Inhibition of p53 by adenovirus type 12 E1B-55K deregulates cell cycle control and sensitizes tumor cells to genotoxic agents

Journal of Virology

Volumn 85, Issue 16, 2011, Pages 7976-7988

  Li, Qiang ^a,b   Zhao, Lisa Y ^a   Zheng, Zhi ^a,c,d   Yang, Heng ^a,c   Santiago, Aleixo ^a,e   Liao, Daiqing ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c BEIJING UNIVERSITY OF CHINESE MEDICINE   (China)

^d Jiangxi Cancer Hospital   (China)

^e JOHNSON AND JOHNSON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DOXORUBICIN; E1B PROTEIN; ETOPOSIDE; HISTIDINE; LENTIVIRUS VECTOR; PHENYLALANINE; PROTEIN MDM2; PROTEIN P21; PROTEIN P53; PUMA PROTEIN; TRYPTOPHAN;

ADENOVIRUS 12; ARTICLE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL LINE; CELL PROLIFERATION; CELL STRAIN A172; CELL STRAIN A549; CELL STRAIN HCT116; CELL STRAIN HEPG2; CHEMOSENSITIZATION; CONTROLLED STUDY; DNA DAMAGE; DRUG CYTOTOXICITY; DRUG POTENTIATION; GENE; GENE ACTIVATION; HUMAN; HUMAN CELL; INHIBITION KINETICS; MDM2 GENE; NONHUMAN; P21 GENE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STABILITY; PUMA GENE; TUMOR CELL; WILD TYPE;

ADENOVIRIDAE; HUMAN ADENOVIRUS TYPE 12;

EID: 79961180962     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00492-11     Document Type: Article

References (57)

1. Berk, A. J. 2005. Recent lessons in gene expression, cell cycle control, and cell biology from adenovirus. Oncogene 24:7673-7685.
2. Bertheau, P., et al. 2007. Exquisite sensitivity of TP53 mutant and basal breast cancers to a dose-dense epirubicin-cyclophosphamide regimen. PLoS Med. 4:e90.
3. Bischoff, J. R., et al. 1996. An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 274:373-376.
4. Blackford, A. N., et al. 2008. A role for E1B-AP5 in ATR signaling pathways during adenovirus infection. J. Virol. 82:7640-7652.
5. Blackford, A. N., and R. J. Grand. 2009. Adenovirus E1B 55-kilodalton protein: multiple roles in viral infection and cell transformation. J. Virol. 83:4000-4012.
6. Brooks, C. L., and W. Gu. 2006. p53 ubiquitination: Mdm2 and beyond. Mol. Cell 21:307-315.
7. Bunz, F., et al. 1999. Disruption of p53 in human cancer cells alters the responses to therapeutic agents. J. Clin. Invest. 104:263-269.
8. Chung, C. H., and M. L. Gillison. 2009. Human papillomavirus in head and neck cancer: its role in pathogenesis and clinical implications. Clin. Cancer Res. 15:6758-6762.
9. Deweese, J. E., and N. Osheroff. 2009. The DNA cleavage reaction of topoisomerase II: wolf in sheep's clothing. Nucleic Acids Res. 37:738-748.
10. Donehower, L. A., and G. Lozano. 2009. 20 years studying p53 functions in genetically engineered mice. Nat. Rev. Cancer 9:831-841.
11. el-Deiry, W. S., et al. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
12. Fakhry, C., et al. 2008. Improved survival of patients with human papillomavirus-positive head and neck squamous cell carcinoma in a prospective clinical trial. J. Natl. Cancer Inst. 100:261-269.
13. Gabler, S., et al. 1998. E1B 55-kilodalton-associated protein: a cellular protein with RNA-binding activity implicated in nucleocytoplasmic transport of adenovirus and cellular mRNAs. J. Virol. 72:7960-7971.
14. Goodrum, F. D., and D. A. Ornelles. 1998. p53 status does not determine outcome of E1B 55-kilodalton mutant adenovirus lytic infection. J. Virol. 72:9479-9490.
15. Grand, R. J., D. Owen, S. M. Rookes, and P. H. Gallimore. 1996. Control of p53 expression by adenovirus 12 early region 1A and early region 1B 54K proteins. Virology 218:23-34.
16. Green, D. R., and G. Kroemer. 2009. Cytoplasmic functions of the tumour suppressor p53. Nature 458:1127-1130.
17. Hall, A. R., B. R. Dix, S. J. O'Carroll, and A. W. Braithwaite. 1998. p53-dependent cell death/apoptosis is required for a productive adenovirus infection. Nat. Med. 4:1068-1072.
18. Harada, J. N., and A. J. Berk. 1999. p53-Independent and -dependent requirements for E1B-55K in adenovirus type 5 replication. J. Virol. 73:5333-5344.
19. Harada, J. N., A. Shevchenko, A. Shevchenko, D. C. Pallas, and A. J. Berk. 2002. Analysis of the adenovirus E1B-55K-anchored proteome reveals its link to ubiquitination machinery. J. Virol. 76:9194-9206.
20. Hickson, I., et al. 2004. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 64:9152-9159.
21. Hobom, U., and M. Dobbelstein. 2004. E1B-55-kilodalton protein is not required to block p53-induced transcription during adenovirus infection. J. Virol. 78:7685-7697.
22. Hutton, F. G., A. S. Turnell, P. H. Gallimore, and R. J. Grand. 2000. Consequences of disruption of the interaction between p53 and the larger adenovirus early region 1B protein in adenovirus E1 transformed human cells. Oncogene 19:452-462.
23. Kim, E., A. Giese, and W. Deppert. 2009. Wild-type p53 in cancer cells: when a guardian turns into a blackguard. Biochem. Pharmacol. 77:11-20.
24. Komarov, P. G., et al. 1999. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 285:1733-1737.
25. Levine, A. J. 1990. The p53 protein and its interactions with the oncogene products of the small DNA tumor viruses. Virology 177:419-426.
26. Li, T. K., and L. F. Liu. 2001. Tumor cell death induced by topoisomerasetargeting drugs. Annu. Rev. Pharmacol. Toxicol. 41:53-77.
27. Liao, D., A. Yu, and A. M. Weiner. 1999. Coexpression of the adenovirus 12 E1B 55 kDa oncoprotein and cellular tumor suppressor p53 is sufficient to induce metaphase fragility of the human RNU2 locus. Virology 254:11-23.
28. Lin, J., J. Chen, B. Elenbaas, and A. J. Levine. 1994. Several hydrophobic amino acids in the p53 amino-terminal domain are required for transcriptional activation, binding to mdm-2 and the adenovirus 5 E1B 55-kD protein. Genes Dev. 8:1235-1246.
29. Liu, Y., A. L. Colosimo, X. J. Yang, and D. Liao. 2000. Adenovirus E1B 55-kilodalton oncoprotein inhibits p53 acetylation by PCAF. Mol. Cell. Biol. 20:5540-5553.
30. Martin, M. E., and A. J. Berk. 1998. Adenovirus E1B 55K represses p53 activation in vitro. J. Virol. 72:3146-3154.
31. Martin, M. E., and A. J. Berk. 1999. Corepressor required for adenovirus E1B 55,000-molecular-weight protein repression of basal transcription. Mol. Cell. Biol. 19:3403-3414.
32. Querido, E., et al. 2001. Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev. 15:3104-3117.
33. Sarnow, P., Y. S. Ho, J. Williams, and A. J. Levine. 1982. Adenovirus E1b-58kd tumor antigen and SV40 large tumor antigen are physically associated with the same 54 kd cellular protein in transformed cells. Cell 28:387-394.
34. Scheffner, M., J. M. Huibregtse, R. D. Vierstra, and P. M. Howley. 1993. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75:495-505.
35. Schreiner, S., et al. 2010. Proteasome-dependent degradation of Daxx by the viral E1B-55K protein in human adenovirus-infected cells. J. Virol. 84:7029-7038.
36. Soria, C., F. E. Estermann, K. C. Espantman, and C. C. O'Shea. 2010. Heterochromatin silencing of p53 target genes by a small viral protein. Nature 466:1076-1081.
37. Soussi, T., and K. G. Wiman. 2007. Shaping genetic alterations in human cancer: the p53 mutation paradigm. Cancer Cell 12:303-312.
38. Steegenga, W. T., N. Riteco, A. G. Jochemsen, F. J. Fallaux, and J. L. Bos. 1998. The large E1B protein together with the E4orf6 protein target p53 for active degradation in adenovirus infected cells. Oncogene 16:349-357.
39. Steegenga, W. T., et al. 1995. Distinct modulation of p53 activity in transcription and cell-cycle regulation by the large (54 kDa) and small (21 kDa) adenovirus E1B proteins. Virology 212:543-554.
40. Tang, J., et al. 2006. Critical role for Daxx in regulating Mdm2. Nat. Cell Biol. 8:855-862.
41. Teodoro, J. G., and P. E. Branton. 1997. Regulation of p53-dependent apoptosis, transcriptional repression, and cell transformation by phosphorylation of the 55-kilodalton E1B protein of human adenovirus type 5. J. Virol. 71:3620-3627.
42. Teodoro, J. G., et al. 1994. Phosphorylation at the carboxy terminus of the 55-kilodalton adenovirus type 5 E1B protein regulates transforming activity. J. Virol. 68:776-786.
43. van den Heuvel, S. J., T. van Laar, I. The, and A. J. van der Eb. 1993. Large E1B proteins of adenovirus types 5 and 12 have different effects on p53 and distinct roles in cell transformation. J. Virol. 67:5226-5234.
44. Varna, M., et al. 2009. p53 dependent cell-cycle arrest triggered by chemotherapy in xenografted breast tumors. Int. J. Cancer 124:991-997.
45. Vogelstein, B., D. Lane, and A. J. Levine. 2000. Surfing the p53 network. Nature 408:307-310.
46. Vousden, K. H., and D. P. Lane. 2007. p53 in health and disease. Nat. Rev. Mol. Cell Biol. 8:275-283.
47. Vousden, K. H., and K. M. Ryan. 2009. p53 and metabolism. Nat. Rev. Cancer 9:691-700.
48. Xu, G. W., J. S. Mymryk, and J. G. Cairncross. 2005. Pharmaceuticalmediated inactivation of p53 sensitizes U87MG glioma cells to BCNU and temozolomide. Int. J. Cancer 116:187-192.
49. Xu, G. W., et al. 2001. Inactivation of p53 sensitizes U87MG glioma cells to 1,3-bis(2-chloroethyl)-1-nitrosourea. Cancer Res. 61:4155-4159.
50. Yew, P. R., and A. J. Berk. 1992. Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein. Nature 357:82-85.
51. Yew, P. R., C. C. Kao, and A. J. Berk. 1990. Dissection of functional domains in the adenovirus 2 early 1B 55K polypeptide by suppressor-linker insertional mutagenesis. Virology 179:795-805.
52. Yew, P. R., X. Liu, and A. J. Berk. 1994. Adenovirus E1B oncoprotein tethers a transcriptional repression domain to p53. Genes Dev. 8:190-202.
53. Yu, A., H. Y. Fan, D. Liao, A. D. Bailey, and A. M. Weiner. 2000. Activation of p53 or loss of the Cockayne syndrome group B repair protein causes metaphase fragility of human U1, U2, and 5S genes. Mol. Cell 5:801-810.
54. Zhao, L. Y., A. L. Colosimo, Y. Liu, Y. Wan, and D. Liao. 2003. Adenovirus E1B 55-kilodalton oncoprotein binds to Daxx and eliminates enhancement of p53-dependent transcription by Daxx. J. Virol. 77:11809-11821.
55. Zhao, L. Y., and D. Liao. 2003. Sequestration of p53 in the cytoplasm by adenovirus type 12 E1B 55-kilodalton oncoprotein is required for inhibition of p53-mediated apoptosis. J. Virol. 77:13171-13181.
56. Zhao, L. Y., et al. 2004. Negative regulation of p53 functions by Daxx and the involvement of MDM2. J. Biol. Chem. 279:50566-50579.
57. Zhao, L. Y., A. Santiago, J. Liu, and D. Liao. 2007. Repression of p53-mediated transcription by adenovirus E1B 55-kDa does not require corepressor mSin3A and histone deacetylases. J. Biol. Chem. 282:7001-7010.