Alteration of cell cycle kinase complexes in human papillomavirus E6- and E7-expressing fibroblasts precedes neoplastic transformation

Journal of Virology

Volumn 70, Issue 2, 1996, Pages 999-1008

  Xiong, Yue ^a   Kuppuswamy, Dhandapani ^b,e   Li, Yan ^a   Livanos, Elizabeth M ^b   Hixon, Mary ^a   White, Alicia ^a   Beach, David ^c   Tlsty, Thea D ^a,b,d  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN B; CYCLIN DEPENDENT KINASE; CYCLINE; ONCOPROTEIN; PROTEIN P21; VIRUS PROTEIN;

ARTICLE; CELL CYCLE; CELL TRANSFORMATION; CONTROLLED STUDY; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; NEOPLASM; PRIORITY JOURNAL; VIRUS GENOME; WART VIRUS;

EID: 0030065394     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.2.999-1008.1996     Document Type: Article

References (68)

1. Androphy, E. J., N, L. Hubbert, J. T. Schiller, and D. R. Lowy. 1987. Identification of the HPV-16 E6 protein from transformed mouse cells and human cervical carcinoma lines. EMBO J. 6:989-992.
2. Aurias, A. 1993. Acquired chromosomal aberrations in normal individuals. p. 125-139. In I. R. Kirsch (ed.). The causes and consequences of chromosomal aberrations CRC Press. Inc., Ann Arbor. Mich.
3. Baker, C. C., W. C. Phelps, V. Lindgren, M. J. Braun. M. A. Gondas, and P. M. Howley. 1987 Structural and translational analysis of human papillomavirus type 16 sequences in cervical carcinoma cell lines. J. Virol. 61:962-971.
4. Bates, S., D. Parry, L. Bonetta, K. Vousden, C. Dickson, and G. Peters. 1994b. Absence of cyclin D/cdk4 complexes in cells lacking functional retinobtastoma protein. Oncogene 9:1633-1640.
5. Chen, J., P. K. Jackson, M. W. Kirschner, and A. Dutta. 1995. Separate domains of p21 involved in the inhibition of cdk kinase and PCNA Nature (London) 374:386-388.
6. Crook, T., J. A. Tidy, and K. H. Vousden. 1991 Degradation of p53 can be targeted by HPV E6 sequences distinct from those required for p53 binding and trans-activation. Cell 67:547-556.
7. Dhanwada, K. R., V. Veerisetty, F. Zhu, A. Razzaque, K. D. Thompson, and C. Jones. 1992. Characterization of primary human fibroblasts transformed by human papillomavirus type 16 and herpes simplex type 2 DNA sequences. J. Gen. Virol. 73:791-799
8. Draetta, G. 1990. Cell cycle control in eukaryotes molecular mechanisms of cdc2 activation. Trends Biol Sci. 15:378-383
9. Durst, M., A. Kleinheinz, M. Hotz, and L. Gismann. 1985. The physical state of human papillomavirus type 16 DNA in benign and malignant genital tumours. Virology 66:1515-1522.
10. Dyson, N., P. Guida, K. Monger, 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.
11. Dyson, N., P. M. Howley, K. Munger. and E. Harlow. 1989. The human papillomavirus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product Science 243:934-937.
12. El-Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, D. M. Lin, W. E. Mercer, K. W. V. Kinzler, and B. Vogelstein. 1993. WAF1. a potential mediator of p53 tumor suppression. Cell 75:817-825.
13. Evans, T., E. T. Rosenthal, J. Youngblom, D. Distel, and T. Hunt. 1983. Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell 33:389-396.
14. Ewen, M. E., H. K. Sluss, C. J. Sherr, H. Matsushime, J. Y. Kato, and D. M. Livingston. 1993. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell 73:487-497.
15. Fidler, I. J., and I. R. Hart 1982. The development ot biological diversity and metastatic potential in malignant neoplasm. Oncodev. Biol. Med. 4:161-176.
16. Firzlaff, J. M., C.-N. L. Hsia, C. P. H. L. Halbert, S. A. Jenison, and D. A. Galloway. 1987. Papillomaviruses Cancer Cells 5:105-113.
17. Flores-Rozas, H., Z. Kelman, F. Dean. Z. Pan, J. W. Harper, S. Elledge, M. O'Donnell, and J. Hurwitz. 1994 Cdk-interacting protein 1 directly binds with proliferating cell nuclear antigen and inhibits DNA replication catalyzed by the DNA polymerase d holoenzyme. Proc. Natl. Acad. Sci. USA 91:8655-8659.
18. Foulds, L. 1959. Neoplastic development, vol. 2. Academic Press. New York.
19. Gage, J. R., C. Meyers, and F. O. Wettstein. 1990. The E7 proteins of the nononcogenic human papillomavirus type 6b (HPV-6b) and of the oncogenic HPV-16 differ in retinoblastoma protein binding and other properties. J. Virol 46:723-730.
20. Gu, Y., C. W. Turck, and D. O. Morgan. 1993. Inhibitor of CDK2 activity in vivo by an associated 20K regulatory subunit. Nature (London) 366:707-710.
21. Halbert, C. L., G. W. Demers, and D. A. Galloway. 1992. The E6 and E7 genes of human papiliomavirus type 6 have weak immortalizing activity in human epithelial cells J. Virol. 66:2125-2134.
22. Harper, J. W., G. R. Adami, N. Wei, K. Keymoarsi, and S. J. Elledge. 1993 The p21 cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases Cell 75:805-816.
23. Harper, J. W., S. J. Elledge, K. Keyomarsi, B. Dynlacht, L. H. Tsai, P. Zhang, S. Donrowolski, C. Bai, L. Connell-Crowley, E. Swindell, M. P. Fox, and N. Wei. 1995. Inhibition of cyclin-dependent kinases by p21. Mol. Biol. Cell 6:387-400.
24. Hartwell, L. H., and T. A. Weinert. 1989. Checkpoints: controls that ensure the order of cell cycle events Science 246:629-633.
25. Hawley-Nelson, P., K. H. Vousden, N. L. Hubbert, D. R. Lowy, and J. T. Schiller. 1989. HPV16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO J. 8:3905-3910.
26. Heppner, G. H. 1984. Tumor heterogeneity. Cancer Res. 44:2259-2265.
27. Hinds, P. W., S. F. Dowdy, E. N. Eaton, A. Arnold, and R. A. Weinberg. 1994. Function of human cyclin gene as an oncogene. Proc Natl. Acad. Sci. USA 91:709-713.
28. Hubbert, N., S. A. Sedman, and J. T. Schiller. 1992 Human papillomavirus type 16 E6 increases the degradation rate of p53 in human keratmocytes. J. Virol. 66:6237-6241.
29. Jonczyk, P., A. White, K. Lum, J. C. Barrett, and T. D. Tlsty. 1992. Amplification potential in preneoplastic and neoplastic Syrian hamster embryo fibroblasts transformed by various carcinogens. Cancer Res. 53:3098-3102.
30. Kato, J.-Y., H. Matsushime, S. W. Hiebert M. Ewen, and C. J. Sherr. 1993. Direct binding of cyclin D to the retinoblastoma gene product (pRb) and pRb phosphorylation by the cyclin D-dependent kinase CDK4. Genes Dev. 7:331-342
31. Lammie, G. A., and G. Peters. 1991 Chromosome 11q13 abnormalities in human cancer. Cancer Cells 3:413-420
32. Lehn, H., P. Krieg, and G. Sauer. 1985. Human papillomavirus genomes in human cervical tumors: analysis of their transcriptional activity. Proc. Natl. Acad Sci. USA 82:5540-5544.
33. Li, Y., M. A. Nichols, J. W. Shay, and Y. Xiong. 1994. Transcriptional repression of the D-type cyclin-dependent kinases inhibitor p16 by the retinoblastoma susceptibility gene product. pRb. Cancer Res. 54:6078-6082.
34. Livingstone, L. R., A. White, J. Sprouse, E. Livanos. T. Jacks, and T. D. Tlsty. 1992. Altered cell cycle arrest and gene amplification potential accompany loss of wild-type p53 Cell 70:923-935.
35. Lovec, H., A. Sewing, F. Lucibello, R. Muller, and T. Moroy. 1994. Oncogenic activity of cyclin D1 revealed through co-operation with Ha-ras: link between cell cycle control and malignant transformation. Oncogene 9:323-326.
36. CIP1. Nature (London) 375:159-161
37. Matsushime, H., D. E. Quelle, S. A. Shurtleff, M. Shibuya, C. J. Sherr, and J.-Y. Kato. 1994. D-type cyclin-dependent kinase activity in mammalian cells. Mol. Cell Biol. 14:2066-2076.
38. 1 kinase activity for cdk6. a novel cyclin D partner Mol. Cell. Biol. 14:2077-2086.
39. Motokura, T., and A. Arnold. 1993. Cyclin D and oncogenesis. Curr. Opin. Genet. Dev. 3:5-10
40. Munger, K.. W. C. Phelps, V. Bubb, P. Howley, and R. Schlegel. 1989. The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes J. Virol. 63:4417-4421.
41. 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
42. Sdn CIPI WAFI EMBO J. 14:555-563.
43. Norbury, C., and P. Nurse. 1992 Animal cell cycles and their control Annu. Rev. Biochem. 61:441-470.
44. Nowell, P. C. 1976. The clonal evolution of tumor cell populations. Science 194:23-28.
45. Pagano, M., A. M. Theodoras, S. W. Tam, and G. F. Draetta. 1994 Cyclin D1-mediated inhibition of repair and replicative DNA synthesis in human fibroblasts Genes Dev. 8:1627-1639.
46. Parry, D., S. Bates, D. J. Mann, and G. Peters. 1995. Lack of cyclin D-Cdk complexes in Rb-negative cells correlates with high levels of p16INK4/MTS1 tumour suppressor gene product. EMBO J. 14:503-511.
47. Pater, M. M., and A. Pater. 1985. Human papillomavirus types 16 and 18 sequences in carcinoma cell lines of the cervix Virology 145:313-318.
48. Pecoraro, G., D. Morgan, and V. Defendi. 1989. Differential effects of human papillomavirus type 6, 16, and 18 DNAs on immortalization and transformation of human cervical epithelial cells. Proc. Natl. Acad. Sci. USA 86: 563-567.
49. Pines, J. 1993 Cyclins and cyclin-dependent kinases: take your partners. Trends Biochem. Sci. 18:195-197.
50. Schaefer, D. L, E. M. Livanos, A. E. White, and T. D. Tlsty. 1993. Multiple mechanisms of N-(phosphonoacctyl)-L-aspartate drug resistance in SV40-infected precrisis human fibroblasts. Cancer Res. 53:4946-4951.
51. Schauer, I. E., S. Siriwardana, T. A. Langan, and R. A. Sclafani. 1994. Cyclin Dl overexpression vs. retinoblastoma inactivation: implication for control evasion in non-small cell and small cell lung cancer Proc Natl. Acad. Sci USA 91:7827-7831.
52. Scheffner, M., B. A. Werness, J. M. Huibregtse, A. J. Levine, and P. M. Howley. 1990 The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53 Cell 63:1129-1136.
53. Serrano, M., G. J. Hannon, and D. Beach. 1993 A new regulatory motif m cell cycle control causing specific inhibition of cyclin D/CDK4. Nature (London) 366:704-707.
54. Sewing, A., C. Burger, S. Brusselbach, C. Schalk, F. C. Lacibello, and R. Muller. 1993. Human cyclin D1 encodes a labile nuclear protein whose synthesis is directly induced by growth factors and suppressed by cyclic AMP. J. Cell Sci. 104:545-554.
55. 1 cyclis. Cell 73:1059-1065.
56. Vousden, K. H., and P. S. Jat 1989 Functional similarity between HPV16 E7. SV40 large T and adenovirus E1a proteins. Oncogene 4:153-158
57. Waga, S., G. Hannon, D. Beach, and B. Stillman. 1994 The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature (London) 369:574-578.
58. WAF1 and proliferating cell nuclear antigen. Curr. Biol. 5:275-282.
59. Watanabe, S., T. Kanda, and K. Yoshiike. 1989. Human papillomavirus type 16 transformation of primary human embryonic fibroblasts requires expression of open reading frames E6 and E7. J. Virol. 63:965-969.
60. Werness, B. A., A. J. Levine, and P. M. Howley. 1990 Association of human papillomavirus types 16 and IS E6 proteins with p53. Science 248:75-79.
61. White, A., E. M. Livanos, and T. D. Tlsty. 1994. Differential disruption of genomic integrity and cell cycle regulation in normal human fibroblasts by the HPV oncoproteins. Genes Dev. 8:666-677.
62. Xiong, Y., and D. Beach. 1991. Population explosion in the cyclin family. Curr. Biol. 1:362-364.
63. Xiong, Y., G. Hannon, H. Zhang, D. Casso, R. Kobayashi, and D. Beach. 1993. p21 is a universal inhibitor of cyclin kinases. Nature (London) 366: 701-704.
64. Xiong, Y., H. Zhang, and D. Beach. 1992. D-type cyclins associate, with multiple protein kinases and the DNA replication and repair factor PCNA. Cell 71:505-514.
65. Xiong, Y., H. Zhang, and D. Beach. 1993 Subunit rearrangement of the cyclin-dependent kinases is associated with cellular transformation Genes Dev. 7:1572-1583.
66. Yin, Y., M. A. Tainsky, F. Z. Bischoff, L. C. Strong, and G. M. Wahl. 1992. Wild-type p53 restores cell cycle control and inhibits gene amplification in cells with mutant p53 alleles. Cell 70:937-948.
67. Zhang, H., Y. Xiong, and D. Beach. 1993. Proliferating cell nuclear antigen and p21 are components of multiple cell cycle kinase complexes. Mol. Biol Cell 4:897-906.
68. zur Hausen, H. 1991. Human papillomaviruses in the pathogenesis of anogenital cancer. Virology 184:9-13.