Human papillomavirus types detected in skin warts and cancer differ in their transforming properties but commonly counteract UVB induced protective responses in human keratinocytes

Virology

Volumn 468, Issue , 2014, Pages 647-659

  Shterzer, Naama ^a   Heyman, Dariya ^a   Shapiro, Beny ^a   Yaniv, Abraham ^a   Jackman, Anna ^a   Serour, Francis ^b   Chaouat, Malka ^c   Gonen, Pinhas ^a   Tommasino, Massimo ^d   Sherman, Levana ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b WOLFSON MEDICAL CENTER   (Israel)

^c HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^d INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

Author keywords

Apoptosis; Bak; Bax; Beta HPVs; Cutaneous HPV types; p53; Skin; Skin cancer; UVB; Warts

Indexed keywords

CALCIUM; PROTEIN BAK; PROTEIN BAX; PROTEIN E6; PROTEIN E7; PROTEIN P53; SURVIVIN; VIRUS PROTEIN;

ADULT; ARTICLE; CELL CYCLE ARREST; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; COLONY FORMATION; COMPARATIVE STUDY; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 10; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 24; HUMAN PAPILLOMAVIRUS TYPE 38; HUMAN PAPILLOMAVIRUS TYPE 49; HUMAN PAPILLOMAVIRUS TYPE 8; INTRACELLULAR SIGNALING; KERATINOCYTE; LIFESPAN; NEWBORN; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SERUM; SKIN CANCER; ULTRAVIOLET B RADIATION; VERRUCA VULGARIS; VIRUS DETECTION; VIRUS IDENTIFICATION; VIRUS REPLICATION; WART VIRUS; 3T3 CELL LINE; ANIMAL; CLASSIFICATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; PAPILLOMA VIRUS; PHYSIOLOGY; PLASMID; RADIATION RESPONSE; SKIN TUMOR; ULTRAVIOLET RADIATION; VIROLOGY; VIRUS CELL TRANSFORMATION;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPES;

ANIMALS; CELL SURVIVAL; CELL TRANSFORMATION, VIRAL; GENE EXPRESSION REGULATION, VIRAL; HUMANS; KERATINOCYTES; MICE; NIH 3T3 CELLS; PAPILLOMAVIRIDAE; PLASMIDS; SKIN NEOPLASMS; ULTRAVIOLET RAYS; VIRAL PROTEINS; WARTS;

EID: 84908011883     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.09.015     Document Type: Article

References (59)

1. Accardi R., Dong W., Smet A., Cui R., Hautefeuille A., Gabet A.S., Sylla B.S., Gissmann L., Hainaut P., Tommasino M. Skin human papillomavirus type 38 alters p53 functions by accumulation of delta Np73. EMBO Rep. 2006, 7(3):334-340.
2. Akgül B., Cooke J.C., Storey A. HPV-associated skin disease. J. Pathol. 2006, 208(2):165-175.
3. Akgül B., Ghali L., Davies D., Pfister H., Leigh I.M., Storey A. HPV8 early genes modulate differentiation and cell cycle of primary human adult keratinocytes. Exp. Dermatol. 2007, 16(7):590-599.
4. Altieri D.C. Survivin and IAP proteins in cell-death mechanisms. Biochem. J. 2010, 430(2):199-205.
5. Asadurian Y., Kurilin H., Lichtig H., Jackman A., Gonen P., Tommasino M., Zehbe I., Sherman L. Activities of human papillomavirus 16 E6 natural variants in human keratinocytes. J. Med. Virol. 2007, 79(11):1751-1760.
6. Bedard K.M., Underbrink M.P., Howie H.L., Galloway D.A. The E6 oncoproteins from human betapapillomaviruses differentially activate telomerase through an E6AP-dependent mechanism and prolong the lifespan of primary keratinocytes. J. Virol. 2008, 82(8):3894-3902.
7. Borbély A.A., Murvai M., Kónya J., Beck Z., Gergely L., Li F., Veress G. Effects of human papillomavirus type 16 oncoproteins on survivin gene expression. J. Gen. Virol. 2006, 87(Pt 2):287-294.
8. Boxman I.L., Mulder L.H., Noya F., Waard V., Gibbs S., Broker T.R., Kate F., Chow L., Schegget T.J. 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. 2001, 117(6):1397-1404.
9. Bzhalava D., Guan P., Franceschi S., Dillner J., Clifford G. A systematic review of the prevalence of mucosal and cutaneous human papillomavirus types. Virology 2013, 445(1-2):224-231.
10. Cogliano V., Baan R., Straif K., Grosse Y., Secretan B, El Ghissassi F. Carcinogenicity of human papillomaviruses. Lancet Oncol. 2005, 6(4):204. WHO International Agency for Research on Cancer.
11. Caldeira S., Zehbe I., Accardi R., Malanchi I., Dong W., Giarrè M., de Villiers E.M., Filotico R., Boukamp P., Tommasino M. The E6 and E7 proteins of the cutaneous human papillomavirus type 38 display transforming properties. J. Virol. 2003, 77(3):2195-2206.
12. Candi E., Schmidt R., Melino G. The cornified envelope: a model of cell death in the skin. Nat. Rev. Mol. Cell Biol. 2005, 6(4):328-340.
13. Cornet I., Bouvard V., Campo M.S., Thomas M., Banks L., Gissmann L., Lamartine J., Sylla B.S., Accardi R., Tommasino M. Comparative analysis of transforming properties of E6 and E7 from different beta human papillomavirus types. J. Virol. 2012, 86(4):2366-2370.
14. de Villiers E.M., Fauquet C., Broker T.R., Bernard H.U., zur Hausen H. Classification of papillomaviruses. Virology 2004, 324(1):17-27.
15. Dong W., Kloz U., Accardi R., Caldeira S., Tong W.M., Wang Z.Q., Jansen L., Dürst M., Sylla B.S., Gissmann L., Tommasino M. Skin hyperproliferation and susceptibility to chemical carcinogenesis in transgenic mice expressing E6 and E7 of human papillomavirus type 38. J. Virol. 2005, 79(23):14899-14908.
16. Gabet A.S., Accardi R., Bellopede A., Popp S., Boukamp P., Sylla B.S., Londoño-Vallejo J.A., Tommasino M. Impairment of the telomere/telomerase system and genomic instability are associated with keratinocyte immortalization induced by the skin human papillomavirus type 38. FASEB J. 2008, 22(2):622-632.
17. Ghiotto F., Fais F., Bruno S. BH3-only proteins: the death-puppeteer[U+05F3]s wires. Cytometry A 2010, 77(1):11-21.
18. 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(11):2203-2209.
19. Hawley-Nelson P., Vousden K.H., Hubbert N.L., Lowy D.R., Schiller J.T. HPV16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO J. 1989, 8(12):3905-3910.
20. Howie H.L., Katzenellenbogen R.A., Galloway D.A. Papillomavirus E6 proteins. Virology 2009, 384(2):324-334.
21. Howie H.L., Koop J.I., Weese J., Robinson K., Wipf G., Kim L., Galloway D.A. Beta-HPV 5 and 8 E6 promote p300 degradation by blocking AKT/p300 association. PLoS Pathog. 2011, 7(8):e1002211.
22. Hudson J.B., Bedell M.A., McCance D.J., Laiminis L.A. Immortalization and altered differentiation of human keratinocytes in vitro by the E6 and E7 open reading frames of human papillomavirus type 18. J. Virol. 1990, 64(2):519-526.
23. Hufbauer M., Biddle A., Borgogna C., Gariglio M., Doorbar J., Storey A., Pfister H., Mackenzie I., Akgül B. Expression of betapapillomavirus oncogenes increases the number of keratinocytes with stem cell-like properties. J. Virol. 2013, 87(22):12158-12165.
24. Hussain I., Fathallah I., Accardi R., Yue J., Saidj D., Shukla R., Hasan U., Gheit T., Niu Y., Tommasino M., Sylla B.S. NF-kappaB protects human papillomavirus type 38 E6/E7-immortalized human keratinocytes against tumor necrosis factor alpha and UV-mediated apoptosis. J. Virol. 2011, 85(17):9013-9022.
25. 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(23):3065-3073.
26. Jackson S., Storey A. E6 proteins from diverse cutaneous HPV types inhibit apoptosis in response to UV damage. Oncogene 2000, 19(4):592-598.
27. Jha S., Vande Pol S., Banerjee N.S., Dutta A.B., Chow L.T., Dutta A. Destabilization of TIP60 by human papillomavirus E6 results in attenuation of TIP60-dependent transcriptional regulation and apoptotic pathway. Mol. Cell 2010, 38(5):700-711.
28. Klingelhutz A.J., Roman A. Cellular transformation by human papillomaviruses: lessons learned by comparing high- and low-risk viruses. Virology 2012, 424(2):77-98.
29. Lippens S., Hoste E., Vandenabeele P., Agostinis P., Declercq W. Cell death in the skin. Apoptosis 2009, 14(4):549-569.
30. Massimi P., Thomas M., Bouvard V., Ruberto I., Campo M.S., Tommasino M., Banks L. Comparative transforming potential of different human papillomaviruses associated with non-melanoma skin cancer. Virology 2008, 371(2):374-379.
31. McLaughlin-Drubin M.E., Münger K. The human papillomavirus E7 oncoprotein. Virology 2009, 384(2):335-344.
32. Meek D.W., Anderson C.W. Posttranslational modification of p53: cooperative integrators of function. Cold Spring Harb. Perspect. Biol. 2009, 1(6):a000950.
33. Mendoza J.A., Jacob Y., Cassonnet P., Favre M. Human papillomavirus type 5 E6 oncoprotein represses the transforming growth factor beta signaling pathway by binding to SMAD3. J. Virol. 2006, 80(24):12420-12424.
34. Michel A., Kopp-Schneider A., Zentgraf H., Gruber A.D., Villier E.M. E6/E7 expression of human papillomavirus type 20 (HPV-20) and HPV-27 influences proliferation and differentiation of the skin in UV-irradiated SKH-hr1 transgenic mice. J. Virol. 2006, 80(22):11153-11164.
35. Milrot E., Jackman A., Kniazhanski T., Gonen P., Flescher E., Sherman L. Methyl jasmonate reduces the survival of cervical cancer cells and downregulates HPV E6 and E7, and survivin. Cancer Lett. 2012, 319(1):31-38.
36. Muench P., Probst S., Schuetz J., Leiprecht N., Busch M., Wesselborg S., Stubenrauch F., Iftner T. Cutaneous papillomavirus E6 proteins must interact with p300 and block p53-mediated apoptosis for cellular immortalization and tumorigenesis. Cancer Res. 2010, 70(17):6913-6924.
37. Muschik D., Braspenning-Wesch I., Stockfleth E., Rösl F., Hofmann T.G., Nindl I. Cutaneous HPV23 E6 prevents p53 phosphorylation through interaction with HIPK2. PLoS One 2011, 6(11):e27655.
38. Nindl I., Gottschling M., Stockfleth E. Human papillomaviruses and non-melanoma skin cancer: basic virology and clinical manifestations. Dis. Markers 2007, 23(4):247-259.
39. Orth G., Jablonska S., Jarzabek-Chorzelska M., Obalek S., Rzesa G., Favre M., Croissant O. Characteristics of the lesions and risk of malignant conversion associated with the type of human papillomavirus involved in epidermodysplasia verruciformis. Cancer Res. 1979, 39(3):1074-1082.
40. Pim D., Banks L. Interaction of viral oncoproteins with cellular target molecules: infection with high-risk vs low-risk human papillomaviruses. APMIS 2010, 118(6-7):471-493.
41. Schaper I.D., Marcuzzi G.P., Weissenborn S.J., Kasper H.U., Dries V., Smyth N., Fuchs P., Pfister H. Development of skin tumors in mice transgenic for early genes of human papillomavirus type 8. Cancer Res. 2005, 65(4):1394-1400.
42. Scheffner M., Werness B.A., Huibregtse J.M., Levine A.J., Howley P.M. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 1990, 63(6):1129-1136.
43. Schlegel R., Phelps W.C., Zhang Y.L., Barbosa M. Quantitative keratinocyte assay detects two biological activities of human papillomavirus DNA and identifies viral types associated with cervical carcinoma. EMBO J. 1988, 7(10):3181-3187.
44. Schmitt A., Harry J.B., Rapp B., Wettstein F.O., Iftner T. 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. 1994, 68(11):7051-7059.
45. Scholzen T., Gerdes J. The Ki-67 protein: from the known and the unknown. J. Cell. Physiol. 2000, 182(3):311-322.
46. Scorrano L., Korsmeyer S.J. Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem. Biophys. Res. Commun. 2003, 304(3):437-444.
47. Sherman L., Schlegel R. Serum- and calcium-induced differentiation of human keratinocytes is inhibited by the E6 oncoprotein of human papillomavirus type 16. J. Virol. 1996, 70(5):3269-3279.
48. Storey A., Thomas M., Kalita A., Harwood C., Gardiol D., Mantovani F., Breuer J., Leigh I.M., Matlashewski G., Banks L. Role of a p53 polymorphism in the development of human papillomavirus-associated cancer. Nature 1998, 393(6682):229-234.
49. Struijk L., van der Meijden E., Kazem S., ter Schegget J., de Gruijl F.R., Steenbergen R.D., Feltkamp M.C. Specific betapapillomaviruses associated with squamous cell carcinoma of the skin inhibit UVB-induced apoptosis of primary human keratinocytes. J. Gen. Virol. 2008, 89(Pt 9):2303-2314.
50. Tan M.J., White E.A., Sowa M.E., Harper J.W., Aster J.C., Howley P.M. Cutaneous β-human papillomavirus E6 proteins bind Mastermind-like coactivators and repress Notch signaling. Proc. Natl. Acad. Sci. USA 2012, 109:E1473-E1480.
51. Thomas M., Tomaic V., Pim D., Myers P.M., Tommasino M., Banks L. Interaction between E6AP and E6 proteins from alpha and beta HPV types. Virology 2013, 435:357-362.
52. Tommasino M. The human papillomavirus family and its role in carcinogenesis. Semin. Cancer Biol. 2014, 26C:13-21.
53. Underbrink M.P., Howie H.L., Bedard K.M., Koop J.I., Galloway D.A. E6 proteins from multiple human betapapillomavirus types degrade Bak and protect keratinocytes from apoptosis after UVB irradiation. J. Virol. 2008, 82(21):10408-10417.
54. Vande Pol S.B., Klingelhutz A.J. Papillomavirus E6 oncoproteins. Virology 2013, 445(1-2):115-137.
55. Wallace N.A., Robinson K., Howie H.L., Galloway D.A. HPV 5 and 8 E6 abrogate ATR activity resulting in increased persistence of UVB induced DNA damage. PLoS Pathog. 2012, 8(7):e1002807.
56. Westphal K., Akgül B., Storey A., Nindl I. Cutaneous human papillomavirus E7 type-specific effects on differentiation and proliferation of organotypic skin cultures. Cell Oncol. 2009, 31(3):213-226.
57. Yang Y.L., Li X.M. The IAP family: endogenous caspase inhibitors with multiple biological activities. Cell Res. 2000, 10(3):169-177.
58. Zahir A., Craig L., Rady P., Tyring S., Ehrlich A. Epidermodysplasia verruciformis associated with HPV 10. Dermatol Online J. 2013, 19(4):2.
59. Zehbe I., Richard C., DeCarlo A., Shai A., Lambert P.F., Lichtig H., Tommasino M., Sherman L. Human papillomavirus 16 E6 variants differ in their dysregulation of human keratinocyte differentiation and apoptosis. Virology 2009, 383(1):69-77.