Phosphorylation of HPV-16 E2 at serine 243 enables binding to Brd4 and mitotic chromosomes

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Chang, Szu Wei ^a   Liu, Wei Chen ^a   Liao, Kuan Yu ^a   Tsao, Yeou Ping ^b   Hsu, Pang Hung ^c   Chen, Show Li ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b MACKAY MEMORIAL HOSPITAL   (Taiwan)

^c NATIONAL TAIWAN OCEAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 CHLOROPHENYL) 2,3,9 TRIMETHYL 6H THIENO[3,2 F][1,2,4]TRIAZOLO[4,3 A][1,4]DIAZEPINE 6 ACETIC ACID TERT BUTYL ESTER; ASPARTIC ACID; BROMODOMAIN PROTEIN 4; GLUTAMIC ACID; HUMAN PAPILLOMAVIRUS 16 E2 PROTEIN; NUCLEIC ACID BINDING PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; BRD4 PROTEIN, HUMAN; DNA BINDING PROTEIN; E2 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 16; GLUTAMINE; NUCLEAR PROTEIN; ONCOPROTEIN; PROTEIN BINDING; SERINE; TRANSCRIPTION FACTOR;

ANAPHASE; ANIMAL CELL; ARTICLE; CHROMOSOME; CONTROLLED STUDY; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN TISSUE; METAPHASE; MITOSIS; NONHUMAN; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; ANIMAL; CHEMISTRY; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; GENETICS; HEK293 CELL LINE; METABOLISM; MUTATION; PHENOTYPE; PHOSPHORYLATION; VIRUS GENOME;

HUMAN PAPILLOMAVIRUS TYPE 16;

ANAPHASE; ANIMALS; ASPARTIC ACID; CERCOPITHECUS AETHIOPS; COS CELLS; DNA-BINDING PROTEINS; GENOME, VIRAL; GLUTAMIC ACID; GLUTAMINE; HEK293 CELLS; HUMAN PAPILLOMAVIRUS 16; HUMANS; METAPHASE; MUTATION; NUCLEAR PROTEINS; ONCOGENE PROTEINS, VIRAL; PHENOTYPE; PHOSPHORYLATION; PROTEIN BINDING; SERINE; TRANSCRIPTION FACTORS;

EID: 84908610689     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110882     Document Type: Article

References (47)

1. zur Hausen H (2009) Papillomaviruses in the causation of human cancers - a brief historical account. Virology 384: 260-265.
2. Moody CA, Laimins LA (2010) Human papillomavirus oncoproteins: pathways to transformation. Nat Rev Cancer 10: 550-560.
3. Parkin DM, Bray F, Ferlay J., Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55: 74-108.
4. Sekhar V, Reed SC, McBride AA (2010) Interaction of the betapapillomavirus E2 tethering protein with mitotic chromosomes. J Virol 84: 543-557.
5. Ilves I, Kivi S, Ustav M (1999) Long-term episomal maintenance of bovine papillomavirus type 1 plasmids is determined by attachment to host chromosomes, which Is mediated by the viral E2 protein and its binding sites. J Virol 73: 4404-4412.
6. Lehman CW, Botchan MR (1998) Segregation of viral plasmids depends on tethering to chromosomes and is regulated by phosphorylation. Proc Natl Acad Sci U S A 95: 4338-4343.
7. McBride AA, Romanczuk H, Howley PM (1991) The papillomavirus E2 regulatory proteins. J Biol Chem 266: 18411-18414.
8. Hamid NA, Brown C, Gaston K (2009) The regulation of cell proliferation by the papillomavirus early proteins. Cell Mol Life Sci 66: 1700-1717.
9. Thierry F (2009) Transcriptional regulation of the papillomavirus oncogenes by cellular and viral transcription factors in cervical carcinoma. Virology 384: 375-379.
10. Yao JM, Breiding DE, Androphy EJ (1998) Functional interaction of the bovine papillomavirus E2 transactivation domain with TFIIB. J Virol 72: 1013-1019.
11. Rehtanz M, Schmidt HM, Warthorst U, Steger G (2004) Direct interaction between nucleosome assembly protein 1 and the papillomavirus E2 proteins involved in activation of transcription. Mol Cell Biol 24: 2153-2168.
12. Muller A, Ritzkowsky A, Steger G (2002) Cooperative activation of human papillomavirus type 8 gene expression by the E2 protein and the cellular coactivator p300. J Virol 76: 11042-11053.
13. Lee D, Hwang SG, Kim J, Choe J (2002) Functional interaction between p/CAF and human papillomavirus E2 protein. J Biol Chem 277: 6483-6489.
14. Wu MH, Chan JY, Liu P.Y., Liu ST, Huang SM (2007) Human papillomavirus E2 protein associates with nuclear receptors to stimulate nuclear receptor- and E2-dependent transcriptional activations in human cervical carcinoma cells. Int J Biochem Cell Biol 39: 413-425.
15. Chang SW, Tsao YP, Lin C.Y., Chen SL (2011) NRIP, a novel calmodulin binding protein, activates calcineurin to dephosphorylate human papillomavirus E2 protein. J Virol 85: 6750-6763.
16. McPhillips MG, Oliveira JG, Spindler J.E., Mitra R., McBride AA (2006) Brd4 is required for e2-mediated transcriptional activation but not genome partitioning of all papillomaviruses. J Virol 80: 9530-9543.
17. Schweiger MR, You J, Howley PM (2006) Bromodomain protein 4 mediates the papillomavirus E2 transcriptional activation function. J Virol 80: 4276-4285.
18. 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. Cell 117: 349-360.
19. Dey A, Chitsaz F, Abbasi A., Misteli T, Ozato K (2003) The double bromodomain protein Brd4 binds to acetylated chromatin during interphase and mitosis. Proc Natl Acad Sci U S A 100: 8758-8763.
20. 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 Virol 79: 4806-4818.
21. McPhillips MG, Ozato K, McBride AA (2005) Interaction of bovine papillomavirus E2 protein with Brd4 stabilizes its association with chromatin. J Virol 79: 8920-8932.
22. Brannon AR, Maresca JA, Boeke J.D., Basrai MA, McBride AA (2005) Reconstitution of papillomavirus E2-mediated plasmid maintenance in Saccha-romyces cerevisiae by the Brd4 bromodomain protein. Proc Natl Acad Sci U S A 102: 2998-3003.
23. You J, Schweiger MR, Howley PM (2005) Inhibition of E2 binding to Brd4 enhances viral genome loss and phenotypic reversion of bovine papillomavirus-transformed cells. J Virol 79: 14956-14961.
24. Abbate EA, Voitenleitner C, Botchan MR (2006) Structure of the papilloma-virus DNA-tethering complex E2:Brd4 and a peptide that ablates HPV chromosomal association. Mol Cell 24: 877-889.
25. Helfer CM, Wang R, You J (2013) Analysis of the papillomavirus E2 and bromodomain protein Brd4 interaction using bimolecular fluorescence complementation. PLoS One 8: e77994.
26. Wang X, Helfer CM, Pancholi N, Bradner J.E., You J (2013) Recruitment of Brd4 to the human papillomavirus type 16 DNA replication complex is essential for replication of viral DNA. J Virol 87: 3871-3884.
27. Sekhar V, McBride AA (2012) Phosphorylation regulates binding of the human papillomavirus type 8 E2 protein to host chromosomes. J Virol 86: 10047-10058.
28. Penrose KJ, Garcia-Alai M, de Prat-Gay G, McBride AA (2004) Casein Kinase II phosphorylation-induced conformational switch triggers degradation of the papillomavirus E2 protein. J Biol Chem 279: 22430-22439.
29. Chang SW, Lu PY, Guo J.H., Tsai TC, Tsao YP, et al. (2012) NRIP enhances HPV gene expression via interaction with either GR or E2. Virology 423: 38-48.
30. McBride AA (2013) The papillomavirus E2 proteins. Virology 445: 57-79.
31. Poddar A, Reed SC, McPhillips M.G., Spindler JE, McBride AA (2009) The human papillomavirus type 8 E2 tethering protein targets the ribosomal DNA loci of host mitotic chromosomes. J Virol 83: 640-650.
32. McBride AA (2008) Replication and partitioning of papillomavirus genomes. Adv Virus Res 72: 155-205.
33. Gagnon D, Joubert S, Senechal H., Fradet-Turcotte A, Torre S, et al. (2009) Proteasomal degradation of the papillomavirus E2 protein is inhibited by overexpression of bromodomain-containing protein 4. J Virol 83: 4127-4139.
34. Lee AY, Chiang CM (2009) Chromatin adaptor Brd4 modulates E2 transcription activity and protein stability. J Biol Chem 284: 2778-2786.
35. Nishiyama A, Dey A, Miyazaki J., Ozato K (2006) Brd4 is required for recovery from antimicrotubule drug-induced mitotic arrest: preservation of acetylated chromatin. Mol Biol Cell 17: 814-823.
36. Yang Z, He N, Zhou Q (2008) Brd4 recruits P-TEFb to chromosomes at late mitosis to promote G1 gene expression and cell cycle progression. Mol Cell Biol 28: 967-976.
37. Donaldson MM, Boner W, Morgan IM (2007) TopBP1 regulates human papillomavirus type 16 E2 interaction with chromatin. J Virol 81: 4338-4342.
38. Gammoh N, Grm HS, Massimi P, Banks L (2006) Regulation of human papillomavirus type 16 E7 activity through direct protein interaction with the E2 transcriptional activator. J Virol 80: 1787-1797.
39. Zheng PS, Brokaw J, McBride AA (2005) Conditional mutations in the mitotic chromosome binding function of the bovine papillomavirus type 1 E2 protein. J Virol 79: 1500-1509.
40. Abroi A, Ilves I, Kivi S., Ustav M (2004) Analysis of chromatin attachment and partitioning functions of bovine papillomavirus type 1 E2 protein. J Virol 78: 2100-2113.
41. Parish JL, Bean AM, Park R.B., Androphy EJ (2006) ChlR1 is required for loading papillomavirus E2 onto mitotic chromosomes and viral genome maintenance. Mol Cell 24: 867-876.
42. Dao LD, Duffy A, Van Tine BA, Wu SY, Chiang CM, et al. (2006) Dynamic localization of the human papillomavirus type 11 origin binding protein E2 through mitosis while in association with the spindle apparatus. J Virol 80: 4792-4800.
43. Yu T, Peng YC, Androphy EJ (2007) Mitotic kinesin-like protein 2 binds and colocalizes with papillomavirus E2 during mitosis. J Virol 81: 1736-1745.
44. Senechal H, Poirier GG, Coulombe B, Laimins L.A., Archambault J (2007) Amino acid substitutions that specifically impair the transcriptional activity of papillomavirus E2 affect binding to the long isoform of Brd4. Virology 358: 10-17.
45. Zheng G, Schweiger MR, Martinez-Noel G, Zheng L., Smith JA, et al. (2009) Brd4 regulation of papillomavirus protein E2 stability. J Virol 83: 8683-8692.
46. Penrose KJ, McBride AA (2000) Proteasome-mediated degradation of the papillomavirus E2-TA protein is regulated by phosphorylation and can modulate viral genome copy number. J Virol 74: 6031-6038.
47. Vosa L, Sudakov A, Remm M., Ustav M, Kurg R (2012) Identification and analysis of papillomavirus E2 protein binding sites in the human genome. J Virol 86: 348-357.