Interaction of NCOR/SMRT Repressor Complexes with Papillomavirus E8^E2C Proteins Inhibits Viral Replication

PLoS Pathogens

Volumn 12, Issue 4, 2016, Pages

  Dreer, Marcel ^a   Fertey, Jasmin ^a   van de Poel, Saskia ^a   Straub, Elke ^a   Madlung, Johannes ^b   Macek, Boris ^b   Iftner, Thomas ^a   Stubenrauch, Frank ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

E8 E2C PROTEIN; NUCLEAR RECEPTOR COREPRESSOR; SILENCING MEDIATOR OF RETINOID AND THYROID HORMONE RECEPTOR; UNCLASSIFIED DRUG; VIRUS PROTEIN; DNA BINDING PROTEIN; NCOR1 PROTEIN, HUMAN; NCOR2 PROTEIN, HUMAN; ONCOGENE PROTEIN E2, HUMAN PAPILLOMAVIRUS TYPE 1; ONCOPROTEIN; RECEPTOR INTERACTING PROTEIN 140; SMALL INTERFERING RNA; VIRUS FUSION PROTEIN;

ARTICLE; CONTROLLED STUDY; GENE REPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; LUCIFERASE ASSAY; MASS SPECTROMETRY; POLYMERASE CHAIN REACTION; PROTEIN INTERACTION; RNA TRANSCRIPTION; SOUTHERN BLOTTING; VIRUS REPLICATION; WART VIRUS; CELL LINE; FLUORESCENCE MICROSCOPY; GENE SILENCING; GENETIC TRANSCRIPTION; HOST PARASITE INTERACTION; KERATINOCYTE; METABOLISM; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTION; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; VIROLOGY;

CELL LINE; CHROMATOGRAPHY, LIQUID; DNA-BINDING PROTEINS; GENE KNOCKDOWN TECHNIQUES; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; KERATINOCYTES; MICROSCOPY, FLUORESCENCE; NUCLEAR RECEPTOR CO-REPRESSOR 1; NUCLEAR RECEPTOR CO-REPRESSOR 2; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; TANDEM MASS SPECTROMETRY; TRANSCRIPTION, GENETIC; TRANSFECTION; VIRAL FUSION PROTEINS; VIRUS REPLICATION;

EID: 84964870464     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005556     Document Type: Article

References (61)

1. Parkin DM, Bray F, (2006) Chapter 2: The burden of HPV-related cancers. Vaccine24Suppl 3: S3/11–25.
2. Howley PM, Pfister HJ, (2015) Beta genus papillomaviruses and skin cancer. Virology479–480: 290–296. doi: 10.1016/j.virol.2015.02.00425724416
3. Stubenrauch F, Laimins LA, (1999) Human papillomavirus life cycle: active and latent phases. Semin Cancer Biol9: 379–386. 10712884
4. Kadaja M, Silla T, Ustav E, Ustav M, (2009) Papillomavirus DNA replication—from initiation to genomic instability. Virology384: 360–368. doi: 10.1016/j.virol.2008.11.03219141359
5. Bergvall M, Melendy T, Archambault J, (2013) The E1 proteins. Virology445: 35–56. doi: 10.1016/j.virol.2013.07.02024029589
6. McBride AA, (2013) The papillomavirus E2 proteins. Virology445: 57–79. doi: 10.1016/j.virol.2013.06.00623849793
7. Stenlund A, (2003) Initiation of DNA replication: lessons from viral initiator proteins. Nat Rev Mol Cell Biol4: 777–785. 14504622
8. Abbate EA, Voitenleitner C, Botchan MR, (2006) Structure of the papillomavirus DNA-tethering complex E2:Brd4 and a peptide that ablates HPV chromosomal association. Mol Cell24: 877–889. 17189190
9. Baxter MK, McPhillips MG, Ozato K, McBride AA, (2005) The mitotic chromosome binding activity of the papillomavirus E2 protein correlates with interaction with the cellular chromosomal protein, Brd4. J Virol79: 4806–4818. 15795266
10. Senechal H, Poirier GG, Coulombe B, Laimins LA, Archambault J, (2007) Amino acid substitutions that specifically impair the transcriptional activity of papillomavirus E2 affect binding to the long isoform of Brd4. Virology358: 10–17. 17023018
11. You J, Croyle JL, Nishimura A, Ozato K, Howley PM, (2004) Interaction of the bovine papillomavirus E2 protein with Brd4 tethers the viral DNA to host mitotic chromosomes. Cell117: 349–360. 15109495
12. Choe J, Vaillancourt P, Stenlund A, Botchan M, (1989) Bovine papillomavirus type 1 encodes two forms of a transcriptional repressor: structural and functional analysis of new viral cDNAs. J Virol63: 1743–1755. 2538655
13. Fertey J, Hurst J, Straub E, Schenker A, Iftner T, et al. (2011) Growth inhibition of HeLa cells is a conserved feature of high-risk human papillomavirus E8^E2C proteins and can also be achieved by an artificial repressor protein. J Virol85: 2918–2926. doi: 10.1128/JVI.01647-1021191025
14. Isok-Paas H, Mannik A, Ustav E, Ustav M, (2015) The transcription map of HPV11 in U2OS cells adequately reflects the initial and stable replication phases of the viral genome. Virol J12: 59. doi: 10.1186/s12985-015-0292-625890000
15. Jeckel S, Loetzsch E, Huber E, Stubenrauch F, Iftner T, (2003) Identification of the E9/E2C cDNA and functional characterization of the gene product reveal a new repressor of transcription and replication in cottontail rabbit papillomavirus. J Virol77: 8736–8744. 12885893
16. Lace MJ, Anson JR, Thomas GS, Turek LP, Haugen TH, (2008) The E8^E2 gene product of human papillomavirus type 16 represses early transcription and replication but is dispensable for viral plasmid persistence in keratinocytes. J Virol82: 10841–10853. doi: 10.1128/JVI.01481-0818753207
17. Lambert PF, Monk BC, Howley PM, (1990) Phenotypic analysis of bovine papillomavirus type 1 E2 repressor mutants. J Virol64: 950–956. 2153256
18. Palermo-Dilts DA, Broker TR, Chow LT, (1990) Human papillomavirus type 1 produces redundant as well as polycistronic mRNAs in plantar warts. J Virol64: 3144–3149. 2159571
19. Sankovski E, Mannik A, Geimanen J, Ustav E, Ustav M, (2014) Mapping of betapapillomavirus human papillomavirus 5 transcription and characterization of viral-genome replication function. J Virol88: 961–973. doi: 10.1128/JVI.01841-1324198410
20. Straub E, Fertey J, Dreer M, Iftner T, Stubenrauch F, (2015) Characterization of the Human Papillomavirus 16 E8 Promoter. J Virol89: 7304–7313. doi: 10.1128/JVI.00616-1525948744
21. Stubenrauch F, Hummel M, Iftner T, Laimins LA, (2000) The E8E2C protein, a negative regulator of viral transcription and replication, is required for extrachromosomal maintenance of human papillomavirus type 31 in keratinocytes. J Virol74: 1178–1186. 10627528
22. Kurg R, Uusen P, Vosa L, Ustav M, (2010) Human papillomavirus E2 protein with single activation domain initiates HPV18 genome replication, but is not sufficient for long-term maintenance of virus genome. Virology408: 159–166. doi: 10.1016/j.virol.2010.09.01020940072
23. Snijders PJ, van den Brule AJ, Schrijnemakers HF, Raaphorst PM, Meijer CJ, et al. (1992) Human papillomavirus type 33 in a tonsillar carcinoma generates its putative E7 mRNA via two E6* transcript species which are terminated at different early region poly(A) sites. J Virol66: 3172–3178. 1313922
24. Straub E, Dreer M, Fertey J, Iftner T, Stubenrauch F, (2014) The viral E8^E2C repressor limits productive replication of human papillomavirus 16. J Virol88: 937–947. doi: 10.1128/JVI.02296-1324198405
25. Zobel T, Iftner T, Stubenrauch F, (2003) The papillomavirus E8-E2C protein represses DNA replication from extrachromosomal origins. Mol Cell Biol23: 8352–8362. 14585992
26. Stubenrauch F, Zobel T, Iftner T, (2001) The E8 domain confers a novel long-distance transcriptional repression activity on the E8E2C protein of high-risk human papillomavirus type 31. J Virol75: 4139–4149. 11287563
27. Ammermann I, Bruckner M, Matthes F, Iftner T, Stubenrauch F, (2008) Inhibition of transcription and DNA replication by the papillomavirus E8-E2C protein is mediated by interaction with corepressor molecules. J Virol82: 5127–5136. doi: 10.1128/JVI.02647-0718353941
28. Powell ML, Smith JA, Sowa ME, Harper JW, Iftner T, et al. (2010) NCoR1 mediates papillomavirus E8;E2C transcriptional repression. J Virol84: 4451–4460. doi: 10.1128/JVI.02390-0920181716
29. Smith JA, White EA, Sowa ME, Powell ML, Ottinger M, et al. (2010) Genome-wide siRNA screen identifies SMCX, EP400, and Brd4 as E2-dependent regulators of human papillomavirus oncogene expression. Proc Natl Acad Sci U S A107: 3752–3757. doi: 10.1073/pnas.091481810720133580
30. Jepsen K, Rosenfeld MG, (2002) Biological roles and mechanistic actions of co-repressor complexes. J Cell Sci115: 689–698. 11865025
31. Karagianni P, Wong J, (2007) HDAC3: taking the SMRT-N-CoRrect road to repression. Oncogene26: 5439–5449. 17694085
32. Watson PJ, Fairall L, Schwabe JW, (2012) Nuclear hormone receptor co-repressors: structure and function. Mol Cell Endocrinol348: 440–449. doi: 10.1016/j.mce.2011.08.03321925568
33. Perissi V, Jepsen K, Glass CK, Rosenfeld MG, (2010) Deconstructing repression: evolving models of co-repressor action. Nat Rev Genet11: 109–123. doi: 10.1038/nrg273620084085
34. Sun Z, Feng D, Fang B, Mullican SE, You SH, et al. (2013) Deacetylase-independent function of HDAC3 in transcription and metabolism requires nuclear receptor corepressor. Mol Cell52: 769–782. doi: 10.1016/j.molcel.2013.10.02224268577
35. Van Doorslaer K, Tan Q, Xirasagar S, Bandaru S, Gopalan V, et al. (2013) The Papillomavirus Episteme: a central resource for papillomavirus sequence data and analysis. Nucleic Acids Res41: D571–578. doi: 10.1093/nar/gks98423093593
36. Crooks GE, Hon G, Chandonia JM, Brenner SE, (2004) WebLogo: a sequence logo generator. Genome Res14: 1188–1190. 15173120
37. Kadaja M, Isok-Paas H, Laos T, Ustav E, Ustav M, (2009) Mechanism of genomic instability in cells infected with the high-risk human papillomaviruses. PLoS Pathog5: e1000397. doi: 10.1371/journal.ppat.100039719390600
38. Tomita A, Buchholz DR, Obata K, Shi YB, (2003) Fusion protein of retinoic acid receptor alpha with promyelocytic leukemia protein or promyelocytic leukemia zinc finger protein recruits N-CoR-TBLR1 corepressor complex to repress transcription in vivo. J Biol Chem278: 30788–30795. 12794076
39. McPhillips MG, Oliveira JG, Spindler JE, Mitra R, McBride AA, (2006) Brd4 is required for e2-mediated transcriptional activation but not genome partitioning of all papillomaviruses. J Virol80: 9530–9543. 16973557
40. Wu SY, Lee AY, Hou SY, Kemper JK, Erdjument-Bromage H, et al. (2006) Brd4 links chromatin targeting to HPV transcriptional silencing. Genes Dev20: 2383–2396. 16921027
41. Schweiger MR, You J, Howley PM, (2006) Bromodomain protein 4 mediates the papillomavirus E2 transcriptional activation function. J Virol80: 4276–4285. 16611886
42. McBride AA, Jang MK, (2013) Current understanding of the role of the Brd4 protein in the papillomavirus lifecycle. Viruses5: 1374–1394. doi: 10.3390/v506137423722886
43. Lambert PF, Hubbert NL, Howley PM, Schiller JT, (1989) Genetic assignment of multiple E2 gene products in bovine papillomavirus-transformed cells. J Virol63: 3151–3154. 2542621
44. Lambert PF, Spalholz BA, Howley PM, (1987) A transcriptional repressor encoded by BPV-1 shares a common carboxy-terminal domain with the E2 transactivator. Cell50: 69–78. 3036366
45. McBride AA, Romanczuk H, Howley PM, (1991) The papillomavirus E2 regulatory proteins. J Biol Chem266: 18411–18414. 1655748
46. Hartman HB, Yu J, Alenghat T, Ishizuka T, Lazar MA, (2005) The histone-binding code of nuclear receptor co-repressors matches the substrate specificity of histone deacetylase 3. EMBO Rep6: 445–451. 15832170
47. Yoon HG, Choi Y, Cole PA, Wong J, (2005) Reading and function of a histone code involved in targeting corepressor complexes for repression. Mol Cell Biol25: 324–335. 15601853
48. Zhang D, Yoon HG, Wong J, (2005) JMJD2A is a novel N-CoR-interacting protein and is involved in repression of the human transcription factor achaete scute-like homologue 2 (ASCL2/Hash2). Mol Cell Biol25: 6404–6414. 16024779
49. Zhou W, Zhu P, Wang J, Pascual G, Ohgi KA, et al. (2008) Histone H2A monoubiquitination represses transcription by inhibiting RNA polymerase II transcriptional elongation. Mol Cell29: 69–80. doi: 10.1016/j.molcel.2007.11.00218206970
50. Fradet-Turcotte A, Moody C, Laimins LA, Archambault J, (2010) Nuclear export of human papillomavirus type 31 E1 is regulated by Cdk2 phosphorylation and required for viral genome maintenance. J Virol84: 11747–11760. doi: 10.1128/JVI.01445-1020844047
51. Frattini MG, Laimins LA, (1994) The role of the E1 and E2 proteins in the replication of human papillomavirus type 31b. Virology204: 799–804. 7941349
52. Gopalakrishnan V, Khan SA, (1994) E1 protein of human papillomavirus type 1a is sufficient for initiation of viral DNA replication. Proc Natl Acad Sci U S A91: 9597–9601. 7937813
53. Stubenrauch F, Colbert AM, Laimins LA, (1998) Transactivation by the E2 protein of oncogenic human papillomavirus type 31 is not essential for early and late viral functions. J Virol72: 8115–8123. 9733852
54. Stubenrauch F, Straub E, Fertey J, Iftner T, (2007) The E8 repression domain can replace the E2 transactivation domain for growth inhibition of HeLa cells by papillomavirus E2 proteins. Int J Cancer121: 2284–2292. 17583574
55. Andrews NC, Faller DV, (1991) A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res19: 2499. 2041787
56. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, et al. (2004) Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J86: 3993–4003. 15189895
57. Borchert N, Dieterich C, Krug K, Schutz W, Jung S, et al. (2010) Proteogenomics of Pristionchus pacificus reveals distinct proteome structure of nematode models. Genome Res20: 837–846. doi: 10.1101/gr.103119.10920237107
58. Rappsilber J, Mann M, Ishihama Y, (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc2: 1896–1906. 17703201
59. Cox J, Mann M, (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol26: 1367–1372. doi: 10.1038/nbt.151119029910
60. Elias JE, Gygi SP, (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods4: 207–214. 17327847
61. Nesvizhskii AI, Aebersold R, (2005) Interpretation of shotgun proteomic data: the protein inference problem. Mol Cell Proteomics4: 1419–1440. 16009968