Epstein-Barr virus-encoded EBNA1 inhibits the canonical NF-κB pathway in carcinoma cells by inhibiting IKK phosphorylation

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Valentine, Robert ^a,b   Dawson, Christopher W ^a   Hu, Chunfang ^a   Shah, Khilan M ^a   Owen, Thomas J ^a,c   Date, Kathryn L ^a   Maia, Sonia P ^a   Shao, Jianyong ^d   Arrand, John R ^a   Young, Lawrence S ^a   O'Neil, John D ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^d SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EPSTEIN BARR VIRUS ANTIGEN; EPSTEIN BARR VIRUS ANTIGEN 1; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR RELA; CCAAT ENHANCER BINDING PROTEIN BETA; EBV ENCODED NUCLEAR ANTIGEN 1; EBV-ENCODED NUCLEAR ANTIGEN 1; I KAPPA B KINASE; INTERLEUKIN 1 RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR;

ARTICLE; CARCINOGENESIS; CARCINOMA CELL; CONTROLLED STUDY; CYTOPLASM; EPSTEIN BARR VIRUS; FIBROBLAST; GENE INTERACTION; GENE LOCATION; GENE TRANSLOCATION; HUMAN; HUMAN CELL; NASOPHARYNX CARCINOMA; NONHUMAN; OBSERVATIONAL STUDY; PHENOTYPE; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; SQUAMOUS CELL CARCINOMA; TRANSACTIVATION; TRANSCRIPTION REGULATION; CELL NUCLEUS; CHEMISTRY; DOWN REGULATION; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NASOPHARYNX TUMOR; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TUMOR CELL LINE; UPREGULATION; VIRUS GENE;

HUMAN HERPESVIRUS 4; MURINAE;

CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL LINE, TUMOR; CELL NUCLEUS; CYTOPLASM; DOWN-REGULATION; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE EXPRESSION REGULATION, VIRAL; GENES, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; I-KAPPA B KINASE; NASOPHARYNGEAL NEOPLASMS; NF-KAPPA B; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, INTERLEUKIN-1; RECEPTORS, TUMOR NECROSIS FACTOR; SEQUENCE DELETION; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 76749150968     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-1     Document Type: Article

References (43)

1. Kieff ERAB. Epstein-Barr virus and its replication. FieldsVirology 2001, 2511-2574. Philadelphia: Lippincott Williams & Wilkins, Knipe Dm HP.
2. Raab-Traub N. Epstein-Barr virus in the pathogenesis of NPC. Semin Cancer Biol 2002, 12:431-441. 10.1016/S1044579X0200086X, 12450729.
3. Young LS, Murray PG. Epstein-Barr virus and oncogenesis: from latent genes to tumours. Oncogene 2003, 22:5108-5121. 10.1038/sj.onc.1206556, 12910248.
4. Holowaty MN, Frappier L. HAUSP/USP7 as an Epstein-Barr virus target. Biochem Soc Trans 2004, 32:731-732. 10.1042/BST0320731, 15494000.
5. Wilson JB, Bell JL, Levine AJ. Expression of Epstein-Barr virus nuclear antigen-1 induces B cell neoplasia in transgenic mice. EMBO J 1996, 15:3117-3126. 450254, 8670812.
6. Kang MS, Soni V, Bronson R, Kieff E. Epstein-Barr virus nuclear antigen 1 does not cause lymphoma in C57BL/6J mice. J Virol 2008, 82:4180-4183. 2292993, 18256159, 10.1128/JVI.02596-07.
7. Kang MS, Hung SC, Kieff E. Epstein-Barr virus nuclear antigen 1 activates transcription from episomal but not integrated DNA and does not alter lymphocyte growth. Proc Natl Acad Sci USA 2001, 98:15233-15238. 65012, 11734622, 10.1073/pnas.211556598.
8. Komano J, Sugiura M, Takada K. Epstein-Barr virus contributes to the malignant phenotype and to apoptosis resistance in Burkitt's lymphoma cell line Akata. J Virol 1998, 72:9150-9156. 110333, 9765461.
9. Ruf IK, Rhyne PW, Yang C, Cleveland JL, Sample JT. Epstein-Barr virus small RNAs potentiate tumorigenicity of Burkitt lymphoma cells independently of an effect on apoptosis. J Virol 2000, 74:10223-10228. 102063, 11024153, 10.1128/JVI.74.21.10223-10228.2000.
10. Baumforth KR, Birgersdotter A, Reynolds GM, Wei W, Kapatai G, Flavell JR, Kalk E, Piper K, Lee S, Machado L, et al. Expression of the Epstein-Barr virus-encoded Epstein-Barr virus nuclear antigen 1 in Hodgkin's lymphoma cells mediates Up-regulation of CCL20 and the migration of regulatory T cells. Am J Pathol 2008, 173:195-204. 2438297, 18502823, 10.2353/ajpath.2008.070845.
11. Kube D, Vockerodt M, Weber O, Hell K, Wolf J, Haier B, Grasser FA, Muller-Lantzsch N, Kieff E, Diehl V, Tesch H. Expression of epstein-barr virus nuclear antigen 1 is associated with enhanced expression of CD25 in the Hodgkin cell line L428. J Virol 1999, 73:1630-1636. 103989, 9882370.
12. Srinivas SK, Sixbey JW. Epstein-Barr virus induction of recombinase-activating genes RAG1 and RAG2. J Virol 1995, 69:8155-8158. 189773, 7494341.
13. O'Neil JD, Owen TJ, Wood VH, Date KL, Valentine R, Chukwuma MB, Arrand JR, Dawson CW, Young LS. Epstein-Barr virus-encoded EBNA1 modulates the AP-1 transcription factor pathway in nasopharyngeal carcinoma cells and enhances angiogenesis in vitro. J Gen Virol 2008, 89:2833-2842. 10.1099/vir.0.2008/003392-0, 18931081.
14. Wood VH, O'Neil JD, Wei W, Stewart SE, Dawson CW, Young LS. Epstein-Barr virus-encoded EBNA1 regulates cellular gene transcription and modulates the STAT1 and TGFbeta signaling pathways. Oncogene 2007, 26:4135-4147. 10.1038/sj.onc.1210496, 17486072.
15. Dresang LR, Vereide DT, Sugden B. Identifying sites bound by Epstein-Barr virus nuclear antigen 1 (EBNA1) in the human genome: defining a position-weighted matrix to predict sites bound by EBNA1 in viral genomes. J Virol 2009, 83:2930-2940. 2655553, 19129441, 10.1128/JVI.01974-08.
16. Stewart S, Dawson CW, Takada K, Curnow J, Moody CA, Sixbey JW, Young LS. Epstein-Barr virus-encoded LMP2A regulates viral and cellular gene expression by modulation of the NF-kappaB transcription factor pathway. Proc Natl Acad Sci USA 2004, 101:15730-15735. 524829, 15498875, 10.1073/pnas.0402135101.
17. Karin M. NF-kappaB and cancer: mechanisms and targets. Mol Carcinog 2006, 45:355-361. 10.1002/mc.20217, 16673382.
18. Renne R, Barry C, Dittmer D, Compitello N, Brown PO, Ganem D. Modulation of cellular and viral gene expression by the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus. J Virol 2001, 75:458-468. 113938, 11119614, 10.1128/JVI.75.1.458-468.2001.
19. Rodrigues L, Filipe J, Seldon MP, Fonseca L, Anrather J, Soares MP, Simas JP. Termination of NF-kappaB activity through a gammaherpesvirus protein that assembles an EC5S ubiquitin-ligase. EMBO J 2009, 28:1283-1295. 2664658, 19322197, 10.1038/emboj.2009.74.
20. Sample J, Henson EB, Sample C. The Epstein-Barr virus nuclear protein 1 promoter active in type I latency is autoregulated. J Virol 1992, 66:4654-4661. 241289, 1321268.
21. Arenzana-Seisdedos F, Fernandez B, Dominguez I, Jacque JM, Thomas D, Diaz-Meco MT, Moscat J, Virelizier JL. Phosphatidylcholine hydrolysis activates NF-kappa B and increases human immunodeficiency virus replication in human monocytes and T lymphocytes. J Virol 1993, 67:6596-6604. 238097, 8411362.
22. Marechal V, Dehee A, Chikhi-Brachet R, Piolot T, Coppey-Moisan M, Nicolas JC. Mapping EBNA-1 domains involved in binding to metaphase chromosomes. J Virol 1999, 73:4385-4392. 104219, 10196336.
23. Wu H, Kapoor P, Frappier L. Separation of the DNA replication, segregation, and transcriptional activation functions of Epstein-Barr nuclear antigen 1. J Virol 2002, 76:2480-2490. 135949, 11836426, 10.1128/jvi.76.5.2480-2490.2002.
24. Hussain SA, Ganesan R, Reynolds G, Gross L, Stevens A, Pastorek J, Murray PG, Perunovic B, Anwar MS, Billingham L, et al. Hypoxia-regulated carbonic anhydrase IX expression is associated with poor survival in patients with invasive breast cancer. Br J Cancer 2007, 96:104-109. 2360224, 17213826, 10.1038/sj.bjc.6603530.
25. Vermeulen L, De Wilde G, Van Damme P, Berghe W, Haegeman G. Transcriptional activation of the NF-kappaB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J 2003, 22:1313-1324. 151081, 12628924, 10.1093/emboj/cdg139.
26. Hayden MS, Ghosh S. Shared principles in NF-kappaB signaling. Cell 2008, 132:344-362. 10.1016/j.cell.2008.01.020, 18267068.
27. Yamaoka S, Courtois G, Bessia C, Whiteside ST, Weil R, Agou F, Kirk HE, Kay RJ, Israel A. Complementation cloning of NEMO, a component of the IkappaB kinase complex essential for NF-kappaB activation. Cell 1998, 93:1231-1240. 10.1016/S0092-8674(00)81466-X, 9657155.
28. Nishikori M. Classical and Alternative NF-κB Activation Pathways and Their Roles in Lymphoid Malignancies. J Clin Exp Hematopathol 2005, 45:15-24.
29. Busson P, Ganem G, Flores P, Mugneret F, Clausse B, Caillou B, Braham K, Wakasugi H, Lipinski M, Tursz T. Establishment and characterization of three transplantable EBV-containing nasopharyngeal carcinomas. Int J Cancer 1988, 42:599-606. 10.1002/ijc.2910420422, 2971626.
30. Huang YT, Sheen TS, Chen CL, Lu J, Chang Y, Chen JY, Tsai CH. Profile of cytokine expression in nasopharyngeal carcinomas: a distinct expression of interleukin 1 in tumor and CD4+ T cells. Cancer Res 1999, 59:1599-1605.
31. Zwergal A, Quirling M, Saugel B, Huth KC, Sydlik C, Poli V, Neumeier D, Ziegler-Heitbrock HW, Brand K. C/EBP beta blocks p65 phosphorylation and thereby NF-kappa B-mediated transcription in TNF-tolerant cells. J Immunol 2006, 177:665-672.
32. Ma N, Kawanishi M, Hiraku Y, Murata M, Huang GW, Huang Y, Luo DZ, Mo WG, Fukui Y, Kawanishi S. Reactive nitrogen species-dependent DNA damage in EBV-associated nasopharyngeal carcinoma: the relation to STAT3 activation and EGFR expression. Int J Cancer 2008, 122:2517-2525. 10.1002/ijc.23415, 18307254.
33. Thornburg NJ, Pathmanathan R, Raab-Traub N. Activation of nuclear factor-kappaB p50 homodimer/Bcl-3 complexes in nasopharyngeal carcinoma. Cancer Res 2003, 63:8293-8301.
34. Bowie AG, Zhan J, Marshall WL. Viral appropriation of apoptotic and NF-kappaB signaling pathways. J Cell Biochem 2004, 91:1099-1108. 10.1002/jcb.20026, 15048867.
35. Cai QL, Knight JS, Verma SC, Zald P, Robertson ES. EC5S ubiquitin complex is recruited by KSHV latent antigen LANA for degradation of the VHL and p53 tumor suppressors. PLoS Pathog 2006, 2:e116. 1626105, 17069461, 10.1371/journal.ppat.0020116.
36. Amir-Zilberstein L, Dikstein R. Interplay between E-box and NF-kappaB in regulation of A20 gene by DRB sensitivity-inducing factor (DSIF). J Biol Chem 2008, 283:1317-1323. 10.1074/jbc.M706767200, 17962196.
37. Seitz CS, Deng H, Hinata K, Lin Q, Khavari PA. Nuclear factor kappaB subunits induce epithelial cell growth arrest. Cancer Res 2000, 60:4085-4092.
38. Gapuzan ME, Yufit PV, Gilmore TD. Immortalized embryonic mouse fibroblasts lacking the RelA subunit of transcription factor NF-kappaB have a malignantly transformed phenotype. Oncogene 2002, 21:2484-2492. 10.1038/sj.onc.1205333, 11971183.
39. Seitz CS, Lin Q, Deng H, Khavari PA. Alterations in NF-kappaB function in transgenic epithelial tissue demonstrate a growth inhibitory role for NF-kappaB. Proc Natl Acad Sci USA 1998, 95:2307-2312. 19329, 9482881, 10.1073/pnas.95.5.2307.
40. Dajee M, Lazarov M, Zhang JY, Cai T, Green CL, Russell AJ, Marinkovich MP, Tao S, Lin Q, Kubo Y, Khavari PA. NF-kappaB blockade and oncogenic Ras trigger invasive human epidermal neoplasia. Nature 2003, 421:639-643. 10.1038/nature01283, 12571598.
41. Chen RA, Ryzhakov G, Cooray S, Randow F, Smith GL. Inhibition of IkappaB kinase by vaccinia virus virulence factor B14. PLoS Pathog 2008, 4:e22. 2233672, 18266467, 10.1371/journal.ppat.0040022.
42. Hiscott J, Kwon H, Genin P. Hostile takeovers: viral appropriation of the NF-kappaB pathway. J Clin Invest 2001, 107:143-151. 199181, 11160127, 10.1172/JCI11918.
43. Santoro MG, Rossi A, Amici C. NF-kappaB and virus infection: who controls whom. EMBO J 2003, 22:2552-2560. 156764, 12773372, 10.1093/emboj/cdg267.