Brd4 regulation of papillomavirus protein E2 stability

Journal of Virology

Volumn 83, Issue 17, 2009, Pages 8683-8692

  Zheng, Gang ^a   Schweiger, Michal Ruth ^a,b   Martinez Noel, Gustavo ^a   Zheng, Leon ^a   Smith, Jennifer A ^a   Harper, J Wade ^a   Howley, Peter M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CULLIN; CULLIN 3; GLYCOPROTEIN E2; PROTEIN BRD4; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VIRUS PROTEIN; BRD4 PROTEIN, HUMAN; CUL3 PROTEIN, HUMAN; DNA BINDING PROTEIN; E2 PROTEIN, BOVINE PAPILLOMAVIRUS; NUCLEAR PROTEIN; ONCOGENE PROTEIN E2, HUMAN PAPILLOMAVIRUS TYPE 1; ONCOPROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; CONTROLLED STUDY; ENZYME STABILITY; FEMALE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; UBIQUITINATION; VIRUS GENOME; VIRUS TRANSCRIPTION; ANIMAL; BOVINE PAPILLOMAVIRUS TYPE 1; CATTLE; METABOLISM; PHYSIOLOGY; PROTEIN STABILITY;

BOVINAE; PAPILLOMAVIRIDAE;

ANIMALS; BOVINE PAPILLOMAVIRUS 1; CATTLE; CULLIN PROTEINS; DNA-BINDING PROTEINS; HUMAN PAPILLOMAVIRUS 16; HUMANS; NUCLEAR PROTEINS; ONCOGENE PROTEINS, VIRAL; PROTEIN STABILITY; TRANSCRIPTION FACTORS; UBIQUITINATION; VIRAL PROTEINS;

EID: 69249215351     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00674-09     Document Type: Article

References (41)

1. Abbate, E. A., C. Voitenleitner, and M. Botchan. 2006. Structure of the papillomavirus DNA-tethering complex E2:Brd4 and a peptide that ablates HPV chromosomal association. Mol. Cell 24:877-889.
2. Ang, X. L., and J. W. Harper. 2005. SCF-mediated protein degradation and cell cycle control. Oncogene 24:2860-2870. (Pubitemid 40638095)
3. Baxter, M. K., M. G. McPhillips, K. Ozato, and A. A. McBride. 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.
4. Bellanger, S., C. Demeret, S. Goyat, and F. Thierry. 2001. Stability of the human papillomavirus type 18 E2 protein is regulated by a proteasome degradation pathway through its amino-terminal transactivation domain. J. Virol. 75:7244-7251. (Pubitemid 32737984)
5. Crawford, N. P., J. Alsarraj, L. Lukes, R. C. Walker, J. S. Officewala, H. H. Yang, M. P. Lee, K. Ozato, and K. W. Hunter. 2008. Bromodomain 4 activation predicts breast cancer survival. Proc. Natl. Acad. Sci. USA 105: 6380-6385.
6. Cullinan, S. B., J. D. Gordan, J. Jin, J. W. Harper, and J. A. Diehl. 2004. The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase. Mol. Cell. Biol. 24:8477-8486.
7. Dey, A., F. Chitsaz, A. Abbasi, T. Misteli, and K. Ozato. 2003. The double bromodomain protein Brd4 binds to acetylated chromatin during interphase and mitosis. Proc. Natl. Acad. Sci. USA 100:8758-8763.
8. 2-to-M transition. Mol. Cell. Biol. 20:6537-6549.
9. French, C. A., I. Miyoshi, J. C. Aster, I. Kubonishi, T. G. Kroll, P. Dal Cin, S. O. Vargas, A. R. Perez-Atayde, and J. A. Fletcher. 2001. BRD4 bromodomain gene rearrangement in aggressive carcinoma with translocation t(15; 19). Am. J. Pathol. 159:1987-1992.
10. French, C. A., I. Miyoshi, I. Kubonishi, H. E. Grier, A. R. Perez-Atayde, and J. A. Fletcher. 2003. BRD4-NUT fusion oncogene: a novel mechanism in aggressive carcinoma. Cancer Res. 63:304-307.
11. Gagnon, D., S. Joubert, H. Senechal, A. Fradet-Turcotte, S. Torre, and J. Archambault. 2009. Proteasomal degradation of papillomavirus E2 protein is inhibited by overexpression of the bromodomain-containing protein 4. J. Virol. 83:4127-4139.
12. Geyer, R., S. Wee, S. Anderson, J. Yates, and D. A. Wolf. 2003. BTB/POZ domain proteins are putative substrate adaptors for cullin 3 ubiquitin ligases. Mol. Cell 12:783-790. (Pubitemid 37222497)
13. Hattori, T., K. Kitagawa, C. Uchida, T. Oda, and M. Kitagawa. 2003. Cks1 is degraded via the ubiquitin-proteasome pathway in a cell cycle-dependent manner. Genes Cells 8:889-896. (Pubitemid 37428017)
14. Houzelstein, D., S. L. Bullock, D. E. Lynch, E. F. Grigorieva, V. A. Wilson, and R. S. Beddington. 2002. Growth and early postimplantation defects in mice deficient for the bromodomain-containing protein Brd4. Mol. Cell. Biol. 22:3794-3802.
15. Howley, P. M., and D. R. Lowy. 2007. Papillomaviruses, p. 2299-2354. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 5th ed., vol.2. Lippincott, Williams and Wilkins, Philadelphia, PA.
16. Ilves, I., K. Maemets, T. Silla, K. Janikson, and M. Ustav. 2006. Brd4 is involved in multiple processes of the bovine papillomavirus type 1 life cycle. J. Virol. 80:3660-3665.
17. Jin, J., X. L. Ang, T. Shirogane, and J. W. Harper. 2005. Identification of substrates for F-box proteins. Methods Enzymol. 399:287-309.
18. Kipreos, E. T., L. E. Lander, J. P. Wing, W. W. He, and E. M. Hedgecock. 1996. cul-1 is required for cell cycle exit in C. elegans and identifies a novel gene family. Cell 85:829-839.
19. Lee, A. Y., and C. M. Chiang. 2009. Chromatin adaptor Brd4 modulates E2 transcription activity and protein stability. J. Biol. Chem. 284:2778-2786.
20. McPhillips, M. G., J. G. Oliveira, J. E. Spindler, R. Mitra, and A. A. McBride. 2006. Brd4 is required for E2-mediated transcriptional activation but not genome partitioning of all papillomaviruses. J. Virol. 80:9530-9543.
21. Mochizuki, K., A. Nishiyama, M. K. Jang, A. Dey, A. Ghosh, T. Tamura, H. Natsume, H. Yao, and K. Ozato. 2008. The bromodomain protein Brd4 stimulates G1 gene transcription and promotes progression to S phase. J. Biol. Chem. 283:9040-9048.
22. Parish, J. L., A. M. Bean, R. B. Park, and E. J. Androphy. 2006. ChlR1 is required for loading papillomavirus E2 onto mitotic chromosomes and viral genome maintenance. Mol. Cell 24:867-876.
23. Penrose, K. J., M. Garcia-Alai, G. de Prat-Gay, and A. A. McBride. 2004. Casein kinase II phosphorylation-induced conformational switch triggers degradation of the papillomavirus E2 protein. J. Biol. Chem. 279:22430-22439.
24. Penrose, K. J., and A. A. McBride. 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.
25. Petroski, M. D., and R. J. Deshaies. 2005. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 6:9-20.
26. Pintard, L., A. Willems, and M. Peter. 2004. Cullin-based ubiquitin ligases: Cul3-BTB complexes join the family. EMBO J. 23:1681-1687. (Pubitemid 38649631)
27. Pintard, L., J. H. Willis, A. Willems, J. L. Johnson, M. Srayko, T. Kurz, S. Glaser, P. E. Mains, M. Tyers, B. Bowerman, and M. Peter. 2003. The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitinligase. Nature 425:311-316. (Pubitemid 37158408)
28. Poddar, A., S. C. Reed, M. G. McPhillips, J. E. Spindler, and A. A. McBride. 2009. The human papillomavirus type 8 E2 tethering protein targets the ribosomal DNA loci of host mitotic chromosomes. J. Virol. 83:640-650.
29. Schweiger, M. R., M. Ottinger, J. You, and P. M. Howley. 2007. Brd4-independent transcriptional repression function of the papillomavirus E2 proteins. J. Virol. 81:9612-9622. (Pubitemid 350067667)
30. Schweiger, M. R., J. You, and P. M. Howley. 2006. Bromodomain protein 4 mediates the papillomavirus E2 transcriptional activation function. J. Virol. 80:4276-4285.
31. Senechal, H., G. G. Poirier, B. Coulombe, L. A. Laimins, and J. Archambault. 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. (Pubitemid 46048882)
32. Spruck, C. H., and H. M. Strohmaier. 2002. Seek and destroy: SCF ubiquitin ligases in mammalian cell cycle control. Cell Cycle 1:250-254.
33. Thierry, F., J. Heard, K. Dartmann, and M. Yaniv. 1987. Characterization of a transcriptional promoter of human papillomavirus 18 and modulation of its expression by simian virus 40 and adenovirus early antigens. J. Virol. 61: 134-142. (Pubitemid 17212454)
34. van den Heuvel, S. 2004. Protein degradation: CUL-3 and BTB - partners in proteolysis. Curr. Biol. 14:R59-R61.
35. von der Lehr, N., S. Johansson, and L. G. Larsson. 2003. Implication of the ubiquitin/proteasome system in Myc-regulated transcription. Cell Cycle 2:403-407.
36. Wang, X., S. R. Naidu, F. Sverdrup, and E. J. Androphy. 2009. Tax1BP1 interacts with papillomavirus E2 and regulates E2-dependent transcription and stability. J. Virol. 83:2274-2284.
37. Wu, S. Y., A. Y. Lee, S. Y. Hou, J. K. Kemper, H. Erdjument-Bromage, P. Tempst, and C. M. Chiang. 2006. Brd4 links chromatin targeting to HPV transcriptional silencing. Genes Dev. 20:2383-2396.
38. Xu, L., Y. Wei, J. Reboul, P. Vaglio, T. H. Shin, M. Vidal, S. J. Elledge, and J. W. Harper. 2003. BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 425:316-321. (Pubitemid 37158409)
39. 1 gene expression and cell cycle progression. Mol. Cell. Biol. 28:967-976.
40. You, J., J. L. Croyle, A. Nishimura, K. Ozato, and P. M. Howley. 2004. Interaction of the bovine papillomavirus E2 protein with Brd4 tethers the viral DNA to host mitotic chromosomes. Cell 117:349-360. (Pubitemid 38534541)
41. You, J., M. R. Schweiger, and P. M. Howley. 2005. Inhibition of E2 binding to Brd4 enhances viral genome loss and phenotypic reversion of bovine papillomavirus-transformed cells. J. Virol. 79:14956-14961. (Pubitemid 41636292)