Cutaneous human papillomavirus E7 type-specific effects on differentiation and proliferation of organotypic skin cultures

Cellular Oncology

Volumn 31, Issue 3, 2009, Pages 213-226

  Westphal, K ^a   Akgul B ^b,c   Storey, A ^b   Nindl, I ^a,d  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UNIVERSITY OF COLOGNE   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

PV; Human papillomavirus (HPV); Human primary keratinocytes (HPK); Organotypic skin cultures; p16INK4a

Indexed keywords

CELL CYCLE PROTEIN; CELL MARKER; CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYCLIN E; CYTOKERATIN 10; CYTOKERATIN 14; INVOLUCRIN; MESSENGER RNA; PROTEIN E7;

ADULT; ARTICLE; BETAPAPILLOMAVIRUS; CELL CULTURE; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DERMIS; GENETIC TRANSDUCTION; HUMAN; HUMAN BETAPAPILLOMAVIRUS TYPE 1; HUMAN BETAPAPILLOMAVIRUS TYPE 38; HUMAN BETAPAPILLOMAVIRUS TYPE 4; HUMAN BETAPAPILLOMAVIRUS TYPE 5; HUMAN BETAPAPILLOMAVIRUS TYPE 8; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; RETROVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN CANCER; SKIN CARCINOGENESIS; SKIN CULTURE; SQUAMOUS CELL CARCINOMA; VIRUS RECOMBINANT;

ALPHAPAPILLOMAVIRUS; ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P16; GENE EXPRESSION; HUMANS; KERATINOCYTES; KERATINS; MICE; NIH 3T3 CELLS; PAPILLOMAVIRUS E7 PROTEINS; PAPILLOMAVIRUS INFECTIONS; SKIN; SPECIES SPECIFICITY; YOUNG ADULT;

EID: 67650217779     PISSN: 15705870     EISSN: None     Source Type: Journal    
DOI: 10.3233/CLO-2009-0476     Document Type: Article

References (40)

1. E.M. de Villiers, C. Fauquet, T.R. Broker, H.U. Bernard and H. zur Hausen, Classification of papillomaviruses, Virology 324(2004), 17-27.
2. M. Gottschling, A. Stamatakis, I. Nindl, E. Stockfleth, A. Alonso and I.G. Bravo, Multiple evolutionary mechanisms drive papillomavirus diversification, Mol. Biol. Evol. 24(2007), 1242-1258.
3. N. Munoz, F.X. Bosch, S. de Sanjose, R. Herrero, X. Castell- sague, K.V. Shah, P.J. Snijders and C.J. Meijer, Epidemiologic classification of human papillomavirus types associated with cervical cancer, N. Engl. J. Med. 348(2003), 518-527.
4. International Agency for Research on Cancer, IARC monographs on the evaluation of carcinogenic risks to humans. Human papillomaviruses, lARCLyon France 64(1995).
5. H. zur Hausen, Molecular pathogenesis of cancer of the cervix and its causation by specific human papillomavirus types, Curr. Top. Microbiol. Immunol. 186(1994), 131-156.
6. H. zur Hausen, Papillomaviruses and cancer: from basic studies to clinical application, Nat. Rev. Cancer 2(2002), 342-350.
7. E. Berezutskaya, B. Yu, A. Morozov, P. Raychaudhuri and S. Bagchi, Differential regulation of the pocket domains of the retinoblastoma family proteins by the HPV16 E7 oncoprotein, Cell Growth Differ. 8(1997), 1277-1286.
8. S.N. Boyer, D.E. Wazer and V. Band, E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway, Cancer Res. 56(1996), 4620-4624.
9. N. Dyson, P.M. Howley, K. Muenger and E. Harlow, The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product, Science 243(1989), 934-937.
10. Y. Li, M.A. Nichols, J.W. Shay and Y. Xiong, Transcriptional repression of the D-type cyclin-dependent kinase inhibitor p16 by the retinoblastoma susceptibility gene product pRb, Cancer Res. 54(1994), 6078-6082.
11. S.N. Khleif, J. DeGregori, C.L. Yee, G.A. Otterson, F.J. Kaye, J.R. Nevins and P.M. Howley, Inhibition of cyclin D-CDK4/CDK6 activity is associated with an E2F-mediated induction of cyclin kinase inhibitor activity, Proc. Natl. Acad. Sci. USA 93(1996), 4350-4354.
12. D. Parry, S. Bates, D.J. Mann and G. Peters, Lack of cyclin D-Cdk complexes in Rb-negative cells correlates with high levels of p16INK4/MTS1 tumour suppressor gene product, EMBO J. 14(1995), 503-511.
13. R. Klaes, T. Friedrich, D. Spitkovsky, R. Ridder, W. Rudy, U. Petry, G. Dallenbach-Hellweg, D. Schmidt and D.M. von Knebel Doeberitz, Overexpression of p16(INK4A) as a specific marker for dysplastic and neoplastic epithelial cells of the cervix uteri, lnt. J. Cancer 92(2001), 276-284.
14. H. Pfister, Chapter 8: Human papillomavirus and skin cancer, J. Natl. Cancer lnst. Monogr. 31(2003), 52-56.
15. B. Akgúl, J.C. Cooke and A. Storey, HPV-associated skin disease, J. Pathol. 208(2006), 165-175.
16. I. Nindl, M. Gottschling and E. Stockfleth, Human papillo- maviruses and non-melanoma skin cancer: Basic virology and clinical manifestations, Dis. Markers 23(2007), 247-259.
17. S. Jablonska, J. Dabrowski and K. Jakubowicz, Epidermodys- plasia verruciformis as a model in studies on the role of papo- vaviruses in oncogenesis, Cancer Res. 32(1972), 583-589.
18. G. Orth, S. Jablonska, M. Favre, O. Croissant, M. Jarzabek- Chorzelska and G. Rzesa, Characterization of two types of human papillomaviruses in lesions of epidermodysplasia verruci- formis, Proc. Natl. Acad. Sci. USA 75(1978), 1537-1541.
19. S.Majewski and S.Jablonska,Human papillomavirus- associated tumors of the skin and mucosa, J. Am. Acad. Dermatol. 36(1997), 659-685.
20. A. Schmitt, J.B. Harry, B. Rapp, F.O. Wettstein and T. Ift-ner, Comparison of the properties of the E6 and E7 genes of low- and high-risk cutaneous papillomaviruses reveals strongly transforming and high Rb-binding activity for the E7 protein of the low-risk human papillomavirus type 1, J. Virol. 68(1994),7051-7059.
21. S. Caldeira, I. Zehbe, R. Accardi, I. Malanchi, W. Dong, M. Gi- arre, E.M. de Villiers, R. Filotico, P. Boukamp and M. Tom- masino, The E6 and E7 proteins of the cutaneous human papil- lomavirus type 38 display transforming properties, J. Virol. 77(2003), 2195-2206.
22. B. Akgúl, L. Ghali, D. Davies, H. Pfister, I.M. Leigh and A. Storey, HPV8 early genes modulate differentiation and cell cycle of primary human adult keratinocytes, Exp. Dermatol. 16(2007), 590-599.
23. L.T. Chow and T.R. Broker, ln vitroexperimental systems for HPV: Epithelial raft cultures for investigations of viral reproduction and pathogenesis and for genetic analyses of viral proteins and regulatory sequences, Clin. Dermatol. 15(1997),217-227.
24. I.L. Boxman, L.H. Mulder, F. Noya, V. de Waard, S. Gibbs, T.R. Broker, F. ten Kate, L.T. Chow and J. ter Schegget, Transduction of the E6 and E7 genes of epidermodysplasia- verruciformis-associated human papillomaviruses alters human keratinocyte growth and differentiation in organotypic cultures, J. Invest. Dermatol. 117(2001), 1397-1404.
25. B. Akgúl, R. Garcia-Escudero, L. Ghali, H.J. Pfister, P.G. Fuchs, H. Navsaria and A. Storey, The E7 protein of cutaneous human papillomavirus type 8 causes invasion of human ker- atinocytes into the dermis in organotypic cultures of skin, Cancer Res. 65(2005), 2216-2223.
26. J.G. Rheinwald, Methods for Clonal Growth and Serial Cultivation of Normal Human Epidermal Keratinocytes and Mesothelial Cells, IRL Press, Oxford, 1989, pp. 81-94.
27. S. Rozen and H. Skaletsky, Primer3 on the WWW for general users and for biologist programmers, Methods Mol. Biol. 132(2000), 365-386.
28. I. Nindl, A. Koehler, T. Meyer, T. Forschner, C.J. Meijer, P.J.Snijders, W. Sterry and E. Stockfleth, Detection of human pa- pillomavirus DNA in primary squamous cell carcinoma and metastases, Br.J.Dermatol. 154(2006), 797-799.
29. L.G. Martin, G.W. Demers and D.A. Galloway, Disruption of the G1/S transition in human papillomavirus type 16 E7- expressing human cells is associated with altered regulation of cyclin E, J. Virol. 72(1998), 975-985.
30. C.L. Halbert, G.W. Demers and D.A. Galloway, The E6 and E7 genes of human papillomavirus type 6 have weak immortalizing activity in human epithelial cells, J. Virol. 66(1992),2125-2134.
31. W. Zhao, F. Noya, W.Y. Chen, T.M. Townes, L.T. Chow and T.R. Broker, Trichostatin A up-regulates human papillomavirus type 11 upstream regulatory region-E6 promoter activity in un- differentiated primary human keratinocytes, J. Virol. 73(1999),5026-5033.
32. J. Steude, R. Kulke and E. Christophers, Interleukin-1- stimulated secretion of interleukin-8 and growth-related oncogene-alpha demonstrates greatly enhanced keratinocyte growth in human raft cultured epidermis, J. Invest. Dermatol. 119(2002), 1254-1260.
33. R.H. Rice and H. Green, Presence in human epidermal cells of a soluble protein precursor of the cross-linked envelope: activation of the cross-linking by calcium ions, Cell 18(1979), 681-694.
34. G.F. Murphy, T.C. Flynn, R.H. Rice and G.S. Pinkus, Involu-crin expression in normal and neoplastic human skin: a marker for keratinocyte differentiation, J. Invest. Dermatol. 82(1984),453-457.
35. INK4a in nonmelanoma skin cancer, Dermatol. Surg. 30(2004), 409-414.
36. V. Dulic, E. Lees and S.I. Reed, Association of human cyclin E with a periodic G1-S phase protein kinase, Science 257(1992),1958-1961.
37. R. Donnellan and R. Chetty, Cyclin E in human cancers, FASEB J. 13(1999), 773-780.
38. T. Sano, T. Oyama, K. Kashiwabara, T. Fukuda and T. Naka- jima, Expression status of p16 protein is associated with human papillomavirus oncogenic potential in cervical and genital lesions, Am. J. Pathol. 153(1998), 1741-1748.
39. S. Smola-Hess, J. Pahne, C. Mauch, P. Zigrino, H. Smola and H.J. Pfister, Expression of membrane type 1 matrix metallo- proteinase in papillomavirus-positive cells: role of the human papillomavirus (HPV) 16 and HPV8 E7 gene products, J. Gen. Virol. 86(2005), 1291-1296.
40. D.J. Griffiths, P.J. Venables, R.A. Weiss and M.T. Boyd, A novel exogenous retrovirus sequence identified in humans, J. Virol. 71(1997), 2866-2872.