Human papillomavirus mediated inhibition of DNA damage sensing and repair drives skin carcinogenesis

Molecular Cancer

Volumn 14, Issue 1, 2015, Pages

  Hufbauer, Martin ^a   Cooke, James ^b   van der Horst, Gijsbertus T ^c   Pfister, Herbert ^a   Storey, Alan ^d   Akgül, Baki ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

DNA damage repair; E6 oncoprotein; HPV of genus betapapillomavirus; Human papillomavirus 8 (HPV8); Non melanoma skin cancer; Photolyase

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE 1; DEOXYRIBODIPYRIMIDINE PHOTOLYASE; DIMER; E1A ASSOCIATED P300 PROTEIN; HISTONE H2AX; LYSINE; MUTANT PROTEIN; PROTEIN E6; THYMINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME PHOSPHORYLATION; EPIDERMIS; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; MONOLAYER CULTURE; MOUSE; MOUSE MUTANT; MOUSE STRAIN; NONHUMAN; POINT MUTATION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RADIATION CARCINOGENESIS; RADIATION RESPONSE; SKIN CANCER; SKIN CARCINOGENESIS; SKIN CULTURE; ULTRAVIOLET RADIATION; WART VIRUS; WESTERN BLOTTING; ADVERSE EFFECTS; ANIMAL; FEMALE; GENETICS; MALE; PAPILLOMAVIRIDAE; SKIN NEOPLASMS;

ANIMALS; DNA DAMAGE; DNA REPAIR; FEMALE; HUMANS; MALE; MICE; PAPILLOMAVIRIDAE; SKIN NEOPLASMS; ULTRAVIOLET RAYS;

EID: 84945921260     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/s12943-015-0453-7     Document Type: Article

References (33)

1. Bowden GT. Prevention of non-melanoma skin cancer by targeting ultraviolet-B-light signalling. Nat Rev Cancer. 2004;4:23-35.
2. Garinis GA, Mitchell JR, Moorhouse MJ, Hanada K, de Waard H, Vandeputte D, et al. Transcriptome analysis reveals cyclobutane pyrimidine dimers as a major source of UV-induced DNA breaks. EMBO J. 2005;24:3952-62.
3. Pfeifer GP, Besaratinia A. UV wavelength-dependent DNA damage and human non-melanoma and melanoma skin cancer. Photochem Photobiol Sci. 2012;11:90-7.
4. Bradford PT, Goldstein AM, Tamura D, Khan SG, Ueda T, Boyle J, et al. Cancer and neurologic degeneration in xeroderma pigmentosum: long term follow-up characterises the role of DNA repair. J Med Genet. 2011;48:168-76.
5. Schul W, Jans J, Rijksen YM, Klemann KH, Eker AP, de Wit J, et al. Enhanced repair of cyclobutane pyrimidine dimers and improved UV resistance in photolyase transgenic mice. EMBO J. 2002;21:4719-29.
6. Jans J, Schul W, Sert YG, Rijksen Y, Rebel H, Eker AP, et al. Powerful skin cancer protection by a CPD-photolyase transgene. Curr Biol. 2005;15:105-15.
7. Jans J, Garinis GA, Schul W, van Oudenaren A, Moorhouse M, Smid M, et al. Differential role of basal keratinocytes in UV-induced immunosuppression and skin cancer. Mol Cell Biol. 2006;26:8515-26.
8. Nindl I, Rosl F. Molecular concepts of virus infections causing skin cancer in organ transplant recipients. Am J Transplant. 2008;8:2199-204.
9. Feltkamp MC, de Koning MN, Bavinck JN, Ter Schegget J. Betapapillomaviruses: innocent bystanders or causes of skin cancer. J Clin Virol. 2008;43:353-60.
10. Weissenborn SJ, Nindl I, Purdie K, Harwood C, Proby C, Breuer J, et al. Human papillomavirus-DNA loads in actinic keratoses exceed those in non-melanoma skin cancers. J Invest Dermatol. 2005;125:93-7.
11. Schaper ID, Marcuzzi GP, Weissenborn SJ, Kasper HU, Dries V, Smyth N, et al. Development of skin tumors in mice transgenic for early genes of human papillomavirus type 8. Cancer Res. 2005;65:1394-400.
12. Marcuzzi GP, Hufbauer M, Kasper HU, Weissenborn SJ, Smola S, Pfister H: Spontaneous tumor development in human papillomavirus type 8 E6 transgenic mice and rapid induction by UV-light exposure and wounding. J Gen Virol. 2009;90: 2855-2864
13. Hufbauer M, Lazic D, Akgül B, Brandsma JL, Pfister H, Weissenborn SJ. Enhanced human papillomavirus type 8 oncogene expression levels are crucial for skin tumorigenesis in transgenic mice. Virology. 2010;403:128-36.
14. Jackson S, Harwood C, Thomas M, Banks L, Storey A. Role of Bak in UV-induced apoptosis in skin cancer and abrogation by HPV E6 proteins. Genes Dev. 2000;14:3065-73.
15. Underbrink MP, Howie HL, Bedard KM, Koop JI, Galloway DA. E6 proteins from multiple human betapapillomavirus types degrade Bak and protect keratinocytes from apoptosis after UVB irradiation. J Virol. 2008;82:10408-17.
16. Wallace NA, Galloway DA: Manipulation of cellular DNA damage repair machinery facilitates propagation of human papillomaviruses. Semin Cancer Biol. 2014;26:30-42.
17. Giampieri S, Storey A. Repair of UV-induced thymine dimers is compromised in cells expressing the E6 protein from human papillomaviruses types 5 and 18. Br J Cancer. 2004;90:2203-9.
18. Simmonds M, Storey A. Identification of the regions of the HPV 5 E6 protein involved in Bak degradation and inhibition of apoptosis. Int J Cancer. 2008;123:2260-6.
19. Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K, et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature. 2005;434:864-70.
20. Ghosal G, Chen J. DNA damage tolerance: a double-edged sword guarding the genome. Transl Cancer Res. 2013;2:107-29.
21. Bonner WM, Redon CE, Dickey JS, Nakamura AJ, Sedelnikova OA, Solier S, et al. GammaH2AX and cancer. Nat Rev Cancer. 2008;8:957-67.
22. Müller-Schiffmann A, Beckmann J, Steger G. The E6 protein of the cutaneous human papillomavirus type 8 can stimulate the viral early and late promoters by distinct mechanisms. J Virol. 2006;80:8718-28.
23. Münch P, Probst S, Schuetz J, Leiprecht N, Busch M, Wesselborg S, et al. Cutaneous papillomavirus E6 proteins must interact with p300 and block p53-mediated apoptosis for cellular immortalization and tumorigenesis. Cancer Res. 2010;70:6913-24.
24. Howie HL, Koop JI, Weese J, Robinson K, Wipf G, Kim L, et al. Beta-HPV 5 and 8 E6 promote p300 degradation by blocking AKT/p300 association. PLoS Pathog. 2011;7:e1002211.
25. White EA, Kramer RE, Tan MJ, Hayes SD, Harper JW, Howley PM. Comprehensive analysis of host cellular interactions with human papillomavirus E6 proteins identifies new E6 binding partners and reflects viral diversity. J Virol. 2012;86:13174-86.
26. Rozenblatt-Rosen O, Deo RC, Padi M, Adelmant G, Calderwood MA, Rolland T, et al. Interpreting cancer genomes using systematic host network perturbations by tumour virus proteins. Nature. 2012;487:491-5.
27. White EA, Howley PM. Proteomic approaches to the study of papillomavirus-host interactions. Virology. 2013;435:57-69.
28. Wallace NA, Robinson K, Howie HL, Galloway DA. HPV 5 and 8 E6 abrogate ATR activity resulting in increased persistence of UVB induced DNA damage. PLoS Pathog. 2012;8:e1002807.
29. Weissenborn SJ, De Koning MN, Wieland U, Quint WG, Pfister HJ. Intrafamilial transmission and family-specific spectra of cutaneous betapapillomaviruses. J Virol. 2009;83:811-6.
30. Akgül B, Karle P, Adam M, Fuchs PG, Pfister HJ. Dual role of tumor suppressor p53 in regulation of DNA replication and oncogene E6-promoter activity of epidermodysplasia verruciformis-associated human papillomavirus type 8. Virology. 2003;308:279-90.
31. Leverrier S, Bergamaschi D, Ghali L, Ola A, Warnes G, Akgül B, et al. Role of HPV E6 proteins in preventing UVB-induced release of pro-apoptotic factors from the mitochondria. Apoptosis. 2007;12:549-60.
32. O'Shaughnessy RF, Akgül B, Storey A, Pfister H, Harwood CA, Byrne C. Cutaneous human papillomaviruses down-regulate AKT1, whereas AKT2 up-regulation and activation associates with tumors. Cancer Res. 2007;67:8207-15.
33. Lazic D, Alborzi F, Marcuzzi GP, Angel P, Hess J, Pfister H, et al. Enhanced StefinA and Sprr2 expression during papilloma formation in HPV8 transgenic mice. J Dermatol Sci. 2011;62:84-90.