Tip60 degradation by adenovirus relieves transcriptional repression of viral transcriptional activator EIA

Oncogene

Volumn 32, Issue 42, 2013, Pages 5017-5025

  Gupta, A ^a   Jha, S ^a   Engel, D A ^a   Ornelles, D A ^b   Dutta, A ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Adenovirus; EIA; HAT; Tip60

Indexed keywords

ACYLTRANSFERASE; E1A PROTEIN; ELONGIN B; HISTONE H4; PROTEIN P53; PROTEIN TIP60; UNCLASSIFIED DRUG;

ACETYLATION; ADENOVIRUS; APOPTOSIS; ARTICLE; CELL CYCLE REGULATION; CONTROLLED STUDY; DNA DAMAGE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HALF LIFE TIME; HUMAN; HUMAN CELL; NEDDYLATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ADENOVIRUS E1A PROTEINS; ADENOVIRUS E4 PROTEINS; CELL LINE; DNA, VIRAL; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, VIRAL; GENE KNOCKDOWN TECHNIQUES; HCT116 CELLS; HISTONE ACETYLTRANSFERASES; HUMANS; LEUPEPTINS; PROMOTER REGIONS, GENETIC; PROTEASOME INHIBITORS;

ADENOVIRIDAE; ANIMALIA; DNA VIRUSES; MUS; RODENTIA;

EID: 84886089696     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.534     Document Type: Article

References (44)

1. Moran E. Interaction of adenoviral proteins with pRB and p53. FASEB J 1993; 7: 880-885. (Pubitemid 23225544)
2. Whyte P, Buchkovich KJ, Horowitz JM, Friend SH, Raybuck M, Weinberg RA et al. Association between an oncogenes and an anti-oncogene: the adenovirus EIA protein binds to retinoblastoma gene product. Nature 1988; 334: 124-129.
3. DeCapri JA, Ludlow JW, Figge J, Shew JY, Huang CM, Lee WH et al. (1988) SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene. Cell 1988; 54: 275-283.
4. Querido E, Blanchette P, Yan Q, Kamura T, Morrison M, Boivin D et al. Degradation of p53 by adenovirus E4orf6 and EIB55k proteins occurs via a novel mechanism involving a cullin containing complex. Genes Dev 2001; 15: 3104-3117. (Pubitemid 33115675)
5. Stracker TH, Carson CT, Weitzman MD. Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 2002; 418: 348-352. (Pubitemid 34790688)
6. Baker A, Rohleder KJ, Hanakahi LA, Ketner G. Adenovirus E4 34K and E1b55K oncoproteins target host DNA ligase IV for proteasomal degradation. J Virol 2007; 81: 7034-7040. (Pubitemid 46986639)
7. Dallaire F, Blanchette P, Groitl P, Dobner T, Branton PE. Identification of integrin alpha3 as a new substrate of the adenovirus E4orf6/E1B55-kilodalton E3 ubiquitin ligase complex. J Virol 2009; 83: 5329-5338.
8. Blackford AN, Patel RN, Forrester NA, Theil K, Groitl P, Stewart GS et al. Adenovirus 12 E4orf6 inhibits ATR activation by promoting TOPBP1 degradation. Proc Natl Acad Sci USA 2010; 107: 12251-12256.
9. Seligson DB, McBrian MA, Mah V, Yu H, Tze S, Wang Q et al. Global levels of histone modifications predict prognosis in different cancers. Am J Pathol 2009; 174: 1619-1628.
10. Ferrari R, Berk AJ, Kurdistani SK. Viral manipulation of the host epigenome for oncogenic transformation. Nat Rev 2009; 10: 290-294.
11. Niller HH, Wolf H, Minarovits J. Viral hit and run oncogenesis: genetic and epigenetic scenarios. Cancer Lett 2011; 305: 200-217.
12. Jha S, Pol SV, Banerjee NM, Dutta AB, Chow LT, Dutta A. Destabilization of Tip60 by human Papillomavirus E6 results in attenuation of Tip60 dependent transcriptional regulation and apoptotic pathway. Mol Cell 2010; 38: 700-711.
13. Reitsma JM, Savaryn JP, Faust K, Sato H, Halligan BD, Scott ST. Antiviral inhibition targeting the HCMV kinase pUL97 requires pUL27 dependent degradation of Tip60 acetyltransferase and cell cycle arrest. Cell Host Microbe 2011; 9: 103-114.
14. Sterner DE, Berger SL. Acetylation of histones and transcription related factors. Microbiol. Mol Biol Rev 2000; 64: 435-459. (Pubitemid 30412680)
15. Doyon Y, Cote J. The highly conserved and multifunctional NuA4 HAT complex. Curr Opin Genet Dev 2004; 14: 147-154. (Pubitemid 38520142)
16. Ruthenburg AJ, Li H, Patel DJ, Allis CD. Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol 2007; 8: 983-994. (Pubitemid 350174643)
17. Hu Y, Fisher JB, Koprowski S, McAllister D, Kim MS, Lough J. Homozyous disruption of Tip60 gene causes early embryonic lethality. Dev Dyn 2009; 238: 2912-2921.
18. Gorrini C, Squatrito M, Luise C, Syed N, Perna D, Wark L et al. Tip60 is a haploinsufficient tumour suppressor required for an oncogenes induced DNA damage response. Nature 2007; 448: 1063-1067. (Pubitemid 47345581)
19. Sancar A, Lindsey Boltz LA, Unsal-Kacmaz K, Linn S. Molecualr mechanism of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 2004; 73: 39-85. (Pubitemid 39050363)
20. Jha S, Shibata E, Dutta A. Human Rvb1/Tip49 is required for the histone Acetyltransferase activity of Tip60/NuA4 and for the downregulation of phosphorylation on H2AX after DNA damage. Mol Cell Biol 2008; 28: 2690-2700. (Pubitemid 351542368)
21. Sykes SM, Mellert HS, Holbert MA, Li K, Marmorstein R, Lane WS et al. Acetylation of the p53 DNA binding domain regulates apoptosis induction. Mol Cell 2006; 24: 841-851. (Pubitemid 44960096)
22. Tang Y, Luo J, Zhang W, Gu W. Tip60 dependent acetylation of p53 modulates the decision between cell cycle arrest and apoptosis. Mol Cell 2006; 24: 827-839. (Pubitemid 44960094)
23. Bhoumik A, Singha N, O'Connell MJ, Ronai ZA. Regulation of Tip60 by ATF2 modulates ATM activation. J Biol Chem 2008; 283: 17605-17614.
24. Chen J, Morral N, Engel DA. Transcription releases protein VII from adenovirus chromatin. Virology 2007; 369: 411-422. (Pubitemid 350087194)
25. Ferrari R, Pellegrini M, Horwitz GA, Xie W, Berk AJ, Kurdistani SK. Epigenetic reprogramming by Adenovirus eIa. Science 2008; 321: 1086-1088.
26. Horwitz GA, Zhang K, McBrian MA, Grunstein M, Kurdistani SK, Berk AJ. Adenovirus small eia alters global patterns of histone modification. Science 2008; 321: 1084-1085.
27. Ghosh MK, Harter ML. A viral mechanism for remodeling chromatin structure in G0 cells. Mol Cell 2003; 12: 255-260. (Pubitemid 36945049)
28. Sha J, Ghosh MK, Zhang K, Harter ML. E1A interacts with two opposing transcriptional pathways to induce quiescent cells into S phase. J Virol 2010; 84: 4050-4059.
29. Nevels M, Tauber B, Spruss T, Wolf H, Dobner T. Hit and Run transformation by adenovirus oncogenes. J Virol 2001; 75: 3089-3094. (Pubitemid 32225872)
30. Sun Y, Jiang X, Chen S, Fernandes N, Price BD. A role for the Tip60 histone Acetyltransferase in the acetylation and activation of ATM. Proc Natl Acad Sci USA 2005; 102: 13182-13187. (Pubitemid 41324998)
31. Sun Y, Xu Y, Roy K, Price BD. DNA damage induced acetylation of lysine 3016 of ATM kinase activity. Mol Cell Biol 2007; 27: 8502-8509.
32. Kusch T, Florens L, Macdonald WH, Swanson SK, Glaser RL, Yates 3rd JR et al. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 2004; 306: 2084-2087. (Pubitemid 40007658)
33. Murr R, Loizou JI, Yang YG, Cuenin C, Li H, Wang ZQ et al. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double strand breaks. Nat Cell Biol 2006; 8: 91-99. (Pubitemid 43064802)
34. Sapountzi V, Logan IR, Robson CN. Cellular functions of Tip60. Int J Biochem Cell Biol 2006; 38: 1496-1436.
35. Squatrito M, Gorrini C, Amati B. Tip60 in DNA damage response and growth control: many tricks in one HAT. Trends Cell Biol 2006; 16: 433-442. (Pubitemid 44293403)
36. Ikura T, Tashiro S, Kakino A, Shima H, Jacob N, Amunugama R et al. DNA damage dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol Cell Biol 2007; 27: 7028-7040. (Pubitemid 47549742)
37. Karen KA, Hearing P. Adenovirus core protein VII protects viral genome from a DNA damage response at early times after infection. J Virol 2011; 85: 4135-4142.
38. Col E, Caron C, Chable-Bessia C, Legube G, Gazzeri S, Komatsu Y et al. HIV-1 Tat targets Tip60 to impair the apoptotic cell response to genotoxic stresses. EMBO J 2005; 24: 2634-2645. (Pubitemid 41076319)
39. Li R, Zhu J, Xie Z, Liao G, Liu J, Chen MR et al. Conserved Herpesvirus kinases target the DNA damage pathway and Tip60 histone acetyltransferase to promote virus replication. Cell Host Microbe 2011; 10: 390-400.
40. Shamay M, Liu J, Li R, Liao G, Shen L, Greenway M et al. A protein array screen for Kaposi's sarcoma associated Herpesvirus LANA interactors link LANA to Tip60, PP2A activity, and telomere shortening. J Virol 2012; 86: 5179-5191.
41. Johnson JS, Osheim YN, Xue Y, Emanuel MR, Lewis PW, Bankovich A et al. Adenovirus protein VII condenses DNA, represses transcription and associate with transcriptional activator EIA. J Virol 2004; 78: 6459-6468. (Pubitemid 38715944)
42. Zantema A, Fransen JA, Davis-olivier A, Ramaekers FC, Vooijs GP, Deleys B et al. Localization of the EIB proteins of adenovirus 5 in transformed cells as revealed by interaction with monoclonal antibodies. Virology 1985; 142: 44-58. (Pubitemid 16200054)
43. Marton MJ, Bain SB, Ornelles DA, Shenk T. The adenovirus E4 17kilodalton protein complexes with the cellular transcription factor E2F, altering its DNA binding properties and stimulating EIA independent accumulation of E2 mRNA. J Virol 1990; 64: 2345-2359. (Pubitemid 20148483)
44. Barker DD, Berk AJ. Adenovirus proteins from both E1B reading frames are required for the transformation of rodent cells by viral infection and DNA transfection. Virology 1987; 156: 107-121. (Pubitemid 17013653)