Adenovirus E1A targets the DREF nuclear factor to regulate virus gene expression, DNA replication, and growth

Journal of Virology

Volumn 88, Issue 22, 2014, Pages 13469-13481

  Radko, Sandi ^a   Koleva, Maria ^a   James, Kris M D ^b   Jung, Richard ^a   Mymryk, Joe S ^b   Pelka, Peter ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DREF NUCLEAR FACTOR; E1A PROTEIN; NUCLEAR FACTOR; UNCLASSIFIED DRUG; PROTEIN BINDING; TRANSCRIPTION FACTOR; ZBED1 PROTEIN, HUMAN;

ADENOVIRUS; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DNA REPLICATION; E1A GENE; GENE DOSAGE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENOME ANALYSIS; GROWTH RATE; LIFE CYCLE STAGE; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; VIROGENESIS; VIRUS GENE; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS REPLICATION; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; HUMAN; HUMAN ADENOVIRUS C; METABOLISM; PHYSIOLOGY; PROTEIN ANALYSIS;

ADENOVIRUS E1A PROTEINS; ADENOVIRUSES, HUMAN; CELL LINE; DNA REPLICATION; GENE EXPRESSION REGULATION, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; TRANSCRIPTION FACTORS; VIRUS REPLICATION;

EID: 84908389427     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02538-14     Document Type: Article

References (47)

1. Pelka P, Ablack JN, Torchia J, Turnell AS, Grand RJ, Mymryk JS. 2009. Transcriptional control by adenovirus E1A conserved region 3 via p300/CBP. Nucleic Acids Res. 37:1095-1106. http://dx.doi.org/10.1093/nar/gkn1057.
2. Pelka P, Miller MS, Cecchini M, Yousef AF, Bowdish DM, Dick F, Whyte P, Mymryk JS. 2011. Adenovirus E1A directly targets the E2F/DP-1 complex. J. Virol. 85:8841-8851. http://dx.doi.org/10.1128/JVI.00539-11.
3. Whyte P, Buchkovich KJ, Horowitz JM, Friend SH, Raybuck M, Weinberg RA, Harlow E. 1988. Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product. Nature 334:124-129. http://dx.doi.org/10.1038/334124a0.
4. Shenk T, Flint J. 1991. Transcriptional and transforming activities of the adenovirus E1A proteins. Adv. Cancer Res. 57:47-85. http://dx.doi.org/10.1016/S0065-230X(08)60995-1.
5. Bayley S, Mymryk J. 1994. Adenovirus e1a proteins and transformation (review). Int. J. Oncol. 5:425-444.
6. Pelka P, Ablack JN, Fonseca GJ, Yousef AF, Mymryk JS. 2008. Intrinsic structural disorder in adenovirus E1A: a viral molecular hub linking multiple diverse processes. J. Virol. 82:7252-7263. http://dx.doi.org/10.1128/JVI.00104-08.
7. Albert R. 2005. Scale-free networks in cell biology. J. Cell Sci. 118:4947-4957. http://dx.doi.org/10.1242/jcs.02714.
8. Almaas E. 2007. Biological impacts and context of network theory. J. Exp. Biol. 210:1548-1558. http://dx.doi.org/10.1242/jeb.003731.
9. Madan Babu M, Balaji S, Aravind L. 2007. General trends in the evolution of prokaryotic transcriptional regulatory networks. Genome Dyn. 3:66-80. http://dx.doi.org/10.1159/000107604.
10. Xue Q, Miller-Jensen K. 2012. Systems biology of virus-host signaling network interactions. BMB Rep. 45:213-220. http://dx.doi.org/10.5483/BMBRep.2012.45.4.213.
11. Rozenblatt-Rosen O, Deo RC, Padi M, Adelmant G, Calderwood MA, Rolland T, Grace M, Dricot A, Askenazi M, Tavares M, Pevzner SJ, Abderazzaq F, Byrdsong D, Carvunis AR, Chen AA, Cheng J, Correll M, Duarte M, Fan C, Feltkamp MC, Ficarro SB, Franchi R, Garg BK, Gulbahce N, Hao T, Holthaus AM, James R, Korkhin A, Litovchick L, Mar JC, Pak TR, Rabello S, Rubio R, Shen Y, Singh S, Spangle JM, Tasan M, Wanamaker S, Webber JT, Roecklein-Canfield J, Johannsen E, Barabasi AL, Beroukhim R, Kieff E, Cusick ME, Hill DE, Munger K, Marto JA, Quackenbush J, Roth FP, et al. 2012. Interpreting cancer genomes using systematic host network perturbations by tumour virus proteins. Nature 487:491-495. http://dx.doi.org/10.1038/nature11288.
12. Ferrari R, Berk AJ, Kurdistani SK. 2009. Viral manipulation of the host epigenome for oncogenic transformation. Nat. Rev. Genet. 10:290-294. http://dx.doi.org/10.1038/nrg2539.
13. Ferrari R, Su T, Li B, Bonora G, Oberai A, Chan Y, Sasidharan R, Berk AJ, Pellegrini M, Kurdistani SK. 2012. Reorganization of the host epigenome by a viral oncogene. Genome Res. 22:1212-1221. http://dx.doi.org/10.1101/gr.132308.111.
14. Yousef AF, Fonseca GJ, Cohen MJ, Mymryk JS. 2012. The C-terminal region of E1A: a molecular tool for cellular cartography. Biochem. Cell Biol. 90:153-163. http://dx.doi.org/10.1139/o11-080.
15. Boyd JM, Subramanian T, Schaeper U, La Regina M, Bayley S, Chinnadurai G. 1993. A region in the C-terminus of adenovirus 2/5 E1a protein is required for association with a cellular phosphoprotein and important for the negative modulation of T24-ras mediated transformation, tumorigenesis and metastasis. EMBO J. 12:469-478.
16. Zhang Z, Smith MM, Mymryk JS. 2001. Interaction of the E1A oncoprotein with Yak1p, a novel regulator of yeast pseudohyphal differentiation, and related mammalian kinases. Mol. Biol. Cell 12:699-710. http://dx.doi.org/10.1091/mbc.12.3.699.
17. Komorek J, Kuppuswamy M, Subramanian T, Vijayalingam S, Lomonosova E, Zhao LJ, Mymryk JS, Schmitt K, Chinnadurai G. 2010. Adenovirus type 5 E1A and E6 proteins of low-risk cutaneous beta-human papillomaviruses suppress cell transformation through interaction with FOXK1/K2 transcription factors. J. Virol. 84:2719-2731. http://dx.doi.org/10.1128/JVI.02119-09.
18. Kohler M, Gorlich D, Hartmann E, Franke J. 2001. Adenoviral E1A protein nuclear import is preferentially mediated by importin alpha3 in vitro. Virology 289:186-191. http://dx.doi.org/10.1006/viro.2001.1151.
19. Cohen MJ, Yousef AF, Massimi P, Fonseca GJ, Todorovic B, Pelka P, Turnell AS, Banks L, Mymryk JS. 2013. Dissection of the C-terminal region of E1A re-defines the roles of CtBP and other cellular targets in oncogenic transformation. J. Virol. 87:10348-10355. http://dx.doi.org/10.1128/JVI.00786-13.
20. Ohshima N, Takahashi M, Hirose F. 2003. Identification of a human homologue of the DREF transcription factor with a potential role in regulation of the histone H1 gene. J. Biol. Chem. 278:22928-22938. http://dx.doi.org/10.1074/jbc.M303109200.
21. Harlow E, Franza BR, Jr, Schley C. 1985. Monoclonal antibodies specific for adenovirus early region 1A proteins: extensive heterogeneity in early region 1A products. J. Virol. 55:533-546.
22. Niman HL, Houghten RA, Walker LE, Reisfeld RA, Wilson IA, Hogle JM, Lerner RA. 1983. Generation of protein-reactive antibodies by short peptides is an event of high frequency: implications for the structural basis of immune recognition. Proc. Natl. Acad. Sci. U. S. A. 80:4949-4953. http://dx.doi.org/10.1073/pnas.80.16.4949.
23. Evan GI, Lewis GK, Ramsay G, Bishop JM. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610-3616.
24. Reich NC, Sarnow P, Duprey E, Levine AJ. 1983. Monoclonal antibodies which recognize native and denatured forms of the adenovirus DNAbinding protein. Virology 128:480-484. http://dx.doi.org/10.1016/0042-6822(83)90274-X.
25. Hardy S, Kitamura M, Harris-Stansil T, Dai Y, Phipps ML. 1997. Construction of adenovirus vectors through Cre-lox recombination. J. Virol. 71:1842-1849.
26. Harlow E, Lane D. 1999. Using antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
27. Pelka P, Scime A, Mandalfino C, Joch M, Abdulla P, Whyte P. 2007. Adenovirus E1A proteins direct subcellular redistribution of Nek9, a NimA-related kinase. J. Cell. Physiol. 212:13-25. http://dx.doi.org/10.1002/jcp.20983.
28. Tatham MH, Jaffray E, Vaughan OA, Desterro JM, Botting CH, Naismith JH, Hay RT. 2001. Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J. Biol. Chem. 276:35368-35374. http://dx.doi.org/10.1074/jbc.M104214200.
29. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45. http://dx.doi.org/10.1093/nar/29.9.e45.
30. Hutten S, Chachami G, Winter U, Melchior F, Lamond AI. 2014. A role for the Cajal-body-associated SUMO isopeptidase USPL1 in snRNA transcription mediated byRNApolymerase II. J. Cell Sci. 127:1065-1078. http://dx.doi.org/10.1242/jcs.141788.
31. Yousef AF, Fonseca GJ, Pelka P, Ablack JN, Walsh C, Dick FA, Bazett-Jones DP, Shaw GS, Mymryk JS. 2010. Identification of a molecular recognition feature in the E1A oncoprotein that binds the SUMO conjugase UBC9 and likely interferes with polySUMOylation. Oncogene 29: 4693-4704. http://dx.doi.org/10.1038/onc.2010.226.
32. Hateboer G, Hijmans EM, Nooij JB, Schlenker S, Jentsch S, Bernards R. 1996. mUBC9, a novel adenovirus E1A-interacting protein that complements a yeast cell cycle defect. J. Biol. Chem. 271:25906-25911. http://dx.doi.org/10.1074/jbc.271.42.25906.
33. Eskiw CH, Dellaire G, Mymryk JS, Bazett-Jones DP. 2003. Size, position and dynamic behavior of PML nuclear bodies following cell stress as a paradigm for supramolecular trafficking and assembly. J. Cell Sci. 116: 4455-4466. http://dx.doi.org/10.1242/jcs.00758.
34. Berscheminski J, Wimmer P, Brun J, Ip WH, Groitl P, Horlacher T, Jaffray E, Hay RT, Dobner T, Schreiner S. 2014. Sp100 isoform-specific regulation of human adenovirus 5 gene expression. J. Virol. 88:6076-6092. http://dx.doi.org/10.1128/JVI.00469-14.
35. Ou HD, Kwiatkowski W, Deerinck TJ, Noske A, Blain KY, Land HS, Soria C, Powers CJ, May AP, Shu X, Tsien RY, Fitzpatrick JA, Long JA, Ellisman MH, Choe S, O'Shea CC. 2012. A structural basis for the assembly and functions of a viral polymer that inactivates multiple tumor suppressors. Cell 151:304-319. http://dx.doi.org/10.1016/j.cell.2012.08.035.
36. Yamashita D, Sano Y, Adachi Y, Okamoto Y, Osada H, Takahashi T, Yamaguchi T, Osumi T, Hirose F. 2007. hDREF regulates cell proliferation and expression of ribosomal protein genes. Mol. Cell. Biol. 27:2003-2013. http://dx.doi.org/10.1128/MCB.01462-06.
37. Matsukage A, Hirose F, Yoo MA, Yamaguchi M. 2008. The DRE/DREF transcriptional regulatory system: a master key for cell proliferation. Biochim. Biophys. Acta 1779:81-89. http://dx.doi.org/10.1016/j.bbagrm.2007.11.011.
38. Ledl A, Schmidt D, Muller S. 2005. Viral oncoproteins E1A and E7 and cellular LxCxE proteins repress SUMO modification of the retinoblastoma tumor suppressor. Oncogene 24:3810-3818. http://dx.doi.org/10.1038/sj.onc.1208539.
39. Bruton RK, Pelka P, Mapp KL, Fonseca GJ, Torchia J, Turnell AS, Mymryk JS, Grand RJ. 2008. Identification of a second CtBP binding site in adenovirus type 5 E1A conserved region 3. J. Virol. 82:8476-8486. http://dx.doi.org/10.1128/JVI.00248-08.
40. Pelka P, Ablack JN, Shuen M, Yousef AF, Rasti M, Grand RJ, Turnell AS, Mymryk JS. 2009. Identification of a second independent binding site for the pCAF acetyltransferase in adenovirus E1A. Virology 391:90-98. http://dx.doi.org/10.1016/j.virol.2009.05.024.
41. Dyson N, Guida P, McCall C, Harlow E. 1992. Adenovirus E1A makes two distinct contacts with the retinoblastoma protein. J. Virol. 66:4606-4611.
42. Jentsch S, Psakhye I. 2013. Control of nuclear activities by substrateselective and protein-group SUMOylation. Annu. Rev. Genet. 47:167-186. http://dx.doi.org/10.1146/annurev-genet-111212-133453.
43. Schulz S, Chachami G, Kozaczkiewicz L, Winter U, Stankovic-Valentin N, Haas P, Hofmann K, Urlaub H, Ovaa H, Wittbrodt J, Meulmeester E, Melchior F. 2012. Ubiquitin-specific protease-like 1 (USPL1) is a SUMO isopeptidase with essential, non-catalytic functions. EMBO Rep. 13:930-938. http://dx.doi.org/10.1038/embor.2012.125.
44. Berscheminski J, Groitl P, Dobner T, Wimmer P, Schreiner S. 2013. The adenoviral oncogene E1A-13S interacts with a specific isoform of the tumor suppressor PML to enhance viral transcription. J. Virol. 87:965-977. http://dx.doi.org/10.1128/JVI.02023-12.
45. Mymryk JS, Bayley ST. 1993. Induction of gene expression by exon 2 of the major E1A proteins of adenovirus type 5. J. Virol. 67:6922-6928.
46. Schreiner S, Wodrich H. 2013. Virion factors that target Daxx to overcome intrinsic immunity. J. Virol. 87:10412-10422. http://dx.doi.org/10.1128/JVI.00425-13.
47. Kawamori A, Shimaji K, Yamaguchi M. 2013. Control of e2f1 and PCNA by Drosophila transcription factor DREF. Genesis 51:741-750. http://dx.doi.org/10.1002/dvg.22419.