Amino acid substitutions reveal distinct functions of serine 186 of the ZEBRA protein in activation of early lytic cycle genes and synergy with the Epstein-Barr virus R transactivator

Journal of Virology

Volumn 73, Issue 6, 1999, Pages 4543-4551

  Francis, Amy ^a,b   Ragoczy, Tobias ^a   Gradoville, Lyn ^a   Heston, Lee ^a   El Guindy, Ayman ^a   Endo, Yoshimi ^a   Miller, George ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; SERINE;

AMINO ACID SUBSTITUTION; ARTICLE; DNA BINDING; EPSTEIN BARR VIRUS; GENE EXPRESSION SYSTEM; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; VIRUS GENOME;

EID: 0033029629     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.6.4543-4551.1999     Document Type: Article

References (47)

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. Bannister, A. J., T. Oehler, D. Wilhelm, P. Angel, and T. Kouzarides. 1995. Stimulation of c-Jun activity by CBP: c-Jun residues Ser63/73 are required for CBP-induced stimulation in vivo and CBP binding in vitro. Oncogene 11:2509-2514.
3. Bartkiewicz, M., H. Gold, and S. Altman. 1989. Identification and characterization of an RNA molecule that copurifies with RNase P activity from HeLa cells. Genes Dev. 3:488-499.
4. Baumann, M., H. Mischak, S. Dammeier, W. Kolch, O. Gires, D. Pich, and W. Hammerschmidt. 1998. Activation of the Epstein-Barr virus transcription factor BZLF1 by 12-O-tetradecanoyphorbol-13-acetate-induced phosphorylation. J. Virol. 72:8105-8114.
5. Bengal, E., O. Flores, P. N. Rangarajan, A. Chen, H. Weintraub, and I. M. Verma. 1994. Positive control mutations in the MyoD basic region fail to show cooperative DNA binding and transcriptional activation in vitro. Proc. Natl. Acad. Sci. USA 91:6221-6225.
6. Chang, Y.-N., D. L.-Y. Dong, G. S. Hayward, and S. D. Hayward. 1990. The Epstein-Barr virus Zta transactivator: a member of the bZIP family with unique DNA-binding specificity and a dimerization domain that lacks the characteristic heptad leucine zipper motif. J. Virol. 64:3358-3369.
7. Chen, H., R, J. Lin, R. L. Schlitz, D. Chakravarti, A. Nash, L. Nagy, M. L. Privalsky, Y. Nakatani, and R. M. Evans. 1997. Nuclear receptor coactivator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell 90:569-580.
8. Chevallier-Greco, A., H. Gruffat, E. Manet, A. Calender, and A. Sergeant. 1989. 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.
9. Chrivia, J. C., R. P. Kwok, N. Lamb, M. Hagiwara, M. R. Montminy, and R. H. Goodman. 1993. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365:855-859.
10. Countryman, J., and G. Miller. 1985. Activation of expression of latent Epstein-Barr herpesvirus after gene transfer with a small cloned subfragment of heterogeneous viral DNA. Proc. Natl. Acad. Sci. USA 82:4085-4089.
11. Countryman, J., H. Jenson, R. Seibl, H. Wolf, and G. Miller. 1987. Polymorphic proteins encoded within BZLF1 of defective and standard Epstein-Barr viruses disrupt latency. J. Virol. 61:3672-3679.
12. Cox, M. A., J. Leahy, and J. M. Hardwick. 1990. An enhancer within the divergent promoter of Epstein-Barr Virus responds synergistically to the R and Z transactivators. J. Virol. 64:313-321.
13. Daibata, M., R. E. Humphreys, and T. Sairenji. 1992. Phosphorylation of the Epstein-Barr virus BZLF1 immediate-early gene product ZEBRA. Virology 188:916-920.
14. Daibata, M., S. H. Speck, C. Mulder, and T. Sairenji. 1994. Regulation of the BZLF1 promoter of Epstein-Barr virus by second messengers in anti-immunoglobulin-treated B cells. Virology 198:446-454.
15. Davis, M. G., and E. S. Huang. 1988. Transfer and expression of plasmids containing human cytomegalovirus immediate-early gene 1 promoter-enhancer sequences in eukaryotic and prokaryotic cells. Biotechnol. Appl. Biochem. 10:6-12.
16. 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.
17. Flemington, E., and S. H. Speck. 1990. Autoregulation of Epstein-Barr virus putative lytic switch gene BZLF1. J. Virol. 64:1227-1232.
18. Flemington, E., A. E. Goldfield, and S. H. Speck. 1991. Efficient transcription of the Epstein-Barr virus immediate-early BZLF1 and BRLF1 genes requires protein synthesis. J. Virol. 65:7073-7077.
19. Francis, A. 1997. Ph.D. thesis. Yale University, New Haven, Conn.
20. Francis, A. L., L. Gradoville, and G. Miller. 1997. Alteration of a single serine in the basic domain of the Epstein-Barr virus ZEBRA protein separates its functions of transcriptional activation and disruption of latency. J. Virol. 71:3054-3061.
21. Giot, J.-F., I. Mikaelian, M. Buisson, E. Manet, I. Joab, J.-C. Nicholas, and A, Sergeant. 1991. Transcriptional interference between the EBV transcription factors EB1 and R: both DNA-binding and activation domains of EB1 are required. Nucleic Acids Res. 19:1251-1258.
22. Glover, J. N., and S. C. Harrison. 1995. Crystal structure of the heterodimeric bZIP transcription factor c-Fos-c-Jun bound to DNA. Nature 373:257-261.
23. Grogan, E. J., J. Jenson, J. Countryman, L. Heston, L. Gradoville, and G. Miller. 1987. Transfection of a rearranged viral DNA fragment WZhet, stably converts latent Epstein-Barr virus infection to productive infection in lymphoid cells. Proc. Natl. Acad. Sci. USA 84:1332-1336.
24. Hardwick, J. M., P. M. Liebermann, and S. D. Hayward. 1988. A new Epstein-Barr virus transactivator, R, induces expression of a cytoplasmic early antigen. J. Virol. 62:2274-2284.
25. Holley-Guthrie, E., E. B. Quinlivan, E.-C. Mar, and M. Smith. 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.
26. Kenney, S., E. Holley-Guthrie, E.-C. Mar, and M. Smith. 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.
27. 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.
28. Kwok, R. P., J. R. Lundblad, J. C. Chrivia, J. P. Richards, H. P. Bachinger, R. G. Brennan, S. G. Roberts, M. R. Green, and R H. Goodman. 1994. Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 370:223-226.
29. 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.
30. Lehman, A. M., K. B. Ellwood, B. E. Middleton, and M. Carey. 1998. Compensatory energetic relationships between upstream activators and the RNA polymerase II general transcription machinery. J. Biol. Chem. 273: 932-939.
31. Lieberman, P. M., and A. J. Berk. 1990. In vitro transcriptional activation, dimerization, and DNA binding of the Epstein-Barr virus Zta protein. J. Virol. 64:2560-2568.
32. Martinez-Balbas, M. A., A. J. Bannister, K. Martin, P. Haus-Seuffert, M. Meisterernst, and T. Kouzarides. 1998. The acetyltransferase activity of CBP stimulates transcription. EMBO J. 17:2886-2893.
33. Mellinghoff, I., M. Daibata, R. E. Humphreys, C. Mulder, K. Takada, and T. Sairenji. 1991. Early events in Epstein-Barr virus genome expression after activation: regulation by second messengers of B cell activation. Virology 185:922-928.
34. Menezes, J., W. Leifbold, G. Klein, and G. Clements. 1975. Establishment and characterization of an Epstein-Barr virus (EBV)-negative lymphoblastoid B cell line (BJA-B) from an exceptional, EBV-genome negative African Burkitt's lymphoma. Biomedicine 22:276-284.
35. Packham, G., A. Economou, C. M. Rooney, D. T. Rowe, and P. J. Farrell. 1990. Structure and function of the Epstein-Barr virus BZLF1 protein. J. Virol. 64:2110-2116.
36. Parker, D., K. Ferreri, T. Nakajima, V. J. LaMorte, R. Evans, S. C. Koerber, C. Hoeger, and M. R. Montminy. 1996. Phosphorylation of CREB at Ser-133 induces complex form with CREB-binding protein via a direct mechanism. Mol. Cell. Biol. 16:694-703.
37. Pearson, G. R., B. Vroman, B. Chase, T. Sculley, M. Hummel, and E. Kieff. 1983. Identification of polypeptide components of the Epstein-Barr virus early antigen complex with monoclonal antibodies. J. Virol. 47:193-201.
38. Quinlivan, E. B., E. A. Holley-Guthrie, M. Morris, D. Gutsch, S. L. Bachenheimer, 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.
39. 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.
40. Rooney, C., D. T. Rowe, T. Ragot, and P. J. Farrell. 1989. The spliced BZLF1 gene of Epstein-Barr virus (EBV) transactivates an early EBV promoter and induces the virus productive cycle. J. Virol. 663:3109-3116.
41. Serio, 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.
42. Takada, K., and Y. Ono. 1989. Synchronous and sequential activation of latently infected Epstein-Barr virus genomes. J. Virol. 63:445-449.
43. Taylor, N., E. Flemington, J. L. Kolman, R. P. Baumann, S. H. Speck, and G. Miller. 1991. ZEBRA and a Fos-GCN4 chimeric protein differ in their DNA-binding specificities for sites in the Epstein-Barr virus BZLF1 promoter. J. Virol. 65:4033-4041.
44. 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.
45. Woodgett, J. R., K. L. Gould, and T. Hunter. 1986. Substrate specificity of protein kinase C. Use of synthetic peptides corresponding to physiological sites as probes for substrate recognition requirements. Eur. J. Biochem. 161:177-184.
46. Zalani, S., E. Holley-Guthrie, and S. Kenney. 1996. Epstein-Barr viral latency is disrupted by the immediate-early BRLF1 protein through a cell-specific mechanism. Proc. Natl. Acad. Sci. USA 93:9194-9199.
47. Zhong, H., R E. Voll, and S. Ghosh. 1998. Phosphorylation of NF-KB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol. Cell 1:661-671.