Repression of CIITA by the epstein-barr virus transcription factor zta is independent of its dimerization and DNA binding

Journal of General Virology

Volumn 97, Issue 3, 2016, Pages 725-732

  Balan, Nicolae ^a,b   Osborn, Kay ^a   Sinclair, Alison J ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

IMMEDIATE EARLY PROTEIN BZLF1; VIRUS DNA; BZLF1 PROTEIN, HERPESVIRUS 4, HUMAN; DNA; MHC CLASS II TRANSACTIVATOR PROTEIN; NUCLEAR PROTEIN; TRANSACTIVATOR PROTEIN;

ARTICLE; CIITA GENE; CONTROLLED STUDY; DIMERIZATION; EPSTEIN BARR VIRUS; GENE ACTIVITY; GENE EXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; VIRUS GENE; VIRUS REPLICATION; VIRUS TRANSCRIPTION; CHEMISTRY; DOWN REGULATION; EPSTEIN BARR VIRUS INFECTION; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; PROTEIN MOTIF; VIROLOGY;

AMINO ACID MOTIFS; DIMERIZATION; DNA; DOWN-REGULATION; EPSTEIN-BARR VIRUS INFECTIONS; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 4, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; TRANS-ACTIVATORS;

EID: 84960445097     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000369     Document Type: Article

References (51)

1. Adamson, A. L. and Kenney, S. (1999). Epstein-Barr virus BZLF1 protein interacts physically and functionally with the histone acetylase CREB-binding protein. J Virol 73, 6551-6558.
2. Adhikary, D., Behrends, U., Moosmann, A., Witter, K., Bornkamm, G. W. and Mautner, J. (2006). Control of Epstein-Barr virus infection in vitro by T helper cells specific for virion glycoproteins. J Exp Med 203, 995-1006.
3. Asai, R., Kato, A. and Kawaguchi, Y. (2009). Epstein-Barr virus protein kinase BGLF4 interacts with viral transactivator BZLF1 and regulates its transactivation activity. J Gen Virol 90, 1575-1581.
4. Babcock, G. J., Decker, L. L., Volk, M. and Thorley-Lawson, D. A. (1998). EBV persistence in memory B cells in vivo. Immunity 9, 395-404.
5. Bailey, S. G., Verrall, E., Schelcher, C., Rhie, A., Doherty, A. J. and Sinclair, A. J. (2009). Functional interaction between Epstein-Barr virus replication protein Zta and host DNA damage response protein 53BP1. J Virol 83, 11116-11122.
6. Bergbauer, M., Kalla, M., Schmeinck, A., Göbel, C., Rothbauer, U., Eck, S., Benet-Pagés, A., Strom, T. M. and Hammerschmidt, W. (2010). CpG-methylation regulates a class of Epstein-Barr virus promoters. PLoS Pathog 6, e1001114.
7. Bhende, P. M., Seaman, W. T., Delecluse, H. J. and Kenney, S. C. (2004). The EBV lytic switch protein, Z, preferentially binds to and activates the methylated viral genome. Nat Genet 36, 1099-1104.
8. Bhende, P. M., Seaman, W. T., Delecluse, H. J. and Kenney, S. C. (2005). BZLF1 activation of the methylated form of the BRLF1 immediate-early promoter is regulated by BZLF1 residue 186. J Virol 79, 7338-7348.
9. Bristol, J. A., Robinson, A. R., Barlow, E. A. and Kenney, S. C. (2010). The Epstein-Barr virus BZLF1 protein inhibits tumor necrosis factor receptor 1 expression through effects on cellular C/EBP proteins. J Virol 84, 12362-12374.
10. Broderick, P., Hubank, M. and Sinclair, A. J. (2009). Effects of Epstein- Barr virus on host gene expression in Burkitt’s lymphoma cell lines. Chinese journal of cancer 28, 813-821.
11. Cai, Q., Banerjee, S., Cervini, A., Lu, J., Hislop, A. D., Dzeng, R. and Robertson, E. S. (2013). IRF-4-mediated CIITA transcription is blocked by KSHV encoded LANA to inhibit MHC II presentation. PLoS Pathog 9, e1003751.
12. Chang, C. H., Gourley, T. S. and Sisk, T. J. (2002). Function and regulation of class II transactivator in the immune system. Immunol Res 25, 131-142.
13. Crawford, D. H. and Ando, I. (1986). EB virus induction is associated with B-cell maturation. Immunology 59, 405-409.
14. Dickerson, S. J., Xing, Y., Robinson, A. R., Seaman, W. T., Gruffat, H. and Kenney, S. C. (2009). Methylation-dependent binding of the epstein-barr virus BZLF1 protein to viral promoters. PLoS Pathog 5, e1000356.
15. Farrell, P. J. (2005). Epstein-Barr virus genome. In Epstein-Barr virus, pp. 263-288. Edited by E. S. Robertson. Wymondham: Caister. Feederle, R., Kost, M., Baumann, M., Janz, A., Drouet, E., Hammerschmidt, W. and Delecluse, H. J. (2000). The Epstein-Barr virus lytic program is controlled by the co-operative functions of two transactivators. EMBO J 19, 3080-3089.
16. Flemington, E. K., Lytle, J. P., Cayrol, C., Borras, A. M. and Speck, S. H. (1994). DNA-binding-defective mutants of the Epstein-Barr virus lytic switch activator Zta transactivate with altered specificities. Mol Cell Biol 14, 3041-3052.
17. Flower, K., Thomas, D., Heather, J., Ramasubramanyan, S., Jones, S. and Sinclair, A. J. (2011). Epigenetic control of viral life-cycle by a DNAmethylation dependent transcription factor. PLoS One 6, e25922.
18. Hagemeier, S. R., Dickerson, S. J., Meng, Q., Yu, X., Mertz, J. E. and Kenney, S. C. (2010). Sumoylation of the Epstein-Barr virus BZLF1 protein inhibits its transcriptional activity and is regulated by the virus-encoded protein kinase. J Virol 84, 4383-4394.
19. Hicks, M. R., Al-Mehairi, S. S. and Sinclair, A. J. (2003). The zipper region of Epstein-Barr virus bZIP transcription factor Zta is necessary but not sufficient to direct DNA binding. J Virol 77, 8173-8177.
20. Holley-Guthrie, E. A., Quinlivan, E. B., Mar, E. C. and 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.
21. Jenkins, P. J., Binné, U. K. and Farrell, P. J. (2000). Histone acetylation and reactivation of Epstein-Barr virus from latency. J Virol 74, 710-720.
22. Kalla, M., Schmeinck, A., Bergbauer, M., Pich, D. and 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.
23. Kalla, M., Göbel, C. and Hammerschmidt, W. (2012). The lytic phase of epstein-barr virus requires a viral genome with 5-methylcytosine residues in CpG sites. J Virol 86, 447-458.
24. Kallin, B. and Klein, G. (1983). Epstein-Barr virus carried by Raji cells: a mutant in early functions? Intervirology 19, 47-51.
25. Karlsson, Q. H., Schelcher, C., Verrall, E., Petosa, C. and Sinclair, A. J. (2008). Methylated DNA recognition during the reversal of epigenetic silencing is regulated by cysteine and serine residues in the Epstein- Barr virus lytic switch protein. PLoS Pathog 4, e1000005.
26. Kenney, S. C. (2007). Reactivation and lytic replication of EBV. In Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis. Edited by A. Arvin and other editors. Cambridge: Cambridge University Press. http://www.ncbi.nlm.nih.gov/books/NBK47442/
27. Kenney, S., Holley-Guthrie, E., Mar, E. C. and 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.
28. Klug, M. and Rehli, M. (2006). Functional analysis of promoter CpG methylation using a CpG-free luciferase reporter vector. Epigenetics: official journal of the DNA Methylation Society 1, 127-130.
29. Laichalk, L. L. and Thorley-Lawson, D. A. (2005). Terminal differentiation into plasma cells initiates the replicative cycle of Epstein-Barr virus in vivo. J Virol 79, 1296-1307.
30. Laichalk, L. L., Hochberg, D., Babcock, G. J., Freeman, R. B. and Thorley-Lawson, D. A. (2002). The dispersal of mucosal memory B cells: evidence from persistent EBV infection. Immunity 16, 745-754.
31. Li, D., Qian, L., Chen, C., Shi, M., Yu, M., Hu, M., Song, L., Shen, B. and Guo, N. (2009). Down-regulation of MHC class II expression through inhibition of CIITA transcription by lytic transactivator Zta during Epstein-Barr virus reactivation. J Immunol 182, 1799-1809.
32. Lieberman, P. M. and Berk, A. J. (1991). The Zta trans-activator protein stabilizes TFIID association with promoter DNA by direct proteinprotein interaction. Genes Dev 5 (12B), 2441-2454.
33. Lieberman, P. M. and Berk, A. J. (1994). A mechanism for TAFs in transcriptional activation: activation domain enhancement of TFIIDTFIIA- promoter DNA complex formation. Genes Dev 8, 995-1006.
34. Long, H. M., Leese, A. M., Chagoury, O. L., Connerty, S. R., Quarcoopome, J., Quinn, L. L., Shannon-Lowe, C. and Rickinson, A. B. (2011). Cytotoxic CD4+ T cell responses to EBV contrast with CD8 responses in breadth of lytic cycle antigen choice and in lytic cycle recognition. J Immunol 187, 92-101.
35. Magrath, I. (2012). Towards Curative Therapy in Burkitt Lymphoma: The Role of Early African Studies in Demonstrating the Value of Combination Therapy and CNS Prophylaxis. Adv Hematol 2012, 130680.
36. Mikaélian, I., Drouet, E., Marechal, V., Denoyel, G., Nicolas, J. C. and Sergeant, A. (1993). The DNA-binding domain of two bZIP transcription factors, the Epstein-Barr virus switch gene product EB1 and Jun, is a bipartite nuclear targeting sequence. J Virol 67, 734-742.
37. Molyneux, E. M., Rochford, R., Griffin, B., Newton, R., Jackson, G., Menon, G., Harrison, C. J., Israels, T. and Bailey, S. (2012). Burkitt’s lymphoma. Lancet 379, 1234-1244.
38. Morrison, T. E. and Kenney, S. C. (2004). BZLF1, an Epstein-Barr virus immediate-early protein, induces p65 nuclear translocation while inhibiting p65 transcriptional function. Virology 328, 219-232.
39. Murata, T., Hotta, N., Toyama, S., Nakayama, S., Chiba, S., Isomura, H., Ohshima, T., Kanda, T. and Tsurumi, T. (2010). Transcriptional repression by sumoylation of Epstein-Barr virus BZLF1 protein correlates with association of histone deacetylase. J Biol Chem 285, 23925-23935.
40. Packham, G., Economou, A., Rooney, C. M., Rowe, D. T. and Farrell, P. J. (1990). Structure and function of the Epstein-Barr virus BZLF1 protein. J Virol 64, 2110-2116.
41. Pulvertaft, J. V. (1965). A Study of Malignant Tumours in Nigeria by Short-Term Tissue Culture. J Clin Pathol 18, 261-273.
42. Ramasubramanyan, S., Kanhere, A., Osborn, K., Flower, K., Jenner, R. G. and Sinclair, A. J. (2012a). Genome-wide analyses of Zta binding to the Epstein-Barr virus genome reveals interactions in both early and late lytic cycles and an epigenetic switch leading to an altered binding profile. J Virol 86, 12494-12502.
43. Ramasubramanyan, S., Osborn, K., Flower, K. and Sinclair, A. J. (2012b). Dynamic chromatin environment of key lytic cycle regulatory regions of the Epstein-Barr virus genome. J Virol 86, 1809-1819.
44. Saha, A. and Robertson, E. S. (2011). Epstein-Barr virus-associated B-cell lymphomas: pathogenesis and clinical outcomes. Clin Cancer Res 17, 3056-3063.
45. Schelcher, C., Valencia, S., Delecluse, H. J., Hicks, M. and Sinclair, A. J. (2005). Mutation of a single amino acid residue in the basic region of the Epstein-Barr virus (EBV) lytic cycle switch protein Zta (BZLF1) prevents reactivation of EBV from latency. J Virol 79, 13822-13828.
46. Sinclair, A. J. (2003). bZIP proteins of human gammaherpesviruses. J Gen Virol 84, 1941-1949.
47. Sinclair, A. J., Brimmell, M., Shanahan, F. and Farrell, P. J. (1991). Pathways of activation of the Epstein-Barr virus productive cycle. J Virol 65, 2237-2244.
48. Woellmer, A., Arteaga-Salas, J. M. and Hammerschmidt, W. (2012). BZLF1 governs CpG-methylated chromatin of Epstein-Barr Virus reversing epigenetic repression. PLoS Pathog 8, e1002902.
49. Young, L. S., Lau, R., Rowe, M., Niedobitek, G., Packham, G., Shanahan, F., Rowe, D. T., Greenspan, D., Greenspan, J. S. and other authors (1991). Differentiation-associated expression of the Epstein-Barr virus BZLF1 transactivator protein in oral hairy leukoplakia. J Virol 65, 2868-2874.
50. Zhang, Q., Gutsch, D. and Kenney, S. (1994). Functional and physical interaction between p53 and BZLF1: implications for Epstein-Barr virus latency. Mol Cell Biol 14, 1929-1938.
51. Zuo, J. and Rowe, M. (2012). Herpesviruses placating the unwilling host: manipulation of the MHC class II antigen presentation pathway. Viruses 4, 1335-1353.