E7 abolishes Raf-induced arrest via mislocalization of p21Cip1

Molecular and Cellular Biology

Volumn 22, Issue 20, 2002, Pages 7041-7052

  Westbrook, Thomas F ^a   Nguyen, Don X ^a   Thrash, Barry R ^a   McCance, Dennis J ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 2; CYCLIN E; DOXYCYCLINE; ONCOPROTEIN; PROTEIN KINASE B; PROTEIN P21; RAF PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MOUSE; MUTATION; NONHUMAN; ONCOGENE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; STOICHIOMETRY; WART VIRUS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; 3T3 CELLS; ANIMALS; CDC2-CDC28 KINASES; CELL DIVISION; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASES; CYCLINS; ENZYME INHIBITORS; HUMANS; MICE; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-RAF; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION;

ANIMALIA; HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPES; PAPILLOMAVIRUS;

EID: 0036787917     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.22.20.7041-7052.2002     Document Type: Article

References (79)

1. Alevizopoulos, K., J. Vlach, S. Hennecke, and B. Amati. 1997. Cyclin E and c-Myc promote cell proliferation in the presence of p16INK4a and of hypophosphorylated retinoblastoma family proteins. EMBO J. 16:5322-5333.
2. Banks, L., C. Edmonds, and K. Vousden. 1990. Ability of the HPV16 E7 protein to bind RB and induce DNA synthesis is not sufficient for efficient transforming activity in NIH3T3 cells. Oncogene 5:1383-1389.
3. Barbosa, M. S., C. Edmonds, C. Fisher, J. T. Schiller, D. R. Lowy, and K. H. Vousden. 1990. The region of the HPV E7 oncoprotein homologous to adenovirus E1a and Sv40 large T antigen contains separate domains for Rb binding and casein kinase II phosphorylation. EMBO J. 9:153-160.
4. Bouchard, C., K. Thieke, A. Maier, R. Saffrich, J. Hanley-Hyde, W. Ansorge, S. Reed, P. Sicinski, J. Bartek, and M. Eilers. 1999. Direct induction of cyclin D2 by Myc contributes to cell cycle progression and sequestration of p27. EMBO J. 18:5321-5333.
5. Boyer, S. N., D. E. Wazer, and V. Band. 1996. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res. 56:4620-4624.
6. Burgering, B. M., and P. J. Coffer. 1995. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376:599-602.
7. Cai, K., and B. D. Dynlacht. 1998. Activity and nature of p21(WAF1) complexes during the cell cycle. Proc. Natl. Acad. Sci. USA 95:12254-12259.
8. Cheng, M., P. Olivier, J. A. Diehl, M. Fero, M. F. Roussel, J. M. Roberts, and C. J. Sherr. 1999. The p21(Cip1) and p27(Kip1) CDK 'inhibitors' are essential activators of cyclin D-dependent kinases in murine fibroblasts. EMBO J. 18:1571-1583.
9. Coffer, P. J., J. Jin, and J. R. Woodgett. 1998. Protein kinase B (c-Akt): a multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem. J. 335:1-13.
10. Datta, S. R., A. Brunet, and M. E. Greenberg. 1999. Cellular survival: a play in three Akts. Genes Dev. 13:2905-2927.
11. Davies, R., R. Hicks, T. Crook, J. Morris, and K. Vousden. 1993. Human papillomavirus type 16 E7 associates with a histone H1 kinase and with p107 through sequences necessary for transformation. J. Virol. 67:2521-2528.
12. Demers, G. W., E. Espling, J. B. Harry, B. G. Etscheid, and D. A. Galloway. 1996. Abrogation of growth arrest signals by human papillomavirus type 16 E7 is mediated by sequences required for transformation. J. Virol. 70:6862-6869.
13. Demers, G. W., S. A. Foster, C. L. Halbert, and D. A. Galloway. 1994. Growth arrest by induction of p53 in DNA damaged keratinocytes is bypassed by human papillomavirus 16 E7. Proc. Natl. Acad. Sci. USA 91:4382-4386.
14. 2/M-phase transition. Mol. Cell. Biol. 18:546-557.
15. Dyson, N., K. Buchkovich, P. Whyte, and E. Harlow. 1989. Cellular proteins that are targetted by DNA tumor viruses for transformation. Princess Takamatsu Symp. 20:191-198.
16. Dyson, N., P. Guida, K. Munger, and E. Harlow. 1992. Homologous sequences in adenovirus E1A and human papillomavirus E7 proteins mediate interaction with the same set of cellular proteins. J. Virol. 66:6893-6902.
17. Dyson, N., P. M. Howley, K. Munger, and E. Harlow. 1989. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243:934-937.
18. Edmonds, C., and K. H. Vousden. 1989. A point mutational analysis of human papillomavirus type 16 E7 protein. J. Virol. 63:2650-2656.
19. el-Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, W. E, Mercer, K. W. Kinzler, and B. Vogelstein. 1993, WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
20. Evan, G. I., A. H. Wyllie, C. S. Gilbert, T. D. Littlewood, H. Land, M. Brooks, C. M. Waters, L. Z. Penn, and D. C. Hancock. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69:119-128.
21. Funk, J. O., S. Waga, J. B. Harry, E. Espling, B. Stillman, and D. A. Galloway. 1997. Inhibition of CDK activity and PCNA-dependent DNA replication by p21 is blocked by interaction with the HPV-16 E7 oncoprotein. Genes Dev. 11:2090-2100.
22. Cip1 cyclin-dependent kinase inhibitor. Oncogene 10:2281-2287.
23. Hanahan, D., and R. A. Weinberg. 2000. The hallmarks of cancer. Cell 100:57-70.
24. Harper, J. W., G. R. Adami, N. Wei, K. Keyomarsi, and S. J. Elledge. 1993. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75:805-816.
25. Harper, J. W., S. J. Elledge, K. Keyomarsi, B. Dynlacht, L. H. Tsai, P. Zhang, S. Dobrowolski, C. Bai, L. Connell-Crowley, and E. Swindell. 1995. Inhibition of cyclin-dependent kinases by p21. Mol. Biol. Cell 6:387-400.
26. Heck, D. V., C. L. Yee, P. M. Howley, and K. Munger. 1992. Efficiency of binding the retinoblastoma protein correlates with the transforming capacity of the E7 oncoproteins of the human papillomaviruses. Proc. Natl. Acad. Sci. USA 89:4442-4446.
27. Hengst, L., U. Gopfert, H. A. Lashuel, and S. I. Reed. 1998. Complete inhibition of Cdk/cyclin by one molecule of p21(Cip1). Genes Dev. 12:3882-3888.
28. Hickman, E. S., S. Bates, and K. H. Vousden. 1997. Pertubation of the p53 response by human papillomavirus type 16 E7. J. Virol. 71:3710-3718.
29. Hirakawa, T., and H. E. Ruley. 1988. Rescue of cells from ras oncogene-induced growth arrest by a second, complementing, oncogene. Proc. Natl. Acad. Sci. USA 85:1519-1523.
30. Hunter, T. 1991. Cooperation between oncogenes. Cell 64: 249-270.
31. Jones, D. L., R. M. Alani, and K. Munger. 1997. The human papillomavirus E7 oncoprotein can uncouple cellular differentiation and proliferation in human keratinocytes by abrogating p21Cip1-mediated inhibition of cdk2. Genes Dev. 11:2101-2111.
32. Kohn, A. D., F. Takeuchi, and R. A. Roth. 1996. Akt, a pleckstrin homology domain containing kinase, is activated primarily by phosphorylation. J. Biol. Chem. 271:21920-21926.
33. LaBaer, J., M. D. Garrett, L. F. Stevenson, J. M. Slingerland, C. Sandhu, H. S. Chou, A. Fattaey, and E. Harlow. 1997. New functional activities for the p21 family of CDK inhibitors. Genes Dev. 11:847-862.
34. Laimins, L. A. 1993. The biology of human papillomaviruses: from warts to cancer. Infect. Agents Dis. 2:74-86.
35. Land, H., A. C. Chen, J. P. Morgenstern, L. F. Parada, and R. A. Weinberg. 1986. Behavior of myc and ras oncogenes in transformation of rat embryo fibroblasts. Mol. Cell. Biol. 6:1917-1925.
36. Lin, A. W., M. Barradas, J. C. Stone, L. van Aelst, M. Serrano, and S. W. Lowe. 1998. Premature senescence involving p53 and p16 is activated in response to constitutive MEK/MAPK mitogenic signaling. Genes Dev. 12:3008-3019.
37. Lloyd, A. C., F. Obermuller, S. Staddon, C. F. Barth, M. McMahon, and H. Land. 1997. Cooperating oncogenes converge to regulate cyclin/cdk complexes. Genes Dev. 11:663-677.
38. Lowe, S. W., T. Jacks, D. E. Housman, and H. E. Ruley. 1994. Abrogation of oncogene-associated apoptosis allows transformation of p53-deficient cells. Proc. Natl. Acad. Sci. USA 91:2026-2030.
39. Lowe, S. W., and H. E. Ruley. 1993. Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis. Genes Dev. 7:535-545.
40. Missero, C., E. Calautti, R. Eckner, J. Chin, L. H. Tsai, D. M. Livingston, and G. P. Dotto. 1995, Involvement of the cell-cycle inhibitor Cip1/WAF1 and the E1A-associated p300 protein in terminal differentiation. Proc. Natl. Acad. Sci. USA 92:5451-5455.
41. Missero, C., F. Di Cunto, H. Kiyokawa, A. Koff, and G. P. Dotto. 1996. The absence of p21Cip1/WAF1 alters keratinocyte growth and differentiation and promotes ras-tumor progression. Genes Dev. 10:3065-3075.
42. Moodie, S. A., B. M. Willumsen, M. J. Weber, and A. Wolfman. 1993. Complexes of Ras.GTP with Raf-1 and mitogen-activated protein kinase kinase. Science 260:1658-1661.
43. Morgenstern, J. P., and H. Land. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18:3587-3596.
44. Munger, K., B. A. Werness, N. Dyson, W. C. Phelps, E. Harlow, and P. M. Howley. 1989. Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J. 8:4099-4105.
45. Nead, M. A., L. A. Baglia, M. J. Antinore, J. W. Ludlow, and D. J. McCance. 1998. Rb binds c-Jun and activates transcription. EMBO J. 17:2342-2352.
46. Noda, A., Y. Ning, S. F. Venahle, O. M. Pereira-Smith, and J. R. Smith. 1994. Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res. 211:90-98.
47. 1-to-S phase transition. Mol. Cell. Biol. 15:2612-2624.
48. Parker, S. B., G. Eichele, P. Zhang, A. Rawls, A. T. Sands, A. Bradley, E. N. Olson, J. W. Harper, and S. J. Elledge. 1995. p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells. Science 267: 1024-1027.
49. Cip1. EMBO J. 18:5310-5320.
50. Kip1 binding to newly formed complexes. Oncogene 14:2373-2381.
51. Phelps, W. C., K. Munger, C. L Yee, J. A. Barnes, and P. M. Howley. 1992. Structure-function analysis of the human papillomavirus type 16 E7 oncoprotein. J. Virol. 66:2418-2427.
52. Phelps, W. C., C. L. Yee, K. Munger, and P. M. Howley. 1988. The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to those of adenovirus E1A. Cell 53:539-547.
53. Polyak, K., M. H. Lee, H. Erdjument-Bromage, A. Koff, J. M. Roberts, P. Tempst, and J. Massague. 1994. Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78:59-66.
54. Reynisdottir, I., and J. Massague. 1997. The subcellular locations of p15(Ink4b) and p27(Kip1) coordinate their inhibitory interactions with cdk4 and cdk2. Genes Dev. 11:492-503.
55. Reynisdottir, I., K. Polyak, A. Iavarone, and J. Massague. 1995. Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-beta. Genes Dev. 9:1831-1845.
56. Ridley, A. J., H. F. Paterson, M. Noble, and H. Land. 1988. Ras-mediated cell cycle arrest is altered by nuclear oncogenes to induce Schwann cell transformation. EMBO J. 7:1635-1645.
57. Rommel, C., B. A. Clarke, S. Zimmermann, L. Nunez, R. Rossman, K. Reid, K. Moelling, G. D. Yancopoulos, and D. J. Glass. 1999. Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science 286:1738-1741.
58. Roper, E., W. Weinberg, F. M. Watt, and H. Land. 2001. p19ARF-independent induction of p53 and cell cycle arrest by Raf in murine keratinocytes. EMBO Rep. 2:145-150.
59. Cip1 regulates PCNA binding and proliferation of endothelial cells. Mol. Cell. Biol. 21:5644-5657.
60. Rudolph, B., R. Saffrich, J. Zwicker, B. Henglein, R. Muller, W. Ansorge, and M. Eilers. 1996. Activation of cyclin-dependent kinases by Myc mediates induction of cyclin A, but not apoptosis. EMBO J. 15:3065-3076.
61. Ruesch, M., and L. A. Laimins. 1997. Initiation of DNA synthesis by human papillomavirus E7 oncoproteins is resistant to p21-mediated inhibition of cyclin E-cdk2 activity. J. Virol. 71:5570-5578.
62. Ruley, H. E. 1990. Transforming collaborations between ras and nuclear oncogenes. Cancer Cells 2:258-268.
63. Schulze, A., B. Mannhardt, K. Zerfass-Thome, W. Zwerschke, and P. Jansen-Dürr. 1998. Anchorage-independent transcription of the cyclin A gene induced by the E7 oncoprotein of human papillomavirus type 16. J. Virol. 72:2323-2334.
64. Serrano, M., A. W. Lin, M. E. McCurrach, D. Beach, and S. W. Lowe. 1997. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88:593-602.
65. Cip1. Mol. Cell. Biol. 17:5588-5597.
66. Sherr, C. J., and J. M. Roberts. 1995. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9:1149-1163.
67. Vlach, J., S. Hennecke, K. Alevizopoulos, D. Conti, and B. Amati. 1996. Growth arrest by the cyclin-dependent kinase inhibitor p27Kip1 is abrogated by c-Myc. EMBO J. 15:6595-6604.
68. Vojtek, A. B., S. M. Hollenberg, and J. A. Cooper. 1993. Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74:205-214.
69. Vousden, K. H., J. Doniger, J. A. DiPaolo, and D. R. Lowy. 1988. The E7 open reading frame of human papillomavirus type 16 encodes a transforming gene. Oncog. Res. 3:167-175.
70. Weinberg, R. A. 1989. Oncogenes, antioncogenes, and the molecular bases of multistep carcinogenesis. Cancer Res, 49:3713-3721.
71. Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
72. Cip1. Mol. Cell. Biol. 17:5598-5611.
73. Zerfass, K., A. Schulze, D. Spitkovsky, V. Friedman, B. Henglein, and P. Jansen-Dürr. 1995. Sequential activation of cyclin E and cyclin A gene expression by human papillomavirus type 16 E7 through sequences necessary for transformation. J. Virol. 69:6389-6399.
74. KIP1 blocks cyclin E-dependent transactivation of cyclin A gene expression. Mol. Cell. Biol. 17:407-415.
75. Zhang, H., G. J. Hannon, and D. Beach. 1994. p21-containing cyclin kinases exist in both active and inactive states. Genes Dev. 8:1750-1758.
76. Zhang, H., G. J. Hannon, D. Casso, and D. Beach. 1994. p21 is a component of active cell cycle kinases. Cold Spring Harbor Symp. Quant. Biol. 59:21-29.
77. Zhou, B. P., Y. Liao, W. Xia, B. Spohn, M. H. Lee, and M. C. Hung. 2001. Cytoplasmic localization of p21Cip1/WAF1 by Akt-induced phosphorylation in HER-2/neu-overexpressing cells. Nat. Cell Biol. 3:245-252.
78. Zimmermann, S., and K. Moelling. 1999. Phosphorylation and regulation of Raf by Akt (protein kinase B). Science 286:1741-1744.
79. Zugasti, O., W. Rul, P. Roux, C. Peyssonnaux, A. Eychene, T. F. Franke, P. Fort, and U. Hibner. 2001. Raf-MEK-Erk cascade in anoikis is controlled by Rac1y and Cdc42 via Akt. Mol. Cell. Biol. 21:6706-6717.