Melanogenesis: A photoprotective response to DNA damage?

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 571, Issue 1-2 SPEC. ISS., 2005, Pages 121-132

  Agar, Nita ^a   Young, Antony R ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

DNA damage; Melanin; Photoprotection; Tanning

Indexed keywords

MELANIN; MONOPHENOL MONOOXYGENASE; PYRIMIDINE DERIVATIVE;

CANCER SUSCEPTIBILITY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; ERYTHEMA; GENE MUTATION; GENE REPLICATION; GENETIC TRANSCRIPTION; HUMAN; IMMUNE DEFICIENCY; MELANOCYTE; MELANOGENESIS; MITOSIS INHIBITION; NONHUMAN; PRIORITY JOURNAL; RADIATION ABSORPTION; RADIATION EXPOSURE; RADIATION INJURY; RADIATION PROTECTION; RADIOSENSITIVITY; REVIEW; SKIN CANCER; SKIN COLOR; SKIN PIGMENTATION; SUNBURN;

EID: 14644425437     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2004.11.016     Document Type: Review

References (91)

1. N. Kollias, R.M. Sayre, L. Zeise, and M.R. Chedekel Photoprotection by melanin J. Photochem. Photobiol. B 9 1991 135 160
2. M.A. Weinstock Epidemiology of melanoma Cancer Treat. Res. 65 1993 29 56
3. B.A. Gilchrest, and M.S. Eller DNA photodamage stimulates melanogenesis and other photoprotective responses J. Invest. Dermatol. Symp. Proc. 4 1999 35 40
4. J.M. Sheehan, N. Cragg, C.A. Chadwick, C.S. Potten, and A.R. Young Repeated ultraviolet exposure affords the same protection against DNA photodamage and erythema in human skin types II and IV but is associated with faster DNA repair in skin type IV J. Invest. Dermatol. 118 2002 825 829
5. D.A. Kelly, A.R. Young, J.M. McGregor, P.T. Seed, C.S. Potten, and S.L. Walker Sensitivity to sunburn is associated with susceptibility to ultraviolet radiation-induced suppression of cutaneous cell-mediated immunity J. Exp. Med. 191 2000 561 566
6. C.S. Sander, H. Chang, F. Hamm, P. Elsner, and J.J. Thiele Role of oxidative stress and the antioxidant network in cutaneous carcinogenesis Int. J. Dermatol. 43 2004 326 335
7. W.L. Morison What is the function of melanin? Arch. Dermatol. 121 1985 1160 1163
8. P.U. Giacomoni Open questions in photobiology III. Melanin and photoprotection J. Photochem. Photobiol. B 29 1995 87 89
9. H.Z. Hill, and G.J. Hill UVA, pheomelanin and the carcinogenesis of melanoma Pigment Cell Res. 13 Suppl. 8 2000 140 144
10. T.B. Fitzpatrick The validity and practicality of sun-reactive skin types I through VI Arch. Dermatol. 124 1988 869 871
11. C.T. Jansen Self-reported skin type and reactivity to UVB, UVA and PUVA irradiation Photodermatology 6 1989 234 236
12. F.H. Rampen, B.A. Fleuren, T.M. de Boo, and W.A. Lemmens Unreliability of self-reported burning tendency and tanning ability Arch. Dermatol. 124 1988 885 888
13. J.L. Ravanat, T. Douki, and J. Cadet Direct and indirect effects of UV radiation on DNA and its components J. Photochem. Photobiol. B 63 2001 88 102
14. K.H. Kraemer, M.M. Lee, and J. Scotto Xeroderma pigmentosum. Cutaneous, ocular, and neurologic abnormalities in 830 published cases Arch. Dermatol. 123 1987 241 250
15. Q. Wei, G.M. Matanoski, E.R. Farmer, M.A. Hedayati, and L. Grossman DNA repair and aging in basal cell carcinoma: a molecular epidemiology study Proc. Natl. Acad. Sci. U.S.A. 90 1993 1614 1618
16. S. Moriwaki, S. Ray, R.E. Tarone, K.H. Kraemer, and L. Grossman The effect of donor age on the processing of UV-damaged DNA by cultured human cells: reduced DNA repair capacity and increased DNA mutability Mutat. Res. 364 1996 117 123
17. T.R. Fears, and J. Scotto Estimating increases in skin cancer morbidity due to increases in ultraviolet radiation exposure Cancer Invest. 1 1983 119 126
18. A.A. Vink, and L. Roza Biological consequences of cyclobutane pyrimidine dimers J. Photochem. Photobiol. B 65 2001 101 104
19. D.E. Brash, J.A. Rudolph, J.A. Simon, A. Lin, G.J. McKenna, H.P. Baden, A.J. Halperin, and J. Ponten A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma Proc. Natl. Acad. Sci. U.S.A. 88 1991 10124 10128
20. A. Ziegler, D.J. Leffell, S. Kunala, H.W. Sharma, M. Gailani, J.A. Simon, A.J. Halperin, H.P. Baden, P.E. Shapiro, and A.E. Bale Mutation hotspots due to sunlight in the p53 gene of non-melanoma skin cancers Proc. Natl. Acad. Sci. U.S.A. 90 1993 4216 4220
21. S.E. Ullrich Photoimmune suppression and photocarcinogenesis Front. Biosci. 7 2002 d684 d703
22. C. Nishigori, D.B. Yarosh, C. Donawho, and ML. Kripke The immune system in ultraviolet carcinogenesis J. Invest. Dermatol. Symp. Proc. 1 1996 143 146
23. L.A. Applegate, R.D. Ley, J. Alcalay, and M.L. Kripke Identification of the molecular target for the suppression of contact hypersensitivity by ultraviolet radiation J. Exp. Med. 170 1989 1117 1131
24. D. Yarosh, J. Klein, A. O'Connor, J. Hawk, E. Rafal, and P. Wolf Effect of topically applied T4 endonuclease V in liposomes on skin cancer in xeroderma pigmentosum: a randomised study. Xeroderma Pigmentosum Study Group Lancet 357 2001 926 929
25. T.B. Fitzpatrick, and A.S. Breathnach The Epidermal Melanin Unit System Dermatol. Wochenschr. 147 1963 481 489
26. W. Montagna, and K. Carlisle The architecture of black and white facial skin J. Am. Acad. Dermatol. 24 1991 929 937
27. J. Duchon, J. Borovansky, and P. Hach Chemical composition of ten kinds of various melanosomes Pigment Cell 1 1973 165 170
28. R. Halaban, D.N. Hebert, and D.E. Fisher Biology of melanocytes I.M. Fredberg A.Z. Eisen K. Wolff K.F. Austen L.A. Goldsmith S.I. Katz Fitzpatrick's Dermatology in General Medicine 2003 McGraw Hill New York 127 148
29. P.S. Friedmann, and B.A. Gilchrest Ultraviolet radiation directly induces pigment production by cultured human melanocytes J. Cell Physiol. 133 1987 88 94
30. D.C. Chu, A.R. Haake, K. Holbrook, and C.A. Loomis The structure and development of skin I.M. Fredberg A.Z. Eisen K. Wolff K.F. Austen L.A. Goldsmith S.I. Katz Fitzpatrick's Dermatology in General Medicine 2003 McGraw Hill New York 58 88
31. C. Rosette, and M. Karin Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors Science 274 1996 1194 1197
32. D. Cohen, and V.A. DeLeo Ultraviolet radiation-induced phospholipase A2 activation occurs in mammalian cell membrane preparations Photochem. Photobiol. 57 1993 383 390
33. B. Gron, L. Iversen, V. Ziboh, and K. Kragballe Distribution of monohydroxy fatty acids in specific human epidermal phospholipids Exp. Dermatol. 2 1993 38 44
34. V.A. De Leo, H. Horlick, D. Hanson, M. Eisinger, and L.C. Harber Ultraviolet radiation induces changes in membrane metabolism of human keratinocytes in culture J. Invest. Dermatol. 83 1984 323 326
35. K. Punnonen, and S.H. Yuspa Ultraviolet light irradiation increases cellular diacylglycerol and induces translocation of diacylglycerol kinase in murine keratinocytes J. Invest. Dermatol. 99 1992 221 226
36. P.R. Gordon, and B.A. Gilchrest Human melanogenesis is stimulated by diacylglycerol J. Invest. Dermatol. 93 1989 700 702
37. A.E. Allan, M. Archambault, E. Messana, and B.A. Gilchrest Topically applied diacylglycerols increase pigmentation in guinea pig skin J. Invest. Dermatol. 105 1995 687 692
38. H.S. Raper The tyrosinase-tyrosine reaction. VI. Production from tyrosine of 5,6-dihydroxyindole and 5,6-dihydroxyindole-2-carboxylic acid-the precursors of melanin J. Biochem. 21 1927 89
39. S. Ito Reexamination of the structure of eumelanin Biochim. Biophys. Acta 883 1986 155 161
40. A.J. Thody, E.M. Higgins, K. Wakamatsu, S. Ito, S.A. Burchill, and J.M. Marks Pheomelanin as well as eumelanin is present in human epidermis J. Invest. Dermatol. 97 1991 340 344
41. N. Kollias, A. Baqer, and I. Sadiq Minimum erythema dose determination in individuals of skin types V and VI with diffuse reflectance spectroscopy Photodermatol. Photoimmunol. Photomed. 10 1994 249 254
42. I.A. Vitkin, J. Woolsey, B.C. Wilson, and R.R. Anderson Optical and thermal characterization of natural (Sepia officinalis) melanin Photochem. Photobiol. 59 1994 455 462
43. M.R. Chedekal Photophysics and photochemistry of melanin J. Norlunds R.E. Boissy V.J. Hearing R.A. King J.-P. Ortonne The Pigmentary System 1998 Oxford University Press Oxford 307 322
44. C. Irwin, A. Barnes, D. Veres, and K. Kaidbey An ultraviolet radiation action spectrum for immediate pigment darkening Photochem. Photobiol. 57 1993 504 507
45. C. Routaboul, A. Denis, and A. Vinche Immediate pigment darkening: description, kinetic and biological function Eur. J. Dermatol. 9 1999 95 99
46. C.F. Rosen, S.L. Jacques, M.E. Stuart, and R.W. Gange Immediate pigment darkening: visual and reflectance spectrophotometric analysis of action spectrum Photochem. Photobiol. 51 1990 583 588
47. R.M. Lavker, and K.H. Kaidbey Redistribution of melanosomal complexes within keratinocytes following UV-A irradiation: a possible mechanism for cutaneous darkening in man Arch. Dermatol. Res. 272 1982 215 228
48. M.S. Eller, and B.A. Gilchrest Tanning as part of the eukaryotic SOS response Pigment Cell Res. 13 Suppl. 8 2000 94 97
49. J.A. Parrish, K.F. Jaenicke, and R.R. Anderson Erythema and melanogenesis action spectra of normal human skin Photochem. Photobiol. 36 1982 187 191
50. N. Kollias, Y.H. Malallah, H. al Ajmi, A. Baqer, B.E. Johnson, and S. Gonzalez Erythema and melanogenesis action spectra in heavily pigmented individuals as compared to fair-skinned Caucasians Photodermatol. Photoimmunol. Photomed. 12 1996 183 188
51. S.E. Freeman, H. Hacham, R.W. Gange, D.J. Maytum, J.C. Sutherland, and B.M. Sutherland Wavelength dependence of pyrimidine dimer formation in DNA of human skin irradiated in situ with ultraviolet light Proc. Natl. Acad. Sci. U.S.A. 86 1989 5605 5609
52. A.R. Young, C.A. Chadwick, G.I. Harrison, O. Nikaido, J. Ramsden, and C.S. Potten The similarity of action spectra for thymine dimers in human epidermis and erythema suggests that DNA is the chromophore for erythema J. Invest. Dermatol. 111 1998 982 988
53. A.R. Young, C.S. Potten, O. Nikaido, P.G. Parsons, J. Boenders, J.M. Ramsden, and C.A. Chadwick Human melanocytes and keratinocytes exposed to UVB or UVA in vivo show comparable levels of thymine dimers J. Invest. Dermatol. 111 1998 936 940
54. M.S. Eller, M. Yaar, and B.A. Gilchrest DNA damage and melanogenesis Nature 372 1994 413 414
55. M.S. Eller, K. Ostrom, and B.A. Gilchrest DNA damage enhances melanogenesis Proc. Natl. Acad. Sci. U.S.A. 93 1996 1087 1092
56. R. Pedeux, N. Al Irani, C. Marteau, F. Pellicier, R. Branche, M. Ozturk, J. Franchi, and DoreF J.F. Thymidine dinucleotides induce S phase cell cycle arrest in addition to increased melanogenesis in human melanocytes J. Invest. Dermatol. 111 1998 472 477
57. I.M. Hadshiew, M.S. Eller, F.P. Gasparro, and B.A. Gilchrest Stimulataion of melanogenesis by DNA oligonucleotides: effect of size, sequence and 5′phosphorylation J. Dermatol. Sci. 25 2001 127 138
58. L. Grossman, P.R. Caron, S.J. Mazur, and E.Y. Oh Repair of DNA-containing pyrimidine dimers FASEB J. 2 1988 2696 2701
59. J. Ceccoli, N. Rosales, J. Tsimis, and D.B. Yarosh Encapsulation of the UV-DNA repair enzyme T4 endonuclease V in liposomes and delivery to human cells J. Invest. Dermatol. 93 1989 190 194
60. D. Yarosh, L.G. Alas, V. Yee, A. Oberyszyn, J.T. Kibitel, D. Mitchell, R. Rosenstein, A. Spinowitz, and M. Citron Pyrimidine dimer removal enhanced by DNA repair liposomes reduces the incidence of UV skin cancer in mice Cancer Res. 52 1992 4227 4231
61. D.B. Yarosh Topical application of liposomes J. Photochem. Photobiol. B 6 1990 445 449
62. B.A. Gilchrest, S. Zhai, M.S. Eller, D.B. Yarosh, and M. Yaar Treatment of human melanocytes and S91 melanoma cells with the DNA repair enzyme T4 endonuclease V enhances melanogenesis after ultraviolet irradiation J. Invest. Dermatol. 101 1993 666 672
63. A.W. Murray Creative blocks: cell-cycle checkpoints and feedback controls Nature 359 1992 599 604
64. M.S. Eller, T. Maeda, C. Magnoni, D. Atwal, and B.A. Gilchrest Enhancement of DNA repair in human skin cells by thymidine dinucleotides: evidence for a p53-mediated mammalian SOS response Proc. Natl. Acad. Sci. U.S.A. 94 1997 12627 12632
65. M.K. Khlgatian, I.M. Hadshiew, P. Asawanonda, M. Yaar, M.S. Eller, M. Fujita, D.A. Norris, and B.A. Gilchrest Tyrosinase gene expression is regulated by p53 J. Invest. Dermatol. 118 2002 126 132
66. M.S. Eller, G.Z. Li, R. Firoozabadi, N. Puri, and B.A. Gilchrest Induction of a p95/Nbs1-mediated S phase checkpoint by telomere 3′ overhang specific DNA FASEB J. 17 2003 152 162
67. J. Courcelle, and P.C. Hanawalt RecA-dependent recovery of DNA repolication forks Annu. Rev. Genet. 37 2003 611 646
68. D.J. Crowley, and P.C. Hanawalt Induction of the SOS response increases the efficiency of global nucleotide excision repair of cyclobutane pyrimidine dimers, but not 6-4 photoproducts, in UV-irradiated Escherichia coli J. Bacteriol. 180 1998 3345 3352
69. D.J. Cripps Natural and artificial photoprotection J. Invest. Dermatol. 77 1981 154 157
70. M. Gniadecka, H.C. Wulf, N.N. Mortensen, and T. Poulsen Photoprotection in vitiligo and normal skin. A quantitative assessment of the role of stratum corneum, viable epidermis and pigmentation Acta Derm. Venereol. 76 1996 429 432
71. J.M. Sheehan, C.S. Potten, and A.R. Young Tanning in human skin types II and III offers modest photoprotection against erythema Photochem. Photobiol. 68 1998 588 592
72. D. Barker, K. Dixon, E.E. Medrano, D. Smalara, S. Im, D. Mitchell, G. Babcock, and Z.A. Abdel-Malek Comparison of the responses of human melanocytes with different melanin contents to ultraviolet B irradiation Cancer Res. 55 1995 4041 4046
73. M. Vermeer, G.J. Schmieder, T. Yoshikawa, J.W. van den Berg, M.S. Metzman, J.R. Taylor, and J.W. Streilein Effects of ultraviolet B light on cutaneous immune responses of humans with deeply pigmented skin J. Invest. Dermatol. 97 1991 729 734
74. M.K. Selgrade, M.V. Smith, J. Oberhelman-Bragg, G.J. LeVee, H.S. Koren, and K.D. Cooper Dose response for UV-induced immune suppression in people of color: differences based on erythemal reactivity rather than skin pigmentation Photochem. Photobiol. 74 2001 88 95
75. T.H. Kim, A.M. Moddycliffe, D.B. Yarosh, M. Norval, M.L. Kripke, and S.E. Ullrich Viability of the antigen determines whether DNA or urocanic acid act as the initiator molecules for UV-induced suppression of delayed-type hypersensitivity Photochem. Photobiol. 78 2003 228 234
76. M.A. Weinstock, G.A. Colditz, W.C. Willett, M.J. Stampfer, B.R. Bronstein, M.C. Mihm Jr., and F.E. Speizer Melanoma and the sun: the effect of swimsuits and a "healthy" tan on the risk of non-familial malignant melanoma in women Am. J. Epidemiol. 134 1991 462 470
77. E.A. Holly, D.A. Aston, R.D. Cress, D.K. Ahn, and J.J. Kristiansen Cutaneous melanoma in women. I. Exposure to sunlight, ability to tan and other risk factors related to ultraviolet light Am. J. Epidemiol. 141 1995 923 933
78. E. Home On the black rete mucosum of the Negro being a defence against the scorching effect of the sun's rays Philos. Trans. R. Soc. Lond. [Biol.] 110 1820 1 7
79. J. Scotto, and F. Fraummeni Skin cancer (other than melanoma) D. Schottenfeld J.F. Fraummeni Cancer Epidemiology and Prevention 1982 Saunders Philadelphia pp. 996-1011
80. H.F. Blum Does the melanin pigment of human skin have adaptive value? An essay in human ecology and the evolution of race Q. Rev. Biol. 36 1961 50 63
81. A.N. Okoro Albinism in Nigeria. A clinical and social study Br. J. Dermatol. 92 1975 485 492
82. N.G. Jablonski, and G. Chaplin The evolution of human skin coloration J. Hum. Evol. 39 2000 57 106
83. C. Kipp, and A.R. Young The soluble eumelanin precursor 5,6-dihydroxyindole-2-carboxylic acid enhances oxidative damage in human keratinocyte DNA after UVA irradiation Photochem. Photobiol. 70 1999 191 198
84. E. Kvam, and R.M. Tyrrell The role of melanin in the induction of oxidative DNA base damage by ultraviolet A irradiation of DNA or melanoma cells J. Invest. Dermatol. 113 1999 209 213
85. E. Kvam, and J. Dahle Melanin synthesis may sensitize melanocytes to oxidative DNA damage by ultraviolet A radiation and protect melanocytes from direct DNA damage by ultraviolet B radiation Pigment Cell Res. 17 2004 549 550
86. W. Korytowski, B. Pilas, T. Sarna, and B. Kalyanaraman Photoinduced generation of hydrogen peroxide and hydroxyl radicals in melanins Photochem. Photobiol. 45 1987 185 190
87. I.A. Menon, S. Persad, N.S. Ranadive, and H.F. Haberman Effects of ultraviolet-visible irradiation in the presence of melanin isolated from human black or red hair upon Ehrlich ascites carcinoma cells Cancer Res. 43 1983 3165 3169
88. L. Marrot, J.P. Belaidi, J.R. Meunier, P. Perez, and C. Agapakis-Causse The human melanocyte as a particular target for UVA radiation and an endpoint for photoprotection assessment Photochem. Photobiol. 69 1999 686 693
89. K.C. Noz, M. Bauwens, P.P. van Buul, H. Vrolijk, A.A. Schothorst, S. Pavel, H.J. Tanke, and B.J. Vermeer Comet assay demonstrates a higher ultraviolet B sensitivity to DNA damage in dysplastic nevus cells than in common melanocytic nevus cells and foreskin melanocytes J. Invest. Dermatol. 106 1996 1198 1202
90. S. Takeuchi, W. Zhang, K. Wakamatsu, S. Ito, V.J. Hearing, K.H. Kraemer, and D.E. Brash Melanin acts as a potent UVB photosensitizer to cause an atypical mode of cell death in murine skin Proc. Natl. Acad. Sci. U.S.A. 101 2004 15076 15081
91. C.J. Streutker, D. McCready, K. Jimbow, and L. From Malignant melanoma in a patient with oculocutaneous albinism J. Cutan. Med. Surg. 4 2000 149 152