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[Cancer Research 56, 4620-4624, October 15, 1996]
© 1996 American Association for Cancer Research

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E7 Protein of Human Papilloma Virus-16 Induces Degradation of Retinoblastoma Protein through the Ubiquitin-Proteasome Pathway1

Sarah N. Boyer, David E. Wazer and Vimla Band2

Department of Radiation Oncology, New England Medical Center [D.E.W., V.B.], and Department of Biochemistry [V.B.] and Genetics Program [S.N.B., V.B.], Tufts University School of Medicine, Boston, Massachusetts 02111

Rb protein is a critical regulator of entry into the cell cycle, and loss of Rb function by deletions, mutations, or interaction with DNA viral oncoproteins leads to oncogenic transformation. We have shown that the human papilloma virus (HPV)-16 E7 gene is sufficient to induce the immortalization of mammary epithelial cells (MECs). Surprisingly, the steady-state level of Rb protein in these immortal cells was drastically decreased. Here, we used pulse-chase analysis to show that the in vivo loss of Rb protein in E7-immortalized MECs is a consequence of enhanced degradation. Expression of HPV16 E7 in a cell line with a temperaturesensitive mutation in the E1 enzyme of the ubiquitin pathway demonstrated that degradation of Rb was ubiquitin dependent. Treatment of E7-immortalized MECs with aldehyde inhibitors of proteasome-associated proteases led to a marked stabilization of Rb protein, particularly the hypophosphorylated form. Taken together, our results provide evidence for HPV-16 E7-induced enhanced degradation of Rb protein via a ubiquitin-proteasome pathway and suggest a second mechanism of oncogenic transformation by E7, in addition to its previously identified ability to sequester Rb from E2F. Our analyses also show that normal Rb levels are regulated by the ubiquitin-proteasome degradation pathway.

1 This work was supported by NIH Grants CA56803 and CA64823 (to V. B.).

2 To whom requests for reprints should be addressed, at Department of Radiation Oncology, New England Medical Center, 750 Washington Street, Boston, MA 02111. Phone: (617) 636-4776; Fax: (617) 636-6205.

Received 7/29/96. Accepted 8/27/96.




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S. Duensing and K. Munger
The Human Papillomavirus Type 16 E6 and E7 Oncoproteins Independently Induce Numerical and Structural Chromosome Instability
Cancer Res., December 1, 2002; 62(23): 7075 - 7082.
[Abstract] [Full Text] [PDF]


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Genes Dev.Home page
X. Zou, D. Ray, A. Aziyu, K. Christov, A. D. Boiko, A. V. Gudkov, and H. Kiyokawa
Cdk4 disruption renders primary mouse cells resistant to oncogenic transformation, leading to Arf/p53-independent senescence
Genes & Dev., November 15, 2002; 16(22): 2923 - 2934.
[Abstract] [Full Text] [PDF]


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Mol. Cell. Biol.Home page
T. F. Westbrook, D. X. Nguyen, B. R. Thrash, and D. J. McCance
E7 Abolishes Raf-Induced Arrest via Mislocalization of p21Cip1
Mol. Cell. Biol., October 15, 2002; 22(20): 7041 - 7052.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
R. B. Park and E. J. Androphy
Genetic Analysis of High-Risk E6 in Episomal Maintenance of Human Papillomavirus Genomes in Primary Human Keratinocytes
J. Virol., October 11, 2002; 76(22): 11359 - 11364.
[Abstract] [Full Text] [PDF]


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Mol. Cell. Biol.Home page
A. Kumar, Y. Zhao, G. Meng, M. Zeng, S. Srinivasan, L. M. Delmolino, Q. Gao, G. Dimri, G. F. Weber, D. E. Wazer, et al.
Human Papillomavirus Oncoprotein E6 Inactivates the Transcriptional Coactivator Human ADA3
Mol. Cell. Biol., August 15, 2002; 22(16): 5801 - 5812.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
D. Spitkovsky, S. P. Hehner, T. G. Hofmann, A. Moller, and M. L. Schmitz
The Human Papillomavirus Oncoprotein E7 Attenuates NF-kappa B Activation by Targeting the Ikappa B Kinase Complex
J. Biol. Chem., July 5, 2002; 277(28): 25576 - 25582.
[Abstract] [Full Text] [PDF]


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Mol. Cell. Biol.Home page
W. Bao, M. Thullberg, H. Zhang, A. Onischenko, and S. Stromblad
Cell Attachment to the Extracellular Matrix Induces Proteasomal Degradation of p21CIP1 via Cdc42/Rac1 Signaling
Mol. Cell. Biol., July 1, 2002; 22(13): 4587 - 4597.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
Q. Gao, A. Kumar, L. Singh, J. M. Huibregtse, S. Beaudenon, S. Srinivasan, D. E. Wazer, H. Band, and V. Band
Human Papillomavirus E6-induced Degradation of E6TP1 Is Mediated by E6AP Ubiquitin Ligase
Cancer Res., June 1, 2002; 62(11): 3315 - 3321.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
F. A. Dick and N. J. Dyson
Three Regions of the pRB Pocket Domain Affect Its Inactivation by Human Papillomavirus E7 Proteins
J. Virol., May 13, 2002; 76(12): 6224 - 6234.
[Abstract] [Full Text] [PDF]


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Physiol. Rev.Home page
M. H. Glickman and A. Ciechanover
The Ubiquitin-Proteasome Proteolytic Pathway: Destruction for the Sake of Construction
Physiol Rev, April 1, 2002; 82(2): 373 - 428.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
S. Dawson, S. Apcher, M. Mee, H. Higashitsuji, R. Baker, S. Uhle, W. Dubiel, J. Fujita, and R. J. Mayer
Gankyrin Is an Ankyrin-repeat Oncoprotein That Interacts with CDK4 Kinase and the S6 ATPase of the 26 S Proteasome
J. Biol. Chem., March 22, 2002; 277(13): 10893 - 10902.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
W.-M. Chien, F. Noya, H. M. Benedict-Hamilton, T. R. Broker, and L. T. Chow
Alternative Fates of Keratinocytes Transduced by Human Papillomavirus Type 18 E7 during Squamous Differentiation
J. Virol., February 22, 2002; 76(6): 2964 - 2972.
[Abstract] [Full Text] [PDF]


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CarcinogenesisHome page
M. Loignon and E. A. Drobetsky
The initiation of UV-induced G1 arrest in human cells is independent of the p53/p21/pRb pathway but can be attenuated through expression of the HPV E7 oncoprotein
Carcinogenesis, January 1, 2002; 23(1): 35 - 45.
[Abstract] [Full Text] [PDF]


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Cell Growth Differ.Home page
E. C. Goodwin and D. DiMaio
Induced Senescence in HeLa Cervical Carcinoma Cells Containing Elevated Telomerase Activity and Extended Telomeres
Cell Growth Differ., November 1, 2001; 12(11): 525 - 534.
[Abstract] [Full Text] [PDF]


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Cancer Epidemiol. Biomarkers Prev.Home page
S. Nam, D. M. Smith, and Q. P. Dou
Tannic Acid Potently Inhibits Tumor Cell Proteasome Activity, Increases p27 and Bax Expression, and Induces G1 Arrest and Apoptosis
Cancer Epidemiol. Biomarkers Prev., October 1, 2001; 10(10): 1083 - 1088.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
S. L. Gonzalez, M. Stremlau, X. He, J. R. Basile, and K. Munger
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., August 15, 2001; 75(16): 7583 - 7591.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
S. Duensing, A. Duensing, E. R. Flores, A. Do, P. F. Lambert, and K. Munger
Centrosome Abnormalities and Genomic Instability by Episomal Expression of Human Papillomavirus Type 16 in Raft Cultures of Human Keratinocytes
J. Virol., August 15, 2001; 75(16): 7712 - 7716.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
A.-M. Helt and D. A. Galloway
Destabilization of the Retinoblastoma Tumor Suppressor by Human Papillomavirus Type 16 E7 Is Not Sufficient To Overcome Cell Cycle Arrest in Human Keratinocytes
J. Virol., August 1, 2001; 75(15): 6737 - 6747.
[Abstract] [Full Text]


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J. Virol.Home page
M. Giarrè, S. Caldeira, I. Malanchi, F. Ciccolini, M. J. Leão, and M. Tommasino
Induction of pRb Degradation by the Human Papillomavirus Type 16 E7 Protein Is Essential To Efficiently Overcome p16INK4a-Imposed G1 Cell Cycle Arrest
J. Virol., May 15, 2001; 75(10): 4705 - 4712.
[Abstract] [Full Text]


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Cancer Epidemiol. Biomarkers Prev.Home page
J. Kim, D. M. Shin, A. El-Naggar, J. S. Lee, C. Corrales, S. M. Lippman, W. K. Hong, and W. N. Hittelman
Chromosome Polysomy and Histological Characteristics in Oral Premalignant Lesions
Cancer Epidemiol. Biomarkers Prev., April 1, 2001; 10(4): 319 - 325.
[Abstract] [Full Text]


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J. Gen. Virol.Home page
K. Webster, A. Taylor, and K. Gaston
Oestrogen and progesterone increase the levels of apoptosis induced by the human papillomavirus type 16 E2 and E7 proteins
J. Gen. Virol., January 1, 2001; 82(1): 201 - 213.
[Abstract] [Full Text]


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Proc. Natl. Acad. Sci. USAHome page
E. C. Goodwin and D. DiMaio
Repression of human papillomavirus oncogenes in HeLa cervical carcinoma cells causes the orderly reactivation of dormant tumor suppressor pathways
PNAS, November 7, 2000; 97(23): 12513 - 12518.
[Abstract] [Full Text] [PDF]


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Mol. Cell. Biol.Home page
L. Wu, E. C. Goodwin, L. K. Naeger, E. Vigo, K. Galaktionov, K. Helin, and D. DiMaio
E2F-Rb Complexes Assemble and Inhibit cdc25A Transcription in Cervical Carcinoma Cells following Repression of Human Papillomavirus Oncogene Expression
Mol. Cell. Biol., October 1, 2000; 20(19): 7059 - 7067.
[Abstract] [Full Text]


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Mol. Cell. Biol.Home page
B. Mannhardt, S. A. Weinzimer, M. Wagner, M. Fiedler, P. Cohen, P. Jansen-Dürr, and W. Zwerschke
Human Papillomavirus Type 16 E7 Oncoprotein Binds and Inactivates Growth-Inhibitory Insulin-Like Growth Factor Binding Protein 3
Mol. Cell. Biol., September 1, 2000; 20(17): 6483 - 6495.
[Abstract] [Full Text]


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Cell Growth Differ.Home page
W.-M. Chien, J. N. Parker, D.-C. Schmidt-Grimminger, T. R. Broker, and L. T. Chow
Casein Kinase II Phosphorylation of the Human Papillomavirus-18 E7 Protein Is Critical for Promoting S-Phase Entry
Cell Growth Differ., August 1, 2000; 11(8): 425 - 435.
[Abstract] [Full Text]


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J. Virol.Home page
W. H. Kao, S. L. Beaudenon, A. L. Talis, J. M. Huibregtse, and P. M. Howley
Human Papillomavirus Type 16 E6 Induces Self-Ubiquitination of the E6AP Ubiquitin-Protein Ligase
J. Virol., July 15, 2000; 74(14): 6408 - 6417.
[Abstract] [Full Text]


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J. Biol. Chem.Home page
Q. Gao, A. Kumar, S. Srinivasan, L. Singh, H. Mukai, Y. Ono, D. E. Wazer, and V. Band
PKN Binds and Phosphorylates Human Papillomavirus E6 Oncoprotein
J. Biol. Chem., May 12, 2000; 275(20): 14824 - 14830.
[Abstract] [Full Text] [PDF]


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JNCI J Natl Cancer InstHome page
H. z. Hausen
Papillomaviruses Causing Cancer: Evasion From Host-Cell Control in Early Events in Carcinogenesis
J Natl Cancer Inst, May 3, 2000; 92(9): 690 - 698.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
M. N. Aronson, A. D. Meyer, J. Györgyey, L. Katul, H. J. Vetten, B. Gronenborn, and T. Timchenko
Clink, a Nanovirus-Encoded Protein, Binds both pRB and SKP1
J. Virol., April 1, 2000; 74(7): 2967 - 2972.
[Abstract] [Full Text]


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J. Cell Sci.Home page
Q. Chen, V. Tu, J Catania, M Burton, O Toussaint, and T Dilley
Involvement of Rb family proteins, focal adhesion proteins and protein synthesis in senescent morphogenesis induced by hydrogen peroxide
J. Cell Sci., January 11, 2000; 113(22): 4087 - 4097.
[Abstract] [PDF]


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J. Biol. Chem.Home page
J.-S. Park, S. Boyer, K. Mitchell, D. Gilfor, M. Birrer, G. Darlington, W. El Deiry, G. L. Firestone, K. Munger, V. Band, et al.
Expression of Human Papilloma Virus E7 Protein Causes Apoptosis and Inhibits DNA Synthesis in Primary Hepatocytes via Increased Expression of p21Cip-1/WAF1/MDA6
J. Biol. Chem., January 7, 2000; 275(1): 18 - 28.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
K. Webster, J. Parish, M. Pandya, P. L. Stern, A. R. Clarke, and K. Gaston
The Human Papillomavirus (HPV) 16 E2 Protein Induces Apoptosis in the Absence of Other HPV Proteins and via a p53-dependent Pathway
J. Biol. Chem., January 7, 2000; 275(1): 87 - 94.
[Abstract] [Full Text] [PDF]


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CROBMHome page
J. L. Schwartz
Biomarkers and Molecular Epidemiology and Chemoprevention of Oral Carcinogenesis
Critical Reviews in Oral Biology & Medicine, January 1, 2000; 11(1): 92 - 122.
[Abstract] [Full Text] [PDF]


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Vet PatholHome page
R. A. Levine and M. A. Fleischli
Inactivation of p53 and Retinoblastoma Family Pathways in Canine Osteosarcoma Cell Lines
Vet. Pathol., January 1, 2000; 37(1): 54 - 61.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
J.-P. Therrien, R. Drouin, C. Baril, and E. A. Drobetsky
Human cells compromised for p53 function exhibit defective global and transcription-coupled nucleotide excision repair, whereas cells compromised for pRb function are defective only in global repair
PNAS, December 21, 1999; 96(26): 15038 - 15043.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
L. Didcock, D. F. Young, S. Goodbourn, and R. E. Randall
The V Protein of Simian Virus 5 Inhibits Interferon Signalling by Targeting STAT1 for Proteasome-Mediated Degradation
J. Virol., December 1, 1999; 73(12): 9928 - 9933.
[Abstract] [Full Text]




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