Melanocyte photobiology, ultraviolet radiation and melanoma

Giornale Italiano di Dermatologia e Venereologia

Volumn 145, Issue 5, 2010, Pages 603-611

  Seo, S J ^a,b   Fisher, D E ^b  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Melanocytes; Melanoma; Skin neoplasms; Skin pigmentation; Ultraviolet rays

Indexed keywords

MELANIN; PROTEIN P53;

ARTICLE; CARCINOGENESIS; CELL DEATH; DNA DAMAGE; GENE MUTATION; HUMAN; MELANOCYTE; MELANOMA; PHOTOBIOLOGY; SKIN CANCER; SKIN PIGMENTATION; ULTRAVIOLET RADIATION;

EID: 78650727965     PISSN: 03920488     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (100)

1. Rigel DS. Cutaneous ultraviolet exposure and its relationship to the development of skin cancer. J Am Acad Dermatol 2008; 58(5 Suppl 2): S 129-32.
2. Giles GG, Marks R, Foley P. Incidence of non-melanocytic skin cancer treated in Australia. Br Med J (Clin Res Ed) 1988; 296: 13-7. (Pubitemid 18025276)
3. Ravanat JL, Douki T, Cadet J. Direct and indirect effects of UV radiation on DNA and its components. J Photochem Photobiol B 2001; 63: 88-102. (Pubitemid 33040727)
4. Freeman SE, Hacham H, Gange RW, Maytum DJ, Sutherland JC, Sutherland BM. Wavelength dependence of pyrimidine dimer formation in DNA of human skin irradiated in situ with ultraviolet light. Proc Natl Acad Sci U S A 1989; 86: 5605-9.
5. Mitchell DL, Jen J, Cleaver JE. Relative induction of cyclobutane dimers and cytosine photohydrates in DNA irradiated in vitro and in vivo with ultraviolet-C and ultraviolet-B light. Photochem Photobiol 1991; 54: 741-6.
6. Lill PH. Latent period and antigenicity of murine tumors induced in C3H mice by short-wavelength ultraviolet radiation. J Invest Dermatol 1983; 81: 342-6.
7. Bruis 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: 485-94.
8. Parrish JA, Jaenicke KF, Anderson RR. Erythema and melanogenesis action spectra of normal human skin. Photochem Photobiol 1982; 36: 187-91.
9. de Gruijl FR. Action spectrum for photocarcinogenesis. Recent Results Cancer Res 1995; 139: 21-30.
10. Peak JG, Peak MJ. Comparison of initial yields of DNA-to-protein crosslinks and single-strand breaks induced in cultured human cells by far- and near-ultraviolet light, blue light and X-rays. Mutat Res 1991; 246: 187-91.
11. Gange RW, Rosen CF. UVA effects on mammalian skin and cells. Photochem Photobiol 1986; 43: 701-5.
12. Mouret S, Baudouin C, Charveron M, Favier A, Cadet J, Douki T. Cyclobutane pyrimidine dimers are predominant DNA lesions in whole human skin exposed to UVA radiation. Proc Natl Acad Sci U S A 2006; 103: 13765-70.
13. Mitchell DL, Nairn RS. The biology of the (6-4) photoproduct. Photochem Photobiol 1989; 49: 805-19.
14. Varghese AJ, Patrick MH. Cytosine derived heteroadduct formation in ultraviolet-irradiated DNA. Nature 1969; 223: 299-300.
15. Kraemer KH, Lee MM, Scotto J. Xeroderma pigmentosum. Cutaneous, ocular, and neurologic abnormalities in 830 published cases. Arch Dermatol. 1987; 123: 241-50.
16. Hauser JE, Kadekaro AL, Kavanagh RJ, Wakamatsu K, Terzieva S, Schwemberger S et al. Melanin content and MCIR function independently affect UVR-induced DNA damage in cultured human melanocytes. Pigment Cell Res 2006; 19: 303-14. (Pubitemid 44015593)
17. Tadokoro T, Kobayashi N, Zmudzka BZ, Ito S, Wakamatsu K, Yamaguchi Y et al. UV-induced DNA damage and melanin content in human skin differing in racial/ethnic origin. FASEB J 2003; 17: 1177-9.
18. Brash DE, Rudolph JA, Simon JA, Lin A, McKenna GJ, Baden HP et al. A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc Natl Acad Sci U S A 1991; 88: 10124-8.
19. Ziegler A, Leffell DJ, Kunala S, Sharma HW, Gailani M, Simon JA et al. Mutation hotspots due to sunlight in the p53 gene of nonmelanoma skin cancers. Proc Natl Acad Sci U S A 1993; 90: 4216-20. (Pubitemid 23134197)
20. Brash DE, Ziegler A, Jonason AS, Simon JA, Kunala S, Leffell DJ. Sunlight and sunburn in human skin cancer: p53, apoptosis, and tumor promotion. J Investig Dermatol Symp Proc 1996; 1: 136-42.
21. 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: 841-51.
22. 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.
23. Albino AP, Vidal MJ, McNutt NS, Shea CR, Prieto VG, Nanus DM et al. Mutation and expression of the p53 gene in human malignant melanoma. Melanoma Res 1994; 4: 35-45.
24. Lubbe J, Reichel M, Burg G, Kleihues P. Absence of p53 gene mutations in cutaneous melanoma. J Invest Dermatol 1994; 102: 819-21. (Pubitemid 24144269)
25. Snell RS, Bischitz PG. The melanocytes and melanin in human abdominal wall skin: a survey made at different ages in both sexes and during pregnancy. J Anat 1963; 97: 361-76.
26. Cotton J, Spandau DF. Ultraviolet B-radiation dose influences the induction of apoptosis and p53 in human keratinocytes. Radiat Res 1997; 147: 148-55. (Pubitemid 27061470)
27. Dallaglio K, Palazzo E, Marconi A, Dumas M, Truzzi F, Lotti R et al. Endogenous survivin modulates survival and proliferation in UVB-treated human keratinocytes. Exp Dermatol 2009; 18: 464-71.
28. Ouhtit A, Muller HK, Davis DW, Ullrich SE, McConkey D, Ananthaswamy HN. Temporal events in skin injury and the early adaptive responses in ultraviolet-irradiated mouse skin. Am J Pathol 2000; 156: 201-7. (Pubitemid 30644453)
29. 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: 773-6.
30. Naik E, Michalak EM, Villunger A, Adams JM, Strasser A. Ultraviolet radiation triggers apoptosis of fibroblasts and skin keratinocytes mainly via the BH3-only protein Noxa. J Cell Biol 2007; 176: 415-24. (Pubitemid 46257269)
31. Hill LL, Ouhtit A, Loughlin SM, Kripke ML, Ananthaswamy HN, Owen-Schaub LB. Fas ligand: a sensor for DNA damage critical in skin cancer etiology. Science 1999; 285: 898-900.
32. El-Abaseri TB, Putta S, Hansen LA. Ultraviolet irradiation induces keratinocyte proliferation and epidermal hyperplasia through the activation of the epidermal growth factor receptor. Carcinogenesis 2006; 27: 225-31.
33. Larsson P, Andersson E, Johansson U, Ollinger K, Rosdahl I. Ultraviolet A and B affect human melanocytes and keratinocytes differently. A study of oxidative alterations and apoptosis. Exp Dermatol 2005; 14: 117-23.
34. Friedmann PS, Gilchrest BA. Ultraviolet radiation directly induces pigment production by cultured human melanocytes. J Cell Physiol 1987; 133: 88-94.
35. Abdel-Malek Z, Swope V, Smalara D, Babcock G, Dawes S, Nordlund J. Analysis of the UV-induced melanogenesis and growth arrest of human melanocytes. Pigment Cell Res 1994; 7: 326-32.
36. Medrano EE, Im S, Yang F, Abdel-Malek ZA. Ultraviolet B light induces G1 arrest in human melanocytes by prolonged inhibition of retinoblastoma protein phosphorylation associated with longterm expression of the p21Waf-1/SDI-1/Cip-1 protein. Cancer Res 1995; 55: 4047-52.
37. Fayolle C, Pourchet J, de Fromentel CC, Puisieux A, Dore JF, Voeltzel T. Gadd45a activation protects melanoma cells from ultraviolet B-induced apoptosis. J Invest Dermatol 2008; 128: 196-202.
38. Song X, Mosby N, Yang J, Xu A, Abdel-Malek Z, Kadekaro AL. alpha-MSH activates immediate defense responses to UV-induced oxidative stress in human melanocytes. Pigment Cell Melanoma Res 2009; 22: 809-18.
39. Bohm M, Wolff I, Scholzen TE, Robinson SJ, Healy E, Luger TA et al. alpha-Melanocyte-stimulating hormone protects from ultraviolet radiation-induced apoptosis and DNA damage. J Biol Chem 2005; 280: 5795-802.
40. Kadekaro AL, Kavanagh R, Kanto H, Terzieva S, Hauser J, Kobayashi N et al. alpha-Melanocortin and endothelin-1 activate antiapoptotic pathways and reduce DNA damage in human melanocytes. Cancer Res 2005; 65: 4292-9.
41. Smith AG, Luk N, Newton RA, Roberts DW, Sturm RA, Muscat GE. Melanocortin-1 receptor signaling markedly induces the expression of the NR4A nuclear receptor subgroup in melanocyte cells. J Biol Chem 2008; 283: 12564-70.
42. Scott MC, Suzuki I, Abdel-Malek ZA. Regulation of the human melanocortin 1 receptor expression in epidermal melanocytes by paracrine and endocrine factors and by ultraviolet radiation. Pigment Cell Res 2002; 15: 433-9.
43. Bayerl C, Taake S, Moll I, Jung EG. Characterization of sunburn cells after exposure to ultraviolet light. Photodermatol Photoimmunol Photomed 1995; 11: 149-54.
44. Plettenberg A, Ballaun C, Pammer J, Mildner M, Strunk D, Weninger W et al. Human melanocytes and melanoma cells constitutively express the Bcl-2 proto-oncogene in situ and in cell culture. Am J Pathol 1995; 146: 651-9.
45. Yohn JJ, Lyons MB, Norris DA. Cultured human melanocytes from black and white donors have different sunlight and ultraviolet A radiation sensitivities. J Invest Dermatol 1992; 99: 454-9.
46. Hornyak TJ, Jiang S, Guzman EA, Scissors BN, Tuchinda C, He H et al. Mitf dosage as a primary determinant of melanocyte survival after ultraviolet irradiation. Pigment Cell Melanoma Res 2009; 22: 307-18.
47. McGill GG, Horstmann M, Widlund HR, Du J, Motyckova G, Nishimura EK et al. Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell 2002; 109: 707-18.
48. Waster PK, Ollinger KM. Redox-dependent translocation of p53 to mitochondria or nucleus in human melanocytes after UVA- and UVB-induced apoptosis. J Invest Dermatol 2009; 129: 1769-81.
49. Sato T, Kawada A. Uptake of tritiated thymidine by epidermal melanocytes of hairless mice during ultraviolet light radiation. J Invest Dermatol 1972; 58: 71-3.
50. Quevedo WC Jr, Szabo G, Virks J, Sinesi SJ. Melanocyte populations in UV-irradiated human skin. J Invest Dermatol 1965; 45: 295-8.
51. Jimbow K, Roth SI, Fitzpatrick TB, Szabo G. Mitotic activity in non-neoplastic melanocytes in vivo as determined by histochemical, autoradiographic, and electron microscope studies. J Cell Biol 1975; 66: 663-70.
52. Rosdahl IK, Szabo G. Mitotic activity of epidermal melanocytes in UV-irradiated mouse skin. J Invest Dermatol 1978; 70: 143-8. (Pubitemid 8305608)
53. Stierner U, Rosdahl I, Augustsson A, Kagedal B. UVB irradiation induces melanocyte increase in both exposed and shielded human skin. J Invest Dermatol 1989; 92: 561-4. (Pubitemid 19122109)
54. Kawaguchi Y, Mori N, Nakayama A. Kit(+) melanocytes seem to contribute to melanocyte proliferation after UV exposure as precursor cells. J Invest Dermatol 2001; 116: 920-5. (Pubitemid 32554379)
55. Mitra D, Fisher DE. Transcriptional regulation in melanoma. Hematol Oncol Clin North Am 2009; 23: 447-65, viii.
56. Ito S, Wakamatsu K. Quantitative analysis of eumelanin and pheomelanin in humans, mice, and other animals: a comparative review. Pigment Cell Res 2003; 16: 523-31. (Pubitemid 37093032)
57. Thody AJ, Higgins EM, Wakamatsu K, Ito S, Burchill SA, Marks JM. Pheomelanin as well as eumelanin is present in human epidermis. J Invest Dermatol 1991; 97: 340-4.
58. Staricco RJ, Pinkus H. Quantitative and qualitative data on the pigment cells of adult human epidermis. J Invest Dermatol 1957; 28: 33-45.
59. Valverde P, Healy E, Jackson I, Rees JL, Thody AJ. Variants of the melanocyte-stimulating hormone receptor gene are associated with red hair and fair skin in humans. Nat Genet 1995; 11: 328-30.
60. Bastiaens M, ter Huurne J, Gruis N, Bergman W, Westendorp R, Vermeer BJ et al. The melanocortin-1 -receptor gene is the major freckle gene. Hum Mol Genet. 2001; 10: 1701-8.
61. Alaluf S, Atkins D, Barrett K, Blount M, Carter N, Heath A. Ethnic variation in melanin content and composition in photoexposed and photoprotected human skin. Pigment Cell Res 2002; 15: 112-8. (Pubitemid 34536324)
62. Kollias N, Sayre RM, Zeise L, Chedekel MR. Photoprotection by melanin. J Photochem Photobiol B 1991; 9: 135-60.
63. Ranadive NS, Shirwadkar S, Persad S, Menon IA. Effects of melanin-induced free radicals on the isolated rat peritoneal mast cells. J Invest Dermatol 1986; 86: 303-7. (Pubitemid 16124167)
64. Kobayashi N, Nakagawa A, Muramatsu T, Yamashina Y, Shirai T, Hashimoto MW et al. Supranuclear melanin caps reduce ultraviolet induced DNA photoproducts in human epidermis. J Invest Dermatol 1998; 110: 806-10.
65. Bustamante J, Bredeston L, Malanga G, Mordoh J. Role of melanin as a scavenger of active oxygen species. Pigment Cell Res 1993; 6: 348-53.
66. Menon IA, Haberman HF. Mechanisms of action of melanins. Br J Dermatol 1977; 97: 109-12.
67. Menon IA, Persad S, Ranadive NS, Haberman HF. Effects of ultraviolet-visible irradiation in the presence of melanin isolated from human black or red hair upon Ehrlich ascites carcinoma cells. Cancer Res 1983; 43: 3165-9. (Pubitemid 13061566)
68. Smit NP, Vink AA, Kolb RM, Steenwinkel MJ, van den Berg PT, van Nieuwpoort F et al. Melanin offers protection against induction of cyclobutane pyrimidine dimers and 6-4 photoproducts by UVB in cultured human melanocytes. Photochem Photobiol 2001; 74: 424-30.
69. Maeda K, Hatao M. Involvement of photooxidation of melanogenic precursors in prolonged pigmentation induced by ultraviolet A. J Invest Dermatol 2004; 122: 503-9. (Pubitemid 38281076)
70. Routaboul C, Denis A, Vinche A. Immediate pigment darkening: description, kinetic and biological function. Eur J Dermatol 1999; 9: 95-9. (Pubitemid 29158975)
71. Virador VM, Muller J, Wu X, Abdel-Malek ZA, Yu ZX, Ferrans VJ et al. Influence of alpha-melanocyte-stimulating hormone and ultraviolet radiation on the transfer of melanosomes to keratinocytes. FASEB J 2002; 16: 105-7.
72. Rosen CF, Seki Y, Farinelli W, Stern RS, Fitzpatrick TB, Pathak MA et al. A comparison of the melanocyte response to narrow band UVA and UVB exposure in vivo. J Invest Dermatol 1987; 88: 774-9.
73. Eller MS, Yaar M, Gilchrest BA. DNA damage and melanogenesis. Nature 1994; 372: 413-4.
74. Eller MS, Ostrom K, Gilchrest BA. DNA damage enhances melanogenesis. Proc Natl Acad Sci U S A 1996; 93: 1087-92.
75. Cui R, Widlund HR, Feige E, Lin JY, Wilensky DL, Igras VE et al. Central role of p53 in the suntan response and pathologic hyperpigmentation. Cell 2007; 128: 853-64.
76. Chakraborty AK, Funasaka Y, Slominski A, Ermak G, Hwang J, Pawelek JM et al. Production and release of proopiomelanocortin (POMC) derived peptides by human melanocytes and keratinocytes in culture: regulation by ultraviolet B. Biochim Biophys Acta 1996; 1313: 130-8.
77. Schauer E, Trautinger F, Kock A, Schwarz A, Bhardwaj R, Simon M et al. Proopiomelanocortin-derived peptides are synthesized and released by human keratinocytes. J Clin Invest 1994; 93: 2258-62.
78. D'Orazio JA, Nobuhisa T, Cui R, Arya M, Spry M, Wakamatsu K et al. Topical drug rescue strategy and skin protection based on the role of Mclr in UV-induced tanning. Nature 2006; 443: 340-4.
79. Tadokoro T, Yamaguchi Y, Batzer J, Coelho SG, Zmudzka BZ, Miller SA et al. Mechanisms of skin tanning in different racial/ethnic groups in response to ultraviolet radiation. J Invest Dermatol 2005; 124: 1326-32.
80. Robbins LS, Nadeau JH, Johnson KR, Kelly MA, Roselli-Rehfuss L, Baack E et al. Pigmentation phenotypes of variant extension locus alleles result from point mutations that alter MSH receptor function. Cell 1993; 72: 827-34.
81. Krude H, Biebermann H, Luck W, Horn R, Brabant G, Gruters A. Severe early-onset obesity, adrenal insufficiency and red hair pigmentation caused by POMC mutations in humans. Nat Genet 1998; 19: 155-7.
82. Lu D, Willard D, Patel IR, Kadwell S, Overton L, Kost T et al. Agouti protein is an antagonist of the melanocyte-stimulating-hormone receptor. Nature 1994; 371: 799-802.
83. Suzuki I, Tada A, Ollmann MM, Barsh GS, Im S, Lamoreux ML et al. Agouti signaling protein inhibits melanogenesis and the response of human melanocytes to alpha-melanotropin. J Invest Dermatol 1997; 108: 838-42.
84. Moan J, Porojnicu AC, Dahlback A. Ultraviolet radiation and malignant melanoma. Adv Exp Med Biol 2008; 624: 104-16.
85. Setlow RB, Grist E, Thompson K, Woodhead AD. Wavelengths effective in induction of malignant melanoma. Proc Natl Acad Sci U S A 1993; 90: 6666-70.
86. Kusewitt DF, Applegate LA, Ley RD. Ultraviolet radiation-induced skin tumors in a South American opossum (Monodelphis domestica). Vet Pathol 1991; 28: 55-65.
87. Walter RB, Kazianis S. Xiphophorus interspecies hybrids as genetic models of induced neoplasia. ILAR J 2001; 42: 299-321.
88. Kelsall SR, Mintz B. Metastatic cutaneous melanoma promoted by ultraviolet radiation in mice with transgene-initiated low melanoma susceptibility. Cancer Res 1998; 58: 4061-5.
89. Strickland FM, Muller HK, Stephens LC, Bucana CD, Donawho CK, Sun Y et al. Induction of primary cutaneous melanomas in C3H mice by combined treatment with ultraviolet radiation, ethanol and aloe emodin. Photochem Photobiol 2000; 72: 407-14.
90. Atillasoy ES, Seykora JT, Soballe PW, Elenitsas R, Nesbit M, Elder DE et al. UVB induces atypical melanocyte lesions and melanoma in human skin. Am J Pathol 1998; 152: 1179-86.
91. Kaidbey KH, Agin PP, Sayre RM, Kligman AM. Photoprotection by melanin-a comparison of black and Caucasian skin. J Am Acad Dermatol 1979; 1: 249-60.
92. Dennis LK, Beane Freeman LE, VanBeek MJ. Sunscreen use and the risk for melanoma: a quantitative review. Ann Intern Med 2003; 139: 966-78.
93. Huncharek M, Kupelnick B. Use of topical sunscreens and the risk of malignant melanoma: a meta-analysis of 9067 patients from 11 case-control studies. Am J Public Health 2002; 92: 1173-7.
94. Levine JA, Sorace M, Spencer J, Siegel DM. The indoor UV tanning industry: a review of skin cancer risk, health benefit claims, and regulation. J Am Acad Dermatol 2005; 53: 1038-44.
95. The association of use of sunbeds with cutaneous malignant melanoma and other skin cancers: A systematic review. Int J Cancer 2007; 120: 1116-22.
96. Lazovich D, Vogel RI, Berwick M, Weinstock MA, Anderson KE, Warshaw EM. Indoor tanning and risk of melanoma: a case-control study in a highly exposed population. Cancer Epidemiol Biomarkers Prev 2010; 19: 1557-68.
97. Mosher CE, Danoff-Burg S. Addiction to indoor tanning: relation to anxiety, depression, and substance use. Arch Dermatol 2010; 146: 412-7.
98. Abdel-Malek ZA, Ruwe A, Kavanagh-Starner R, Kadekaro AL, Swope V, Haskell-Luevano C et al. alpha-MSH tripeptide analogs activate the melanocortin 1 receptor and reduce UV-induced DNA damage in human melanocytes. Pigment Cell Melanoma Res 2009; 22: 635-44.
99. Abdel-Malek ZA, Kadekaro AL, Kavanagh RJ, Todorovic A, Koikov LN, McNulty JC et al. Melanoma prevention strategy based on using tetrapeptide alpha-MSH analogs that protect human melanocytes from UV-induced DNA damage and cytotoxicity. FASEB J 2006; 20: 1561-3.
100. Arad S, Konnikov N, Goukassian DA, Gilchrest BA. T-oligos augment UV-induced protective responses in human skin. FASEB J 2006; 20: 1895-7.