Downregulation of Bax mRNA expression and protein stability by the E6 protein of human papillomavirus 16

Journal of General Virology

Volumn 86, Issue 3, 2005, Pages 611-621

  Magal, Sharon Shnitman ^a   Jackman, Anna ^a   Ish Shalom, Shahar ^a   Botzer, Liat Edri ^a   Gonen, Pinhas ^a   Schlegel, Richard ^b   Sherman, Levana ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; MESSENGER RNA; PROTEIN BAX; PROTEIN E6; PROTEIN P53;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL STRAIN; COMPLEX FORMATION; DOWN REGULATION; GENETIC TRANSFECTION; HALF LIFE TIME; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; IN VITRO STUDY; KERATINOCYTE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN STABILITY; STEADY STATE;

BCL-2-ASSOCIATED X PROTEIN; DOWN-REGULATION; GENE EXPRESSION; HUMANS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PROTO-ONCOGENE PROTEINS C-BCL-2; REPRESSOR PROTEINS; RNA, MESSENGER;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16;

EID: 14744287798     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.80453-0     Document Type: Article

References (73)

1. Alfandari, J., Shnitman Magal, S., Jackman, A., Schlegel, R., Gonen, P. & Sherman, L. (1999). HPV16 E6 oncoprotein inhibits apoptosis induced during serum-calcium differentiation of foreskin human keratinocytes. Virology 257, 383-396.
2. Bargou, R. C., Daniel, P. T., Mapara, M. Y., Bommert, K., Wagener, C., Kallinich, B., Royer, H. D. & Dorken, B. (1995). Expression of the bcl-2 gene family in normal and malignant breast tissue: low bax-alpha expression in tumor cells correlates with resistance towards apoptosis. Int J Cancer 60, 854-859.
3. Budtz, P. E. (1994). Epidermal homeostasis: a new model that includes apoptosis. In Apoptosis II: the Molecular Basis of Apoptosis in Disease, pp. 165-184. Edited by L. D. Tomei & F. O. Cope. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
4. Burd, E. M. (2003). Human papillomavairus and cervical cancer. Clin Microbiol Rev 16, 1-17.
5. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W. W. & Prasher, D. C. (1994). Green fluorescent protein as a marker for gene expression. Science 263, 802-805.
6. Chang, Y.-C., Lee, Y.-S., Tejima, T., Tanaka, K., Omura, S., Heintz, N. H., Mitsui, Y. & Magae, J. (1998). mdm2 and bax, downstream mediators of the p53 response, are degraded by the ubiquitin-proteasome pathway. Cell Growth Differ 9, 79-84.
7. Chen, J. J., Reid, C. E., Band, V. & Androphy, E. J. (1995). Interaction of papillomavirus E6 oncoproteins with a putative calcium-binding protein. Science 269, 529-531.
8. Degenhardt, Y.-Y. & Silverstein, S. J. (2001). Gps2, a protein partner for human papillomavirus E6 protein. J Virol 75 151-160.
9. Degli Esposti, M. & Dive, C. (2003). Mitochondrial membrane permeabization by Bax/Bak. Biochem Biophys Res Commun 304, 455-461.
10. Delehedde, M., Cho, S. H., Sarkiss, M., Brisbay, S., Davies, M., El-Naggar, A. K. & McDonnell, T. J. (1999). Altered expression of bcl-2 family member proteins in nonmelanoma skin cancer. Cancer 85, 1514-1522.
11. Dewson, G., Snowden, R. T., Almond, J. B., Dyer, M. J. S. & Cohen, G. M. (2003). Conformational change and mitochondrial translocation of Bax accompany proteasome inhibitor-induced apoptosis of chronic lymphocytic leukemic cells. Oncogene 22, 2643-2654.
12. Eckert, R. L. & Green, H. (1986). Structure and evolution of the human involucrin gene. Cell 46, 583-589.
13. Filippova, M., Song, H., Connolly, J. L., Dermody, T. S. & Duerksen-Hughes, P. J. (2002). The human papillomavirus 16 E6 protein binds to tumor necrosis factor (TNF) R1 and protects cells from TNT-induced apoptosis. J Biol Chem 277, 21730-21739.
14. Gandarillas, A., Goldsmith, L. A., Gschmeissner, S., Leigh, I. M. & Watt, F. M. (1999). Evidence that apoptosis and terminal differentiation of epidermal keratinocytes are distinct processes. Exp Dermatol 8, 71-79.
15. Gao, G. & Dou, Q. P. (2000). N-terminal cleavage of Bax by calpain generates a potent proapoptotic 18-kDa fragment that promotes Bcl-2-independent cytochrome c release and apoptotic cell death. J Cell Biochem 80, 53-72.
16. Gao, Q., Srinivasan, S., Boyer, S. N., Wazer, D. E. & Band, V. (1999). The E6 oncoprotein of high-risk papillomaviruses bind to a novel putative GAP protein E6TP1, and target it for degradation. Mol Cell Biol 19, 733-744.
17. Gao, Q., Kumar, A., Srinivasan, S., Singh, L., Mukai, H., Ono, Y., Wazer, D. E. & Band, V. (2000). PKN binds and phosphorylates human papillomavirus E6 oncoprotein. J Biol Chem 275, 14824-14830.
18. Gewin, L. & Galloway, D. (2001). E-Box-dependent activation of telomerase by human papillomavirus, type 16 E6 does not require induction of c-myc. J Virol 75, 7198-7201.
19. Glaunsinger, B. A., Lee, S. S., Thomas, M., Banks, L. & Javier, R. (2000). Interaction of the PDZ-protein MAGI-1 with adenovirus E4-ORF1 and high-risk papillomavirus E6 oncoproteins. Oncogene 19, 5270-5280.
20. Gross-Mesilaty, S., Reinstein, E., Bercovich, B., Tobias, K. E., Schwartz, A. L., Kahana, C. & Ciechanover, A. (1998). Basal and human papillomavirus E6 oncoprotein-induced degradation of Myc proteins by the ubiquitin pathway. Proc Natl Acad Sci U S A 95, 8058-8063.
21. Han, J., Modha, D. & White, E. (1998). Interaction of E1B 19K with Bax is required to block Bax-induced loss of mitochrondrial membrane potential and apoptosis. Oncogene 17, 2993-3005.
22. Hawley-Nelson, P., Vousden, K. H., Hubbert, N. L., Lowy, D. R. & Schiller, J. T. (1989). HPV16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO J 8, 3905-3910.
23. Hockenbery, D. M., Zutter, M., Hickey, W., Nahm, M. & Korsmeyer, S. J. (1991). BCL2 protein is topographically restricted in tissues characterized by apoptotic cell death. Proc Natl Acad Sci U S A 88, 6961-6965.
24. Huibregtse, J. M., Scheffner, M. & Howley, P. M. (1991). A cellular protein mediates association of p53 with E6 oncoprotein of human papillomavirus tyes 16 or 18. EMBO J 10, 4129-4135.
25. Huibregtse, J. M., Scheffner, M. & Howley, P. M. (1993). Cloning and expression of the cDNA for E6-AP, a protein that mediates the interaction of the human papilllomavirus E6 oncoprotein with p53. Mol Cell Biol 13, 775-784.
26. Jordan, R. C. K., Catzavelos, G. C., Barrett, A. W. & Speight, P. M. (1996). Differential expression of bcl-2 and bax in squamous cell carcinomas of the oral cavity. Eur J Cancer B Oral Oncol 32B, 394-400.
27. L on Bax-induced caspase activation and apoptosis. Oncogene 15, 1763-1772.
28. Kiyono, T., Hiraiwa, H., Fujita, M., Hayashi, Y., Akiyama, T. & Ishibashi, M. (1997). Binding of high-risk human papillomavirus E6 oncoproteins to the human homologue of the Drosophila discs large tumor suppressor protein. Proc Natl Acad Sci U S A 94, 11612-11616.
29. Kuhne, C. & Banks, L. (1998). E3-ubiquitin ligase/E6-AP links multicopy maintenance protein 7 to the ubiquitination pathway by a novel motif, the L2G Box. J Biol Chem 273, 34302-34309.
30. Kukimoto, I., Aihara, S., Yoshiike, K. & Kanda, T. (1998). Human papillomavirus oncoprotein E6 binds to the C-terminal region of human minichromosome maintenance 7 protein. Biochem Biophys Res Commun 249, 258-262.
31. Kumar, A., Zhao, Y., Meng, G. & 9 other authors (2002). Human papillomavirus oncoprotein E6 inactivates the transcriptional coactivator human ADA3. Mol Cell Biol 22, 5801-5812.
32. Lee, S. S., Weiss, R. S. & Javier, R. T. (1997). Binding of human virus oncoproteins to hDlg/SAP97, a mammalian homolog of the Drosophila discs large tumor suppressor protein. Proc Natl Acad Sci U S A 94, 6670-6675.
33. Lee, S. S., Glaunsinger, B., Mantovani, F., Banks, L. & Javier, R. T. (2000). Multi-PDZ domain protein MUPP1 is a cellular target for both adenovirus E4-ORF1 and high-risk papillomavirus type 18 E6 oncoproteins. J Virol 74, 9680-9693.
34. Li, B. & Dou, Q. P. (2000). Bax degradation by the ubiquitin/proteasome-dependent pathway: involvement in tumor survival and progression. Proc Natl Acad Sci U S A 97, 3850-3855.
35. Mantovani, F. & Banks, L. (2001). The human papillomavirus E6 protein and its contribution to malignant progression. Oncogene 20, 7874-7887.
36. Marshall, W. L., Yim, C., Gustafson, E., Graf, T., Sage, D. R., Hanify, K., Williams, L., Fingeroth, J. & Finberg, R. W. (1999). Epstein-Barr virus encodes a novel homolog of the bcl-2 oncogene that inhibits apoptosis and associates with Bax and Bak. J Virol 73, 5181-5185.
37. Marshansky, V., Wang, X., Bertrand, R., Luo, H., Duguid, W., Chinnadurai, G., Kanaan, N., Vu, M. D. & Wu, J. (2001). Proteasomes modulate balance among proapoptotic and antiapoptotic Bcl-2 family members and compromise functioning of the electron transport chain in leukemic cells. J Immunol 166, 3130-3142.
38. Maruoka, Y., Harada, H., Mitsuyasu, T., Seta, Y., Kurokawa, H., Kajiyama, M. & Toyoshima, K. (1997). Keratinocytes become terminally differentiated in a process involving programmed cell death. Biochem Biophys Res Commun 238, 886-890.
39. Mitchell, K. O., Ricci, M. S., Miyashita, T., Dicker, D. T., Jin, Z., Reed, J. C. & El-Deiry, W. S. (2000). Bax is a transcriptional target and mediator of c-Myc-induced apoptosis. Cancer Res 60, 6318-6325.
40. Mitra, R. S., Wrone-Smith, T., Simonian, P., Foreman, K. E., Nunez, G. & Nickoloff, B. J. (1997). Apoptosis in keratinocytes is not dependent on induction of differentiation. Lab Invest 76, 99-107.
41. Miyashita, T. & Reed, J. C. (1995). Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80, 293-299.
42. Miyashita, T., Krajewski, S., Krajewska, M., Wang, H. G., Lin, H. K., Leibermann, D. A., Hoffman, B. & Reed, J. C. (1994). Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9, 1799-1805.
43. Munger, K. & Howley, P. M. (2002). Human papillomavirus immortalizaton and transformation functions. Virus Res 89, 213-228.
44. Nakagawa, S. & Huibregtse, J. M. (2000). Human scribble (Vartul) is targeted for ubiquitin-mediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitin-protein ligase. Mol Cell Biol 20, 8244-8253.
45. Oh, S. T., Kyo, S. & Laimins, L. A. (2001). Telomerase activation by human papillomavirus type 16 E6 protein: induction of human telomerase reverse transcriptase expression through Myc and GC-rich Sp1 binding sites. J Virol 75, 5559-5566.
46. Patel, D., Huang, S. M., Baglia, L. A. & McCance, D. J. (1999). The E6 protein of human papillomavirus type 16 binds to and inhibits co-activation by CBP and p300. EMBO J 18, 5061-5072.
47. Perez, D. & White, E. (2000). TNF-α signals apoptosis through a bid-dependent conformational change in bax that is inhibited by E1B 19K. Mol Cell 6, 53-63.
48. Polakowska, R. R., Piacentini, M., Barlett, R., Goldsmith, L. A. & Haake, A. R. (1994). Apoptosis in human skin development: morphogenesis periderm and stem cells. Dev Dyn 199, 176-188.
49. Reed, J. C. (1998). Bcl-2 family proteins. Oncogene 17, 3225-3236.
50. Ronco, L. V., Karpova, A. Y., Vidal, M. & Howley, P. M. (1998). Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity. Genes Dev 12, 2061-2072.
51. Scheffner, M. & Whitaker, N. J. (2003). Human papillomavirus-induced carcinogenesis and the ubiquitin-proteasome system. Semin Cancer Biol 13, 59-67.
52. Scheffner, M., Werness, B. A., Huibregtse, J. M., Levine, A. J. & Howley, P. M. (1990). The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63, 1129-1136.
53. Schlegel, R., Phelps, W. C., Zhang, Y.-L. & Barbosa, M. (1988). Quantitative keratinocyte assay detects two biological activities of human papillomavirus and identifies viral types associated with cervical carcinoma. EMBO J 7, 3181-3187.
54. Scorrano, L. & Korsmeyer, S. J. (2003). Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem Biophys Res Commun 304, 437-444.
55. Sherman, L. & Schlegel, R. (1996). Serum- and calcium-induced differentiation of human keratinocytes is inhibited by the E6 oncoprotein of human papillomavirus type 16. J Virol 70 3269-3279.
56. Sherman, L., Gazit, A., Yaniv, A., Kawakami, T., Dahlberg, J. E. & Tronick, S. R. (1988). Localization of sequences responsible for trans-activation of the equine infectious anemia virus long terminal repeat. J Virol 62, 120-126.
57. Sherman, L., Jackman, A., Itzhaki, H., Stoppler, M. C., Koval, D. & Schlegel, R. (1997). Inhibition of serum- and calcium-induced differentiation of human keratinocytes by HPV 16 E6 oncoprotein: role of p53 inactivation. Virology 237, 296-306.
58. Sherman, L., Itzhaki, H., Jackman, A., Chen, J. J., Koval, D. & Schlegel, R. (2002). Inhibition of serum- and calcium-induced terminal differentiation of human keratinocytes by HPV 16 E6: study of the association with p53 degradation, inhibition of p53 transactivation and binding to E6BP. Virology 292, 309-320.
59. 6-methylguanine-DNA methyltransferase is a proteolytic target for the E6 human papillomavirus oncoprotein. Oncogene 21 5940-5945.
60. Thomas, M. & Banks, L. (1998). Inhibition of Bak-induced apoptosis by HPV-18 E6. Oncogene 17, 2943-2954.
61. Thomas, M. & Banks, L. (1999). Human papillomavirus (HPV) E6 interactions with Bak are conserved amongst E6 proteins from high and low risk HPV types. J Gen Virol 80, 1513-1517.
62. Thomas, M., Pim, D. & Banks, L. (1999). The role of the E6-p53 interaction in the molecular pathogenesis of HPV. Oncogene 18, 7690-7700.
63. Thomas, M., Laura, R., Hepner, K., Guccione, E., Sawyers, C., Lasky, L. & Banks, L. (2002). Oncogenic human papillomavirus E6 proteins target the MAGI-2 and MAGI-3 proteins for degradation. Oncogene 21, 5088-5096.
64. Thomson, B. J. (2001). Viruses and apoptosis. Int J Exp Pathol 82, 65-76.
65. Tong, X. & Howley, P. M. (1997). The bovine papillomavirus E6 oncoprotein interacts with paxillin and disrupts the actin cytoskeleton. Proc Natl Acad Sci U S A 94, 4412-4417.
66. Tsujimoto, Y. & Shimizu, S. (2000). Bcl-2 family: life-or-death switch. FEBS Lett 466, 6-10.
67. Veldman, T., Horikawa, I., Barrett, J. C. & Schlegel, R. (2001). Transcriptional activation of the telomerase hTERT gene by human papillomavirus type 16 E6 oncoprotein. J Virol 75, 4467-4472.
68. Veldman, T., Liu, X., Yuan, H. & Schlegel, R. (2003). Human papillomavirus E6 and Myc proteins associate in vivo and bind to and cooperatively activate the telomerase reverse-transcriptase. Proc Natl Acad Sci U S A 100, 8211-8216.
69. Wood, D. E., Thomas, A., Devi, L. A., Berman, Y., Beavis, R. C., Reed, J. C. & Newcomb, E. W. (1998). Bax cleavage is mediated by calpain during drug-induced apoptosis. Oncogene 17, 1069-1078.
70. Zimmermann, H., Degenkolbe, R., Bernard, H. U. & O'Connor, M. J. (1999). The human papillomavirus type 16 E6 oncoprotein can down-regulate p53 activity by targeting the transcriptional coactivator CBP/p300. J Virol 73, 6209-6219.
71. Zur-Hausen, H. (1996). Papilloma virus infection - a major cause of human cancers. Biochim Biophys Acta 1288, F55-78.
72. Zur-Hausen, H. (2002). Papillomaviruses and cancer: from basic studies to clinical applications. Nature 2, 342-350.
73. Zwerschke, W. & Jansen-Durr, P. (2000). Cell transformation by the E7 oncoprotein of human papillomavirus type 16: interactions with nuclear and cytoplasmic target proteins. Adv Cancer Res 78, 1-29.