Deregulation of eIF4E: 4E-BP1 in differentiated human papillomavirus- containing cells leads to high levels of expression of the E7 oncoprotein

Journal of Virology

Volumn 80, Issue 14, 2006, Pages 7079-7088

  Oh, Kwang Jin ^a   Kalinina, Anna ^a   Park, No Hee ^b   Bagchi, Srilata ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 4E; INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MESSENGER RNA; METHYLCELLULOSE; PROTEIN E7; RAPAMYCIN;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL LINE; CULTURE MEDIUM; HUMAN; HUMAN CELL; KERATINOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; RNA TRANSLATION; STEADY STATE; TRANSCRIPTION REGULATION; TUMOR CELL; UTERINE CERVIX CANCER; VIRUS INFECTION; VIRUS REPLICATION; WART VIRUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTIBIOTICS, ANTINEOPLASTIC; CELL DIFFERENTIATION; EUKARYOTIC INITIATION FACTOR-4E; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE EXPRESSION REGULATION, VIRAL; HELA CELLS; HUMANS; KERATINOCYTES; MODELS, GENETIC; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS E7 PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, MESSENGER; RNA, VIRAL; SIROLIMUS; TIME FACTORS; UP-REGULATION; UTERINE CERVICAL NEOPLASMS; VIRUS REPLICATION;

HUMAN PAPILLOMAVIRUS; PAPILLOMAVIRIDAE;

EID: 33745813943     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02380-05     Document Type: Article

References (46)

1. Avdulov, S., S. Li, V. Michalek, D. Burrichter, M. Peterson, D. M. Perlman, J. C. Manivel, N. Sonenberg, D. Yee, P. B. Bitterman, and V. A. Polunovsky. 2004. Activation of translation complex eIF4F is essential for the genesis and maintenance of the malignant phenotype in human mammary epithelial cells. Cancer Cell 5:553-563.
2. Beretta, L., A. C. Gingras, Y. V. Svitkin, M. N. Hall, and N. Sonenberg. 1996. Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. EMBO J. 15:658-664.
3. Berezutskaya, E., A. Morozov, P. Raychaudhuri, and S. Bagchi. 1997. Differential regulation of the pocket domains of the retinoblastoma family proteins by the HPV16 E7 oncoprotein. Cell Growth Differ. 8:1277-1286.
4. Bjornsti, M. A., and P. J. Houghton. 2004. Lost in translation: dysregulation of cap-dependent translation and cancer. Cancer Cell 5:519-523.
5. Boyer, S. N., D. E. Wazer, and V. Band. 1996. E7 protein of human papillomavirus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res. 56:4620-4624.
6. Bromberg-White, J. L., E. Sen, S. Alam, J. M. Bodily, and C. Meyers. 2003. Induction of the upstream regulatory region of human papillomavirus type 31 by dexamethasone is differentiation dependent. J. Virol. 77:10975-10983.
7. Caron, S., M. Charon, E. Cramer, N. Sonenberg, and I. Dusanter-Fourt. 2004. Selective modification of eukaryotic initiation factor 4F (eIF4F) at the onset of cell differentiation: recruitment of eIF4GII and long-lasting phosphorylation of eIF4E. Mol. Cell. Biol. 24:4920-4928.
8. Cheng, S., D. C. Schmidt-Grimminger, T. Murant, T. R. Broker, and L. T. Chow. 1995. Differentiation-dependent up-regulation of the human papillomavirus E7 gene reactivates cellular DNA replication in suprabasal differentiated keratinocytes. Genes Dev. 9:2335-2349.
9. Dyson, N. 1998. The regulation of E2F by pRb-family proteins. Genes Dev. 12:2245-2262.
10. Fingar, D. C., C. J. Richardson, A. R. Tee, L. Cheatham, C. Tsou, and J. Blenis. 2004. mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol. Cell. Biol. 24:200-216.
11. Flores, E. R., and P. F. Lambert. 1997. Evidence for a switch in the mode of human papillomavirus type 16 DNA replication during the viral life cycle. J. Virol. 71:7167-7179.
12. Flores, E. R., B. L. Allen-Hoffmann, D. Lee, and P. F. Lambert. 2000. The human papillomavirus type 16 E7 oncogene is required for the productive stage of the viral life cycle. J. Virol. 74:6622-6631.
13. Forastiere, A., W. Koch, A. Trotti, and D. Sidransky. 2001. Head and neck cancer. N. Engl. J. Med. 345:1890-1900.
14. Gebauer, F., and M. W. Hentze. 2004. Molecular mechanisms of translational control. Nat. Rev. Mol. Cell Biol. 5:827-835.
15. Gingras, A. C., B. Raught, and N. Sonenberg. 1999. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68:913-963.
16. Gonzalez, S. L., M. Stremlau, X. He, J. R. Basile, and K. Munger. 2001. Degradation of the retinoblastoma tumor suppressor by the human papillomavirus type 16 E7 oncoprotein is important for functional inactivation and is separable from proteasomal degradation of E7. J. Virol. 75:7583-7591.
17. Green, H. 1977. Terminal differentiation of cultured human epidermal cells. Cell 11:405-416.
18. Hall, A. H., and K. A. Alexander. 2003. RNA interference of human papillomavirus type 18 E6 and E7 induces senescence in HeLa cells. J. Virol. 77:6066-6069.
19. Harbour, J. W., and D. C. Dean. 2000. The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev. 14:2393-2409.
20. Hummel, M., J. B. Hudson, and L. A. Laimins. 1992. Differentiation- induced and constitutive transcription of human papillomavirus type 31b in cell lines containing viral episomes. J. Virol. 66:6070-6080.
21. Jeon, S., B. L. Allen-Hoffmann, and P. Lambert. 1995. Integration of human papillomavirus type 16 into the human genome correlates with the selective growth advantage of cells. J. Virol. 69:2989-2997.
22. Jiang, M., and J. Milner. 2002. Selective silencing of viral gene expression in HPV-positive human cervical carcinoma cells treated with siRNA, a primer of RNA interference. Oncogene 21:6041-6048.
23. Joosten, M., M. Blazquez-Domingo, F. Lindeboom, F. Boulme, A. Van Hoven-Beijen, B. Habermann, B. Lowenberg, H. Beug, E. W. Mullner, R. Delwel, and M. Von Lindern. 2004. Translational control of putative proto-oncogene Nm23-M2 by cytokines via phosphoinositide 3-kinase signaling. J. Biol. Chem. 279:38169-38176.
24. 23a.Kazemi, S., S. Papadopoulou, S. Li, Q. Su, S. Wang, A. Yoshimura, G. Matlashewski, T. E. Dever, and A. E. Koromilas. 2004. Control of α subunit of eukaryotic translation initiation factor 2 (eIF2α) phosphorylation by the human papillomavirus type 18 E6 oncoprotein: implications for e1F2α-dependent gene expression and cell death. Mol. Cell. Biol. 24:3415-3429.
25. Kim, M. S., K. H. Shin, J. H. Baek, H. M. Cherrick, and N.-H. Park. 1993. HPV-16, tobacco-specific N-nitrosamine, and N-methyl-N′-nitro-N- nitrosoguanidine in oral carcinogenesis. Cancer Res. 53:4811-4816.
26. Ly, C., A. F. Arechiga, J. V. Melo, C. M. Walsh, and S. T. Ong. 2003. Bcr-Abl kinase modulates the translation regulators ribosomal protein S6 and 4E-BP1 in chronic myelogenous leukemia cells via the mammalian target of rapamycin. Cancer Res. 15;63:5716-5722.
27. Mamane, Y., E. Petroulakis, L. Rong, K. Yoshida, L. Ler, and N. Sonenberg. 2004. eIF4E from translation to transformation. Oncogene 23:3172-3179.
28. McMurray, H. R., D. Nguyen, T. F. Westbrook, and D. J. McAnce. 2001. Biology of human papillomaviruses. Int. J. Exp. Pathol. 82:15-33.
29. Montanaro, L., and P. P. Pandolfi. 2004. Initiation of mRNA translation in oncogenesis: the role of eIF4E. Cell Cycle 3:1387-1389.
30. Morris, D. R., and A. P. Geballe. 2000. Upstream open reading frames as regulators of mRNA translation. Mol. Cell. Biol. 20:8635-8642.
31. Munger, K., A. Baldwin, K. M. Edwards, H. Hayakawa, C. L. Nguyen, M. Owens, M. Grace, and K. W. Hug. 2004. Mechanisms of human papillomavirus-induced oncogenesis. J. Virol. 78:11451-11460.
32. Oh, K.-J., A. Kalinina, J. Wang, K. Nakayama, K. I. Nakayama, and S. Bagchi. 2004. The papillomavirus E7 oncoprotein is ubiquitinated by UbcH7 and Cullin 1- and Skp2-containing E3 ligase. J. Virol. 78:5338-5346.
33. Park, N.-H., B.-M. Min, S.-L. Li, M. Z. Huang, H. M. Cherick, and J. Doniger. 1991. Immortalization of normal human oral keratinocytes with type 16 human papillomavirus. Carcinogenesis 12:1627-1631.
34. Pause, A., G. J. Belsham, A. C. Gingras, O. Donze, T. A. Lin, J. C. Lawrence, Jr., and N. Sonenberg. 1994. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 371:762-767.
35. Reinstein, E., M. Scheffner, M. Oren, A. Ciechanover, and A. Schwartz. 2000. Degradation of the E7 human papillomavirus oncoprotein by the ubiquitin-proteasome system: targeting via ubiquitination of the N-terminal residue. Oncogene 19:5944-5950.
36. Reusch, M. N., F. Stubenrauch, and L. A. Laimins. 1998. Activation of papillomavirus late gene transcription and genome amplification upon differentiation in semisolid medium is coincident with expression of involucrin and transglutaminase but not keratin-10. J. Virol. 72:5016-5024.
37. Ruggero, D., and P. P. Pandolfi. 2003. Does the ribosome translate cancer? Nat. Rev. Cancer 3:179-192.
38. Ruggero, D., L. Montanaro, L. Ma, W. Xu, P. Londei, C. Cordon-Cardo, and P. P. Pandolfi. 2004. The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis. Nat. Med. 10:484-486.
39. Schneider, R. J., and I. Mohr. 2003. Translation initiation and viral tricks. Trends Biochem. Sci. 28:130-136.
40. Terhune, S. S., W. G. Hubert, J. T. Thomas, and L. A. Laimins. 2001. Early polyadenylation signals of human papillomavirus type 31 negatively regulate capsid gene expression. J. Virol. 75:8147-8157.
41. Thomas, J. T., W. G. Hubert, M. N. Ruesch, and L. A. Laimins. 1999. Human papillomavirus type 31 oncoprotein E6 and E7 are required for the maintenance of episomes during the virus life cycles in normal human keratinocytes. Proc. Natl. Acad. Sci. USA 96:8449-8454.
42. Walsh, D., and I. Mohr. 2004. Phosphorylation of eIF4E by Mnk-1 enhances HSV-1 translation and replication in quiescent cells. Genes Dev. 18:660-672.
43. Walsh, D., P. Meleady, B. Power, S. J. Morley, and M. Clynes. 2003. Increased levels of the translation initiation factor eIF4E in differentiating epithelial lung tumor cell lines. Differentiation 71:126-134.
44. Wang, J., A. Sampath, P. Raychaudhuri, and S. Bagchi. 2001. Both Rb and E7 are regulated by the ubiquitin proteasome pathway in HPV-containing cervical tumor cells. Oncogene 20:4740-4749.
45. Zheng, Z.-M., M. Tao, K. Yamanegi, S. Bodaghi, and W. Xiao. 2004. Splicing of a Cap-proximal human papillomavirus 16 E6E7 intron promotes E7 expression, but can be restrained by distance of the intron from its RNA 5′ Cap. J. Mol. Biol. 337:1091-1108.
46. zur Hausen, H. 2002. Papillomaviruses and cancer: from basic studies to clinical application. Nat. Rev. Cancer 2:342-350.