Epigenetic repression of p16INK4A by latent epstein-barr virus requires the interaction of EBNA3A and EBNA3C with CtBP

PLoS Pathogens

Volumn 6, Issue 6, 2010, Pages

  Skalska, Lenka ^a   White, Robert E ^a   Franz, Melanie ^a   Ruhmann, Michaela ^a   Allday, Martin J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; BINDING PROTEIN; C TERMINAL BINDING PROTEIN; CYCLIN DEPENDENT KINASE; EBNA3A ANTIGEN; EBNA3B ANTIGEN; EBNA3C ANTIGEN; HISTONE; LATENCY ASSOCIATED NUCLEAR ANTIGEN; P16INK4A KINASE; POLYCOMB GROUP PROTEIN; UNCLASSIFIED DRUG; ALCOHOL DEHYDROGENASE; C-TERMINAL BINDING PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DNA BINDING PROTEIN; EBNA 3A ANTIGEN; EBNA 3C, EPSTEIN BARR VIRUS; EBNA-3A ANTIGEN; EBNA-3C, EPSTEIN-BARR VIRUS; EPSTEIN BARR VIRUS ANTIGEN; MESSENGER RNA; VIRUS ANTIGEN;

ARTICLE; B LYMPHOCYTE; CELL PROLIFERATION; DNA METHYLATION; EPIGENETICS; EPSTEIN BARR VIRUS; LYMPHOBLASTOID CELL LINE; NONHUMAN; VIRUS RECOMBINANT; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; EPSTEIN BARR VIRUS INFECTION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HUMAN; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION; WESTERN BLOTTING;

HUMAN HERPESVIRUS 4;

ALCOHOL OXIDOREDUCTASES; ANTIGENS, VIRAL; B-LYMPHOCYTES; BLOTTING, WESTERN; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA METHYLATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; EPSTEIN-BARR VIRUS INFECTIONS; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HERPESVIRUS 4, HUMAN; HUMANS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSCRIPTIONAL ACTIVATION;

EID: 77954664053     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000951     Document Type: Article

References (71)

1. Bornkamm GW, Hammerschmidt W (2001) Molecular virology of Epstein-Barr virus. Philos Trans R Soc Lond B Biol Sci 356: 437-459.
2. Thorley-Lawson DA, Gross A (2004) Persistence of the Epstein-Barr Virus and the Origins of Associated Lymphomas. The New England journal of medicine 350: 1328-1337.
3. Roughan JE, Thorley-Lawson DA (2009) The intersection of Epstein-Barr virus with the germinal center. J Virol 83: 3968-3976.
4. Crawford DH (2001) Biology and disease associations of Epstein-Barr virus. Philos Trans R Soc Lond B Biol Sci 356: 461-473.
5. Touitou R, O'Nions J, Heaney J, Allday MJ (2005) Epstein-Barr virus EBNA3 proteins bind to the C8/alpha7 subunit of the 20S proteasome and are degraded by 20S proteasomes in vitro, but are very stable in latently infected B cells. J Gen Virol 86: 1269-1277.
6. Tomkinson B, Robertson E, Kieff E (1993) Epstein-Barr virus nuclear proteins EBNA-3A and EBNA-3C are essential for B-lymphocyte growth transformation. J Virol 67: 2014-2025.
7. Tomkinson B, Kieff E (1992) Use of second-site homologous recombination to demonstrate that Epstein-Barr virus nuclear protein 3B is not important for lymphocyte infection or growth transformation in vitro. J Virol 66: 2893-2903.
8. Hertle ML, Popp C, Petermann S, Maier S, Kremmer E, et al. (2009) Differential gene expression patterns of EBV infected EBNA-3A positive and negative human B lymphocytes. PLoS Pathogens 5: e1000506.
9. Le Roux A, Kerdiles B, Walls D, Dedieu JF, Perricaudet M (1994) The Epstein-Barr virus determined nuclear antigens EBNA-3A, -3B, and -3C repress EBNA-2-mediated transactivation of the viral terminal protein 1 gene promoter. Virology 205: 596-602.
10. Waltzer L, Perricaudet M, Sergeant A, Manet E (1996) Epstein-Barr virus EBNA3A and EBNA3C proteins both repress RBP-J kappa-EBNA2-activated transcription by inhibiting the binding of RBP-J kappa to DNA. J Virol 70: 5909-5915.
11. Radkov SA, Touitou R, Brehm A, Rowe M, West M, et al. (1999) Epstein-Barr virus nuclear antigen 3C interacts with histone deacetylase to repress transcription. J Virol 73: 5688-5697.
12. Cludts I, Farrell PJ (1998) Multiple functions within the Epstein-Barr virus EBNA-3A protein. J Virol 72: 1862-1869.
13. Bain M, Watson RJ, Farrell PJ, Allday MJ (1996) Epstein-Barr virus nuclear antigen 3C is a powerful repressor of transcription when tethered to DNA. J Virol 70: 2481-2489.
14. Bourillot PY, Waltzer L, Sergeant A, Manet E (1998) Transcriptional repression by the Epstein-Barr virus EBNA3A protein tethered to DNA does not require RBP-Jkappa. J Gen Virol 79 (Pt2): 363-370.
15. Knight JS, Lan K, Subramanian C, Robertson ES (2003) Epstein-Barr virus nuclear antigen 3C recruits histone deacetylase activity and associates with the corepressors mSin3A and NCoR in human B-cell lines. J Virol 77: 4261-4272.
16. Touitou R, Hickabottom M, Parker G, Crook T, Allday MJ (2001) Physical and Functional Interactions between the Corepressor CtBP and the Epstein-Barr Virus Nuclear Antigen EBNA3C. J Virol 75: 7749-7755.
17. Hickabottom M, Parker GA, Freemont P, Crook T, Allday MJ (2002) Two nonconsensus sites in the Epstein-Barr virus oncoprotein EBNA3A cooperate to bind the co-repressor carboxyl-terminal-binding protein (CtBP). J Biol Chem 277: 47197-47204.
18. Chinnadurai G (2007) Transcriptional regulation by C-terminal binding proteins. Int J Biochem Cell Biol 39: 1593-1607.
19. Shi Y, Sawada J, Sui G, Affar el B, Whetstine JR, et al. (2003) Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature 422: 735-738.
20. Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, et al. (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119: 941-953.
21. Dahiya A, Wong S, Gonzalo S, Gavin M, Dean DC (2001) Linking the Rb and polycomb pathways. Mol Cell 8: 557-569.
22. Mroz EA, Baird AH, Michaud WA, Rocco JW (2008) COOH-terminal binding protein regulates expression of the p16INK4A tumor suppressor and senescence in primary human cells. Cancer Res 68: 6049-6053.
23. Gil J, Peters G (2006) Regulation of the INK4b-ARF-INK4a tumour suppressor locus: all for one or one for all. Nat Rev Mol Cell Biol 7: 667-677.
24. Parker GA, Crook T, Bain M, Sara EA, Farrell PJ, et al. (1996) Epstein-Barr virus nuclear antigen (EBNA)3C is an immortalizing oncoprotein with similar properties to adenovirus E1A and papillomavirus E7. Oncogene 13: 2541-2549.
25. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88: 593-602.
26. Parker GA, Touitou R, Allday MJ (2000) Epstein-Barr virus EBNA3C can disrupt multiple cell cycle checkpoints and induce nuclear division divorced from cytokinesis. Oncogene 19: 700-709.
27. Choudhuri T, Verma SC, Lan K, Murakami M, Robertson ES (2007) The ATM/ATR signaling effector Chk2 is targeted by Epstein-Barr virus nuclear antigen 3C to release the G2/M cell cycle block. J Virol 81: 6718-6730.
28. Gruhne B, Sompallae R, Masucci MG (2009) Three Epstein-Barr virus latency proteins independently promote genomic instability by inducing DNA damage, inhibiting DNA repair and inactivating cell cycle checkpoints. Oncogene 28: 3997-4008.
29. Knight JS, Robertson ES (2004) Epstein-Barr virus nuclear antigen 3C regulates cyclin A/p27 complexes and enhances cyclin A-dependent kinase activity. J Virol 78: 1981-1991.
30. Knight JS, Sharma N, Robertson ES (2005) Epstein-Barr virus latent antigen 3C can mediate the degradation of the retinoblastoma protein through an SCF cellular ubiquitin ligase. Proc Natl Acad Sci U S A 102: 18562-18566.
31. Knight JS, Sharma N, Robertson ES (2005) SCFSkp2 complex targeted by Epstein-Barr virus essential nuclear antigen. Mol Cell Biol 25: 1749-1763.
32. Bajaj BG, Murakami M, Cai Q, Verma SC, Lan K, et al. (2008) Epstein-Barr virus nuclear antigen 3C interacts with and enhances the stability of the c-Myc oncoprotein. J Virol 82: 4082-4090.
33. Saha A, Murakami M, Kumar P, Bajaj B, Sims K, et al. (2009) Epstein-Barr virus nuclear antigen 3C augments Mdm2-mediated p53 ubiquitination and degradation by deubiquitinating Mdm2. J Virol 83: 4652-4669.
34. Yi F, Saha A, Murakami M, Kumar P, Knight JS, et al. (2009) Epstein-Barr virus nuclear antigen 3C targets p53 and modulates its transcriptional and apoptotic activities. Virology 388: 236-247.
35. Maruo S, Wu Y, Ishikawa S, Kanda T, Iwakiri D, et al. (2006) Epstein-Barr virus nuclear protein EBNA3C is required for cell cycle progression and growth maintenance of lymphoblastoid cells. Proc Natl Acad Sci U S A 103: 19500-19505.
36. Maruo S, Johannsen E, Illanes D, Cooper A, Kieff E (2003) Epstein-Barr Virus nuclear protein EBNA3A is critical for maintaining lymphoblastoid cell line growth. J Virol 77: 10437-10447.
37. Anderton E, Yee J, Smith P, Crook T, White RE, et al. (2008) Two Epstein-Barr virus (EBV) oncoproteins cooperate to repress expression of the proapoptotic tumour-suppressor Bim: clues to the pathogenesis of Burkitt's lymphoma. Oncogene 27: 421-433.
38. Paschos K, Smith P, Anderton E, Middeldorp JM, White RE, et al. (2009) Epstein-barr virus latency in B cells leads to epigenetic repression and CpG methylation of the tumour suppressor gene Bim. PLoS Pathogens 5: e1000492.
39. Simon JA, Kingston RE (2009) Mechanisms of Polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 10: 697.
40. Bracken AP, Helin K (2009) Polycomb group proteins: navigators of lineage pathways led astray in cancer. Nat Rev Cancer 9: 773-784.
41. Delecluse HJ, Hilsendegen T, Pich D, Zeidler R, Hammerschmidt W (1998) Propagation and recovery of intact, infectious Epstein-Barr virus from prokaryotic to human cells. Proc Natl Acad Sci U S A 95: 8245-8250.
42. White RE, Calderwood MA, Whitehouse A (2003) Generation and precise modification of a herpesvirus saimiri bacterial artificial chromosome demonstrates that the terminal repeats are required for both virus production and episomal persistence. J Gen Virol 84: 3393-3403.
43. Neuhierl B, Feederle R, Hammerschmidt W, Delecluse HJ (2002) Glycoprotein gp110 of Epstein-Barr virus determines viral tropism and efficiency of infection. Proc Natl Acad Sci U S A 99: 15036-15041.
44. Kia SK, Gorski MM, Giannakopoulos S, Verrijzer CP (2008) SWI/SNF Mediates Polycomb Eviction and Epigenetic Reprogramming of the INK4b-ARF-INK4a Locus. Mol Cell Biol 28: 3457-3464.
45. Barradas M, Anderton E, Acosta JC, Li S, Banito A, et al. (2009) Histone demethylase JMJD3 contributes to epigenetic control of INK4a/ARF by oncogenic RAS. Genes Dev 23: 1177-1182.
46. Agger K, Cloos PA, Rudkjaer L, Williams K, Andersen G, et al. (2009) The H3K27me3 demethylase JMJD3 contributes to the activation of the INK4A-ARF locus in response to oncogene- and stress-induced senescence. Genes Dev 23: 1171-1176.
47. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
48. Lukas J, Parry D, Aagaard L, Mann DJ, Bartkova J, et al. (1995) Retinoblastoma-protein-dependent cell-cycle inhibition by the tumour suppressor p16. Nature 375: 503-506.
49. Sewalt RG, Gunster MJ, van der Vlag J, Satijn DPE, Otte AP (1999) C-Terminal Binding Protein Is a Transcriptional Repressor That Interacts with a Specific Class of Vertebrate Polycomb Proteins. Mol Cell Biol 19: 777-787.
50. Atchison L, Ghias A, Wilkinson F, Bonini N, Atchison ML (2003) Transcription factor YY1 functions as a PcG protein in vivo. EMBO Journal 22: 1347-1358.
51. Srinivasan L, Atchison ML (2004) YY1 DNA binding and PcG recruitment requires CtBP. Genes Dev 18: 2596-2601.
52. Li H, Collado M, Villasante A, Strati K, Ortega S, et al. (2009) The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 460: 1136-1139.
53. Krivtsov AV, Armstrong SA (2007) MLL translocations, histone modifications and leukaemia stem-cell development. Nature Rev Cancer 7: 823-833.
54. Tiwari VK, McGarvey KM, Licchesi JD, Ohm JE, Herman JG, et al. (2008) PcG proteins, DNA methylation, and gene repression by chromatin looping. PLoS Biology 6: 2911-2927.
55. Mujtaba S, Manzur KL, Gurnon JR, Kang M, Van Etten JL, et al. (2008) Epigenetic transcriptional repression of cellular genes by a viral SET protein. Nat Cell Biol 10: 1114-1122.
56. Yang X, He Z, Xin B, Cao L (2000) LMP1 of Epstein-Barr virus suppresses cellular senescence associated with the inhibition of p16INK4a expression. Oncogene 19: 2002-2013.
57. Ohtani N, Brennan P, Gaubatz S, Sanij E, Hertzog P, et al. (2003) Epstein-Barr virus LMP1 blocks p16INK4a-RB pathway by promoting nuclear export of E2F4/5. J Cell Biol 162: 173-183.
58. Keshet I, Schlesinger Y, Farkash S, Rand E, Hecht M, et al. (2006) Evidence for an instructive mechanism of de novo methylation in cancer cells. Nat Genet 38: 149-153.
59. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, et al. (2007) Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 39: 232-236.
60. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, et al. (2006) The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439: 871-874.
61. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, et al. (2007) A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 39: 237-242.
62. Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, et al. (2007) Epigenetic stem cell signature in cancer. Nat Genet 39: 157-158.
63. Cedar H, Bergman Y (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nature Rev Genet 10: 295-304.
64. Klangby U, Okan I, Magnusson KP, Wendland M, Lind P, et al. (1998) p16/ INK4a and p15/INK4b gene methylation and absence of p16/INK4a mRNA and protein expression in Burkitt's lymphoma. Blood 91: 1680-1687.
65. Lindstrom MS, Wiman KG (2002) Role of genetic and epigenetic changes in Burkitt lymphoma. Semin Cancer Biol 12: 381-387.
66. Hernandez-Munoz I, Taghavi P, Kuijl C, Neefjes J, van Lohuizen M (2005) Association of BMI1 with polycomb bodies is dynamic and requires PRC2/ EZH2 and the maintenance DNA methyltransferase DNMT1. Mol Cell Biol 25: 11047-11058.
67. Schaeper U, Boyd JM, Verma S, Uhlmann E, Subramanian T, et al. (1995) Molecular cloning and characterization of a cellular phosphoprotein that interacts with a conserved C-terminal domain of adenovirus E1A involved in negative modulation of oncogenic transformation. Proc Natl Acad Sci U S A 92: 10467-10471.
68. Brown AC, Baigent SJ, Smith LP, Chattoo JP, Petherbridge LJ, et al. (2006) Interaction of MEQ protein and C-terminal-binding protein is critical for induction of lymphomas by Marek's disease virus. Proc Natl Acad Sci U S A 103: 1687-1692.
69. Lee S, Sakakibara S, Maruo S, Zhao B, Calderwood MA, et al. (2009) Epstein-Barr virus nuclear protein 3C domains necessary for lymphoblastoid cell growth: interaction with RBP-Jkappa regulates TCL1. J Virol 83: 12368-12377.
70. Maruo S, Wu Y, Ito T, Kanda T, Kieff ED, et al. (2009) Epstein-Barr virus nuclear protein EBNA3C residues critical for maintaining lymphoblastoid cell growth. Proc Natl Acad Sci U S A 106: 4419-4424.
71. Howley PM, Livingston DM (2009) Small DNA tumor viruses: large contributors to biomedical sciences. Virology 384: 256-259.