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Mechanisms of and variables affecting UVR photoadaptation in human skin

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Abstract

Humans have been exposed to solar UV radiation since their appearance on Earth and evolution has enabled most individuals to adapt to this exposure, to some degree. UV radiation produces several deleterious effects in human skin and light-skinned individuals are at greatest risk for both acute and long-term negative effects such as DNA damage, sunburn, immune suppression and skin cancer. The benefits of photoadaptation, which leads to a decreased response after acclimatization, are that humans who have skin that is capable of photoadaptation can work and play in the sun with reduced fear of painful sunburn. However, the effects of photoadaptation on DNA damage and development of skin cancer are quite complex and less well-understood. In this article, we have reviewed the current state of knowledge of UVR photoadaptation in human skin. However, more studies are needed to explore the use of UVR photoadaptation to protect against critical endpoints, such as skin cancer.

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References

  1. F. R. de Gruijl, H. J. van Kranen and L. H. Mullenders, UV induced DNA damage, repair, mutations and oncogenic pathways in skin cancer, J. Photochem. Photobiol., B, 2001, 63(1-3), 19–27.

    Article  Google Scholar 

  2. A. Tewari, R. P. Sarkany and A. R. Young, UVA1 induces cyclobutane pyrimidine dimers but not 6-4 photoproducts in human skin in vivo, J. Invest. Dermatol., 2012, 132, 394–400.

    Article  CAS  PubMed  Google Scholar 

  3. J. Cadet and M. Ber, Effects of UV and visible light on DNAfinal base damage, Biol. Chem., 1997, 378(11), 1275–1286, Review.

    CAS  PubMed  Google Scholar 

  4. P. H. Hart and M. Norval, Ultraviolet radiation-induced immunosuppression and its relevance for skin carcinogenesis, Photochem. Photobiol. Sci., 2017, DOI: 10.1039/c7pp00312a [Epub ahead of print].

    Google Scholar 

  5. G. I. Harrison, A. R. Young and S. B. McMahon, Ultraviolet radiation-induced inflammation as a model for cutaneous hyperalgesia, J. Invest. Dermatol., 2004, 122, 183–189.

    Article  CAS  PubMed  Google Scholar 

  6. M. A. Pathak, K. Jimbow and J. A. Parrish, {etet al.}, Effect of UV-A, UV-B, and psoralen on in vivo human melanin pigmentation. Cellular and subcellular characterization on delayed tanning reaction induced by single or multiple exposures to UV-A, UV-B or UV-A plus 8-methoxypsoralen, in Pigment Cell, 1976, vol. 3, pp. 291–298.

    Google Scholar 

  7. H. Y. Park, M. Kosmadaki, M. Yaar and B. A. Gilchrest, Cellular mechanisms regulating human melanogenesis, Cell. Mol. Life Sci., 2009, 66, 1493–1506.

    Article  CAS  PubMed  Google Scholar 

  8. S. G. Jarrett, {etet al.}, The melanocortin signaling cAMP axis accelerates repair and reduces mutagenesis of platinum-induced DNA damage, Sci. Rep., 2017, 7(1), 11708.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. P. Valverde, {etet al.}, Variants of the melanocyte-stimulating hormone receptor gene are associated with red hair and fair skin in humans, Nat. Genet., 1995, 11(3), 328–330.

    Article  CAS  PubMed  Google Scholar 

  10. B. A. Gilchrest and M. S. Eller, DNA photodamage stimulates melanogenesis and other photoprotective responses, J. Invest. Dermatol. Symp. Proc., 1999, 4(1), 35–40.

    Article  CAS  Google Scholar 

  11. Review: K. Nylander, J. C. Bourdon, S. E. Bray, {etet al.}, Transcriptional activation of tyrosinase and TRP-1 by p53 links UV irradiation to the protective tanning response, J. Pathol., 2000, 190, 39–46.

    Article  CAS  PubMed  Google Scholar 

  12. N. K. Khlgatiam, I. N. Hadshiew, P. Asawanoda, {etet al.}, Tyrosinase gene expression is regulated by p53, J. Invest. Dermatol., 2002, 118, 126–130.

    Article  Google Scholar 

  13. N. Agar and A. R. Young, Melanogenesis: a protective response to DNA damage? Mutat. Res., 2005, 571(1-2), 121–132.

    Article  CAS  PubMed  Google Scholar 

  14. M. S. Eller and B. A. Gilchrest, Tanning as part of the eukaryotic SOS response, Pigm. Cell Res., 2000, 13(Suppl 8), 94–97.

    Article  Google Scholar 

  15. R. Cui, {etet al.}, Central role of p53 in the suntan response and pathologic hyperpigmentation, Cell., 2007, 128(5), 853–864.

    Article  CAS  PubMed  Google Scholar 

  16. B. A. Gilchrest, H. Y. Park, M. S. Eller and M. Yaar, Mechanisms of ultraviolet light-induced pigmentation, Photochem. Photobiol., 1996, 63(1), 1–10.

    Article  CAS  PubMed  Google Scholar 

  17. G. E. Costin and V. J. Hearing, Human skin pigmentation: melanocytes modulate skin color in response to stress, FASEB J., 2007, 21(4), 976–994.

    Article  CAS  PubMed  Google Scholar 

  18. N. L. Wicks, J. W. Chan, J. A. Najera, J. M. Ciriello and E. Oancea, UVA phototransduction drives early melanin synthesis in human melanocytes, Curr. Biol., 2011, 21(22), 1906–1911.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. L. R. Sklar, F. Almutawa, H. W. Lim and I. Hamzavi, Effects of ultraviolet radiation, visible light, and infrared on erythema and pigmentation, a review, Photochem. Photobiol. Sci., 2013, 12, 54–64.

    Article  CAS  PubMed  Google Scholar 

  20. C. Regazzetti, {etet al.}, Melanocytes sense blue light and regulate pigmentation through Opsin-e, J. Invest. Dermatol., 2018, 138(1), 171–178.

    Article  CAS  PubMed  Google Scholar 

  21. Y. Yamaguchi, M. Brenner and V. J. Hearing, The regulation of skin pigmentation, J. Biol. Chem., 2007, 282, 27557–27561.

    Article  CAS  PubMed  Google Scholar 

  22. K. S. Suh, H. J. Roh, S. Y. Choi, {etet al.} Long-term evaluation of erythema and pigmentation induced by ultraviolet radiations of different wavelengths, Skin Res. Technol., 2007, 13(2), 154–161.

    Article  PubMed  Google Scholar 

  23. S. G. Coelho, Y. Zhou, H. F. Bushar, {etet al.}, Long-lasting pigmentation of human skin, a new look at an overlooked response to UV, Pigm. Cell Melanoma Res., 2009, 22(2), 238–241.

    Article  Google Scholar 

  24. S. G. Coelho, J. C. Valencia, L. Yin, {etet al.}, UV exposure modulates hemidesmosome plasticity, contributing to long-term pigmentation in human skin, J. Pathol., 2015, 236(1), 17–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. J. H. Lee, J. H. Chung, {etet al.}, Acute effects of UVB irradiation on the proliferation and differentiation of keratinocytes, Photodermatol., Photoimmunol. Photomed., 2002, 18, 253–261.

    Article  CAS  Google Scholar 

  26. A. Cabral, A. Sayin, S. de Winter, {etet al.}, SPRR4, a novel cornified envelope precursor: UV-dependent epidermal expression and selective incorporation into fragile envelopes, J. Cell Sci., 2001, 114, 3837–3843.

    CAS  PubMed  Google Scholar 

  27. S. Nonaka, K. H. Kaidbey and A. M. Kligman, Photoprotective adaptation, Arch. Dermatol., 1984, 120, 609–612.

    Article  CAS  PubMed  Google Scholar 

  28. M. A. Everett, Protection from sunlight in vitiligo, Arch. Dermatol., 1961, 84, 997–998.

    Article  CAS  PubMed  Google Scholar 

  29. S. S. David, V. L. O’Shea and S. Kundu, Base-excision repair of oxidative DNA damage, Nature, 2007, 447, 941–950.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. W. L. De Laat, N. F. Jaspers and J. H. Hoeijmakers, Molecular mechanisms of nucleotide excsison repair, Genes Dev., 1999, 13(7), 768–785.

    Article  PubMed  Google Scholar 

  31. R. M. Costa, V. Chigancas, R. S. Galhardo, H. Carvalho and C. F. Menck, The eukaryotic nucleotide excsison repair pathway, Biochemie, 2003, 85(11), 1083–1010.

    Article  CAS  Google Scholar 

  32. A. R. Young, C. A. Chadwick, G. I. Harrison, {etet al.}, The in situ repair kinetics of epidermal thymine dimers and 6-4 photoproducts in human skin types I and II, J. Invest. Dermatol., 1996, 106, 1307–1313.

    Article  CAS  PubMed  Google Scholar 

  33. A. R. Young, G. E. Orchard, G. I. Harrison and J. L. Klock, The detrimental effects of daily sub-erythemal exposure on human skin in vivo can be prevented by a daily-care broad-spectrum sunscreen, J. Invest. Dermatol., 2006, 127(4), 975–978.

    Article  PubMed  CAS  Google Scholar 

  34. L. Verschooten, L. Declercq and M. Garmyn, Adaptive response of the skin to UVB damage: role of the p53 protein, Int. J Cosmet. Sci., 2006, 28(1), 1–7.

    Article  CAS  PubMed  Google Scholar 

  35. D. Decraene, K. Smaers, D. Maes, M. Matsui, L. Declercq and M. Garmyn, A low UVB dose with the potential to trigger a protective p53-dependent gene program, increases the resilience of keratinocytes against further UVB insults, J. Invest. Dermatol., 2005, 125(5), 1026–1031.

    Article  CAS  PubMed  Google Scholar 

  36. C. Meewes, A. Poswig, J. Dissemond, P. Brenneisen and K. Scharffetter-Kochanek, Adaptive antioxidant defence in human dermal fibroblasts, Br. J. Dermatol., 2000, 143, 662–663.

    Article  CAS  PubMed  Google Scholar 

  37. C. Meewes, P. Brenneisen, J. Wenk, L. Kuhr, W. Ma, J. Alikoski, A. Poswig, T. Krieg and K. Scharffetter-Kochanek, Adaptive antioxidant response protects dermal fibroblasts from UVA induced phototoxicity, Free Radicals Biol. Med., 2001, 30, 238–247.

    Article  CAS  Google Scholar 

  38. A. Poswig, J. Wenk, P. Brenneisen, {etet al.}, Adaptive antioxidant response of manganese-superoxide dismutase following repetitive UVA irradiation, J. Invest. Dermatol., 1999, 112, 13–18.

    Article  CAS  PubMed  Google Scholar 

  39. R. Kohen, Skin antioxidants: their role in aging and in oxidative stress- new approaches for their evaluation, Biomed. Pharmacother., 1999, 53(4), 181–192.

    Article  CAS  PubMed  Google Scholar 

  40. L. A. Schneider, J. Dissemond, P. Brenneisen, A. Hainzl, K. Briviba, M. Wlaschek and K. Scharffetter-Kochanek, Adaptive cellular protection against UVA-1-induced lipid peroxidation in human dermal fibroblasts shows donor-to-donor variability and is glutathione dependent, Arch. Dermatol. Res., 2006, 297, 324–328.

    Article  CAS  PubMed  Google Scholar 

  41. R. M. Tyrrell, Solar ultraviolet A radiation: an oxidizing skin carcinogen that activates heme oxygenase-1, Antioxid. Redox Signaling, 2004, 6(5), 835–840.

    CAS  Google Scholar 

  42. M. Schäfer and S. Werner, Nrf2-A regulator of keratinocyte redox signaling, Free Radicals Biol. Med., 2015, 88(Pt B), 243–252.

    Article  CAS  Google Scholar 

  43. P. De Haes, M. Garmyn, H. de Greef, K. Vantieghem, R. Bouillon and S. Segaert, 1,25-dihydroxyvitamin D3 and two low-calcemic analogues protect keratinocytes against UVB-induced damage, J. Photochem. Photobiol., B, 2005, 78(2), 141–148.

    Article  CAS  Google Scholar 

  44. R. Gupta, K. M. Dixon, S. S. Deo, C. J. Holliday, M. Slater, G. M. Halliday, V. E. Reeve and R. S. Mason, Photoprotection by 1,25 dihydroxyvitamin D3 is associated with an increase in p53 and a decrease in nitric oxide products, J. Invest. Dermatol., 2007, 127(3), 707–715.

    Article  CAS  PubMed  Google Scholar 

  45. C. Gordon-Thomson, R. Gupta, W. Tongkao-on, A. Ryan, G. M. Halliday and R. S. Mason, 1a,25 dihydroxyvitamin D3 enhances cellular defences against UV-induced oxidative and other forms of DNA damage in skin, Photochem. Photobiol. Sci., 2012, 11(12), 1837–1847.

    Article  CAS  PubMed  Google Scholar 

  46. E. J. Song, C. Gordon-Thomson, L. Cole, H. Stern, G. M. Halliday, D. L. Damian, V. E. Reeve and R. S. Mason, 1a,25-Dihydroxyvitamin D3 reduces several types of UV-induced DNA damage and contributes to Photoprotection, J. Steroid Biochem. Mol. Biol., 2013, 136, 131–138.

    Article  CAS  PubMed  Google Scholar 

  47. B. Krynitz, G. Edgren, B. Lindelof, {etet al.}, Risk of skin cancer and other malignances in kidney, liver, heart and lung transplant recipients 1970 to 2008 - A Swedish populationbased study, Int. J. Cancer, 2013, 132(6), 1429–1438.

    Article  CAS  PubMed  Google Scholar 

  48. N. R. Attard and P. Karran, UVA photosensitiziation of thiopurines and skin cancer in organ transplant recipients, Photochem. Photobiol. Sci., 2012, 11, 62–68.

    Article  CAS  PubMed  Google Scholar 

  49. M. Norval, P. McLoone, A. Lesiak and J. Narbutt, The effect of chronic ultraviolet radiation on the human immune system, Photochem. Photobiol., 2008, 84, 19–28.

    Article  CAS  PubMed  Google Scholar 

  50. G. Miescher, [Das problem des lichtschutzes und der licht-gewohnung], Strahlentherapie, 1930, 35, 403–443.

    Google Scholar 

  51. R. B. Rottier, [Studies with a small spectrograph for the determination of skin sensitivity to 300 and 250 millimicrons], Strahlentherapie, 1962, 119, 591–606.

    CAS  PubMed  Google Scholar 

  52. W. A. G. Bruls, H. Van Weelden and J. C. van der Leun, Transmission of UV-radiation through human epidermal layers as a factor influencing the minimal erythema dose, Photochem. Photobiol., 1984, 39, 63–67.

    Article  CAS  PubMed  Google Scholar 

  53. F. R. de Gruijl, UV adaptation: Pigmentation and protection against overexposure, Exp. Dermatol., 2017, 26(7), 557–562.

    Article  PubMed  CAS  Google Scholar 

  54. S. Darne, L. C. Stewart, P. M. Farr and P. J. Hampto, Investigation of cutaneous photoadaptation to narrowband ultraviolet B, Br. J. Dermatol., 2014, 170, 392–397.

    Article  CAS  PubMed  Google Scholar 

  55. S. Gonzalez, V. Hegyi, A. Baqer, I. Sadiq and N. Kollias, Development of cutaneous tolerance to ultraviolet B during ultraviolet B phototherapy for psoriasis, Photodermatol., Photoimmunol. Photomed., 1996, 12(2), 73–78.

    Article  CAS  Google Scholar 

  56. R. W. Gange, A. D. Blackett, E. A. Matzinger, B. M. Sutherland and I. E. Kochevar, Comparative protection efficiency of UVA- and UVB-induced tans against erythema and formation of endonuclease-sensitive sites in DNA by UVB in human skin, J. Invest. Dermatol., 1985, 85, 362.

    Article  CAS  PubMed  Google Scholar 

  57. R. M. Sayre, D. L. Desrochers, C. J. Wilson and E. Marlowe, Skin type, minimal erythema dose (MED), and sunlight acclimatization, J Am. Acad. Dermatol., 1981, 5, 439–443.

    Article  CAS  PubMed  Google Scholar 

  58. L. A. Applegate, C. Scaletta, G. Treina, R. E. Mascotto, A. Fourtanier and E. Frenk, Erythema induction by ultraviolet radiation points to a possible acquired defense mechanism in chronically sun-exposed human skin, Dermatology, 1997, 194(1), 41–49.

    Article  CAS  PubMed  Google Scholar 

  59. S. de Winter, A. A. Vink, L. Roza and S. Pavel, Solar-simulated skin adaptation and its effect on subsequent UV-induced epidermal DNA damage, J. Invest. Dermatol., 2001, 117, 68.

    Article  Google Scholar 

  60. J. M. Elwood, Melanoma and sun exposure: contrasts between intermittent and chronic exposure, World J. Surg., 1992, 16, 157–165.

    Article  CAS  PubMed  Google Scholar 

  61. K. Vuong, K. McGeechan, B. K. Armstrong, {etet al.}, Occupational sun exposure and risk of melanoma according to anatomical site, Int. J. Cancer, 2014, 134(11), 2735–2741.

    Article  CAS  PubMed  Google Scholar 

  62. A. Kricker, {etet al.}, Early life UV and risk of basal and squamous cell carcinoma in New South Wales, Australia, Photochem. Photobiol., 2017, 93(6), 1483–1491.

    Article  CAS  PubMed  Google Scholar 

  63. 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., 1998, 68, 588–592.

    Article  CAS  PubMed  Google Scholar 

  64. Y. Yamaguchi, S. G. Coelho, B. Z. Zmudzka, K. Takahashi, J. Z. Beer, V. J. Hearing and S. A. Miller, Cyclobutane pyrimidine dimer formation and p53 production in human skin after repeated UV irradiation, Exp. Dermatol., 2008, 17, 916–924.

    Article  CAS  PubMed  Google Scholar 

  65. S. A. Miller, S. G. Coelho, Y. Yamaguchi, V. Hearing, J. Z. Beer and F. R. De Gruijl, The evaluation of non-invasive measurements of erythema as a potential surrogate for DNA damage in repetitively UV-exposed human skin, Photochem. Photobiol., 2017, 93(5), 1282–1288.

    Article  CAS  PubMed  Google Scholar 

  66. S. A. Miller, S. G. Coelho, Y. Yamaguchi, J. Z. Beer, B. Z. Zmudzka, H. F. Bushar and V. Hearing, Dynamics of pigmentation induction by repeated UV exposures: dose, dose interval and UV spectrum dependence, Br. J. Dermatol., 2008, 159, 921–930.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. 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., 2002, 118, 825–829.

    Article  CAS  PubMed  Google Scholar 

  68. V. Bataille, V. J. Bykov, P. Sasieni, S. Harulow, J. Cuzick and K. Hemminki, Photoadaptation ultraviolet (UV) radiation in vivo: photoproducts in epidermal cells following UVB therapy for psoriasis, Br. J. Dermatol., 2000, 143(3), 477–483.

    Article  CAS  PubMed  Google Scholar 

  69. D. Fajuyigbe and A. R. Young, The impact of skin colour on human photobiological responses, Pigm. Cell Melanoma Res., 2016, 29(6), 607–618.

    Article  CAS  Google Scholar 

  70. D. Fajuyigbe, {etet al.}, Melanin distribution in human epidermis affords localized protection against DNA photodamage and concurs with skin cancer incidence difference in extreme phototypes, FASEB J., 2018, DOI: 10.1096/fj.201701472R [Epub ahead of print].

    Google Scholar 

  71. R. A. Palmer, A. Aquilina, P. J. Milligan, S. L. Walker, J. L. Hawk and A. R. Young, Photoadaptation during narrowband ultraviolet-B therapy is independent of skin type: a study of 352 patients, J. Invest. Dermatol., 2006, 126(6), 1256–1263.

    Article  CAS  PubMed  Google Scholar 

  72. Z. F. Jasim and K. E. McKenna, Treatment of psoriasis with ultraviolet B TL-01; response according to skin types, minimal erythema dose and total dose received, Br. J. Dermatol., 2005, 153(Suppl 1), 17, (Abstract).

    Google Scholar 

  73. A. R. Young, C. S. Potten, C. A. Chadwick, {etet al.}, Photoprotection and 5-MOP photochemoprotection from UVR-induced DNA damage in humans: the role of skin type, J. Invest. Dermatol., 1991, 97, 942–948.

    Article  CAS  PubMed  Google Scholar 

  74. K. Waterston, L. Naysmith and J. L. Rees, Physiological variation in the erythemal response to ultraviolet radiation and photoadaptation, J. Invest. Dermatol., 2004, 123(5), 958–964.

    Article  CAS  PubMed  Google Scholar 

  75. D. Goukassian, F. Gad, M. Yaar, {etet al.}, Mechanisms and implications of the age-associated decrease in DNA repair capacity, FASEB J., 2000, 14(10), 1325–1334.

    CAS  PubMed  Google Scholar 

  76. S. Moriwaki and Y. Takahashi, Photoaging and DNA repair, J. Dermatol. Sci., 2008, 50, 169–176.

    Article  CAS  PubMed  Google Scholar 

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We thank Dr Karl Lawrence for his assistance in creating the graphical abstract.

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Garmyn, M., Young, A.R. & Miller, S.A. Mechanisms of and variables affecting UVR photoadaptation in human skin. Photochem Photobiol Sci 17, 1932–1940 (2018). https://doi.org/10.1039/c7pp00430c

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