Epstein-barr virus BGLF4 kinase downregulates NF-κB transactivation through phosphorylation of coactivator UXT

Journal of Virology

Volumn 86, Issue 22, 2012, Pages 12176-12186

  Chang, Ling Shih ^a   Wang, Jiin Tarng ^a   Doong, Shin Lian ^a   Lee, Chung Pei ^a,b   Chang, Chou Wei ^a   Tsai, Ching Hwa ^a   Yeh, Sheng Wen ^a   Hsieh, Ching Yueh ^a   Chen, Mei Ru ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIPEI UNIVERSITY OF NURSING AND HEALTH SCIENCES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

IMMEDIATE EARLY PROTEIN BZLF1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BGLF4; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR UXT; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; AUTOPHOSPHORYLATION; BINDING AFFINITY; CONTROLLED STUDY; DOWN REGULATION; EPSTEIN BARR VIRUS; GENE EXPRESSION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TRANSACTIVATION; TRANSCRIPTION REGULATION; VIRUS REPLICATION;

DOWN-REGULATION; GENE EXPRESSION REGULATION, VIRAL; HEK293 CELLS; HELA CELLS; HUMANS; LENTIVIRUS; NEOPLASM PROTEINS; NF-KAPPA B; PHOSPHORYLATION; PLASMIDS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; TRANSCRIPTIONAL ACTIVATION; TUMOR NECROSIS FACTOR-ALPHA; TWO-HYBRID SYSTEM TECHNIQUES; VIRAL PROTEINS;

HERPESVIRIDAE; HUMAN HERPESVIRUS 4; LENTIVIRUS;

EID: 84869131708     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01918-12     Document Type: Article

References (62)

1. Baumforth KR, Young LS, Flavell KJ, Constandinou C, Murray PG. 1999. The Epstein-Barr virus and its association with human cancers. Mol. Pathol. 52:307-322.
2. Brown HJ, et al. 2003. NF-kappaB inhibits gammaherpesvirus lytic replication. J. Virol. 77:8532-8540.
3. Chang Y, et al. 1999. Requirement for cell-to-cell contact in Epstein-Barr virus infection of nasopharyngeal carcinoma cells and keratinocytes. J. Virol. 73:8857-8866.
4. Chen C, Okayama H. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745-2752.
5. Chen MR, Chang SJ, Huang H, Chen JY. 2000. A protein kinase activity associated with Epstein-Barr virus BGLF4 phosphorylates the viral early antigen EA-D in vitro. J. Virol. 74:3093-3104.
6. Chen YJ, et al. 2011. Epstein-Barr virus (EBV) Rta-mediated EBV and Kaposi's sarcoma-associated herpesvirus lytic reactivations in 293 cells. PLoS One 6:e17809. doi:10.1371/journal.pone.0017809.
7. Chua HH, et al. 2007. Role of the TSG101 gene in Epstein-Barr virus late gene transcription. J. Virol. 81:2459-2471.
8. DiDonato JA, Hayakawa M, Rothwarf DM, Zandi E, Karin M. 1997. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB. Nature 388:548-554.
9. Fitzgerald KA, et al. 2003. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4:491-496.
10. Gershburg E, Raffa S, Torrisi MR, Pagano JS. 2007. Epstein-Barr virusencoded protein kinase (BGLF4) is involved in production of infectious virus. J. Virol. 81:5407-5412.
11. Ghosh S, Karin M. 2002. Missing pieces in the NF-kappaB puzzle. Cell 109(Suppl.):S81-S96.
12. Ghosh S, May MJ, Kopp EB. 1998. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16:225-260.
13. Gstaiger M, et al. 2003. Control of nutrient-sensitive transcription programs by the unconventional prefoldin URI. Science 302:1208-1212.
14. Gutsch DE, et al. 1994. The bZIP transactivator of Epstein-Barr virus, BZLF1, functionally and physically interacts with the p65 subunit of NFkappa B. Mol. Cell. Biol. 14:1939-1948.
15. Hagemeier SR, et al. 2010. Sumoylation of the Epstein-Barr virus BZLF1 protein inhibits its transcriptional activity and is regulated by the virusencoded protein kinase. J. Virol. 84:4383-4394.
16. Hahn AM, Huye LE, Ning S, Webster-Cyriaque J, Pagano JS. 2005. Interferon regulatory factor 7 is negatively regulated by the Epstein-Barr virus immediate-early gene, BZLF-1. J. Virol. 79:10040-10052.
17. Hatakeyama S, et al. 1999. Ubiquitin-dependent degradation of IkappaBalpha is mediated by a ubiquitin ligase Skp1/Cul 1/F-box protein FWD1. Proc. Natl. Acad. Sci. U. S. A. 96:3859-3863.
18. Hayden MS, Ghosh S. 2008. Shared principles in NF-kappaB signaling. Cell 132:344-362.
19. Hayden MS, Ghosh S. 2004. Signaling to NF-kappaB. Genes Dev. 18: 2195-2224.
20. Hiscott J, Kwon H, Genin P. 2001. Hostile takeovers: viral appropriation of the NF-kappaB pathway. J. Clin. Invest. 107:143-151.
21. Hislop AD, et al. 2007. A CD8+ T cell immune evasion protein specific to Epstein-Barr virus and its close relatives in Old World primates. J. Exp. Med. 204:1863-1873.
22. Horst D, et al. 2009. Specific targeting of the EBV lytic phase protein BNLF2a to the transporter associated with antigen processing results in impairment of HLA class I-restricted antigen presentation.J. Immunol. 182:2313-2324.
23. Hsu TY, et al. 2005. Reactivation of Epstein-Barr virus can be triggered by an Rta protein mutated atthe nuclear localization signal. J. Gen. Virol. 86:317-322.
24. James P, Halladay J, Craig EA. 1996. Genomic libraries and a host straindesigned for highly efficienttwo-hybrid selection in yeast. Genetics 144: 1425-1436.
25. Kudoh A, et al. 2006. Phosphorylation of MCM4 at sites inactivating DNA helicase activity of the MCM4-MCM6-MCM7 complex during Epstein- Barr virus productive replication. J. Virol. 80:10064-10072.
26. Lee CP, et al. 2007. Epstein-Barr virus BGLF4 kinase induces premature chromosome condensation through activation of condensin and topoisomerase II. J. Virol. 81:5166-5180.
27. Lee CP, et al. 2008. Epstein-Barr virus BGLF4 kinase induces disassembly of the nuclear lamina to facilitate virion production. J. Virol. 82:11913-11926.
28. Li D, et al. 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.
29. Li Q, Verma IM. 2002. NF-kappaB regulation in the immune system. Nat. Rev. Immunol. 2:725-734.
30. Li R, et al. 2011. Conserved herpesvirus kinases target the DNA damage response pathway and TIP60 histone acetyltransferase to promote virus replication. Cell Host Microbe 10:390-400.
31. Liu L, Amy V, Liu G, McKeehan WL. 2002. Novel complex integrating mitochondria and the microtubular cytoskeleton with chromosome remodeling and tumor suppressor RASSF1 deduced by in silico homology analysis, interaction cloning in yeast, and colocalization in cultured cells. In Vitro Cell. Dev. Biol. Anim. 38:582-594.
32. Liu L, McKeehan WL. 2002. Sequence analysis of LRPPRC and its SEC1 domain interaction partners suggests roles in cytoskeletal organization, vesicular trafficking, nucleocytosolic shuttling, and chromosome activity. Genomics 79:124-136.
33. Lu J, et al. 2000. Upregulation of tyrosine kinase TKT by the Epstein-Barr virus transactivator Zta. J. Virol. 74:7391-7399.
34. Makarova O, Kamberov E, Margolis B. 2000. Generation of deletion and point mutations with one primer in a single cloning step. Biotechniques 29:970-972.
35. Markus SM, et al. 2002. Identification and characterization of ART-27, a novel coactivator for the androgen receptor N terminus. Mol. Biol. Cell 13:670-682.
36. McGilvray R, Walker M, Bartholomew C. 2007. UXT interacts with the transcriptional repressor protein EVI1 and suppresses cell transformation. FEBS J. 274:3960-3971.
37. Mogensen TH, Paludan SR. 2001. Molecular pathways in virus-induced cytokine production. Microbiol. Mol. Biol. Rev. 65:131-150.
38. Morrison TE, Kenney SC. 2004. BZLF1, an Epstein-Barr virus immediate-early protein, induces p65 nuclear translocation while inhibiting p65 transcriptional function. Virology 328:219-232.
39. Morrison TE, Mauser A, Wong A, Ting JP, Kenney SC. 2001. Inhibition of IFN-gamma signaling by an Epstein-Barr virus immediate-early protein. Immunity 15:787-799.
40. Murata T, et al. 2009. Efficient production of infectious viruses requires enzymatic activity of Epstein-Barr virus protein kinase. Virology 389:75-81.
41. Nichols DB, Shisler JL. 2006. The MC160 protein expressed by the dermatotropic poxvirus molluscum contagiosum virus prevents tumor necrosis factor alpha-induced NF-kappaB activation via inhibition of I kappa kinase complex formation. J. Virol. 80:578-586.
42. Perkins ND. 2007. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat. Rev. Mol. Cell Biol. 8:49-62.
43. Prince S, et al. 2003. Latent membrane protein 1 inhibits Epstein-Barr virus lytic cycle induction and progress via different mechanisms. J. Virol. 77:5000-5007.
44. Reference deleted.
45. 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.
46. Ressing ME, et al. 2005. Epstein-Barr virus gp42 is posttranslationally modified to produce soluble gp42 that mediates HLA class II immune evasion. J. Virol. 79:841-852.
47. Rowe M, et al. 2007. Host shutoff during productive Epstein-Barr virus infection is mediated by BGLF5 and may contribute to immune evasion. Proc. Natl. Acad. Sci. U. S. A. 104:3366-3371.
48. Santoro MG, Rossi A, Amici C. 2003. NF-kappaB and virus infection: who controls whom. EMBO J. 22:2552-2560.
49. Sarisky RT, et al. 1996. A replication function associated with the activation domain of the Epstein-Barr virus Zta transactivator. J. Virol. 70: 8340-8347.
50. Schepers A, Pich D, Mankertz J, Hammerschmidt W. 1993. cis-acting elements in the lytic origin of DNA replication of Epstein-Barr virus. J. Virol. 67:4237-4245.
51. Siegert R, Leroux MR, Scheufler C, Hartl FU, Moarefi I. 2000. Structure of the molecular chaperone prefoldin: unique interaction of multiple coiled coil tentacles with unfolded proteins. Cell 103:621-632.
52. Sun S, et al. 2007. UXT is a novel and essential cofactor in the NF-kappaB transcriptional enhanceosome. J. Cell Biol. 178:231-244.
53. Taneja SS, et al. 2004. ART-27, an androgen receptor coactivator regulated in prostate development and cancer. J. Biol. Chem. 279:13944-13952.
54. Taylor RT, Bresnahan WA. 2006. Human cytomegalovirus IE86 attenuates virus- and tumor necrosis factor alpha-induced NFkappaBdependent gene expression. J. Virol. 80:10763-10771.
55. Vainberg IE, et al. 1998. Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell 93:863-873.
56. Wang JT, et al. 2009. Epstein-Barr virus BGLF4 kinase suppresses the interferon regulatory factor 3 signaling pathway. J. Virol. 83:1856-1869.
57. Wang JT, et al. 2005. Detection of Epstein-Barr virus BGLF4 protein kinase in virus replication compartments and virus particles. J. Gen. Virol. 86:3215-3225.
58. Yang PW, Chang SS, Tsai CH, Chao YH, Chen MR. 2008. Effect of phosphorylation on the transactivation activity of Epstein-Barr virus BMRF1, a major target of the viral BGLF4 kinase. J. Gen. Virol. 89:884-895.
59. Young LS, Rickinson AB. 2004. Epstein-Barr virus: 40 years on. Nat. Rev. Cancer 4:757-768.
60. Yue W, Gershburg E, Pagano JS. 2005. Hyperphosphorylation of EBNA2 by Epstein-Barr virus protein kinase suppresses transactivation of the LMP1 promoter. J. Virol. 79:5880-5885.
61. Zhao H, et al. 2005. UXT is a novel centrosomal protein essential for cell viability. Mol. Biol. Cell 16:5857-5865.
62. Zhu J, et al. 2009. Protein array identification of substrates of the Epstein-Barr virus protein kinase BGLF4. J. Virol. 83:5219-5231.