UV-radiation as a Risk Factor for Non-melanoma Skin Cancer. Genetic Determinants of Carcinogenesis

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Abstract

The review presents modern data on the role of ultraviolet (UV) radiation in the pathogenesis of non-melanoma skin cancer (NMSC), the problem of THE risk of developing NMSC, in particular, squamous cell and basal cell skin cancer both in the population and in long-term repeated irradiation of phototherapy (PUVA therapy, UVB therapy, UVB-311 therapy) in patients with psoriasis. The paper considers the mechanisms of UV-induced cell damage by different spectral ranges (UVA, UVB) including the formation of photoproducts, damage to genomic DNA and other cellular structures, violation of the regulation of signaling pathways, the development of chronic inflammation, secondary immunosuppression. The review summarizes the results of large epidemiological studies discussing the role of gene polymorphisms in the homologous DNA repair XRCC3, gene telomerase TERT-CLPTMI, cytokine IL10 gene, MTHFR gene, encoding the folate synthesis, genes involved in pigmentirovanie MC1R, EXOC2, UBAC2 in the modulation of risk of carcinogenic effect of UV radiation. According to the authors’ opinion, the most vital and significant is data on the role of vitamin D receptor (VDR) gene polymorphisms as possible predictors of the risk of NMSC development. The further prospects of academic research on the cumulative role of the genome and environmental factors in the risk assessment of NMSC are revealed.

About the authors

Marianna B. Zhilova

State Scientific Center of Dermatovenereology and Cosmetology

Author for correspondence.
Email: zhilova2@mail.ru
ORCID iD: 0000-0003-2545-2129

MD, PhD.

3 bld. 6 Korolenko street, 107076 Moscow.

Tel.: +7 (495) 785-20-47.

SPIN-код: 8930-4073

Россия

Maria M. Butareva

State Scientific Center of Dermatovenereology and Cosmetology

Email: butareva@cnikvi.ru
ORCID iD: 0000-0003-1521-1989

MD, PhD.

3 bld. 6 Korolenko street, 107076 Moscow.

SPIN-код: 8092-5896

Россия

References

  1. Archier E, Devaux S, Castela E, et al. Carcinogenic risks of psoralen UV-A therapy and narrowband UV-B therapy in chronic plaque psoriasis: a systematic literature review. J Eur Acad Dermatol Venereol. 2012;26 Suppl 3:22–31. doi: 10.1111/j.1468-3083.2012.04520.x.
  2. Stern RS, Lunder EJ. Risk of squamous cell carcinoma and methoxsalen (psoralen) and UV-A radiation (PUVA). A meta-analysis. Arch Dermatol. 1998;134(12):1582–1585. doi: 10.1001/archderm.134.12.1582.
  3. Patel RV, Clark LN, Lebwohl M, Weinberg JM. Treatments for psoriasis and the risk of malignancy. J Am Acad Dermatol. 2009;60(6):1001–1017. doi: 10.1016/j.jaad.2008.12.031.
  4. Feehan RP, Shantz LM. Molecular signaling cascades involved in nonmelanoma skin carcinogenesis. Biochem J. 2016;473(19):2973–2994. doi: 10.1042/BCJ20160471.
  5. Xiang F, Lucas R, Hales S, Neale R. Incidence of nonmelanoma skin cancer in relation to ambient UV radiation in white populations, 1978–2012: empirical relationships. JAMA Dermatol. 2014;150(10):1063–1071. doi: 10.1001/jamadermatol.2014.762.
  6. Armstrong BK, Kricker A. The epidemiology of UV induced skin cancer. J Photochem Photobiol B. 2001;63(1–3):8–18. doi: 10.1016/s1011-1344(01)00198-1.
  7. D’Orazio J, Jarrett S, Amaro-Ortiz A, Scott T. UV radiation and the skin. Int J Mol Sci. 2013;14(6):12222–12248. doi: 10.3390/ijms140612222.
  8. Reichrath J, Rass K. Ultraviolet damage, DNA repair and vitamin D in nonmelanoma skin cancer and in malignant melanoma: an update. Adv Exp Med Biol. 2014;810:208−233. doi: 10.1007/978-1-4939-0437-2_12.
  9. Katalinic A, Kunze U, Schäfer T. Epidemiology of cutaneous melanoma and non-melanoma skin cancer in Schleswig-Holstein, Germany: incidence, clinical subtypes, tumour stages and localization (epidemiology of skin cancer). Br J Dermatol. 2003;149(6):1200–1206. doi: 10.1111/j.1365-2133.2003.05554.x.
  10. Bichakjian CK, Olencki T, Aasi SZ, et al. Basal cell skin cancer version 1.2016: Clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2016;14(5):574−597. doi: 10.6004/jnccn.2016.0065.
  11. Каприн А.Д., Старинский В.В., Петрова Г.В. Злокачественные новообразования в России в 2015 году (заболеваемость и смертность). ― М.; 2017. ― 250 с.
  12. Wadhera A, Fazio M, Bricca G, Stanton O. Metastatic basal cell carcinoma: a case report and literature review. How accurate is our incidence data? Dermatol Online J. 2006;12(5):7.
  13. Leiter U, Garbe C. Epidemiology of melanoma and nonmelanoma skin cancer — the role of sunlight. Adv Exp Med Biol. 2008;624:89–103. doi: 10.1007/978-0-387-77574-6_8.
  14. Madan V, Lear JT, Szeimies RM. Non-melanoma skin cancer. Lancet. 2010;375(9715):673–685. doi: 10.1016/S0140-6736(09)61196-X.
  15. Christenson LJ, Borrowman TA, Vachon CM, et al. Incidence of basal cell and squamous cell carcinomas in a population younger than 40 years. JAMA. 2005;294(6):681–690. doi: 10.1001/jama.294.6.681.
  16. Bowden GT. Prevention of non-melanoma skin cancer by targeting ultraviolet-B-light signalling. Nat Rev Cancer. 2004;4(1):23–35. doi: 10.1038/nrc1253.
  17. Courdavault S, Baudouin C, Charveron M, et al. Repair of the three main types of bipyrimidine DNA photoproducts in human keratinocytes exposed to UVB and UVA radiations. DNA Repair (Amst). 2005;4(7):836–844. doi: 10.1016/j.dnarep.2005.05.001.
  18. Kim RH, Armstrong AW. Nonmelanoma skin cancer. Dermatol Clin. 2012;30(1):125–139. doi: 10.1016/j.det.2011.08.008.
  19. You YH, Lee DH, Yoon, JH, et al. Cyclobutane pyrimidine dimers are responsible for the vast majority of mutations induced by UVB irradiation in mammalian cells. J Biol Chem. 2001;276(48):44688–44694. doi: 10.1074/jbc.M107696200.
  20. Beani JC. [Ultraviolet A-induced DNA damage: role in skin cancer. (In French).] Bull Acad Natl Med. 2014;198(2):273−295.
  21. Banerjee G, Gupta N, Tiwari J, Raman G. Ultraviolet-induced transformation of keratinocytes: possible involvement of long interspersed element-1 reverse transcriptase. Photodermatol Photoimmunol Photomed. 2005;21(1):32–39. doi: 10.1111/j.1600-0781.2005.00136.x.
  22. Bowden NA, Ashton KA, Avery-Kiejda KA, et al. Nucleotide excision repair gene expression after Cisplatin treatment in melanoma. Cancer Res. 2010;70(20):7918–7926. doi: 10.1158/0008-5472.CAN-10-0161.
  23. Aragane Y, Kulms D, Metze D, et al. Ultraviolet light induces apoptosis via direct activation of CD95 (Fas/APO-1) independently of it’s ligand CD95L. J Cell Biol. 1998;140(1):171–182. doi: 10.1083/jcb.140.1.171.
  24. Brugarolas J, Chandrasekaran C, Gordon JI, et al. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature. 1995;377(6549):552–557. doi: 10.1038/377552a0.
  25. Kamijo Т, Weber J, Zambetti G, et al. Functional and physical interactions of the ARF tumor suppressor with p53 and Mdm2. Proc Natl Acad Sci U S A. 1998;95(14):8292–8297. doi: 10.1073/pnas.95.14.8292.
  26. Setlow RB. DNA repair, ageing, and cancer. Natl Cancer Inst Monogr. 1982;60:249–255.
  27. Sinha RP, Häder DP. UV-induced DNA damage and repair: a review. Photochem Photobiol Sci. 2002;1(4):225–236. doi: 10.1039/b201230h.
  28. Lane D. Cancer. p53, guardian of the genome. Nature. 1992;358(6381):15–16. doi: 10.1038/358015a0.
  29. Ziegler A, Jonason AS, Leffell DJ, et al. Sunburn and p53 in the onset of skin cancer. Nature. 1994;372(6508):773–776. doi: 10.1038/372773a0.
  30. Chaturvedi V, Qin JZ, Stennett L, et al. Resistance to UV induced apoptosis in human keratinocytes during accelerated senescence is associated with functional inactivation of p53. J Cell Physiol. 2004;198(1):100–109. doi: 10.1002/jcp.10392.
  31. Leffell DJ. The scientific basis of skin cancer. J Am Acad Dermatol. 2000;42(1 Pt 2):18–22. doi: 10.1067/mjd.2000.103340.
  32. Ibbotson SH, Bilsland D, Cox NH, et al. An update and guidance on narrowband ultraviolet B phototherapy: a British Photodermatology Group Workshop Report. Br J Dermatol. 2004;151(2):283–297. doi: 10.1111/j.1365-2133.2004.06128.x.
  33. Ramos J, Villa J, Ruiz A, et al. UV dose determines key characteristics of nonmelanoma skin cancer. Cancer Epidemiol Biomarkers Prev. 2004;13(12):2006–2011.
  34. Rünger TM. How different wavelengths of the ultraviolet spectrum contribute to skin carcinogenesis: the role of cellular damage responses. J Invest Dermatol. 2007;127(9):2103–2105. doi: 10.1038/sj.jid.5700988.
  35. Ananthaswamy HN, Pierceall WE. Molecular mechanisms of ultraviolet radiation carcinogenesis. Photochem Photobiol. 1990;52(6):1119–1136. doi: 10.1111/j.1751-1097.1990.tb08452.x.
  36. Nishisgori C. Current concept of photocarcinogenesis. Photochem Photobiol Sci. 2015;14(9):1713–1721. doi: 10.1039/c5pp00185d.
  37. Strozyk E, Kulms D. The role of AKT/mTOR pathway in stress response to UV-irradiation: implication in skin carcinogenesis by regulation of apoptosis, autophagy and senescence. Int J Mol Sci. 2013;14(8):15260–15285. doi: 10.3390/ijms140815260.
  38. Bruls WA, Slaper H, van der Leun JC, Berrens L. Transmission of human epidermis and stratum corneum as a function of thickness in the ultraviolet and visible wavelengths. Photochem Photobiol. 1984;40(4):485–494. doi: 10.1111/j.1751-1097.1984.tb04622.x.
  39. Shinozaki T, Nota A, Taya Y, Okamoto K. Functional role of Mdm2 phosphorylation by ATR in attenuation of p53 nuclear export. Oncogene. 2003;22(55):8870–8880. doi: 10.1038/sj.onc.1207176.
  40. Stokes MР, Rush J, Macneill J, et al. Profiling of UV-induced ATM/ATR signaling pathways. Proc Natl Acad Sci U S A. 2007;104(50):19855–19860. doi: 10.1073/pnas.0707579104.
  41. Kim C, Pasparakis M. Epidermal p65/NF-kB signalling is essential for skin carcinogenesis. EMBO Mol Med. 2014;6(7):970–983. doi: 10.15252/emmm.201303541.
  42. Leverkus M, Diessenbacher P, Geserick P. FLIP ing the coin? Death receptor-mediated signals during skin tumorigenesis. Exp Dermatol. 2008;17(7):614–622. doi: 10.1111/j.1600-0625.2008.00728.х.
  43. Gaffney DC, Soyer HP, Simpson F. The epidermal growth factor receptor in squamous cell carcinoma: an emerging drug target. Australas J Dermatol. 2014;55(1):24–34. doi: 10.1111/ajd.12025.
  44. Rodust PМ, Stockfleth E, Ulrich C, et al. UV-induced squamous cell carcinoma ― a role for antiapoptotic signalling pathways. Br J Dermatol. 2009;161 Suppl 3:107–115. doi: 10.1111/j.1365-2133.2009.09458.x.
  45. Coffer PJ, Burgering BM, Peppelenbosch MP, et al. UV activation of receptor tyrosine kinase activity. Oncogene. 1995;11(3):561–569.
  46. Einspahr JG, Calvert V, Alberts DS, et al. Functional protein pathway activation mapping of the progression of normal skin to squamous cell carcinoma. Cancer Prev Res (Phila). 2012;5(3):403–413. doi: 10.1158/1940-6207.
  47. Populo H, Lopes JM, Soares P. The mTOR signalling pathway in human cancer. Int J Mol Sci. 2012;13(2):1886–1918. doi: 10.3390/ijms13021886.
  48. Albanell J, Dalmases A, Rovira A, Rojo F. mTOR signalling in human cancer. Clin Transl Oncol. 2007;9(8):484–493. doi: 10.1007/s12094-007-0092-6.
  49. Marini KD, Payne BJ, Watkins DN, Martelotto LG. Mechanisms of Hedgehog signaling in cancer. Growth Factors. 2011;29(6):221−234. doi: 10.3109/08977194.2011.610756.
  50. Duarte I, Cunha J, Bedrikow RВ, Lazzarini R. What is the most common phototherapy prescription for psoriasis: NB-UVB or PUVA? Prescription behavior. An Bras Dermatol. 2009;84(3):244–248. doi: 10.1590/s0365-05962009000300005.
  51. Lapolla W, Yentzer BA, Bagel J, et al. A review of phototherapy protocols for psoriasis treatment. J Am Acad Dermatol. 2011;64(5):936–949. doi: 10.1016/j.jaad.2009.12.054.
  52. Spuls PI, Witkamp L, Bossuyt P, Bos JD. A systematic review of five systemic treatments for severe psoriasis. Br J Dermatol. 1997;137(6):943−949. doi: 10.1046/j.1365-2133.1997.19902071.x.
  53. Almutawa F, Alnomair N, Wang Y, et al. Systematic review of UV-based therapy for psoriasis. Am J Clin Dermatol. 2013;14(2):87−109. doi: 10.1007/s40257-013-0015-y.
  54. Racz E, Prens EР. Phototherapy and photochemotherapy for psoriasis. Dermatol Clin. 2015;33(1):79−89. doi: 10.1016/j.det.2014.09.007.
  55. Stern RS; PUVA Follow-Up Study. The risk of squamous cell and basal cell cancer associated with psoralen and ultraviolet A therapy: a 30-year prospective study. J Am Acad Dermatol. 2012;66(4):553–562. doi: 10.1016/j.jaad.2011.04.004.
  56. McKenna KE, Patterson CC, Handley J, et al. Cutaneous neoplasia following PUVA therapy for psoriasis. Br J Dermatol. 1996;134(4):639–642. doi: 10.1111/j.1365-2133.1996.tb06962.x.
  57. Abdullah AN, Keczkes. K. Cutaneous and ocular side-effects of PUVA photochemotherapy — a 10-year follow-up study. Clin Exp Dermatol. 1989;14(6):421–424. doi: 10.1111/j.1365-2230.1989.tb02602.x.
  58. Maier H, Schemper M, Ortel B, et al. Skin tumors in photochemotherapy for psoriasis: a single-center follow-up of 496 patients. Dermatology. 1996;193(3):185−191. doi: 10.1159/000246243.
  59. Osmancevic A, Gillstedt M, Wennberg AМ, Larkö O. The risk of skin cancer in psoriasis patients treated with UVB therapy. Acta Derm Venereol. 2014;94(4):425−430. doi: 10.2340/00015555-1753.
  60. Maiorino A, De Simone C, Perino F, et al. Melanoma and non-melanoma skin cancer in psoriatic patients treated with high-dose phototherapy. J Dermatolog Treat. 2016;27(5):443−447. doi: 10.3109/09546634.2015.1133882.
  61. Khalesi M, Whiteman DС, Doi SА, et al. Сutaneous markers of photodamage and risk of Basal cell carcinoma of the skin: a meta-analysis. Cancer Epidemiol Biomarkers Prev. 2013;22(9):1483−1489. doi: 10.1158/1055-9965.EPI-13-0424.
  62. Кипень В.Н., Мельнов С.Б., Смолякова Р.М. Роль генов XRCC1, XRCC3 и PALB2 в генезе спорадических форм рака молочной железы // Экологическая генетика. ― 2015. ― T.13. ―№4 ― C. 91−98.
  63. Chen X, Wang Z, Yan Y, et al. XRCC3 C18067T polymorphism contributes a decreased risk to both basal cell carcinoma and squamous cell carcinoma: evidence from a meta-analysis. PLoS One. 2014;9(1):e84195. doi: 10.1371/journal.pone.0084195.
  64. Nan H, Xu M, Kraft P, et al. Genome-wide association study identifies novel alleles associated with risk of cutaneous basal cell carcinoma and squamous cell carcinoma. Hum Mol Genet. 2011;20(18):3718–3724. doi: 10.1093/hmg/ddr287.
  65. Карпова Н.С, Абдулкадыров K.M., Селиванов E.A., Балашова В.A. Современные представления о роли теломер и теломеразы в патогенезе гематологических и онкологических заболеваний // Medline.ru. Российский биомедицинский журнал. ― 2012. ― Т.13. ― №1 ― С. 38−57.
  66. Yang X, Yang B, Li B, Liu Y. Association between TERT-CLPTM1L rs401681[C] allele and NMSC cancer risk: a meta-analysis including 45,184 subjects. Arch Dermatol Res. 2013;305(1):49−52. doi: 10.1007/s00403-012-1275-8.
  67. Welsh MM, Karagas MR, Kuriger JK, et al. Genetic determinants of UV-susceptibility in non-melanoma skin cancer. PLoS One. 2011;6(7):e20019. doi: 10.1371/journal.pone.0020019.
  68. Burns EM, Elmets CA, Yusuf N. Vitamin D and skin cancer. Photochem Photobiol. 2015;91(1):201–209. doi: 10.1111/php.12382.
  69. Holick MF, Chen TC, Lu Z, Sauter E. Vitamin D and skin physiology: a D-lightful story. J Bone Miner Res. 2007;22 Suppl 2:V28–33. doi: 10.1359/jbmr.07s211.
  70. Walters MR. Newly identified actions of the vitamin D endocrine system. Endocr Rev. 1992;13(4):719–764. doi: 10.1210/edrv-13-4-719.
  71. DeLuca HF. Overview of general physiologic features and functions of vitamin D. Am J Clin Nutr. 2004;80(6 Suppl):1689S–1696S. doi: 10.1093/ajcn/80.6.1689S.
  72. Haussler MR, Whitfield GK, Kaneko I, et al. Molecular mechanisms of vitamin D action. Calcif Tissue Int. 2013;92(2):77–98. doi: 10.1007/s00223-012-9619-0.
  73. Battault S, Whiting SJ, Peltier SL, et al. Vitamin D metabolism functions and needs: from science to health claims. Eur J Nutr. 2013;52(2):429–441. doi: 10.1007/s00394-012-0430-5.
  74. Zhao XZ, Yang BH, Yu GH, et al. Polymorphisms in the vitamin D receptor (VDR) genes and skin cancer risk in European population: a meta-analysis. Arch Dermatol Res. 2014;306(6):545−553. doi: 10.1007/s00403-014-1464-8.
  75. Raimondi S, Johansson H, Maisonneuve P, Gandini S. Review and meta-analysis on vitamin D receptor polymorphisms and cancer risk. Carcinogenesis. 2009;30(7):1170–1180. doi: 10.1093/carcin/bgp103.
  76. Raimondi S, Pasquali E, Gnagnarella P, et al. BsmI polymorphism of vitamin D receptor gene and cancer risk: a comprehensive meta-analysis. Mutat Res. 2014;769:17−34. doi: 10.1016/j.mrfmmm.2014.06.001.
  77. Köstner K, Denzer N, Koreng M, et al. Association of genetic variants of the vitamin D receptor (VDR) with cutaneous squamous cell carcinomas (SCC) and basal cell carcinomas (BCC): a pilot study in a German population. Anticancer Res. 2012;32(1):327−333.
  78. Von Schuckmann LA, Law MH, Montgomery GW, et al. Vitamin D pathway gene polymorphisms and keratinocyte cancers: a nested case-control study and meta-analysis. Anticancer Res. 2016;36(5):2145−2152.
  79. Lesiak A, Norval M, Wodz-Naskiewicz K, et al. An enhanced risk of basal cell carcinoma is associated with particular polymorphisms in the VDR and MTHFR genes. Exp Dermatol. 2011;20(10):800–804. doi: 10.1111/j.1600-0625.2011.01328.x.

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