HPV-associated skin disease

Journal of Pathology

Volumn 208, Issue 2, 2006, Pages 165-175

  Akgül, Baki ^a   Cooke, James C ^a   Storey, Alan ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Apoptosis; HPV; Non melanoma skin cancer; Stem cell; Transformation; UV

Indexed keywords

PROTEIN P53; RETINOBLASTOMA PROTEIN; VIRUS DNA;

APOPTOSIS; CANCER CELL; CANCER RISK; CARCINOGENESIS; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; DNA REPAIR; EPIDERMODYSPLASIA VERRUCIFORMIS; GENE LOCUS; GENETIC PREDISPOSITION; GENETIC SUSCEPTIBILITY; HETEROZYGOSITY LOSS; HISTOPATHOLOGY; HUMAN; IMMUNE DEFICIENCY; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; MOLECULAR MECHANICS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SKIN CANCER; ULTRAVIOLET RADIATION; VIRUS INFECTION; WART VIRUS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; CELL CYCLE; CELLS, CULTURED; DNA REPAIR; EPIDERMODYSPLASIA VERRUCIFORMIS; HUMANS; IMMUNE TOLERANCE; KERATINOCYTES; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; SKIN DISEASES, INFECTIOUS; SKIN NEOPLASMS; ULTRAVIOLET RAYS;

EID: 31144451594     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.1893     Document Type: Review

References (135)

1. de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H. Classification of papillomaviruses. Virology 2004; 324:17-27.
2. Dahle J, Kvam E, Stokke T. Bystander effects in UV-induced genomic instability: antioxidants inhibit delayed mutagenesis induced by ultraviolet A and B radiation. J Carcinog 2005;4:11.
3. Durham SE, Krishnan KJ, Betts J, Birch-Machin MA. Mitochondrial DNA damage in non-melanoma skin cancer. Br J Cancer 2003;88:90-95.
4. Sander CS, Hamm F, Elsner P, Thiele JJ. Oxidative stress in malignant melanoma and non-melanoma skin cancer. Br J Dermatol 2003;148:913-922.
5. Stern RS. The mysteries of geographic variability in non-melanoma skin cancer incidence. Arch Dermatol 1999:135: 843-844.
6. Jemal A, Clegg LX, Ward E, Ries LA, Wu X, Jamison PM, et al. Annual report to the nation on the status of cancer, 1975-2001, with a special feature regarding survival. Cancer 2004;101:3-27.
7. Goodwin RG, Holme SA, Roberts DL. Variations in registration of skin cancer in the United Kingdom. Clin Exp Dermatol 2004;29:328-330.
8. Munoz N. Human papillomavirus and cancer: the epidemiological evidence. J Clin Virol 2000;19:1-5.
9. Pfister H. Chapter 8: Human papillomavirus and skin cancer. J Natl Cancer Inst Monogr 2003;52-56.
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;125:93-97.
11. Lewandowsky F, Lutz W. Ein Fall einer bisher nicht beschriebenen Hauterkrankungn (Epidermodysplasia verruciformis). Arch Dermatol Syphilol 1922;141:193-203.
12. Orth G. Epidermodysplasia Verruciformis. Plenum Press: London, 1987.
13. Jablonska S, Majewski S. Epidermodysplasia verruciformis: immunological and clinical aspects. Curr Top Microbiol Immunol 1994;186:157-175.
14. Jablonska S, Dabrowski J, Jakubowicz K. Epidermodysplasia verruciformis as a model in studies on the role of papovaviruses in oncogenesis. Cancer Res 1972;32:583-589.
15. Tanigaki T, Kanda R, Yutsudo M, Hakura A. Epidemiologic aspects of epidermodysplasia verruciformis (L-L 1922) in Japan. Jpn J Cancer Res 1986;77:896-900.
16. Jablonska S. Epidermodysplasia Verruciformis. WB Saunders: Philadelphia, 1991.
17. Majewski S, Jablonska S. Epidermodysplasia verruciformis as a model of human papillomavirus-induced genetic cancer of the skin. Arch Dermatol 1995;131:1312-1318.
18. de Oliveira WR, Festa Neto C, Rady PL, Tyring SK. Clinical aspects of epidermodysplasia verruciformis. J Eur Acad Dermatol Venereol 2003;17:394-398.
19. Majewski S, Jablonska S. Do epidermodysplasia verruciformis human papillomaviruses contribute to malignant and benign epidermal proliferations? Arch Dermatol 2002;138:649-654.
20. Majewski S, Malejczyk J, Jablonska S, Misiewicz J, Rudnicka L, Obalek S, et al. Natural cell-mediated cytotoxicity against various target cells in patients with epidermodysplasia verruciformis. J Am Acad Dermatol 1990;22:423-427.
21. Cooper KD, Androphy EJ, Lowy D, Katz SI. Antigen presentation and T-cell activation in epidermodysplasia verruciformis. J Invest Dermatol 1990;94:769-776.
22. Ramoz N, Rueda LA, Bouadjar B, Favre M, Orth G. A susceptibility locus for epidermodysplasia verruciformis, an abnormal predisposition to infection with the oncogenic human papillomavirus type 5, maps to chromosome 17qter in a region containing a psoriasis locus. J Invest Dermatol 1999;112:259-263.
23. Ramoz N, Taieb A, Rueda LA, Montoya LS, Bouadjar B, Favre M, et al. Evidence for a nonallelic heterogeneity of epidermodysplasia verruciformis with two susceptibility loci mapped to chromosome regions 2p21-p24 and 17q25. J Invest Dermatol 2000;114:1148-1153.
24. Ramoz N, Rueda LA, Bouadjar B, Montoya LS, Orth G, Favre M. Mutations in two adjacent novel genes are associated with epidermodysplasia verruciformis. Nature Genet 2002;32:579-581.
25. Tate G, Suzuki T, Kishimoto K, Mitsuya T. Novel mutations of EVER1/TMC6 gene in a Japanese patient with epidermodysplasia verruciformis. J Hum Genet 2004;49:223-225.
26. Keresztes G, Mutai H, Heller S. TMC and EVER genes belong to a larger novel family, the TMC gene family encoding transmembrane proteins. BMC Genomics 2003;4:24.
27. Walder BK, Robertson MR, Jeremy D. Skin cancer and immunosuppression. Lancet 1971;2:1282-1283.
28. Boyle J, MacKie RM, Briggs JD, Junor BJ, Aitchison TC. Cancer, warts, and sunshine in renal transplant patients. A case-control study. Lancet 1984;1:702-705.
29. Stockfleth E, Ulrich C, Meyer T, Arndt R, Christophers E. Skin diseases following organ transplantation - risk factors and new therapeutic approaches. Transplant Proc 2001;33:1848-1853.
30. Berkhout RJ, Tieben LM, Smits HL, Bavinck JN, Vermeer BJ, ter Schegget J. Nested PCR approach for detection and typing of epidermodysplasia verruciformis-associated human papillomavirus types in cutaneous cancers from renal transplant recipients. J Clin Microbiol 1995;33:690-695.
31. Pfister H, Ter Schegget J. Role of HPV in cutaneous premalignant and malignant tumors. Clin Dermatol 1997;15:335-347.
32. Harwood CA, Surentheran T, McGregor JM, Spink PJ, Leigh IM, Breuer J, et al. Human papillomavirus infection and non-melanoma skin cancer in immunosuppressed and immunocompetent individuals. J Med Virol 2000;61:289-297.
33. Harwood CA, Proby CM. Human papillomaviruses and non-melanoma skin cancer. Curr Opin Infect Dis 2002;15:101-114.
34. Purdie KJ, Surentheran T, Sterling JC, Bell L, McGregor JM, Proby CM, et al. Human papillomavirus gene expression in cutaneous squamous cell carcinomas from immunosuppressed and immunocompetent individuals. J Invest Dermatol 2005;125: 98-107.
35. de Jong-Tieben LM, Berkhout RJ, Smits HL, Bouwes Bavinck JN, Vermeer BJ, van der Woude FJ, et al. High frequency of detection of epidermodysplasia verruciformis-associated human papillomavirus DNA in biopsies from malignant and premalignant skin lesions from renal transplant recipients. J Invest Dermatol 1995;105:367-371.
36. de Villiers EM, Lavergne D, McLaren K, Benton EC. Prevailing papillomavirus types in non-melanoma carcinomas of the skin in renal allograft recipients. Int J Cancer 1997;73:356-361.
37. Berkhout RJ, Bouwes Bavinck JN, ter Schegget J. Persistence of human papillomavirus DNA in benign and (pre)malignant skin lesions from renal transplant recipients. J Clin Microbiol 2000;38:2087-2096.
38. Astori G, Lavergne D, Benton C, Hockmayr B, Egawa K, Garbe C, et al. Human papillomaviruses are commonly found in normal skin of immunocompetent hosts. J Invest Dermatol 1998;110:752-755.
39. Boxman IL, Russell A, Mulder LH, Bavinck JN, Schegget JT, Green A. Case-control study in a subtropical Australian population to assess the relation between non-melanoma skin cancer and epidermodysplasia verruciformis human papillomavirus DNA in plucked eyebrow hairs. The Nambour Skin Cancer Prevention Study Group. Int J Cancer 2000;86:118-121.
40. Antonsson A, Erfurt C, Hazard K, Holmgren V, Simon M, Kataoka A, et al. Prevalence and type spectrum of human papillomaviruses in healthy skin samples collected in three continents. J Gen Virol 2003;84:1881-1886.
41. Masini C, Fuchs PG, Gabrielli F, Stark S, Sera F, Ploner M, et al. Evidence for the association of human papillomavirus infection and cutaneous squamous cell carcinoma in immunocompetent individuals. Arch Dermatol 2003;139:890-894.
42. de Villiers EM. Human papillomavirus infections in skin cancers. Biomed Pharmacother 1998;52:26-33.
43. Wieland U, Ritzkowsky A, Stoltidis M, Weissenborn S, Stark S, Ploner M, et al. Communication: papillomavirus DNA in basal cell carcinomas of immunocompetent patients: an accidental association? J Invest Dermatol 2000;115:124-128.
44. Pfister H, Fuchs PG, Majewski S, Jablonska S, Pniewska I, Malejczyk M. High prevalence of epidermodysplasia verruciformis-associated human papillomavirus DNA in actinic keratoses of the immunocompetent population. Arch Dermatol Res 2003;295:273-279.
45. Lerma E, Matias-Guiu X, Lee SJ, Prat J. Squamous cell carcinoma of the vulva: study of ploidy, HPV, p53, and pRb. Int J Gynecol Pathol 1999;18:191-197.
46. von Knebel Doeberitz M. New markers for cervical dysplasia to visualise the genomic chaos created by aberrant oncogenic papillomavirus infections. Eur J Cancer 2002;38:2229-2242.
47. Rufforny I, Wilkinson EJ, Liu C, Zhu H, Buteral M, Massoll NA. Human papillomavirus infection and p16(INK4a) protein expression in vulvar intraepithelial neoplasia and invasive squamous cell carcinoma. J Low Genit Tract Dis 2005;9:108-113.
48. Nindl I, Meyer T, Schmook T, Ulrich C, Ridder R, Audring H, et al. Human papillomavirus and overexpression of P16INK4a in nonmelanoma skin cancer. Dermatol Surg 2004;30:409-414.
49. Moy RL, Eliezri YD, Nuovo GJ, Zitelli JA, Bennett RG, Silverstein S. Human papillomavirus type 16 DNA in periungual squamous cell carcinomas. J Am Med Assoc 1989;261:2669-2673.
50. Sato T, Morimoto A, Ishida Y, Matsuo I. Human papillomavirus associated with Bowen's disease of the finger. J Dermatol 2004;31:927-930.
51. Favre M, Orth G, Majewski S, Baloul S, Pura A, Jablonska S. Psoriasis: a possible reservoir for human papillomavirus type 5, the virus associated with skin carcinomas of epidermodysplasia verruciformis. J Invest Dermatol 1998;110:311-317.
52. Weissenborn SJ, Hopfl R, Weber F, Smola H, Pfister HJ, Fuchs PG. High prevalence of a variety of epidermodysplasia verruciformis-associated human papillomaviruses in psoriatic skin of patients treated or not treated with PUVA. J Invest Dermatol 1999;113:122-126.
53. Mahe E, Bodemer C, Descamps V, Mahe I, Crickx B, De Prost Y, et al. High frequency of detection of human papillomaviruses associated with epidermodysplasia verruciformis in children with psoriasis. Br J Dermatol 2003;149:819-825.
54. Prignano G, Ferraro C, Mussi A, Stivali F, Trento E, Bordignon V, et al. Prevalence of human papilloma virus type 5 DNA in lesional and non-lesional skin scales of Italian plaque-type psoriatic patients: association with disease severity. Clin Microbiol Infect 2005;11:47-51.
55. Wolf P, Seidl H, Back B, Binder B, Hofler G, Quehenberger F, et al. Increased prevalence of human papillomavirus in hairs plucked from patients with psoriasis treated with psoralen-UV-A. Arch Dermatol 2004;140:317-324.
56. Iftner T, Bierfelder S, Csapo Z, Pfister H. Involvement of human papillomavirus type 8 genes E6 and E7 in transformation and replication. J Virol 1988;62:3655-3661.
57. Kiyono T, Nagashima K, Ishibashi M. The primary structure of major viral RNA in a rat cell line transfected with type 47 human papillomavirus DNA and the transforming activity of its cDNA and E6 gene. Virology 1989;173:551-565.
58. Kiyono T, Hiraiwa A, Ishibashi M. Differences in transforming activity and coded amino acid sequence among E6 genes of several papillomaviruses associated with epidermodysplasia verruciformis. Virology 1992;186:628-639.
59. Hiraiwa A, Kiyono T, Segawa K, Utsumi KR, Ohashi M, Ishibashi M. Comparative study on E6 and E7 genes of some cutaneous and genital papillomaviruses of human origin for their ability to transform 3Y1 cells. Virology 1993;192:102-111.
60. Yamashita T, Segawa K, Fujinaga Y, Nishikawa T, Fujinaga K. Biological and biochemical activity of E7 genes of the cutaneous human papillomavirus type 5 and 8. Oncogene 1993;8: 2433-2441.
61. Schmitt A, Harry JB, Rapp B, Wettstein FO, 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;68:7051-7059.
62. Caldeira S, Zehbe I, Accardi R, Malanchi I, Dong W, Giarre M, et al. The E6 and E7 proteins of the cutaneous human papillomavirus type 38 display transforming properties. J Virol 2003;77:2195-2206.
63. Boxman IL, Mulder LH, Noya F, de Waard V, Gibbs S, Broker TR, et al. 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;117:1397-1404.
64. Akgül B, Garcia-Escudero R, Ghali L, Pfister HJ, Fuchs PG, Navsaria H, et al. The E7 protein of cutaneous human papillomavirus type 8 causes invasion of human keratinocytes into the dermis in organotypic cultures of skin. Cancer Res 2005;65:2216-2223.
65. Smola-Hess S, Pahne J, Mauch C, Zigrino P, Smola H, Pfister HJ. Expression of membrane type 1 matrix metalloproteinase in papillomavirus-positive cells: role of the human papillomavirus (HPV) 16 and HPV8 E7 gene products. J Gen Virol 2005;86:1291-1296.
66. Iftner T, Fuchs PG, Pfister H. Two independently transforming functions of human papillomavirus 8. Curr Top Microbiol Immunol 1989;144:167-173.
67. Fuchs PG, Horn S, Iftner T, May M, Stubenrauch F, Pfister H. Molecular Biology of Epidermodysplasia Verruciformis-Associated Human Papillomaviruses. Verlag Chemie: Weinheim, 1993.
68. Muller A, Ritzkowsky A, Steger G. Cooperative activation of human papillomavirus type 8 gene expression by the E2 protein and the cellular coactivator p300. J Virol 2002;76:11 042-11 053.
69. 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: 279-290.
70. Hadaschik D, Hinterkeuser K, Oldak M, Pfister HJ, Smola-Hess S. The papillomavirus E2 protein binds to and synergizes with C/EBP factors involved in keratinocyte differentiation. J Virol 2003;77:5253-5265.
71. Steger G, Schnabel C, Schmidt HM. The hinge region of the human papillomavirus type 8 E2 protein activates the human p21(WAF1/CIP1) promoter via interaction with Sp1. J Gen Virol 2002;83:503-510.
72. Oldak M, Smola H, Aumailley M, Rivero F, Pfister H, Smola-Hess S. The human papillomavirus type 8 E2 protein suppresses beta4-integrin expression in primary human keratinocytes. J Virol 2004;78:10 738-10 746.
73. Tinsley JM, Fisher C, Searle PF. Abnormalities of epidermal differentiation associated with expression of the human papillomavirus type 1 early region in transgenic mice. J Gen Virol 1992;73:1251-1260.
74. 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;65:1394-1400.
75. Akgül B, Pfefferle R, Marcuzzi GP, Zigrino P, Krieg T, Pfister H, et al. Expression of matrix metalloproteinases-2, -9, -13 and MT1-MMP in skin tumors of human papillomavirus type 8 transgenic mice. Exper Dermatol 2006;15:35-42.
76. Greenhalgh DA, Wang XJ, Rothnagel JA, Eckhardt JN, Quintanilla MI, Barber JL, et al. Transgenic mice expressing targeted HPV-18 E6 and E7 oncogenes in the epidermis develop verrucous lesions and spontaneous, rasHa-activated papillomas. Cell Growth Differ 1994;5:667-675.
77. Helfrich I, Chen M, Schmidt R, Furstenberger G, Kopp-Schneider A, Trick D, et al. Increased incidence of squamous cell carcinomas in Mastomys natalensis papillomavirus E6 transgenic mice during two-stage skin carcinogenesis. J Virol 2004;78:4797-4805.
78. Arbeit JM, Munger K, Howley PM, Hanahan D. Progressive squamous epithelial neoplasia in K14-human papillomavirus type 16 transgenic mice. J Virol 1994;68:4358-4368.
79. zur Hausen H. Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis. J Natl Cancer Inst 2000;92:690-698.
80. Munger K, Basile JR, Duensing S, Eichten A, Gonzalez SL, Grace M, et al. Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene 2001;20: 7888-7898.
81. Duensing S, Munger K. Centrosome abnormalities, genomic instability and carcinogenic progression. Biochim Biophys Acta 2001;1471:M81-M88.
82. Duensing S, Duensing A, Crum CP, Munger K. Human papillomavirus type 16 E7 oncoprotein-induced abnormal centrosome synthesis is an early event in the evolving malignant phenotype. Cancer Res 2001;61:2356-2360.
83. Southern SA, Lewis MH, Herrington CS. Induction of tetrasomy by human papillomavirus type 16 E7 protein is independent of pRb binding and disruption of differentiation. Br J Cancer 2004;90:1949-1954.
84. Munger K. The role of human papillomaviruses in human cancers. Front Biosci 2002;7:d641-d649.
85. Jackson S, Storey A. E6 proteins from diverse cutaneous HPV types inhibit apoptosis in response to UV damage. Oncogene 2000;19:592-598.
86. Storey A, Massimi P, Dawson K, Banks L. Conditional immortalization of primary cells by human papillomavirus type 18 E6 and EJ-ras defines an E6 activity in G0/G1 phase which can be substituted for mutations in p53. Oncogene 1995;11:653-661.
87. Fisher MS, Kripke ML. Systemic alteration induced in mice by ultraviolet light irradiation and its relationship to ultraviolet carcinogenesis. Proc Natl Acad Sci U S A 1977;74:1688-1692.
88. Pfeifer GP, You YH, Besaratinia A. Mutations induced by ultraviolet light. Mutat Res 2005;571:19-31.
89. Cleaver JE, Bootsma D. Xeroderma pigmentosum: biochemical and genetic characteristics. Annu Rev Genet 1975;9:19-38.
90. Pan H, Griep AE. Altered cell cycle regulation in the lens of HPV-16 E6 or E7 transgenic mice: implications for tumor suppressor gene function in development. Genes Dev 1994;8: 1285-1299.
91. Wahl GM, Carr AM. The evolution of diverse biological responses to DNA damage: insights from yeast and p53. Nature Cell Biol 2001;3:E277-E286.
92. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 1990;63:1129-1136.
93. Werness BA, Levine AJ, Howley PM. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 1990;248:76-79.
94. Elbel M, Carl S, Spaderna S, Iftner T. A comparative analysis of the interactions of the E6 proteins from cutaneous and genital papillomaviruses with p53 and E6AP in correlation to their transforming potential. Virology 1997;239:132-149.
95. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA Jr, Butel JS, et al. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 1992;356:215-221.
96. Ziegler A, Jonason AS, Leffell DJ, Simon JA, Sharma HW, Kimmelman J, et al. Sunburn and p53 in the onset of skin cancer. Nature 1994;372:773-776.
97. Li G, Ho VC, Berean K, Tron VA. Ultraviolet radiation induction of squamous cell carcinomas in p53 transgenic mice. Cancer Res 1995;55:2070-2074.
98. Li G, Tron V, Ho V. Induction of squamous cell carcinoma in p53-deficient mice after ultraviolet irradiation. J Invest Dermatol 1998;110:72-75.
99. Steger G, Pfister H. In vitro expressed HPV 8 E6 protein does not bind p53. Arch Virol 1992;125:355-360.
100. 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;14:3065-3073.
101. Giampieri S, Garcia-Escudero R, Green J, Storey A. Human papillomavirus type 77 E6 protein selectively inhibits p53-dependent transcription of proapoptotic genes following UV-B irradiation. Oncogene 2004;23:5864-5870.
102. Jonason AS, Kunala S, Price GJ, Restifo RJ, Spinelli HM, Persing JA, et al. Frequent clones of p53-mutated keratinocytes in normal human skin. Proc Natl Acad Sci U S A 1996;93: 14 025-14 029.
103. Ren ZP, Hedrum A, Ponten F, Nister M, Ahmadian A, Lundeberg J, et al. Human epidermal cancer and accompanying precursors have identical p53 mutations different from p53 mutations in adjacent areas of clonally expanded non-neoplastic keratinocytes. Oncogene 1996;12:765-773.
104. Malkin D, Li FP, Strong LC, Fraumeni JF Jr, Nelson CE, Kim DH, et al. Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms. Science 1990;250:1233-1238.
105. Brash DE, Zhang W, Grossman D, Takeuchi S. Colonization of adjacent stem cell compartments by mutant keratinocytes. Semin Cancer Biol 2005;15:97-102.
106. Storey A. Papillomaviruses: death-defying acts in skin cancer. Trends Mol Med 2002;8:417-421.
107. Erster S, Mihara M, Kim RH, Petrenko O, Moll UM. In vivo mitochondrial p53 translocation triggers a rapid first wave of cell death in response to DNA damage that can precede p53 target gene activation. Mol Cell Biol 2004;24:6728-6741.
108. Leu JI, Dumont P, Hafey M, Murphy ME, George DL. Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nature Cell Biol 2004;6:443-450.
109. Mitra RS, Wrone-Smith T, Simonian P, Foreman KE, Nunez G, Nickoloff BJ. Apoptosis in keratinocytes is not dependent on induction of differentiation. Lab Invest 1997;76:99-107.
110. Tomkova H, Fujimoto W, Arata J. Expression of bcl-2 antagonist bak in inflammatory and neoplastic skin diseases. Br J Dermatol 1997;137:703-708.
111. Thomas M, Banks L. Inhibition of Bak-induced apoptosis by HPV-18 E6. Oncogene 1998;17:2943-2954.
112. Thomas M, Banks L. Human papillomavirus (HPV) E6 interactions with Bak are conserved amongst E6 proteins from high and low risk HPV types. J Gen Virol 1999;80:1513-1517.
113. Jackson S, Ghali L, Harwood C, Storey A. Reduced apoptotic levels in squamous but not basal cell carcinomas correlate with detection of cutaneous human papillomavirus. Br J Cancer 2002;87:319-323.
114. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 2004;73:39-85.
115. 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: 2203-2209.
116. Iftner T, Elbel M, Schopp B, Hiller T, Loizou JI, Caldecott KW, et al. Interference of papillomavirus E6 protein with single-strand break repair by interaction with XRCC1. EMBO J 2002;21:4741-4748.
117. Struijk L, Bouwes Bavinck JN, Wanningen P, van der Meijden E, Westendorp RG, Ter Schegget J, et al. Presence of human papillomavirus DNA in plucked eyebrow hairs is associated with a history of cutaneous squamous cell carcinoma. J Invest Dermatol 2003;121:1531-1535.
118. Tsai RY. A molecular view of stem cell and cancer cell self-renewal. Int J Biochem Cell Biol 2004;36:684-694.
119. Lechler T, Fuchs E. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 2005;437: 275-280.
120. Benitah SA, Frye M, Glogauer M, Watt FM. Stem cell depletion through epidermal deletion of Rac1. Science 2005;309:933-935.
121. Quinn AG, Sikkink S, Rees JL. Delineation of two distinct deleted regions on chromosome 9 in human non-melanoma skin cancers. Genes Chromosomes Cancer 1994;11:222-225.
122. Quinn AG, Campbell C, Healy E, Rees JL. Chromosome 9 allele loss occurs in both basal and squamous cell carcinomas of the skin. J Invest Dermatol 1994;102:300-303.
123. Hahn H, Wicking C, Zaphiropoulous PG, Gailani MR, Shanley S, Chidambaram A, et al. Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell 1996;85:841-851.
124. Johnson RL, Rothman AL, Xie J, Goodrich LV, Bare JW, Bonifas JM, et al. Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science 1996;272:1668-1671.
125. Shanley SM, Dawkins H, Wainwright BJ, Wicking C, Heenan P, Eldon M, et al. Fine deletion mapping on the long arm of chromosome 9 in sporadic and familial basal cell carcinomas. Hum Mol Genet 1995;4:129-133.
126. Holmberg E, Rozell BL, Toftgard R. Differential allele loss on chromosome 9q22.3 in human non-melanoma skin cancer. Br J Cancer 1996;74:246-250.
127. Shen T, Park WS, Boni R, Saini N, Pham T, Lash AE, et al. Detection of loss of heterozygosity on chromosome 9q22.3 in microdissected sporadic basal cell carcinoma. Hum Pathol 1999;30:284-287.
128. Reifenberger J, Wolter M, Knobbe CB, Kohler B, Schonicke A, Scharwachter C, et al. Somatic mutations in the PTCH, SMOH, SUFUH and TP53 genes in sporadic basal cell carcinomas. Br J Dermatol 2005;152:43-51.
129. Daya-Grosjean L, Couve-Privat S. Sonic hedgehog signaling in basal cell carcinomas. Cancer Lett 2005;225:181-192.
130. Ping XL, Ratner D, Zhang H, Wu XL, Zhang MJ, Chen FF, et al. PTCH mutations in squamous cell carcinoma of the skin. J Invest Dermatol 2001;116:614-616.
131. Quinn AG, Sikkink S, Rees JL. Basal cell carcinomas and squamous cell carcinomas of human skin show distinct patterns of chromosome loss. Cancer Res 1994;54:4756-4759.
132. Brown VL, Harwood CA, Crook T, Cronin JG, Kelsell DP, Proby CM. p16INK4a and p14ARF tumor suppressor genes are commonly inactivated in cutaneous squamous cell carcinoma. J Invest Dermatol 2004;122:1284-1292.
133. Fischer A. Primary immunodeficiency diseases: an experimental model for molecular medicine. Lancet 2001;357:1863-1869.
134. Laffort C, Le Deist F, Favre M, Caillat-Zucman S, Radford-Weiss I, Debre M, et al. Severe cutaneous papillomavirus disease after haemopoietic stem-cell transplantation in patients with severe combined immune deficiency caused by common γc cytokine receptor subunit or JAK-3 deficiency. Lancet 2004;363:2051-2054.
135. Evan GI, Vousden KH. Proliferation, cell cycle and apoptosis in cancer. Nature 2001;411:342-348.