-ACTIVATORS; VIRAL PROTEINS;

HUMAN HERPESVIRUS 4;

EID: 33947355348     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02445-06     Document Type: Article

References (49)

1. Adamson, A. L., and S. C. Kenney. 1998. Rescue of the Epstein-Barr virus BZLF1 mutant, Z(S186A), early gene activation defect by the BRLF1 gene product. Virology 251:187-197.
2. Amon, W., U. K. Binne, H. Bryant, P. J. Jenkins, C. E. Karstegl, and P. J. Farrell. 2004. Lytic cycle gene regulation of Epstein-Barr virus. J. Virol. 78:13460-13469.
3. Bell, S. P., and B. Stillman. 1992. ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 357:128-134.
4. Chang, P. J., D. Shedd, L. Gradoville, M. S. Cho, L. W. Chen, J. Chang, and G. Miller. 2002. Open reading frame 50 protein of Kaposi's sarcoma-associated herpesvirus directly activates the viral PAN and K12 genes by binding to related response elements. J. Virol. 76:3168-3178.
5. Cho, M. S., K. T. Jeang, and S. D. Hayward. 1985. Localization of the coding region for an Epstein-Barr virus early antigen and inducible expression of this 60-kilodalton nuclear protein in transfected fibroblast cell lines. J. Virol. 56:852-859.
6. El-Guindy, A., L. Heston, Y. Endo, M. S. Cho, and G. Miller. 2002. Disruption of Epstein-Barr virus latency in the absence of phosphorylation of ZEBRA by protein kinase C. J. Virol. 76:11199-11208.
7. El-Guindy, A. S., and G. Miller. 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 bv Rta. J. Virol. 78:7634-7644.
8. El-Guindy, A. S., S. Y. Paek, J. Countryman, and G. Miller. 2006. Identification of constitutive phosphorylation sites on the Epstein-Barr virus ZEBRA protein. J. Biol. Chem. 281:3085-3095.
9. Farrell, P. J., D. T. Rowe, C. M. Rooney, and T. Kouzarides. 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.
10. Feederle, R., and H. J. Delecluse. 2004. Low level of lytic replication in a recombinant Epstein-Barr virus carrying an origin of replication devoid of BZLF1-binding sites. J. Virol. 78:12082-12084.
11. Feederle, R., M. Kost, M. Baumann, A. Janz, E. Drouet, W. Hammer schmidt, and H. J. Delecluse. 2000. The Epstein-Barr virus lytic program is controlled by the co-operative functions of two transactivators. EMBO J. 19:3080-3089.
12. Fixman, E. D., G. S. Hayward, and S. D. Hayward. 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.
13. Fixman, E. D., G. S. Hayward, and S. D. Hayward. 1992. trans-Acting requirements for replication of Epstein-Barr virus ori-Lyt. J. Virol. 66:5030-5039.
14. Flemington, E., and S. H. Speck. 1990. Evidence for coiled-coil dimer formation by an Epstein-Barr virus transactivator that lacks a heptad repeat of leucine residues. Proc. Natl. Acad. Sci. USA 87:9459-9463.
15. Francis, A., T. Ragoczy, L. Gradoville, A. El-Guindy, and G. Miller. 1999. Amino acid substitutions reveal distinct functions of serine 186 of the ZEBRA protein in activation of lytic cycle genes and synergy with the EBV Rta transactivator. J. Virol. 73:4543-4551.
16. Frappier, L., and M. O'Donnell. 1991. Overproduction, purification, and characterization of EBNA1, the origin binding protein of Epstein-Barr virus. J. Biol. Chem. 266:7819-7826.
17. Gao, Z., A. Krithivas, J. E. Finan, O. J. Semmes, S. Zhou, Y. Wang, and S. D. Hayward. 1998. The Epstein-Barr virus lytic transactivator Zta interacts with the helicase-primase replication proteins. J. Virol. 72:8559-8567.
18. Heston, L., A. El-Guindy, J. Countryman, C. Dela Cruz, H. J. Delecluse, and G. Miller. 2006. Amino acids in the basic domain of Epstein-Barr virus ZEBRA protein play distinct roles in DNA binding, activation of early lytic gene expression, and promotion of viral DNA replication. J. Virol. 80:9115-9133.
19. Heston, L., M. Rabson, N. Brown, and G. Miller. 1982. New Epstein-Barr virus variants from cellular subclones of P3J-HR-1 Burkitt lymphoma. Nature 295:160-163.
20. Johannsen, E., M. Luftig, M. R. Chase, S. Weicksel, E. Cahir-McFarland, D. Illanes, D. Sarracino, and E. Kieff. 2004. Proteins of purified Epstein-Barr virus. Proc. Natl. Acad. Sci. USA 101:16286-16291.
21. Katz, D. A., R. P. Baumann, R. Sun, J. L. Kolman, N. Taylor, and G. Miller. 1992. Viral proteins associated with the Epstein-Barr virus transactivator, ZEBRA. Proc. Natl. Acad. Sci. USA 89:378-382.
22. Klemm, R. D., R. J. Austin, and S. P. Bell. 1997. Coordinate binding of ATP and origin DNA regulates the ATPase activity of the origin recognition complex. Cell 88:493-502.
23. Kolman, J. L., N. Taylor, L. Gradoville, J. Countryman, and G. Miller. 1996. Comparing transcriptional activation and autostimulation by ZEBRA and ZEBRA/c-Fos chimeras. J. Virol. 70:1493-1504.
24. Kolman, J. L., N. Taylor, D. R. Marshak, and G. Miller. 1993. Serine-173 of the Epstein-Barr virus ZEBRA protein is required for DNA binding and is a target for casein kinase II phosphorylation. Proc. Natl. Acad. Sci. USA 90:10115-10119.
25. Le Roux, F., A. Sergeant, and L. Corbo. 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.
26. Llao, G., F. Y. Wu, and S. D. Hayward. 2001. Interaction with the Epstein-Barr virus helicase targets Zta to DNA replication compartments. J. Virol. 75:8792-8802.
27. Lieberman, P. M., J. M. Hardwick, J. Sample, G. S. Hayward, and S. D. Hayward. 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.
28. Makise, M., H. Takenaka, W. Kuwae, N. Takahashi, T. Tsuchiya, and T. Mizushima. 2003. Kinetics of ATP binding to the origin recognition complex of Saccharomyces cerevisiae. J. Biol. Chem. 278:46440-46445.
29. Marahrens, Y., and B. Stillman. 1992. A yeast chromosomal origin of DNA replication defined by multiple functional elements. Science 255:817-823.
30. Mizushima, T., T. Takaki, T. Kubota, T. Tsuchiya, T. Miki, T. Katayama, and K. Sekimizu. 1998. Site-directed mutational analysis for the ATP binding of DnaA protein. Functions of two conserved amino acids (Lys-178 and Asp-235) located in the ATP-binding domain of DnaA protein in vitro and in vivo. J. Biol. Chem. 273:20847-20851.
31. Mysiak, M. E., C. Wyman, P. E. Holthuizen, and P. C. van der Vliet. 2004. NFI and Oct-1 bend the Ad5 origin in the same direction leading to optimal DNA replication. Nucleic Acids Res. 32:6218-6225.
32. Petosa, C., P. Morand, F. Baudin, M. Moulin, J. B. Artero, and C. W. Muller. 2006. Structural basis of lytic cycle activation by the Epstein-Barr virus ZEBRA protein. Mol. Cell 21:565-572.
33. Quinlivan, E. B., E. A. Holley-Guthrie, M. Norris, D. Gutsch, S. L. Bachen heimer, and S. C. Kenney. 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.
34. Raab-Traub, N., and K. Flynn. 1986. The structure of the termini of the Epstein-Barr virus as a marker of clonal cellular proliferation. Cell 47:883-889.
35. Ragoczy, T., L. Heston, and G. Miller. 1998. The Epstein-Barr virus Rta protein activates lytic cycle genes and can disrupt latency in B lymphocytes. J. Virol. 72:7978-7984.
36. Rao, H., Y. Marahrens, and B. Stillman. 1994. Functional conservation of multiple elements in yeast chromosomal replicators. Mol. Cell. Biol. 14: 7643-7651.
37. Rao, H., and B. Stillman. 1995. The origin recognition complex interacts with a bipartite DNA binding site within yeast replicators. Proc. Natl. Acad. Sci. USA 92:2224-2228.
38. Schepers, A., D. Pich, and W. Hammerschmidt. 1996. Activation of oriLyt, the lytic origin of DNA replication of Epstein-Barr virus, by BZLF1. Virology 220:367-376.
39. Schepers, A., M. Ritzi, K. Bousset, E. Kremmer, J. L. Yates, J. Harwood, J. F. Diflley, and W. Hammerschmidt. 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.
40. Sekimizu, K., D. Bramhill, and A. Kornberg. 1987. ATP activates dnaA protein in initiating replication of plasmids bearing the origin of the E. coli chromosome. Cell 50:259-265.
41. Serio, T. R., A. Angeloni, J. L. Kolman, L. Gradoville, R. Sun, D. A. Katz, W. Van Grunsven, J. Middeldorp, and G. Miller. 1996. Two 21-kilodalton components of the Epstein-Barr virus capsid antigen complex and their relationship to ZEBRA-associated protein p21 (ZAP21). J. Virol. 70:8047-8054.
42. Serlo, T. R., J. L. Kolman, and G. Miller. 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.
43. Sinclair, A. J., M. Brimmell, F. Shanahan, and P. J. Farrell. 1991. Pathways of activation of the Epstein-Barr virus productive cycle. J. Virol. 65:2237-2244.
44. Speck, C., and W. Messer. 2001. Mechanism of origin unwinding: sequential binding of DnaA to double- and single-stranded DNA. EMBO J. 20:1469-1476.
45. Speck, C., C. Weigel, and W. Messer. 1999. ATP- and ADP-dnaA protein, a molecular switch in gene regulation. EMBO J. 18:6169-6176.
46. Taylor, N., J. Countryman, C. Rooney, D. Katz, and G. Miller. 1989. Expression of the BZLF1 latency-disrupting gene differs in standard and defective Epstein-Barr viruses. J. Virol. 63:1721-1728.
47. Wysokenski, D. A., and J. L. Yates. 1989. Multiple EBNA1-binding sites are required to form an EBNA1-dependent enhancer and to activate a minimal replicative origin within oriP of Epstein-Barr virus. J. Virol. 63:2657-2666.
48. Young, L. S., R. Lau, M. Rowe, G. Niedobitek, G. Packham, F. Shanahan, D. T. Rowe, D. Greenspan, J. S. Greenspan, A. B. Rickinson, et al. 1991. Differentiation-associated expression of the Epstein-Barr virus BZLF1 transactivator protein in oral hairy leukoplakia. J. Virol. 65:2868-2874.
49. Zhang, Q., Y. Hong, D. Dorsky, E. Holley-Guthrie, S. Zalani, N. A. Elshiekh, A. Kiehl, T. Le, and S. Kenney. 1996. Functional and physical interactions between the Epstein-Barr virus (EBV) proteins BZLF1 and BMRF1: effects on EBV transcription and lytic replication. J. Virol. 70:5131-5142.