The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability

Cancer Research

Volumn 62, Issue 23, 2002, Pages 7075-7082

  Duensing, Stefan ^a   Münger, Karl ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2A; ONCOPROTEIN;

ANAPHASE; ARTICLE; CARCINOGENESIS; CELL ACTIVATION; CELL CYCLE; CELL DIVISION; CHROMOSOME BREAKAGE; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; GENOME; HOST CELL; HUMAN; HUMAN CELL; MITOSIS; NEWBORN; NONHUMAN; NUMERICAL CHROMOSOME ABERRATION; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRUCTURAL CHROMOSOME ABERRATION; VIRUS TYPING; WART VIRUS;

ANAPHASE; CELL CYCLE; CHROMOSOME ABERRATIONS; DNA DAMAGE; HUMANS; KERATINOCYTES; MITOSIS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; REPRESSOR PROTEINS;

EID: 0036897282     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (51)

1. zur Hausen, H. Papillomavirus infections: A major cause of human cancers. Biochim. Biophys. Acta, 1288: F55-78, 1996.
2. Scheffner, M., Werness, B. A., Huibregtse, J. M., Levine, A. J., and Howley, P. M. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell., 63: 1129-1136, 1990.
3. Boyer, S. N., Wazer, D. E., and Band, V. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res., 56: 4620-4624, 1996.
4. Dyson, N., Howley, P. M., Munger, K., and Harlow, E. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science (Washington DC), 243: 934-937, 1989.
5. Funk, J. O., Waga, S., Harry, J. B., Espling, E., Stillman, B., and Galloway, D. A. 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, 1997.
6. Cipl-mediated inhibition of cdk2. Genes Dev., 11: 2101-2111, 1997.
7. KIP1 by the human papillomavirus type 16 E7 oncoprotein. Oncogene., 13: 2323-2330, 1996.
8. zur Hausen, H. Viruses in human cancers. Science (Washington DC), 254: 1167-1173, 1991.
9. Heselmeyer, K., Schrock, E., du Manoir, S., Blegen, H., Shah, K., Steinbeck, R., Auer, G., and Ried, T. Gain of chromosome 3q defines the transition from severe dysplasia to invasive carcinoma of the uterine cervix. Proc. Natl. Acad. Sci. USA, 93: 479-484, 1996.
10. Solinas-Toldo, S., Dürst, M., and Lichter, P. Specific chromosomal imbalances in human papillomavirus-transfected cells during progression toward immortality. Proc. Natl. Acad. Sci. USA, 94: 3854-3859, 1997.
11. White, A. E., Livanos, E. M., and Tlsty, T. D. Differential disruption of genomic integrity and cell cycle regulation in normal human fibroblasts by the HPV oncoproteins. Genes Dev., 8: 666-677, 1994.
12. Thompson, D. A., Belinsky, G., Chang, T. H., Jones, D. L., Schlegel, R., and Munger, K. The human papillomavirus-16 E6 oncoprotein decreases the vigilance of mitotic checkpoints. Oncogene, 15: 3025-3035, 1997.
13. Thomas, J. T., and Laimins, L. A. Human papillomavirus oncoproteins E6 and E7 independently abrogate the mitotic spindle checkpoint. J. Virol., 72: 1131-1137, 1998.
14. Duensing, S., Lee, L. Y., Duensing, A., Basile, J., Piboonniyom, S., Gonzalez, S,. Crum, C. P., and Munger, K. The human papillomavirus type 16 E6 and E7 oncoproteins cooperate to induce mitotic defects and genomic instability by uncoupling centrosome duplication from the cell division cycle. Proc. Natl. Acad. Sci. USA, 97: 10002-10007, 2000.
15. Duensing, S., Duensing, A., Crum, C. P., and Munger, K. Human papillomavirus type 16 E7 oncoprotein-induced abnormal centrosome synthesis is an early event in the evolving malignant phenotype. Cancer Res., 61: 2356-2360, 2001.
16. Lengauer, C., Kinzler, K. W., and Vogelstein, B. Genetic instabilities in human cancers. Nature (London), 396: 643-649, 1998.
17. Lingle, W. L., Barrett, S. L., Negron, V. C., D'Assoro, A. B., Boeneman, K., Liu, W., Whitehead, C. M., Reynolds, C., and Salisbury, J. L. Centrosome amplification drives chromosomal instability in breast tumor development. Proc. Natl. Acad. Sci. USA, 99: 1978-1983, 2002.
18. Lu, X., Magrane, G., Yin, C., Louis, D. N., Gray, J., and Van Dyke, T. Selective inactivation of p53 facilitates mouse epithelial tumor progression without chromosomal instability. Mol. Cell. Biol., 21: 6017-6030, 2001.
19. Bunz, F., Fauth, C., Speicher, M. R., Dutriaux, A., Sedivy, J. M., Kinzler, K. W., Vogelstein, B., and Lengauer, C. Targeted inactivation of p53 in human cells does not result in aneuploidy. Cancer Res., 62: 1129-1133, 2002.
20. -/- cells. EMBO J., 21: 483-492, 2002.
21. Halbert, C. L., Demers, G. W., and Galloway, D. A. The E6 and E7 genes of human papillomavirus type 6 have weak immortalizing activity in human epithelial cells. J. Virol., 66: 2125-2134, 1992.
22. Stearns, T., Evans, L., and Kirschner, M. γ-Tubulin is a highly conserved component of the centrosome. Cell., 65: 825-836, 1991.
23. Sluder, G., Thompson, E. A., Miller, F. J., Hayes, J., and Rieder, C. L. The checkpoint control for anaphase onset does not monitor excess numbers of spindle poles or bipolar spindle symmetry. J. Cell Sci., 1997: 421-429, 1997.
24. Gisselsson, D., Pettersson, L., Hoglund, M., Heidenblad, M., Gorunova, L., Wiegant, J., Mertens, F., Dal Cin, P., Mitelman, F., and Mandahl, N. Chromosomal breakage-fusion-bridge events cause genetic intratumor heterogeneity. Proc. Natl. Acad. Sci. USA, 97: 5357-5362, 2000.
25. Gisselsson, D., Jonson, T., Petersen, A., Strombeck, B., Dal Cin, P., Hoglund, M., Mitelman, F., Mertens, F., and Mandahl, N. Telomere dysfunction triggers extensive DNA fragmentation and evolution of complex chromosome abnormalities in human malignant tumors. Proc. Natl. Acad. Sci. USA, 98: 12683-12688, 2001.
26. Gisselsson, D. Chromosomal instability in cancer: Causes and consequences. Atlas of Genetics and Cytogenetics in Oncology and Hematology. URL://www.infobiogen.fr/services/chromcancer/Deep/ChromosomInstabil ID20023.html, 2001.
27. Kessis, T. D., Connolly, D. C., Hedrick, L., and Cho, K. R. Expression of HPV 16 E6 or E7 increases integration of foreign DNA. Oncogene, 13: 427-431, 1996.
28. Tong, W. M., Cortes, U., and Wang, Z. Q. Poly(ADP-ribose) polymerase: A guardian angel protecting the genome and suppressing tumorigenesis. Biochim. Biophys. Acta, 1552: 27-37, 2001.
29. D'Amours, D., Desnoyers, S., D'Silva, I., and Poirier, G. G. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J., 342: 249-268, 1999.
30. Oei, S. L., and Shi, Y. Poly(ADP-ribosyl)ation of transcription factor Yin Yang 1 under conditions of DNA damage. Biochem. Biophys. Res. Commun., 285: 27-31, 2001.
31. Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S., and Bonner, W. M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem., 273: 5858-5868, 1998.
32. Paull, T. T., Rogakou, E. P., Yamazaki, V., Kirchgessner, C. U., Gellert, M., and Bonner, W. M. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol., 10: 886-895, 2000.
33. Ward, I. M., and Chen, J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem., 276: 47759-47762, 2001.
34. Canman, C. E., Lim, D. S., Cimprich, K. A., Taya, Y., Tamai, K., Sakaguchi, K., Appella, E., Kastan, M. B., and Siliciano, J. D. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science (Washington DC). 281: 1677-1679, 1998.
35. Gould, K. L., and Nurse, P. Tyrosine phosphorylation of the fission yeast cdc2 protein kinase regulates entry into mitosis. Nature, 342: 39-45, 1989.
36. Klausner, R. D. The fabric of cancer cell biology: Weaving together the strands. Cancer Cell, 1: 3-10, 2002.
37. Howley, P. M. and Lowy, D. R. Papillomaviruses and their replication. In: D. M. Knipe and P. M. Howley (eds.), Field's Virology, Vol. 2, pp. 2197-2229. Philadelphia: Lippincott Williams & Wilkins, 2001.
38. Bibbo, M., Dytch, H. E., Alenghat, E., Bartels, P. H., and Wied, G. L. DNA ploidy profiles as prognostic indicators in CIN lesions. Am. J. Clin. Pathol., 92: 261-265, 1989.
39. Fu, Y. S., Reagan, J. W., and Richart, R. M. Definition of precursors. Gynecol. Oncol., 12: S220-S231, 1981.
40. Reid, R., Crum, C. P., Herschman, B. R., Fu, Y. S., Braun, L., Shah, K. V., Agronow, S. J., and Stanhope, C. R. Genital warts and cervical cancer. III. Subclinical papillomaviral infection and cervical neoplasia are linked by a spectrum of continuous morphologic and biologic changes. Cancer, 53: 943-953, 1984.
41. Southern, S. A., Evans, M. F., and Herrington, C. S. Basal cell tetrasomy in low-grade cervical squamous intraepithelial lesions infected with high-risk human papillomaviruses. Cancer Res., 57: 4210-4213, 1997.
42. Heselmeyer, K., Macville, M., Schrock, E., Blegen, H., Hellström, A. C., Shah, K., Auer, G., and Ried, T. Advanced-stage cervical carcinomas are defined by a recurrent pattern of chromosomal aberrations revealing high genetic instability and a consistent gain of chromosome arm 3q. Genes Chromosomes Cancer, 19: 233-240, 1997.
43. Amon, A. The spindle checkpoint. Curr. Opin. Genet. Dev., 9: 69-75, 1999.
44. Lanni, J. S., and Jacks, T. Characterization of the p53-dependent postmitotic checkpoint following spindle disruption. Mol. Cell. Biol., 18: 1055-1064, 1998.
45. Jin, D. Y., Spencer, F., and Jeang, K. T. Human T cell leukemia virus type 1 oncoprotein Tax targets the human mitotic checkpoint protein MADI. Cell, 93: 81-91, 1998.
46. McClintock, B. The stability of broken ends of chromosomes in Zea mays. Genetics, 26: 234-282, 1940.
47. Carbone, R., Pearson, M., Minucci, S., and Pelicci, P. G. PML NBs associate with the hMre11 complex and p53 at sites of irradiation induced DNA damage. Oncogene, 21: 1633-1640, 2002.
48. Weinert, T. A DNA damage checkpoint meets the cell cycle engine. Science (Washington DC), 277: 1450-1451, 1997.
49. Harrington, E. A., Bruce, J. L., Harlow, E., and Dyson, N. pRB plays an essential role in cell cycle arrest induced by DNA damage. Proc. Natl. Acad. Sci. USA, 95: 11945-11950, 1998.
50. Zheng, L., Flesken-Nikitin, A., Chen, P. L., and Lee, W. H. Deficiency of retinoblastoma gene in mouse embryonic stem cells leads to genetic instability. Cancer Res., 62: 2498-2502, 2002.
51. Cahill, D. P., Kinzler, K. W., Vogelstein, B., and Lengauer, C. Genetic instability and darwinian selection in tumours. Trends Cell Biol., 9: M57-M60, 1999.