E7 oncoprotein of novel human papillomavirus type 108 lacking the E6 gene induces dysplasia in organotypic keratinocyte cultures

Journal of Virology

Volumn 83, Issue 7, 2009, Pages 2907-2916

  Nobre, Rui Jorge ^a,b   Herráez Hernández, Elsa ^a   Fei, Jian Wei ^a   Langbein, Lutz ^a   Kaden, Sylvia ^a   Gröne, Hermann Josef ^a   De Villiers, Ethel Michele ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b Instituto Portugues de Oncologia Francisco Gentil Centro Regional de Oncologia de Coimbra SA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CYTOKERATIN 10; CYTOKERATIN 14; CYTOKERATIN 16; INVOLUCRIN; LORICRIN; PROTEIN E6; PROTEIN E7; PROTEIN P21; PROTEIN P53; VIRUS DNA;

ADULT; APOPTOSIS; ARTICLE; CELL CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; DYSPLASIA; FEMALE; GENETIC POLYMORPHISM; GENITAL SYSTEM; GENOME ANALYSIS; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 101; HUMAN PAPILLOMAVIRUS TYPE 103; HUMAN PAPILLOMAVIRUS TYPE 108; HUMAN TISSUE; KERATINOCYTE; LIPID STORAGE; NONHUMAN; PAPILLOMA VIRUS; PHYLOGENY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; UTERINE CERVIX CARCINOMA IN SITU; UTERINE CERVIX EPITHELIUM; VIRUS GENE; VIRUS GENOME; VIRUS ISOLATION; VIRUS TYPING; BIOSYNTHESIS; CASE REPORT; CELL TRANSFORMATION; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; LIPID METABOLISM; PATHOGENICITY; UNITED STATES; UTERINE CERVIX TUMOR; VIROLOGY; VIRUS INFECTION;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPES; PAPILLOMAVIRIDAE;

ADULT; APOPTOSIS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DNA, VIRAL; FEMALE; GENOME, VIRAL; HUMANS; KERATINOCYTES; LIPID METABOLISM; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS E7 PROTEINS; PAPILLOMAVIRUS INFECTIONS; UNITED STATES; UTERINE CERVICAL NEOPLASMS;

EID: 63149124929     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02490-08     Document Type: Article

References (43)

1. Alazawi, W. O. F., L. S. Morris, M. A. Stanley, D. R. Garrod, and N. Coleman. 2003. Altered expression of desmosomal components in high-grade squamous intraepithelial lesions of the cervix. Virchows Arch. 443: 51-56.
2. Allen-Hoffmann, B., S. J. Schlosser, C. A. R. Ivarie, C. A. Sattler, L. F. Meisner, and S. L. O'Connor. 2000. Normal growth and differentiation in spontaneously immortalized near-diploid human keratinocyte cell line, NIKS. J. Investig. Dermatol. 114:444-455.
3. Balsitis, S., F. Dick, N. Dyson, and P. F. Lambert. 2006. Critical roles for non-pRb targets of human papillomavirus type 16 E7 in cervical carcinogen-esis. Cancer Res. 66:9393-9400.
4. Balsitis, S., F. Dick, D. Lee, L. Farrell, R. K. Hyde, A. Griep, N. Dyson, and P. F. Lambert. 2005. Examination of the pRb-dependent and pRb-independent functions of E7 in vivo. J. Virol. 79:11392-11402.
5. Band, V., D. Zajchowski, V. Kulesa, and R. Sager. 1990. Human papillomavirus DNAs immortalize normal human mammary epithelial cells and reduce their growth factor requirements. Proc. Natl. Acad. Sci. USA 87:463-467.
6. Banerjee, N. S, N. J. Genovese, F. Noya, W.-M. Chien, T. R. Broker, and L. T. Chow. 2006. Conditionally activated E7 proteins of high-risk and low-risk human papillomaviruses induce S phase in postmitotic, differentiated human keratinocytes. J. Virol. 80:6517-6524.
7. Brokaw, J. L., C. L. Yee, and K. Münger. 1994. A mutational analysis of the amino terminal domain of the human papillomavirus type 16 E7 oncoprotein. Virology 205:603-607.
8. Candi, E., R. Schmidt, and G. Melino. 2005. The cornified envelope: a model of cell death in the skin. Nat. Rev. Mol. Cell Biol. 6:328-340.
9. Chen, Z., M. Schiffman, R. Herrero, R. DeSalle, and R. D. Burk. 2007. Human papillomavirus (HPV) types 101 and 103 isolated from cervicovaginal cells lack an E6 open reading frame (ORF) and are related to gamma-papillomaviruses. Virology 360:447-453.
10. Davis, H. E., J. R. Morgan, and M. L. Yarmush. 2002. Polybrene increases retrovirus gene transfer efficiency by enhancing receptor-independent virus adsorption on target cell membranes. Biophys. Chem. 97:159-172.
11. 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.
12. Demers, G. W., C. L. Halbert, and D. A. Galloway. 1994. Elevated wild-type p53 protein levels in human epithelial cell lines immortalized by the human papillomavirus type 16 E7 gene. Virology 198:169-174.
13. de Villiers, E.-M., C. Fauquet, T. R. Broker, H.-U. Bernard, and H. zur Hausen. 2004. Classification of papillomaviruses. Virology 324:17-27.
14. de Villiers, E.-M., D. Lavergne, F. Chang, K. Syrjänen, P. Tosi, M. Cintorino, R. Santopietro, and S. Syrjänen. 1999. An interlaboratory study to determine the presence of human papillomavirus DNA in esophageal carcinoma in China. Int. J. Cancer 81:225-228.
15. Fei, J.-W., Q.-X. Wei, P. Angel, and E.-M. de Villiers. 2005. Differential enhancement of a cutaneous HPV promoter by p63, Jun and mutant p53. Cell Cycle 4:689-696.
16. Fei, J.-W., and E.-M. de Villiers. 2008. Degradation of HPV20E6 by p53: ΛNp63α and p53mutR248W protect the wild type p53 mediated caspase-degradation. Int. J. Cancer 123:108-116.
17. Flores, E. R., L. Allen-Hoffmann, D. Lee, and P. F. Lambert. 2000. The human papillomavirus type 16 E7 oncogene is required for the productive stage of the viral life cycle. J. Virol. 74:6622-6631.
18. Forslund, O., A. Antonsson, P. Nordin, B. Stenquist, and B. G. Hansson. 1999. A broad range of human papillomavirus types detected with a general PCR method suitable for analysis of cutaneous tumours and normal skin. J. Gen. Virol. 80:2437-2443.
19. Galy, B., D. Ferring-Appel, S. Kaden, H.-J. Gröne, and M. W. Hentze. 2008. Iron regulatory proteins are essential for intestinal function and control key iron absorption molecules in the duodenum. Cell Metab. 7:79-85.
20. Geiger, T., H. Sabanay, N. Kravchenko-Balasha, B. Geiger, and A. Levitzki. 2008. Anomalous features of EMT during keratinocyte transformation. PLoS ONE 3:e1574.
21. Gulliver, G. A., R. L. Herber, A. Liem, and P. F. Lambert. 1997. Both conserved region 1 (CR1) and CR2 of the human papillomavirus type 16 E7 oncogene are required for induction of epidermal hyperplasia and tumor formation in transgenic mice. J. Virol. 71:5905-5914.
22. Halbert, C. L. G. W. Demers, and D. A. Galloway. 1991. The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J. Virol. 65:473-478.
23. 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.
24. Helt, A. M., J. O. Funk, and D. A. Galloway. 2002. Inactivation of both the retinoblastoma tumor suppressor and p21 by the human papillomavirus type 16 E7 oncoprotein is necessary to inhibit cell cycle arrest in human epithelial cells. J. Virol. 76:10559-10568.
25. Hervé, J.-C. 2008. The apical junctional complexes, composition, structure, and characteristics. Biochim. Biophys. Acta 1778:559-561.
26. Jennemann, R., R. Sandhoff, L. Langbein, S. Kaden, U. Rothermel, H. Gallala, K. Sandhoff, H. Wiegandt, and H.-J. Gröne. 2007. Integrity and barrier function of the epidermis critically depend on glucosylceramide synthesis. J. Biol. Chem. 282:3083-3094.
27. Jewers, R. J., P. Hildebrandt, J. W. Ludlow, B. Kell, and D. J. McCance. 1992. Regions of human papillomavirus type 16 E7 oncoprotein required for immortalization of human keratinocytes. J. Virol. 66:1329-1335.
28. Jones, D. L., D. A. Thompson, E. Suh-Bürgmann, M. Grace, and K. Münger. 1999. Expression of the HPV E7 oncoprotein mimics but does not evoke a p53-dependent cellular DNA damage response pathway. Virology 258:406-414.
29. Langbein, L., C. Grand, C. Kuhn, S. Praetzel, J. Kartenbeck, J. M. Brandner, I. Moll, and W. W. Franke. 2002. Tight junctions and compositionally related junctional structures in mammalian stratified epithelia and cell cultures derived therefrom. Eur. J. Cell Biol. 81:419-435.
30. Longworth, M. S., and L. A. Laimins. 2004. Pathogenesis of human papillomavirus in differentiating epithelia. Microbiol. Mol. Biol. Rev. 68:362-372.
31. Mantovani, F., and L. Banks. 2001. The human papillomavirus E6 protein and its contribution to malignant progression. Oncogene 20:7874-7887.
32. Massimi, P., and L. Banks. 1997. Repression of p53 transcriptional activity by the HPV E7 proteins. Virology 27:255-259.
33. Moll, R., M. Divo, and L. Langbein. 2008. The human keratins: biology and pathology. Histochem. Cell Biol. 129:705-733.
34. Münger, K., J. R. Basile, S. Duensing, A. Eichten, S. L. Gonzalez, M. Grace, and V. L. Zacny. 2001. Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene 20:7888-7898.
35. Münger, K., W. C. Phelps, V. Bubb, P. M. 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.
36. cip1 degradation in differentiated keratinocytes is abrogated by costabilization with cyclin E induced by human papillomavirus E7. J. Virol. 75:6121-6134.
37. Smedts, F., F. Ramaekers, S. Troyanovsky, M. Pruszczynski, M. Link, B. Lane, I. Leigh, C. Schijf, and P. Vooijs. 1992. Keratin expression in cervical cancer. Am. J. Pathol. 141:497-511.
38. Song, S., A. Liem, J. A. Miller, and P. F. Lambert. 2000. Human papillomavirus types 16 E6 and E7 contribute differently to carcinogenesis. Virology 267:141-150.
39. Stokes, D. L. 2007. Desmosomes from a structural perspective. Curr. Opin. Cell Biol. 19:565-571.
40. Thomas, J. T., and L. A. Laimins. 1998. Human papillomavirus oncoproteins E6 and E7 independently abrogate the mitotic spindle checkpoint. J. Virol. 72:1131-1137.
41. Wilson, R., and L. A. Laimins. 2005. Differentiation of HPV-containing cells using organotypic "raft" culture or methylcellulose. Methods Mol. Med. 119:157-169.
42. Wu, R., S. Sun, and B. Steinberg. 2003. Requirement of STAT3 activation for differentiation of mucosal stratified squamous epithelium. Mol. Med. 90:77-84.
43. zur Hausen, H. 2002. Papillomaviruses and cancer: from basic studies to clinical application. Nat. Rev. Cancer 2:342-350.