Impairment of the telomere/telomerase system and genomic instability are associated with keratinocyte immortalization induced by the skin human papillomavirus type 38

FASEB Journal

Volumn 22, Issue 2, 2008, Pages 622-632

  Gabet, Anne Sophie ^a   Accardi, Rosita ^a   Bellopede, Angelica ^a   Popp, Susanne ^b   Boukamp, Petra ^b   Sylla, Bakary S ^a   Londoño Vallejo, J Arturo ^c   Tommasino, Massimo ^a  

^a INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c INSTITUT CURIE   (France)

Author keywords

Chromosomal abnormalities; HPV38 E6 and E7; Telomere dysfunctions

Indexed keywords

PROTEIN E6; PROTEIN E7; PROTEIN P53; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; VIRUS PROTEIN;

ANAPHASE; ARTICLE; CELL IMMORTALIZATION; CHROMOSOME ABERRATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; KARYOTYPE; KERATINOCYTE; MITOSIS; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TELOMERE; UPREGULATION; WART VIRUS;

ANAPHASE; CELL SURVIVAL; CELLS, CULTURED; CHROMOSOMES, HUMAN; FEMALE; GENOMIC INSTABILITY; HUMANS; KERATINOCYTES; MEIOSIS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; POLYPLOIDY; RNA, MESSENGER; SKIN DISEASES; TELOMERASE; TELOMERE; UP-REGULATION;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 38; HUMAN PAPILLOMAVIRUS TYPES;

EID: 38949092837     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.07-8389com     Document Type: Article

References (40)

1. De Villiers, E. M., Fauquet, C., Broker, T. R., Bernard, H. U., and zur Hausen, H. (2004) Classification of papillomaviruses. Virology 324, 17-27
2. Munoz, N., Bosch, F. X., de Sanjose, S., Herrero, R., Castellsague, X., Shah, K. V., Snijders, P. J., and Meijer, C. J. (2003) Epidemiologic classification of human papillomavirus types associated with cervical cancer. N. Engl. J. Med. 348, 518-527
3. Munger, K., Baldwin, A., Edwards, K. M., Hayakawa, H., Nguyen, C. L., Owens, M., Grace, M., and Huh, K. (2004) Mechanisms of human papillomavirus-induced oncogenesis. J. Virol. 78, 11451-11460
4. Pfister, H. (2003) Chapter 8: human papillomavirus and skin cancer. J. Natl. Cancer Inst. Monogr. 31, 52-56
5. Jackson, S., and Storey, A. (2000) E6 proteins from diverse cutaneous HPV types inhibit apoptosis in response to UV damage. Oncogene 19, 592-598
6. Caldeira, S., Zehbe, I., Accardi, R., Malanchi, I., Dong, W., Giarre, M., deVilliers, E.-M., Filotico, R., Boukamp, P., and Tommasino, M. (2003) The E6 and E7 proteins of cutaneous human papillomavirus type 38 display transforming properties. J. Virol. 77, 2195-2206
7. Accardi, R., Dong, W., Smet, A., Cui, R., Hautefeuille, A., Gabet, A. S., Sylla, B. S., Gissmann, L., Hainaut, P., and Tommasino, M. (2006) Skin human papillomavirus type 38 alters p53 functions by accumulation of deltaNp73. EMBO Rep. 7, 334-340
8. Shay, J. W., and Wright, W. E. (2005) Senescence and immortalization: role of telomeres and telomerase. Carcinogenesis 26, 867-874
9. Artandi, S. E., Chang, S., Lee, S. L., Alson, S., Gottlieb, G. J., Chin, L., and DePinho, R. A. (2000) Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature 406, 641-645
10. Rudolph, K. L., Millard, M., Bosenberg, M. W., and DePinho, R. A. (2001) Telomere dysfunction and evolution of intestinal carcinoma in mice and humans. Nat. Genet. 28, 155-159
11. Gewin, L., Myers, H., Kiyono, T., and Galloway, D. A. (2004) Identification of a novel telomerase repressor that interacts with the human papillomavirus type-16 E6/E6-AP complex. Genes Dev. 18, 2269-2282
12. James, M. A., Lee, J. H., and Klingelhutz, A. J. (2006) HPV16-E6-associated hTERT promoter acetylation is E6AP dependent, increased in later passage cells and enhanced by loss of p300. Int. J. Cancer 119, 1878-1885
13. Klingelhutz, A. J., Foster, S. A., and Mcdougall, J. K. (1996) Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature 380, 79-82
14. Stoppler, H., Hartmann, D. P., Sherman, L., and Schlegel, R. (1997) The human papillomavirus type 16 E6 and E7 oncoproteins dissociate cellular telomerase activity from the maintenance of telomere length. J. Biol. Chem. 272, 13332-13337
15. Plug-DeMaggio, A. W., Sundsvold, T., Wurscher, M. A., Koop, J. I., Klingelhutz, A. J., and McDougall, J. K. (2004) Telomere erosion and chromosomal instability in cells expressing the HPV oncogene 16E6. Oncogene 23, 3561-3571
16. Zhang, A., Wang, J., Zheng, B., Fang, X., Angstrom, T., Liu, C., Li, X., Erlandsson, F., Bjorkholm, M., Nordenskjord, M., Gruber, A., Wallin, K. L., and Xu, D. (2004) Telomere attrition predominantly occurs in precursor lesions during in vivo carcinogenic process of the uterine cervix. Oncogene 23, 7441-7447
17. Bickenbach, J. R., Vormwald-Dogan, V., Bachor, C., Bleuel, K., Schnapp, G., and Boukamp, P. (1998) Telomerase is not an epidermal stem cell marker and is downregulated by calcium. J. Invest. Dermatol. 111, 1045-1052
18. Morgenstern, J. P., and Land, H. (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
19. Gomez, D., Aouali, N., Londono-Vallejo, A., Lacroix, L., Megnin-Chanet, F., Lemarteleur, T., Douarre, C., Shin-ya, K., Mailliet, P., Trentesaux, C., Morjani, H., Mergny, J. L., and Riou, J. F. (2003) Resistance to the short- term antiproliferative activity of the G-quadruplex ligand 12459 is associated with telomerase overexpression and telomere capping alteration. J. Biol. Chem. 278, 50554-50562
20. Wu, K. J., Grandori, C., Amacker, M., Simon-Vermot, N., Polack, A., Lingner, J., and Dalla-Favera, R. (1999) Direct activation of TERT transcription by c-MYC. Nat. Genet. 21, 220-224
21. Boukamp, P., Tilgen, W., Dzarlieva, R. T., Breitkreutz, D., Haag, D., Riehl, R. K., Bohnert, A., and Fusenig, N. E. (1982) Phenotypic and genotypic characteristics of a cell line from a squamous cell carcinoma of human skin. J. Natl. Cancer Inst. 68, 415-427
22. Popp, S., Waltering, S., Herbst, C., Moll, I., and Boukamp, P. (2002) UV-B-type mutations and chromosomal imbalances indicate common pathways for the development of Merkel and skin squamous cell carcinomas. Int. J. Cancer 99, 352-360
23. Beitzinger, M., Oswald, C., Beinoraviciute-Kellner, R., and Stiewe, T. (2006) Regulation of telomerase activity by the p53 family member p73. Oncogene 25, 813-826
24. Aisner, D. L., Wright, W. E., and Shay, J. W. (2002) Telomerase regulation: not just flipping the switch. Curr. Opin. Genet. Dev. 12, 80-85
25. Ulaner, G. A., Hu, J. F., Vu, T. H., Oruganti, H., Giudice, L. C., and Hoffman, A. R. (2000) Regulation of telomerase by alternate splicing of human telomerase reverse transcriptase (hTERT) in normal and neoplastic ovary, endometrium, and myometrium. Int. J. Cancer 85, 330-335
26. Yi, X., White, D. M., Aisner, D. L., Baur, J. A., Wright, W. E., and Shay, J. W. (2000) An alternate splicing variant of the human telomerase catalytic subunit inhibits telomerase activity. Neoplasia 2, 433-440
27. Gisselsson, D., Jonson, T., Yu, C., Martins, C., Mandahl, N., Wiegant, J., Jin, Y., Mertens, F., and Jin, C. (2002) Centrosomal abnormalities, multipolar mitoses, and chromosomal instability in head and neck tumours with dysfunctional telomeres. Br. J. Cancer 87, 202-207
28. Stewenius, Y., Gorunova, L., Jonson, T., Larsson, N., Hoglund, M., Mandahl, N., Mertens, F., Mitelman, F., and Gisselsson, D. (2005) Structural and numerical chromosome changes in colon cancer develop through telomere-mediated anaphase bridges, not through mitotic multipolarity. Proc. Natl. Acad. Sci. U. S. A. 102, 5541-5546
29. Pantic, M., Zimmermann, S., El Daly, H., Opitz, O. G., Popp, S., Boukamp, P., and Martens, U. M. (2006) Telomere dysfunction and loss of p53 cooperate in defective mitotic segregation of chromosomes in cancer cells. Oncogene 25, 4413-4420
30. Dong, W., Kloz, U., Accardi, R., Caldeira, S., Tong, W. M., Wang, Z. Q., Jansen, L., Durst, M., Sylla, B. S., Gissmann, L., and Tommasino, M. (2005) Skin hyperproliferation and susceptibility to chemical carcinogenesis in transgenic mice expressing E6 and E7 of human papillomavirus type 38. J. Virol. 79, 14899-14908
31. Schaper, I. D., Marcuzzi, G. P., Weissenborn, S. J., Kasper, H. U., Dries, V., Smyth, N., Fuchs, P., and Pfister, H. (2005) Development of skin tumors in mice transgenic for early genes of human papillomavirus type 8. Cancer Res. 65, 1394-1400
32. Racek, T., Mise, N., Li, Z., Stoll, A., and Putzer, B. M. (2005) C-terminal p73 isoforms repress transcriptional activity of the human telomerase reverse transcriptase (hTERT) promoter. J. Biol. Chem. 280, 40402-40405
33. Boldrini, L., Loggini, B., Gisfredi, S., Zucconi, Y., Di Quirico, D., Biondi, R., Cervadoro, G., Barachini, P., Basolo, F., Pingitore, R., and Fontanini, G. (2003) Evaluation of telomerase in non-melanoma skin cancer. Int. J. Mol. Med. 11, 607-611
34. Parris, C. N., Jezzard, S., Silver, A., MacKie, R., McGregor, J. M., and Newbold, R. F. (1999) Telomerase activity in melanoma and non-melanoma skin cancer. Br. J. Cancer 79, 47-53
35. Murnane, J. P., and Sabatier, L. (2004) Chromosome rearrangements resulting from telomere dysfunction and their role in cancer. Bioessays 26, 1164-1174
36. Steenbergen, R. D., de Wilde, J., Wilting, S. M., Brink, A. A., Snijders, P. J., and Meijer, C. J. (2005) HPV-mediated transformation of the anogenital tract. J. Clin. Virol. 32 (Suppl. 1), S25-S33
37. Jin, Y., Martins, C., Jin, C., Salemark, L., Jonsson, N., Persson, B., Roque, L., Fonseca, I., and Wennerberg, J. (1999) Nonrandom karyotypic features in squamous cell carcinomas of the skin. Genes Chromosomes Cancer 26, 295-303
38. Boukamp, P. (2005) Non-melanoma skin cancer: what drives tumor development and progression? Carcinogenesis 26, 1657-1667
39. Der-Sarkissian, H., Bacchetti, S., Cazes, L., and Londono-Vallejo, J. A. (2004) The shortest telomeres drive karyotype evolution in transformed cells. Oncogene 23, 1221-1228
40. Filatov, L., Golubovskaya, V., Hurt, J. C., Byrd, L. L., Phillips, J. M., and Kaufmann, W. K. (1998) Chromosomal instability is correlated with telomere erosion and inactivation of G2 checkpoint function in human fibroblasts expressing human papillomavirus type 16 E6 oncoprotein. Oncogene 16, 1825-1838