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Endogenous UVA-photosensitizers: mediators of skin photodamage and novel targets for skin photoprotection

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Abstract

Endogenous chromophores in human skin serve as photosensitizers involved in skin photocarcinogenesis and photoaging. Absorption of solar photons, particularly in the UVA region, induces the formation of photoexcited states of skin photosensitizers with subsequent generation of reactive oxygen species (ROS), organic free radicals and other toxic photoproducts that mediate skin photooxidative stress. The complexity of endogenous skin photosensitizers with regard to molecular structure, pathways of formation, mechanisms of action, and the diversity of relevant skin targets has hampered progress in this area of photobiology and most likely contributed to an underestimation of the importance of endogenous sensitizers in skin photodamage. Recently, UVA-fluorophores in extracellular matrix proteins formed posttranslationally as a consequence of enzymatic maturation or spontaneous chemical damage during chronological and actinic aging have been identified as an abundant source of light-driven ROS formation in skin upstream of photooxidative cellular stress. Importantly, sensitized skin cell photodamage by this bystander mechanism occurs after photoexcitation of sensitizers contained in skin structural proteins without direct cellular photon absorption thereby enhancing the potency and range of phototoxic UVA action in deeper layers of skin. The causative role of photoexcited states in skin photodamage suggests that direct molecular antagonism of photosensitization reactions using physical quenchers of photoexcited states offers a novel chemopreventive opportunity for skin photoprotection.

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References

  1. R. M. Tyrrell, Ultraviolet radiation and free radical damage to skin, Biochem. Soc. Symp., 1995, 61, 47–53.

    Article  CAS  PubMed  Google Scholar 

  2. E. Kvam, R. M. Tyrrell, Induction of oxidative DNA base damage in human skin cells by UV and near visible radiation, Carcinogenesis, 1997, 18, 2379–2384.

    Article  CAS  PubMed  Google Scholar 

  3. K. Scharffetter-Kochanek, M. Wlaschek, P. Brenneisen, M. Schauen, R. Blaudschun, J. Wenk, UV-induced reactive oxygen species in photocarcinogenesis and photoaging, Biol. Chem., 1997, 378, 11, 1247–1257.

    CAS  PubMed  Google Scholar 

  4. F. R. de Gruijl, Photocarcinogenesis: UVA vs UVB, Methods Enzymol., 2000, 319, 359–366.

    Article  PubMed  Google Scholar 

  5. N. S. Agar, G. M. Halliday, R. S. Barnetson, H. N. Ananthaswamy, M. Wheller, A. M. Jones, The basal layer in human squamous tumors harbors more UVA than UVB fingerprint mutations: A role for UVA in human skin carcinogenesis, PNAS, 2004, 101, 14, 4954–4959.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Carbonare M. Dalle, M. A. Pathak, Skin photosensitizing agents and the role of reactive oxygen species in photoaging, J. Photochem. Photobiol. B., 1992, 14, 1–2, 105–124.

    Google Scholar 

  7. G. T. Wondrak, M. J. Roberts, M. K. Jacobson, E. L. Jacobson, Photosensitized growth inhibition of cultured human skin cells: mechanism and suppression of oxidative stress from solar irradiation of glycated proteins, J. Invest. Dermatol., 2002, 119, 2, 489–498.

    Article  CAS  PubMed  Google Scholar 

  8. G. T. Wondrak, M. J. Roberts, D. Cervantes-Laurean, M. K. Jacobson, E. L. Jacobson, Proteins of the Extracellular Matrix Are Sensitizers of Photo-oxidative Stress in Human Skin Cells, J. Invest. Dermatol., 2003, 121, 3, 578–586.

    Article  CAS  PubMed  Google Scholar 

  9. K. H. Kaidbey, P. P. Agin, R. M. Sayre, A. M. Kligman, Photoprotection by melanin-a comparison of black and Caucasian skin, J. Am. Acad. Dermatol., 1979, 1, 3, 249–260.

    Article  CAS  PubMed  Google Scholar 

  10. W. A. Bruls, H. van Weelden, 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, 1, 63–67.

    Article  CAS  PubMed  Google Scholar 

  11. F. P. Gasparro, Sunscreens, skin photobiology, and skin cancer: the need for UVA protection and evaluation of efficacy, Environ. Health. Perspect., 2000, 108, Suppl 1, 71–78.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. H. J. Sterenborg, J. C. van der Leun, Tumorigenesis by a long wavelength UV-A source, Photochem. Photobiol., 1990, 51, 3, 325–330.

    Article  CAS  PubMed  Google Scholar 

  13. G. Kelfkens, F. R. de Gruijl, J. C. van der Leun, Tumorigenesis by short-wave ultraviolet A: papillomas versus squamous cell carcinomas, Carcinogenesis, 1991, 12, 8, 1377–1382.

    Article  CAS  PubMed  Google Scholar 

  14. A. de Laat, J. C. van der Leun, F. R. de Gruijl, Carcinogenesis induced by UVA (365-nm) radiation: the dose-time dependence of tumor formation in hairless mice, Carcinogenesis, 1997, 18, 5, 1013–1020.

    Article  PubMed  Google Scholar 

  15. G. Kelfkens, F. R. de Gruijl, J. C. van der Leun, Ozone depletion and increase in annual carcinogenic ultraviolet dose, Photochem. Photobiol., 1990, 52, 4, 819–823.

    Article  CAS  PubMed  Google Scholar 

  16. R. B. Setlow, E. Grist, K. Thompson, A. D. Woodhead, Wavelengths effective in induction of malignant melanoma, Proc. Natl. Acad. Sci. USA, 1993, 90, 14, 6666–6670.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. S. Q. Wang, R. Setlow, M. Berwick, D. Polsky, A. A. Marghoob, A. W. Kopf, R. S. Bart, Ultraviolet A and melanoma: a review, J. Am. Acad. Dermatol., 2001, 44, 5, 837–846.

    Article  CAS  PubMed  Google Scholar 

  18. J. Westerdahl, H. Olsson, A. Masback, C. Ingvar, N. Jonsson, L. Brandt, P. E. Jonsson, T. Moller, Use of sunbeds or sunlamps and malignant melanoma in southern Sweden, Am. J. Epidemiol., 1994, 140, 8, 691–699.

    Article  CAS  PubMed  Google Scholar 

  19. R. S. Stern, The risk of melanoma in association with long-term exposure to PUVA, J. Am. Acad. Dermatol., 2001, 44, 5, 755–761.

    Article  CAS  PubMed  Google Scholar 

  20. L. H. Kligman, F. J. Akin, A. M. Kligman, The contributions of UVA and UVB to connective tissue damage in hairless mice, J. Invest. Dermatol., 1985, 84, 4, 272–276.

    Article  CAS  PubMed  Google Scholar 

  21. R. Lavker, K. Kaidbey, The spectral dependence for UVA-induced cumulative damage in human skin, J. Invest. Dermatol., 1997, 108, 1, 17–21.

    Article  CAS  PubMed  Google Scholar 

  22. M. Wlaschek, I. Tantcheva-Poor, L. Naderi, W. Ma, L. A. Schneider, Z. Razi-Wolf, J. Schuller, K. Scharffetter-Kochanek, Solar UV. irradiation and dermal photoaging, J. Photochem. Photobiol. B., 2001, 63, 1–3, 41–51.

    Article  CAS  PubMed  Google Scholar 

  23. C. Nishigori, Y. Hattori, S. Toyokuni, Role of reactive oxygen species in skin carcinogenesis, Antioxid. Redox Signal., 2004, 6, 3, 561–570.

    Article  CAS  PubMed  Google Scholar 

  24. C. S. Sander, F. Hamm, P. Elsner, J. J. Thiele, Oxidative stress in malignant melanoma and non-melanoma skin cancer, Br. J. Dermatol., 2003, 148, 5, 913–922.

    Article  CAS  PubMed  Google Scholar 

  25. J. Nishi, R. Ogura, M. Sugiyama, T. Hidaka, M. Kohno, Involvement of active oxygen in lipid peroxide radical reaction of epidermal homogenate following ultraviolet light exposure, J. Invest. Dermatol., 1991, 97, 1, 115–119.

    Article  CAS  PubMed  Google Scholar 

  26. D. Peus, R. A. Vasa, A. Meves, M. Pott, A. Beyerle, K. Squillace, M. R. Pittelkow, H2O2 is an important mediator of UVB-induced EGF-receptor phosphorylation in cultured keratinocytes, J. Invest. Dermatol., 1998, 110, 6, 966–971.

    Article  CAS  PubMed  Google Scholar 

  27. H. Yasui, H. Sakurai, Chemiluminescent detection and imaging of reactive oxygen species in live mouse skin exposed to UVA, Biochem. Biophys. Res. Commun., 2000, 269, 1, 131–136.

    Article  CAS  PubMed  Google Scholar 

  28. S. Kang, J. H. Chung, J. H. Lee, G. J. Fisher, Y. S. Wan, E. A. Duell, J. J. Voorhees, Topical N-Acetyl Cysteine and Genistein Prevent Ultraviolet-Light-Induced Signaling That Leads to Photoaging in Human Skin in vivo, J. Invest. Dermatol., 2003, 120, 5, 835–841.

    Article  CAS  PubMed  Google Scholar 

  29. C. Routaboul, A. Denis, A. Vinche, Immediate pigment darkening: description, kinetic and biological function, Eur. J. Dermatol., 1999, 9, 2, 95–99.

    CAS  PubMed  Google Scholar 

  30. K. Maeda, M. Hatao, Involvement of photooxidation of melanogenic precursors in prolonged pigmentation induced by ultraviolet A, J. Invest. Dermatol., 2004, 122, 2, 503–509.

    Article  CAS  PubMed  Google Scholar 

  31. J. J. Thiele, C. Schroeter, S. N. Hsieh, M. Podda, L. Packer, The antioxidant network of the stratum corneum, Curr. Probl. Dermatol., 2001, 29, 26–42.

    Article  CAS  PubMed  Google Scholar 

  32. C. S. Sander, H. Chang, S. Salzmann, C. S. Muller, S. Ekanayake-Mudiyanselage, P. Elsner, J. J. Thiele, Photoaging is associated with protein oxidation in human skin in vivo, J. Invest. Dermatol., 2002, 118, 4, 618–625.

    Article  CAS  PubMed  Google Scholar 

  33. L. A. Applegate, C. Scaletta, R. Panizzon, E. Frenk, Evidence that ferritin is UV inducible in human skin: part of a putative defense mechanism, J. Invest. Dermatol., 1998, 111, 1, 159–163.

    Article  CAS  PubMed  Google Scholar 

  34. C. Meewes, P. Brenneisen, J. Wenk, L. Kuhr, W. Ma, J. Alikoski, A. Poswig, T. Krieg, K. Scharffetter-Kochanek, Adaptive antioxidant response protects dermal fibroblasts from UVA-induced phototoxicity, Free Radical Biol. Med., 2001, 30, 3, 238–247.

    Article  CAS  Google Scholar 

  35. M. T. Leccia, M. Yaar, N. Allen, M. Gleason, B. A. Gilchrest, Solar simulated irradiation modulates gene expression and activity of antioxidant enzymes in cultured human dermal fibroblasts, Exp. Dermatol., 2001, 10, 4, 272–279.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  37. L. Rittie, G. J. Fisher, UV-light-induced signal cascades and skin aging, Ageing. Res. Rev., 2002, 1, 4, 705–720.

    Article  CAS  PubMed  Google Scholar 

  38. S. Gross, A. Knebel, T. Tenev, A. Neininger, M. Gaestel, P. Herrlich, F. D. Bohmer, Inactivation of protein-tyrosine phosphatases as mechanism of UV-induced signal transduction, J. Biol. Chem., 1999, 274, 37, 26378–26386.

    Article  CAS  PubMed  Google Scholar 

  39. Y. S. Wan, Z. Q. Wang, J. Voorhees, G. Fisher, EGF receptor crosstalks with cytokine receptors leading to the activation of c-Jun kinase in response to UV irradiation in human keratinocytes, Cell. Signal., 2001, 13, 2, 139–144.

    Article  CAS  PubMed  Google Scholar 

  40. S. Grether-Beck, G. Bonizzi, H. Schmitt-Brenden, I. Felsner, A. Timmer, H. Sies, J. P. Johnson, J. Piette, J. Krutmann, Non-enzymatic triggering of the ceramide signalling cascade by solar UVA radiation, EMBO J., 2000, 19, 21, 5793–5800.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. M. Karin, Mitogen-activated protein kinase cascades as regulators of stress responses, Ann. N. Y. Acad. Sci., 1998, 851, 139–146.

    Article  CAS  PubMed  Google Scholar 

  42. L. O. Klotz, C. Pellieux, K. Briviba, C. Pierlot, J. M. Aubry, H. Sies, Mitogen-activated protein kinase (p38-, JNK-, ERK-) activation pattern induced by extracellular and intracellular singlet oxygen and UVA, Eur. J. Biochem., 1999, 260, 3, 917–922.

    Article  CAS  PubMed  Google Scholar 

  43. D. Peus, M. R. Pittelkow, Reactive oxygen species as mediators of UVB-induced mitogen-activated protein kinase activation in keratinocytes, Curr. Probl. Dermatol., 2001, 29, 114–127.

    Article  CAS  PubMed  Google Scholar 

  44. M. A. Bachelor, A. L. Silvers, G. T. Bowden, The role of p38 in UVA-induced cyclooxygenase-2 expression in the human keratinocyte cell line, HaCaT, Oncogene, 2002, 21, 46, 7092–7099.

    Article  CAS  PubMed  Google Scholar 

  45. G. F. Vile, A. Tanew-Ilitschew, R. M. Tyrrell, Activation of NF-kappa B. in human skin fibroblasts by the oxidative stress generated by UVA radiation, Photochem. Photobiol., 1995, 62, 3, 463–468.

    Article  CAS  PubMed  Google Scholar 

  46. S. Grether-Beck, S. Olaizola-Horn, H. Schmitt, M. Grewe, A. Jahnke, J. P. Johnson, K. Briviba, H. Sies, J. Krutmann, Activation of transcription factor AP-2 mediates UVA radiation- and singlet oxygen-induced expression of the human intercellular adhesion molecule 1 gene, Proc. Natl. Acad. Sci. USA, 1996, 93, 25, 14586–14591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. H. Nakano, F. P. Gasparro, J. Uitto, UVA-340 as energy source, mimicking natural sunlight, activates the transcription factor AP-1 in cultured fibroblasts: evidence for involvement of protein kinase-C, Photochem. Photobiol., 2001, 74, 2, 274–282.

    Article  CAS  PubMed  Google Scholar 

  48. L. O. Klotz, N. J. Holbrook, H. Sies, UVA and singlet oxygen as inducers of cutaneous signaling events, Curr. Probl. Dermatol., 2001, 29, 95–113.

    Article  CAS  PubMed  Google Scholar 

  49. M. S. Matsui, V. A. DeLeo, Longwave ultraviolet radiation and promotion of skin cancer, Cancer Cells, 1991, 3, 1, 8–12.

    CAS  PubMed  Google Scholar 

  50. T. Schwarz, Photoimmunosuppression, Photodermatol. Photoimmunol. Photomed., 2002, 18, 3, 141–145.

    Article  CAS  PubMed  Google Scholar 

  51. L. O. Klotz, K. D. Kroncke, H. Sies, Singlet oxygen-induced signaling effects in mammalian cells, Photochem. Photobiol. Sci., 2003, 2, 2, 88–94.

    Article  CAS  PubMed  Google Scholar 

  52. S. S. Brar, T. P. Kennedy, A. B. Sturrock, T. P. Huecksteadt, M. T. Quinn, T. M. Murphy, P. Chitano, J. R. Hoidal, NADPH oxidase promotes NF-kappaB activation and proliferation in human airway smooth muscle, Am. J. Physiol. Lung Cell. Mol. Physiol., 2002, 282, 4, L782–L795.

    Article  CAS  PubMed  Google Scholar 

  53. T. P. Szatrowski, C. F. Nathan, Production of large amounts of hydrogen peroxide by human tumor cells, Cancer Res., 1991, 51, 3, 794–798.

    CAS  PubMed  Google Scholar 

  54. R. Gniadecki, T. Thorn, J. Vicanova, A. Petersen, H. C. Wulf, Role of mitochondria in ultraviolet-induced oxidative stress, J. Cell. Biochem., 2000, 80, 2, 216–222.

    Article  CAS  PubMed  Google Scholar 

  55. R. Gniadecki, N. Christoffersen, H. C. Wulf, Cholesterol-rich plasma membrane domains (lipid rafts) in keratinocytes: importance in the baseline and UVA-induced generation of reactive oxygen species, J. Invest. Dermatol., 2002, 118, 4, 582–588.

    Article  CAS  PubMed  Google Scholar 

  56. C. S. Foote, Definition of type I and type II photosensitized oxidation, Photochem. Photobiol., 1991, 54, 5, 659.

    Article  CAS  PubMed  Google Scholar 

  57. J. Paczkowski, J. J. Lamberts, B. Paczkowska, D. C. Neckers, Photophysical properties of rose bengal and its derivatives (XII), J. Free Radical Biol. Med., 1985, 1, 5–6, 341–351.

    Article  CAS  Google Scholar 

  58. C. S. Foote, Mechanisms of photosensitized oxidation. There are several different types of photosensitized oxidation which may be important in biological systems, Science, 1968, 162, 857, 963–970.

    Article  CAS  PubMed  Google Scholar 

  59. F. Elisei, L. Latterini, G. G. Aloisi, U. Mazzucato, G. Viola, G. Miolo, D. Vedaldi, F. Dall℉Acqua, Excited-state properties and in vitro phototoxicity studies of three phenothiazine derivatives, Photochem. Photobiol., 2002, 75, 1, 11–21.

    Article  CAS  PubMed  Google Scholar 

  60. M. J. Davies, Reactive species formed on proteins exposed to singlet oxygen, Photochem. Photobiol. Sci., 2004, 3, 1, 17–25.

    Article  CAS  PubMed  Google Scholar 

  61. A. W. Girotti, Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms, J. Photochem. Photobiol. B., 2001, 63, 1-3, 103–113.

    Article  CAS  PubMed  Google Scholar 

  62. G. D. Ouedraogo, R. W. Redmond, Secondary reactive oxygen species extend the range of photosensitization effects in cells: DNA damage produced via initial membrane photosensitization, Photochem. Photobiol., 2003, 77, 2, 192–203.

    Article  CAS  PubMed  Google Scholar 

  63. M. J. Peak, J. G. Peak, B. A. Carnes, Induction of direct and indirect single-strand breaks in human cell DNA by far- and near-ultraviolet radiations: action spectrum and mechanisms, Photochem. Photobiol., 1987, 45, 3, 381–387.

    Article  CAS  PubMed  Google Scholar 

  64. C. Kielbassa, L. Roza, B. Epe, Wavelength dependence of oxidative DNA damage induced by UV and visible light, Carcinogenesis, 1997, 18, 4, 811–816.

    Article  CAS  PubMed  Google Scholar 

  65. D. E. Brash, J. A. Rudolph, J. A. Simon, A. Lin, G. J. McKenna, H. P. Baden, A. J. Halperin, J. Ponten, A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma, Proc. Natl. Acad. Sci. USA, 1991, 88, 22, 10124–10128.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. A. Ziegler, D. J. Leffell, S. Kunala, H. W. Sharma, M. Gailani, J. A. Simon, A. J. Halperin, H. P. Baden, P. E. Shapiro, A. E. Bale, et al., Mutation hotspots due to sunlight in the p53 gene of nonmelanoma skin cancers, Proc. Natl. Acad. Sci. USA, 1993, 90, 9, 4216–4220.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. J. Cadet, C. Anselmino, T. Douki, L. Voituriez, Photochemistry of nucleic acids in cells, J. Photochem. Photobiol. B., 1992, 15, 4, 277–298.

    Article  CAS  PubMed  Google Scholar 

  68. A. A. Lamola, J. P. Mittal, Solution photochemistry of thymine and uracil, Science, 1966, 154, 756, 1560–1561.

    Article  CAS  PubMed  Google Scholar 

  69. T. Delatour, T. Douki, C. D℉Ham, J. Cadet, Photosensitization of thymine nucleobase by benzophenone through energy transfer, hydrogen abstraction and one-electron oxidation, J. Photochem. Photobiol. B., 1998, 9, 105–116.

    Google Scholar 

  70. A. Moysan, A. Viari, P. Vigny, L. Voituriez, J. Cadet, E. Moustacchi, E. Sage, Formation of cyclobutane thymine dimers photosensitized by pyridopsoralens: quantitative and qualitative distribution within DNA, Biochemistry, 1991, 30, 29, 7080–7088.

    Article  CAS  PubMed  Google Scholar 

  71. T. Douki, A. Reynaud-Angelin, J. Cadet, E. Sage, Bipyrimidine photoproducts rather than oxidative lesions are the main type of DNA damage involved in the genotoxic effect of solar UVA radiation, Biochemistry, 2003, 42, 30, 9221–9226.

    Article  CAS  PubMed  Google Scholar 

  72. S. Courdavault, C. Baudouin, M. Charveron, A. Favier, J. Cadet, T. Douki, Larger yield of cyclobutane dimers than 8-oxo-7,8-dihydroguanine in the DNA of UVA-irradiated human skin cells, Mutat. Res., 2004, 556, 1–2, 135–142.

    Article  CAS  PubMed  Google Scholar 

  73. H. Kasai, Z. Yamaizumi, F. Yamamoto, T. Bessho, S. Nishimura, M. Berger, J. Cadet, Photosensitized formation of 8-hydroxyguanine (7,8-dihydro-8-oxoguanine) in DNA by riboflavin, Nucleic. Acids. Symp. Ser., 1992, 27, 181–182.

    CAS  Google Scholar 

  74. K. Ito, S. Kawanishi, Site-specific DNA. damage induced by UVA radiation in the presence of endogenous photosensitizer, Biol. Chem., 1997, 378, 11, 1307–1312.

    CAS  PubMed  Google Scholar 

  75. G. M. Halliday, N. S. Agar, R. S. Barnetson, H. N. Ananthaswamy, A. M. Jones, UV-A fingerprint mutations in human skin cancer, Photochem. Photobiol., 2005, 81, 1, 3–8.

    Article  CAS  PubMed  Google Scholar 

  76. M. Berneburg, S. Grether-Beck, V. Kurten, T. Ruzicka, K. Briviba, H. Sies, J. Krutmann, Singlet oxygen mediates the UVA-induced generation of the photoaging-associated mitochondrial common deletion, J. Biol. Chem., 1999, 274, 22, 15345–15349.

    Article  CAS  PubMed  Google Scholar 

  77. J. Moan, Q. Peng, An outline of the hundred-year history of PDT, Anticancer Res., 2003, 23, 5A, 3591–3600.

    PubMed  Google Scholar 

  78. L. Kaestner, A. Juzeniene, J. Moan, Erythrocytes-the ‘house elves’ of photodynamic therapy, Photochem. Photobiol. Sci., 2004, 3, 11–12, 981–989.

    Article  CAS  PubMed  Google Scholar 

  79. F. Ricchelli, Photophysical properties of porphyrins in biological membranes, J. Photochem. Photobiol. B, 1995, 29, 2–3, 109–118.

    Article  CAS  PubMed  Google Scholar 

  80. I. A. Menon, M. A. Becker, S. D. Persad, H. F. Haberman, Quantitation of hydrogen peroxide formed during UV-visible irradiation of protoporphyrin, coproporphyrin and uroporphyrin, Clin. Chim. Acta., 1990, 186, 3, 375–381.

    Article  CAS  PubMed  Google Scholar 

  81. D. P. Buchczyk, L. O. Klotz, K. Lang, C. Fritsch, H. Sies, High efficiency of 5-aminolevulinate - photodynamic treatment using UVA irradiation, Carcinogenesis, 2001, 22, 6, 879–883.

    Article  CAS  PubMed  Google Scholar 

  82. L. Ma, S. Bagdonas, J. Moan, The photosensitizing effect of the photoproduct of protoporphyrin IX, J. Photochem. Photobiol. B., 2001, 60, 2–3, 108–113.

    Article  CAS  PubMed  Google Scholar 

  83. D. E. Heck, A. M. Vetrano, T. M. Mariano, J. D. Laskin, UVB light stimulates production of reactive oxygen species: unexpected role for catalase, J. Biol. Chem., 2003, 278, 25, 22432–22436.

    Article  CAS  PubMed  Google Scholar 

  84. A. King, E. Gottlieb, D. G. Brooks, M. P. Murphy, J. L. Dunaief, Mitochondria-derived reactive oxygen species mediate blue light-induced death of retinal pigment epithelial cells, Photochem. Photobiol., 2004, 79, 5, 470–475.

    Article  CAS  PubMed  Google Scholar 

  85. S. Dore, M. Takahashi, C. D. Ferris, R. Zakhary, L. D. Hester, D. Guastella, S. H. Snyder, Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury, Proc. Natl. Acad. Sci. USA, 1999, 96, 5, 2445–2450.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. L. Cheng, D. A. Lightner, A new photoisomerization of bilirubin, Photochem. Photobiol., 1999, 70, 6, 941–948.

    Article  CAS  PubMed  Google Scholar 

  87. B. S. Rosenstein, J. M. Ducore, S. W. Cummings, The mechanism of bilirubin-photosensitized DNA strand breakage in human cells exposed to phototherapy light, Mutat. Res., 1983, 112, 6, 397–406.

    CAS  PubMed  Google Scholar 

  88. T. Christensen, E. B. Roll, A. Jaworska, G. Kinn, Bilirubin- and light induced cell death in a murine lymphoma cell line, J. Photochem. Photobiol. B., 2000, 58, 2-3, 170–174.

    Article  CAS  PubMed  Google Scholar 

  89. Melanin: Its role in human photoprotection, ed. L. Zeise, M. R. Chedekel and T. B. Fitzpatrick, Valdenmar Publishing Company, Overland Park, KS, 1995, pp. 1–320.

    Google Scholar 

  90. J. Moan, A. Dahlback, R. B. Setlow, Epidemiological support for an hypothesis for melanoma induction indicating a role for UVA radiation, Photochem. Photobiol., 1999, 70, 2, 243–247.

    Article  CAS  PubMed  Google Scholar 

  91. A. Yoneta, T. Yamashita, H. Y. Jin, S. Kondo, K. Jimbow, Ectopic expression of tyrosinase increases melanin synthesis and cell death following UVB irradiation in fibroblasts from familial atypical multiple mole and melanoma (FAMMM) patients, Melanoma. Res., 2004, 14, 5, 387–394.

    Article  CAS  PubMed  Google Scholar 

  92. F. L. Meyskens, Jr., P. Farmer, J. P. Fruehauf, Redox regulation in human melanocytes and melanoma, Pigm. Cell. Res., 2001, 14, 3, 148–154.

    Article  CAS  Google Scholar 

  93. Y. Liu, L. Hong, K. Wakamatsu, S. Ito, B. Adhyaru, C. Cheng, C. R. Bowers, J. D. Simon, Comparison of structural and chemical properties of black and red human hair melanosomes, Photochem. Photobiol., 2005, 81, 135–144.

    Article  CAS  PubMed  Google Scholar 

  94. A. Napolitano, Donato P. Di, G. Prota, New regulatory mechanisms in the biosynthesis of pheomelanins: rearrangement vs. redox exchange reaction routes of a transient 2H-1,4-benzothiazine-o-quinonimine intermediate, Biochim. Biophys. Acta., 2000, 1475, 1, 47–45.

    Article  CAS  PubMed  Google Scholar 

  95. T. G. Salopek, K. Yamada, S. Ito, K. Jimbow, Dysplastic melanocytic nevi contain high levels of pheomelanin: quantitative comparison of pheomelanin/eumelanin levels between normal skin, common nevi, and dysplastic nevi, Pigm. Cell. Res., 1991, 4, 4, 172–179.

    Article  CAS  Google Scholar 

  96. G. Agrup, C. Lindbladh, G. Prota, H. Rorsman, A. M. Rosengren, E. Rosengren, Trichochromes in the urine of melanoma patients, J. Invest. Dermatol., 1978, 70, 2, 90–91.

    Article  CAS  PubMed  Google Scholar 

  97. T. Horikoshi, S. Ito, K. Wakamatsu, H. Onodera, H. Eguchi, Evaluation of melanin-related metabolites as markers of melanoma progression, Cancer, 1994, 73, 3, 629–636.

    Article  CAS  PubMed  Google Scholar 

  98. M. R. Vincensi, M. d℉Ischia, A. Napolitano, E. M. Procaccini, G. Riccio, G. Monfrecola, P. Santoianni, G. Prota, Phaeomelanin vs. eumelanin as a chemical indicator of ultraviolet sensitivity in fair-skinned subjects at high risk for melanoma: a pilot study, Melanoma Res., 1998, 8, 1, 53–58.

    Article  CAS  PubMed  Google Scholar 

  99. I. A. Menon, S. Persad, N. S. Ranadive, 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., 1983, 43, 7, 3165–3169.

    CAS  PubMed  Google Scholar 

  100. E. Kvam, 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., 1999, 113, 2, 209–213.

    Article  CAS  PubMed  Google Scholar 

  101. C. Kipp, 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., 1999, 70, 2, 191–198.

    Article  CAS  PubMed  Google Scholar 

  102. L. Marrot, J. P. Belaidi, J. R. Meunier, P. Perez, C. Agapakis-Causse, The human melanocyte as a particular target for UVA radiation and an endpoint for photoprotection assessment, Photochem. Photobiol., 1999, 69, 6, 686–693.

    Article  CAS  PubMed  Google Scholar 

  103. E. Wenczl, G. P. van der Schans, L. Roza, R. M. Kolb, A. J. Timmerman, N. P. Smit, S. Pavel, A. A. Schothorst, (Pheo)melanin photosensitizes UVA-induced DNA. damage in cultured human melanocytes, J. Invest. Dermatol., 1998, 111, 4, 678–682.

    Article  CAS  PubMed  Google Scholar 

  104. S. Takeuchi, W. Zhang, K. Wakamatsu, S. Ito, V. J. Hearing, K. H. Kraemer, 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. USA, 2004, 101, 42, 15076–15081.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. E. Kvam, 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, Pigm. Cell. Res., 2004, 17, 5, 549–550.

    Article  CAS  Google Scholar 

  106. E. J. Land, A. Thompson, T. G. Truscott, K. V. Subbarao, M. R. Chedekel, Photochemistry of melanin precursors: dopa, 5-S-cysteinyldopa and 2,5-S,S℉-dicysteinyldopa, Photochem. Photobiol., 1986, 44, 6, 697–702.

    Article  CAS  PubMed  Google Scholar 

  107. W. H. Koch, M. R. Chedekel, Photoinitiated DNA. damage by melanogenic intermediates in vitro, Photochem. Photobiol., 1986, 44, 6, 703–710.

    Article  CAS  PubMed  Google Scholar 

  108. B. Pilas, C. C. Felix, T. Sarna, B. Kalyanaraman, Photolysis of pheomelanin precursors: an ESR-spin trapping study, Photochem. Photobiol., 1986, 44, 6, 689–696.

    Article  CAS  PubMed  Google Scholar 

  109. W. Korytowski, B. Pilas, T. Sarna, B. Kalyanaraman, Photoinduced generation of hydrogen peroxide and hydroxyl radicals in melanins, Photochem. Photobiol., 1987, 45, 2, 185–190.

    Article  CAS  PubMed  Google Scholar 

  110. K. Jimbow, K. Reszka, S. Schmitz, T. Salopek and P. Thomas, Distribution of eu- and pheomelanins in human skin and melanocytic tumors, and their photoprotective vs. phototoxic properties, in Melanin: Its role in human photoprotection, ed. L. Zeise, M. R. Chedekel and T. B. Fitzpatrick, Valdenmar Publishing Company, Overland Park, KS, 1995, pp. 155–175.

    Google Scholar 

  111. T. Ye, L. E. Lamb, K. Wakamatsu, S. Ito, J. D. Simon, Ultrafast absorption and photothermal studies of decarboxytrichochrome C in solution, Photochem. Photobiol. Sci., 2003, 2, 7, 821–823.

    Article  CAS  PubMed  Google Scholar 

  112. A. M. Edwards, C. Bueno, A. Saldano, E. Silva, K. Kassab, L. Polo, G. Jori, Photochemical and pharmacokinetic properties of selected flavins, J. Photochem. Photobiol. B., 1999, 48, 1, 36–41.

    Article  CAS  PubMed  Google Scholar 

  113. R. M. Kowalczyk, E. Schleicher, R. Bittl, S. Weber, The photoinduced triplet of flavins and its protonation states, J. Am. Chem. Soc., 2004, 126, 36, 11393–11399.

    Article  CAS  PubMed  Google Scholar 

  114. E. Silva, M. Jopia, A. M. Edwards, E. Lemp, J. R. de la Fuente, E. Lissi, Protective effect of Boldo and tea infusions on the visible light-mediated pro-oxidant effects of vitamin B2, riboflavin, Photochem. Photobiol., 2002, 75, 6, 585–590.

    CAS  PubMed  Google Scholar 

  115. D. R. Cardoso, D. W. Franco, K. Olsen, M. L. Andersen, L. H. Skibsted, Reactivity of bovine whey proteins, peptides, and amino acids toward triplet riboflavin as studied by laser flash photolysis, J. Agric. Food Chem., 2004, 52, 21, 6602–6606.

    Article  CAS  PubMed  Google Scholar 

  116. R. Ugarte, A. M. Edwards, M. S. Diez, A. Valenzuela, E. Silva, Riboflavin-photosensitized anaerobic modification of rat lens proteins. A correlation with age-related changes, J. Photochem. Photobiol. B., 1992, 13, 2, 161–168.

    Article  CAS  PubMed  Google Scholar 

  117. Y. Kato, K. Uchida, S. Kawakishi, Aggregation of collagen exposed to UVA in the presence of riboflavin: a plausible role of tyrosine modification, Photochem. Photobiol., 1994, 59, 3, 343–349.

    Article  CAS  PubMed  Google Scholar 

  118. K. Sato, H. Taguchi, T. Maeda, H. Minami, Y. Asada, Y. Watanabe, K. Yoshikawa, The primary cytotoxicity in ultraviolet-a-irradiated riboflavin solution is derived from hydrogen peroxide, J. Invest. Dermatol., 1995, 105, 4, 608–612.

    Article  CAS  PubMed  Google Scholar 

  119. A. Mahns, I. Melchheier, C. V. Suschek, H. Sies, L. O. Klotz, Irradiation of cells with ultraviolet-A (320-400 nm) in the presence of cell culture medium elicits biological effects due to extracellular generation of hydrogen peroxide, Free Radical Res., 2003, 37, 4, 391–397.

    Article  CAS  Google Scholar 

  120. W. T. Speck, C. C. Chen, H. S. Rosenkranz, In vitro studies of effects of light and riboflavin on DNA and HeLa cells, Pediatr. Res., 1975, 9, 3, 150–153.

    Article  CAS  PubMed  Google Scholar 

  121. K. Ito, S. Inoue, K. Yamamoto, S. Kawanishi, 8-Hydroxydeoxyguanosine formation at the 5℉ site of 5℉-GG-3℉ sequences in double-stranded DNA by UV radiation with riboflavin, J. Biol. Chem., 1993, 268, 18, 13221–13227.

    Article  CAS  PubMed  Google Scholar 

  122. F. Yamamoto, S. Nishimura, H. Kasai, Photosensitized formation of 8-hydroxydeoxyguanosine in cellular DNA by riboflavin, Biochem. Biophys. Res. Commun., 1992, 187, 2, 809–813.

    Article  CAS  PubMed  Google Scholar 

  123. A. H. Thomas, C. Lorente, A. L. Capparelli, C. G. Martinez, A. M. Braun, E. Oliveros, Singlet oxygen (1Δg) production by pterin derivatives in aqueous solutions, Photochem. Photobiol. Sci., 2003, 2, 3, 245–250.

    Article  CAS  PubMed  Google Scholar 

  124. K. Ito, S. Kawanishi, Photoinduced hydroxylation of deoxyguanosine in DNA by pterins: sequence specificity and mechanism, Biochemistry, 1997, 36, 7, 1774–1781.

    Article  CAS  PubMed  Google Scholar 

  125. H. Rokos, W. D. Beazley, K. U. Schallreuter, Oxidative stress in vitiligo: photo-oxidation of pterins produces H(2)O(2) and pterin-6-carboxylic acid, Biochem. Biophys. Res. Commun., 2002, 292, 4, 805–811.

    Article  CAS  PubMed  Google Scholar 

  126. R. F. Branda, J. W. Eaton, Skin color and nutrient photolysis: an evolutionary hypothesis, Science, 1978, 201, 4356, 625–626.

    Article  CAS  PubMed  Google Scholar 

  127. G. Cremer-Bartels, I. Ebels, Pteridines as nonretinal regulators of light-dependent melatonin biosynthesis, Proc. Natl. Acad. Sci. USA, 1980, 77, 5, 2415–2418.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Y. Murata, K. Kumano, T. Ueda, N. Araki, T. Nakamura, M. Tani, Photosensitive dermatitis caused by pyridoxine hydrochloride, J. Am. Acad. Dermatol., 1998, 39, 2 Pt 2, 314–317.

    Article  CAS  PubMed  Google Scholar 

  129. G. Shwartzman, A. Fisher, Studies on antibacterial properties of irradiated pyridoxamine, J. Biol. Chem., 1947, 167, 345–362.

    Article  CAS  PubMed  Google Scholar 

  130. G. T. Wondrak, M. J. Roberts, M. K. Jacobson, E. L. Jacobson, 3-hydroxypyridine chromophores are endogenous sensitizers of photooxidative stress in human skin cells, J. Biol. Chem., 2004, 279, 29, 30009–30020.

    Article  CAS  PubMed  Google Scholar 

  131. S. P. Coburn, A. Slominski, J. D. Mahuren, J. Wortsman, L. Hessle, J. L. Millan, Cutaneous metabolism of vitamin B-6, J. Invest. Dermatol., 2003, 120, 2, 292–300.

    Article  CAS  PubMed  Google Scholar 

  132. K. Sato, H. Taguchi, T. Maeda, K. Yoshikawa, Pyridoxine toxicity to cultured fibroblasts caused by near-ultraviolet light, J. Invest. Dermatol, 1993, 100, 3, 266–270.

    Article  CAS  PubMed  Google Scholar 

  133. B. K. Ohta, C. S. Foote, Characterization of endoperoxide and hydroperoxide intermediates in the reaction of pyridoxine with singlet oxygen, J. Am. Chem. Soc., 2002, 124, 41, 12064–12065.

    Article  CAS  PubMed  Google Scholar 

  134. P. Bilski, M. Y. Li, M. Ehrenshaft, M. E. Daub, C. F. Chignell, Vitamin B6 (pyridoxine) and its derivatives are efficient singlet oxygen quenchers and potential fungal antioxidants, Photochem. Photobiol., 2000, 71, 2, 129–134.

    Article  CAS  PubMed  Google Scholar 

  135. M. L. Cunningham, N. I. Krinsky, S. M. Giovanazzi, M. J. Peak, Superoxide anion is generated from cellular metabolites by solar radiation and its components, J. Free Radical Biol. Med., 1985, 1, 5-6, 381–385.

    Article  CAS  Google Scholar 

  136. T. G. Burchuladze, G. Fraikin, [Mechanism of NADH-sensitized formation of DNA breaks during irradiation with near UV light], Mol. Biol. (Moscow), 1991, 25, 4, 955–959.

    CAS  Google Scholar 

  137. B. Czochralska, W. G. B. Kawczynski, D. Shugar, Oxidation of excited state NADH and NAD dimer in aqueous medium: involvement of O2- as a mediator in the presence of oxygen, Biochim. Biophys. Acta., 1984, 801, 403–409.

    Article  CAS  Google Scholar 

  138. R. S. Bodaness, P. C. Chan, Singlet oxygen as a mediator in the hematoporphyrin-catalyzed photooxidation of NADPH to NADP+ in deuterium oxide, J. Biol. Chem., 1977, 252, 23, 8554–8560.

    Article  CAS  PubMed  Google Scholar 

  139. V. Kirveliene, R. Rotomskis, A. Pugzlys, G. Slekys, V. Krasauskas, A. Piskarskas, B. Juodka, Fluence-rate-dependent photosensitized oxidation of NADH, J. Photochem. Photobiol. B., 1993, 21, 1, 53–60.

    Article  CAS  PubMed  Google Scholar 

  140. B. W. Pogue, J. D. Pitts, M. A. Mycek, R. D. Sloboda, C. M. Wilmot, J. F. Brandsema, J. A. O℉Hara, In vivo NADH fluorescence monitoring as an assay for cellular damage in photodynamic therapy, Photochem. Photobiol., 2001, 74, 6, 817–824.

    Article  CAS  PubMed  Google Scholar 

  141. F. Petrat, S. Pindiur, M. Kirsch, H. de Groot, NAD(P)H, a primary target of 1O2 in mitochondria of intact cells, J. Biol. Chem., 2003, 278, 5, 3298–3307.

    Article  CAS  PubMed  Google Scholar 

  142. M. Kirsch, Groot H. De, NAD(P)H, a directly operating antioxidant?, FASEB J., 2001, 15, 9, 1569–1574.

    Article  CAS  PubMed  Google Scholar 

  143. C. C. Winterbourn, Free radical toxicology and antioxidant defence, Clin. Exp. Pharmacol. Physiol., 1995, 22, 11, 877–880.

    Article  CAS  PubMed  Google Scholar 

  144. M. K. Jacobson, B. Tastoush, D. L. Coyle, M. Kim, H. Kim, E. L. Jacobson, Elevation of Skin Cell NAD Content by Topical Application of Pro-NAD Compounds, J. Invest. Dermatol., 2000, 114, 849.

    Google Scholar 

  145. E. L. Jacobson, P. U. Giacomoni, M. J. Roberts, G. T. Wondrak, M. K. Jacobson, Optimizing the energy status of skin cells during solar radiation, J. Photochem. Photobiol. B., 2001, 63, 1-3, 141–147.

    Article  CAS  PubMed  Google Scholar 

  146. T. Mohammad, H. Morrison, H. HogenEsch, Urocanic acid photochemistry and photobiology, Photochem. Photobiol., 1999, 69, 2, 115–135.

    Article  CAS  PubMed  Google Scholar 

  147. C. M. Chuong, B. J. Nickoloff, P. M. Elias, L. A. Goldsmith, E. Macher, P. A. Maderson, J. P. Sundberg, H. Tagami, P. M. Plonka, K. Thestrup-Pederson, B. A. Bernard, J. M. Schroder, P. Dotto, C. M. Chang, M. L. Williams, K. R. Feingold, L. E. King, A. M. Kligman, J. L. Rees, E. Christophers, What is the ‘true’ function of skin?, Exp. Dermatol., 2002, 11, 2, 159–187.

    Article  CAS  PubMed  Google Scholar 

  148. H. Morrison, D. Avnir, C. Bernasconi, G. Fagan, Z/E Photoisomerization of urocanic acid, Photochem. Photobiol., 1980, 32, 711–714.

    Article  CAS  Google Scholar 

  149. N. Haralampus-Grynaviski, C. Ransom, T. Ye, M. Rozanowska, M. Wrona, T. Sarna, J. D. Simon, Photogeneration and quenching of reactive oxygen species by urocanic acid, J. Am. Chem. Soc., 2002, 124, 13, 3461–3468.

    Article  CAS  PubMed  Google Scholar 

  150. E. L. Menon, H. Morrison, Formation of singlet oxygen by urocanic acid by UVA irradiation and some consequences thereof, Photochem. Photobiol., 2002, 75, 6, 565–569.

    Article  CAS  PubMed  Google Scholar 

  151. K. M. Hanson, J. D. Simon, Epidermal trans-urocanic acid and the UV-A-induced photoaging of the skin, Proc. Natl. Acad. Sci. USA, 1998, 95, 18, 10576–10578.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. J. P. McCormick, J. R. Fischer, J. P. Pachlatko, A. Eisenstark, Characterization of a cell-lethal product from the photooxidation of tryptophan: hydrogen peroxide, Science, 1976, 191, 4226, 468–469.

    Article  CAS  PubMed  Google Scholar 

  153. J. Craggs, S. H. Kirk, S. I. Ahmad, Synergistic action of near-UV and phenylalanine, tyrosine or tryptophan on the inactivation of phage T7: role of superoxide radicals and hydrogen peroxide, J. Photochem. Photobiol. B., 1994, 24, 2, 123–128.

    Article  CAS  PubMed  Google Scholar 

  154. P. Walrant, R. Santus, N-formyl-kynurenine, a tryptophan photooxidation product, as a photodynamic sensitizer, Photochem. Photobiol., 1974, 19, 6, 411–417.

    Article  CAS  PubMed  Google Scholar 

  155. A. Pirie, Formation of N℉-formylkynurenine in proteins from lens and other sources by exposure to sunlight, Biochem. J., 1971, 125, 1, 203–208.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. L. I. Grossweiner, Photochemistry of proteins: a review, Curr. Eye Res., 1984, 3, 1, 137–144.

    Article  CAS  PubMed  Google Scholar 

  157. J. A. Aquilina, R. J. Truscott, Identifying sites of attachment of UV filters to proteins in older human lenses, Biochim. Biophys. Acta., 2002, 1596, 1, 6–15.

    Article  CAS  PubMed  Google Scholar 

  158. N. R. Parker, J. F. Jamie, M. J. Davies, R. J. Truscott, Protein-bound kynurenine is a photosensitizer of oxidative damage, Free Radical Biol. Med., 2004, 37, 9, 1479–1489.

    Article  CAS  Google Scholar 

  159. R. K. Sindhu, F. E. Wagner, Y. Kikkawa, Induction of cytochrome p450 1A1 and 1B1 by photooxidized tryptophan in transformed human keratinocytes, Adv. Exp. Med. Biol., 2003, 527, 297–306.

    Article  CAS  PubMed  Google Scholar 

  160. J. J. Thiele, S. N. Hsieh, K. Briviba, H. Sies, Protein oxidation in human stratum corneum: susceptibility of keratins to oxidation in vitro and presence of a keratin oxidation gradient in vivo, J. Invest. Dermatol., 1999, 113, 3, 335–339.

    Article  CAS  PubMed  Google Scholar 

  161. G. J. Smith, New trends in photobiology: photodegradation of keratin and other structural proteins, J. Photochem. Photobiol. B., 1995, 27, 187–198.

    Article  CAS  Google Scholar 

  162. G. J. Smith, W. H. Melhuish, Relaxation and quenching of the excited states of tryptophan in keratin, J. Photochem. Photobiol. B., 1993, 17, 63–68.

    Article  CAS  PubMed  Google Scholar 

  163. D. G. Dyer, J. A. Dunn, S. R. Thorpe, K. E. Bailie, T. J. Lyons, D. R. McCance, J. W. Baynes, Accumulation of Maillard reaction products in skin collagen in diabetes and aging, J. Clin. Invest., 1993, 91, 6, 2463–2469.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. C. Jeanmaire, L. Danoux, G. Pauly, Glycation during human dermal intrinsic and actinic ageing: an in vivo and in vitro model study, Br. J. Dermatol., 2001, 145, 1, 10–18.

    Article  CAS  PubMed  Google Scholar 

  165. G. T. Wondrak, D. Cervantes-Laurean, M. J. Roberts, J. G. Qasem, M. Kim, E. L. Jacobson, M. K. Jacobson, Identification of alpha-dicarbonyl scavengers for cellular protection against carbonyl stress, Biochem. Pharmacol., 2002, 63, 3, 361–373.

    Article  CAS  PubMed  Google Scholar 

  166. R. Abe, T. Shimizu, H. Sugawara, H. Watanabe, H. Nakamura, H. Choei, N. Sasaki, S. Yamagishi, M. Takeuchi, H. Shimizu, Regulation of human melanoma growth and metastasis by AGE-AGE receptor interactions, J. Invest. Dermatol., 2004, 122, 2, 461–467.

    Article  CAS  PubMed  Google Scholar 

  167. R. Tressl, G. T. Wondrak, R. P. Kruger, D. Rewicki, New Melanoidin-like Maillard Polymers from 2-Deoxypentoses, J. Agric. Food Chem., 1998, 46, 1, 104–110.

    Article  CAS  PubMed  Google Scholar 

  168. S. R. Thorpe, J. W. Baynes, Maillard reaction products in tissue proteins: new products and new perspectives, Amino. Acids., 2003, 25, 3-4, 275–281.

    Article  CAS  PubMed  Google Scholar 

  169. B. J. Ortwerth, M. Prabhakaram, R. H. Nagaraj, M. Linetsky, The relative UV sensitizer activity of purified advanced glycation endproducts, Photochem. Photobiol., 1997, 65, 4, 666–672.

    Article  CAS  PubMed  Google Scholar 

  170. G. T. Wondrak, E. L. Jacobson, M. K. Jacobson, Photosensitization of DNA damage by glycated proteins, Photochem. Photobiol. Sci., 2002, 1, 355–363.

    Article  CAS  PubMed  Google Scholar 

  171. H. Masaki, Y. Okano, H. Sakurai, Generation of active oxygen species from advanced glycation end-products (AGEs) during ultraviolet light A (UVA) irradiation and a possible mechanism for cell damaging, Biochim. Biophys. Acta, 1999, 1428, 1, 45–56.

    Article  CAS  PubMed  Google Scholar 

  172. Y. Okano, H. Masaki, H. Sakurai, Pentosidine in advanced glycation end-products (AGEs) during UVA irradiation generates active oxygen species and impairs human dermal fibroblasts, J. Dermatol. Sci., 2001, 27, Suppl 1, S11–S18.

    Article  CAS  PubMed  Google Scholar 

  173. T. Usui, S. Shizuuchi, H. Watanabe, F. Hayase, Cytotoxicity and oxidative stress induced by the glyceraldehyde-related Maillard reaction products for HL-60 cells, Biosci. Biotechnol. Biochem., 2004, 68, 2, 333–340.

    Article  CAS  PubMed  Google Scholar 

  174. R. Nagai, C. M. Hayashi, L. Xia, M. Takeya, S. Horiuchi, Identification in human atherosclerotic lesions of GA-pyridine, a novel structure derived from glycolaldehyde-modified proteins, J. Biol. Chem., 2002, 277, 50, 48905–48912.

    Article  CAS  PubMed  Google Scholar 

  175. F. J. Tessier, V. M. Monnier, L. M. Sayre, J. A. Kornfield, Triosidines: novel Maillard reaction products and cross-links from the reaction of triose sugars with lysine and arginine residues, Biochem. J., 2003, 369, Pt 3, 705–719.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. A. B. Petersen, H. C. Wulf, R. Gniadecki, B. Gajkowska, Dihydroxyacetone, the active browning ingredient in sunless tanning lotions, induces DNA damage, cell-cycle block and apoptosis in cultured HaCaT keratinocytes, Mutat. Res., 2004, 560, 2, 173–186.

    Article  CAS  PubMed  Google Scholar 

  177. H. Inano, H. Ohba, B. Tamaoki, Photochemical inactivation of human placental estradiol 17 beta-dehydrogenase in the presence of 2,3-butanedione, J. Steroid Biochem., 1983, 19, 5, 1617–1622.

    Article  CAS  PubMed  Google Scholar 

  178. W. M. Nau, J. C. Scaiano, Qxygen quenching of excited aliphatic ketones and diketones, J. Phys. Chem., 1996, 100, 11360–11367.

    Article  CAS  Google Scholar 

  179. A. Kornhauser, M. A. Pathak, Studies on the mechanism of the photosensitized dimerization of pyrimidines, Z. Naturforsch., Teil B, 1972, 27, 5, 550–553.

    Article  CAS  Google Scholar 

  180. I. G. Gut, P. D. Wood, R. W. Redmond, Interaction of triplet photosensitizers with nucleotides and DNA in aqueous solution at room temperature, J. Am. Chem. Soc., 1996, 118, 2366–2373.

    Article  CAS  Google Scholar 

  181. U. T. Brunk, A. Terman, Lipofuscin: mechanisms of age-related accumulation and influence on cell function, Free Radical Biol. Med., 2002, 33, 5, 611–619.

    Article  CAS  Google Scholar 

  182. M. Boulton, M. Rozanowska, B. Rozanowski, T. Wess, The photoreactivity of ocular lipofuscin, Photochem. Photobiol. Sci., 2004, 3, 8, 759–764.

    Article  CAS  PubMed  Google Scholar 

  183. L. E. Lamb, J. D. Simon, A2E: a component of ocular lipofuscin, Photochem. Photobiol., 2004, 79, 2, 127–136.

    Article  CAS  PubMed  Google Scholar 

  184. N. Sitte, K. Merker, T. Grune, T. von Zglinicki, Lipofuscin accumulation in proliferating fibroblasts in vitro: an indicator of oxidative stress, Exp. Gerontol., 2001, 36, 3, 475–486.

    Article  CAS  PubMed  Google Scholar 

  185. N. Kollias, R. Gillies, M. Moran, I. E. Kochevar, R. R. Anderson, Endogenous skin fluorescence includes bands that may serve as quantitative markers of aging and photoaging, J. Invest. Dermatol, 1998, 111, 5, 776–780.

    Article  CAS  PubMed  Google Scholar 

  186. L. Brancaleon, G. Lin, N. Kollias, The in vivo fluorescence of tryptophan moieties in human skin increases with UV exposure and is a marker for epidermal proliferation, J. Invest. Dermatol., 1999, 113, 6, 977–982.

    Article  CAS  PubMed  Google Scholar 

  187. J. M. Menter, G. D. Williamson, K. Carlyle, C. L. Moore, I. Willis, Photochemistry of type I acid-soluble calf skin collagen: dependence on excitation wavelength, Photochem. Photobiol., 1995, 62, 3, 402–408.

    Article  CAS  PubMed  Google Scholar 

  188. S. Fu, M. X. Fu, J. W. Baynes, S. R. Thorpe, R. T. Dean, Presence of dopa and amino acid hydroperoxides in proteins modified with advanced glycation end products (AGEs): amino acid oxidation products as a possible source of oxidative stress induced by AGE proteins, Biochem. J., 1998, 330, Pt 1, 233–239.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. M. J. Petersen, C. Hansen, S. Craig, Ultraviolet A. irradiation stimulates collagenase production in cultured human fibroblasts, J. Invest. Dermatol., 1992, 99, 4, 440–444.

    Article  CAS  PubMed  Google Scholar 

  190. G. Herrmann, M. Wlaschek, T. S. Lange, K. Prenzel, G. Goerz, K. Scharffetter-Kochanek, UVA irradiation stimulates the synthesis of various matrix-metalloproteinases (MMPs) in cultured human fibroblasts, Exp. Dermatol., 1993, 2, 2, 92–97.

    Article  CAS  PubMed  Google Scholar 

  191. G. J. Fisher, S. C. Datta, H. S. Talwar, Z. Q. Wang, J. Varani, S. Kang, J. J. Voorhees, Molecular basis of sun-induced premature skin ageing and retinoid antagonism, Nature, 1996, 379, 6563, 335–339.

    Article  CAS  PubMed  Google Scholar 

  192. J. Varani, D. Spearman, P. Perone, S. E. Fligiel, S. C. Datta, Z. Q. Wang, Y. Shao, S. Kang, G. J. Fisher, J. J. Voorhees, Inhibition of type I procollagen synthesis by damaged collagen in photoaged skin and by collagenase-degraded collagen in vitro, Am. J. Pathol., 2001, 158, 3, 931–942.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. T. K. Hei, R. Persaud, H. Zhou, M. Suzuki, Genotoxicity in the eyes of bystander cells, Mutat. Res., 2004, 568, 1, 111–120.

    Article  CAS  PubMed  Google Scholar 

  194. B. Ponnaiya, G. Jenkins-Baker, A. Bigelow, S. Marino, C. R. Geard, Detection of chromosomal instability in alpha-irradiated and bystander human fibroblasts, Mutat. Res., 2004, 568, 1, 41–48.

    Article  CAS  PubMed  Google Scholar 

  195. H. Maier, G. Schauberger, K. Brunnhofer, H. Honigsmann, Change of ultraviolet absorbance of sunscreens by exposure to solar-simulated radiation, J. Invest. Dermatol., 2001, 117, 2, 256–262.

    Article  CAS  PubMed  Google Scholar 

  196. J. M. Allen, C. J. Gossett, S. K. Allen, Photochemical formation of singlet molecular oxygen in illuminated aqueous solutions of several commercially available sunscreen active ingredients, Chem. Res. Toxicol., 1996, 9, 3, 605–609.

    Article  CAS  PubMed  Google Scholar 

  197. N. Serpone, A. Salinaro, A. V. Emeline, S. Horikoshi, H. Hidaka, J. Zhao, An in vitro systematic spectroscopic examination of the photostabilities of a random set of commercial sunscreen lotions and their chemical UVB/UVA active agents, Photochem. Photobiol. Sci., 2002, 1, 12, 970–981.

    Article  CAS  PubMed  Google Scholar 

  198. G. T. Wondrak, M. K. Jacobson, E. L. Jacobson, Identification of quenchers of photoexcited states as novel agents for skin photoprotection, J. Pharmacol. Exp. Ther., 2005, 312, 2, 482–491.

    Article  CAS  PubMed  Google Scholar 

  199. A. Meves, S. N. Stock, A. Beyerle, M. R. Pittelkow, D. Peus, Vitamin C. derivative ascorbyl palmitate promotes ultraviolet-B-induced lipid peroxidation and cytotoxicity in keratinocytes, J. Invest. Dermatol., 2002, 119, 5, 1103–1108.

    Article  CAS  PubMed  Google Scholar 

  200. Y. P. Lu, Y. R. Lou, P. Yen, H. L. Newmark, O. I. Mirochnitchenko, M. Inouye, M. T. Huang, Enhanced skin carcinogenesis in transgenic mice with high expression of glutathione peroxidase or both glutathione peroxidase and superoxide dismutase, Cancer. Res., 1997, 57, 8, 1468–1474.

    CAS  PubMed  Google Scholar 

  201. Y. Koyama, Structures and functions of carotenoids in photosynthetic systems, J. Photochem. Photobiol. B., 1991, 9, 265–280.

    Article  CAS  Google Scholar 

  202. N. E. Holt, D. Zigmantas, L. Valkunas, X. P. Li, K. K. Niyogi, G. R. Fleming, Carotenoid cation formation and the regulation of photosynthetic light harvesting, Science, 2005, 307, 5708, 433–436.

    Article  CAS  PubMed  Google Scholar 

  203. S. Beutner, B. Bloedorn, T. Hoffmann, H. D. Martin, Synthetic singlet oxygen quenchers, Methods Enzymol., 2000, 319, 226–241.

    Article  CAS  PubMed  Google Scholar 

  204. C. Schweitzer, R. Schmidt, Physical mechanisms of generation and deactivation of singlet oxygen, Chem. Rev., 2003, 103, 1685–1757.

    Article  CAS  PubMed  Google Scholar 

  205. A. U. Khan, Y.-H. Mei, T. Wilson, A proposed function for spermine and spermidine: protection of replicating DNA against damage by singlet oxygen, Proc. Natl. Acad. Sci. USA, 1992, 89, 11426–11427.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  206. Y. Lion, M. Delmelle, A van De Vorst, New method of detecting singlet oxygen production, Nature, 1976, 263, 442–443.

    Article  CAS  PubMed  Google Scholar 

  207. E. L. Clennan, L. J. Noe, T. Wen, E. Szneler, Solvent Effects on the Ability of Amines to Physically Quench Singlet Oxygen As Determined by Time-Resolved Infrared Emission Studies, J. Org. Chem., 1989, 54, 3581–3584.

    Article  CAS  Google Scholar 

  208. Mascio P. Di, S. Kaiser, H. Sies, Lycopene as the most efficient biological carotenoid singlet oxygen quencher, Arch. Biochem. Biophys., 1989, 274, 2, 532–538.

    Article  Google Scholar 

  209. A. A. Krasnovsky, Jr., M. A. Rodgers, M. G. Galpern, B. Rihter, M. E. Kenney, E. A. Lukjanetz, Quenching of singlet molecular oxygen by phthalocyanines and naphthalocyanines, Photochem. Photobiol., 1992, 55, 5, 691–696.

    Article  CAS  PubMed  Google Scholar 

  210. P. Douglas, J. D. Thomas, H. Strohm, C. Winscom, D. Clarke, M. S. Garley, Triplet energies and the singlet oxygen quenching mechanism for 7H-pyrazolo[5,1-c]-1,2,4-triazole azomethine dyes, Photochem. Photobiol. Sci., 2003, 2 5, 563–568.

    Article  CAS  PubMed  Google Scholar 

  211. G. Cosa, L. J. Martinez, J. C. Scaiano, Influence of solvent polarity and base concentration on the photochemistry of ketoprofen: independent singlet and triplet pathways, Phys. Chem. Chem. Phys., 1999, 1, 3533–3537.

    Article  CAS  Google Scholar 

  212. M. C. Cuquerella, F. Bosca, M. A. Miranda, Photonucleophilic aromatic substitution of 6-fluoroquinolones in basic media: triplet quenching by hydroxide anion, J. Org. Chem., 2004, 69, 7256–7261.

    Article  CAS  PubMed  Google Scholar 

  213. E. F. Ullman, P. Singh, 3,3,4,4-Tetramethyl-1,2-diazetine-1,2-dioxide, a useful low-energy triplet quencher, J. Am. Chem. Soc., 1972, 94, 5077–5078.

    Article  CAS  Google Scholar 

  214. F. Rizzuto, J. D. Spikes, Mechanisms involved in the chemical inhibition of the eosin-sensitized photooxidation of trypsin, Radiat. Environ. Biophys., 1975, 12, 3, 217–232.

    Article  CAS  PubMed  Google Scholar 

  215. P. D. Sima, J. R. Kanofsky, Cyanine dyes as protectors of K562 cells from photosensitized cell damage, Photochem. Photobiol., 2000, 71, 4, 413–421.

    Article  CAS  PubMed  Google Scholar 

  216. D. L. Bissett, S. Majeti, J. J. Fu, J. F. McBride, W. E. Wyder, Protective effect of topically applied conjugated hexadienes against ultraviolet radiation-induced chronic skin damage in the hairless mouse, Photodermatol. Photoimmunol. Photomed., 1990, 7, 2, 63–67.

    CAS  PubMed  Google Scholar 

  217. H. J. Suh, H. W. Lee, J. Jung, Mycosporine glycine protects biological systems against photodynamic damage by quenching singlet oxygen with a high efficiency, Photochem. Photobiol., 2003, 78, 2, 109–113.

    Article  CAS  PubMed  Google Scholar 

  218. J. M. Gaullier, M. Bazin, A. Valla, M. Giraud, R. Santus, Amino acid-pyrrole N-conjugates; a new class of antioxidants II. Effectiveness of singlet oxygen quenching by luminescence measurements, J. Photochem. Photobiol. B., 1995, 30, 195–200.

    Article  CAS  Google Scholar 

  219. H. Sies, W. Stahl, Nutritional Protection Against Skin Damage From Sunlight, Annu. Rev. Nutr., 2004, 24, 173–200.

    Article  CAS  PubMed  Google Scholar 

  220. W. H. Chan, H. J. Wu, Anti-apoptotic effects of curcumin on photosensitized human epidermal carcinoma A431 cells, J. Cell. Biochem., 2004, 92, 1, 200–212.

    Article  CAS  PubMed  Google Scholar 

  221. T. A. Dahl, W. R. Midden, P. E. Hartman, Some prevalent biomolecules as defenses against singlet oxygen damage, Photochem. Photobiol., 1988, 47, 3, 357–362.

    Article  CAS  PubMed  Google Scholar 

  222. M. Rougee, R. V. Bensasson, E. J. Land, R. Pariente, Deactivation of singlet molecular oxygen by thiols and related compounds, possible protectors against skin photosensitivity, Photochem. Photobiol., 1988, 47, 4, 485–489.

    Article  CAS  PubMed  Google Scholar 

  223. P. Morliere, G. Huppe, D. Averbeck, A. R. Young, R. Santus, L. Dubertret, In vitro photostability and photosensitizing properties of bergamot oil. Effects of a cinnamate sunscreen, J. Photochem. Photobiol. B., 1990, 7, 2–4, 199–208.

    Article  CAS  PubMed  Google Scholar 

  224. P. Morliere, O. Avice, T. S. Melo, L. Dubertret, M. Giraud, R. Santus, A study of the photochemical properties of some cinnamate sunscreens by steady state and laser flash photolysis, Photochem. Photobiol., 1982, 36, 4, 395–399.

    Article  CAS  PubMed  Google Scholar 

  225. E. Chatelain, B. Gabard, Photostabilization of butyl methoxydibenzoylmethane (Avobenzone) and ethylhexyl methoxycinnamate by bis-ethylhexyloxyphenol methoxyphenyl triazine (Tinosorb S.), a new UV broadband filter, Photochem. Photobiol., 2001, 74, 3, 401–406.

    Article  CAS  PubMed  Google Scholar 

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  1. Department of Pharmacology and Toxicology, College of Pharmacy, Arizona Cancer Center, 1515 North Campbell Avenue, Tucson, AZ, USA

    Georg T. Wondrak, Myron K. Jacobson & Elaine L. Jacobson

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  1. Georg T. Wondrak
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Wondrak, G.T., Jacobson, M.K. & Jacobson, E.L. Endogenous UVA-photosensitizers: mediators of skin photodamage and novel targets for skin photoprotection. Photochem Photobiol Sci 5, 215–237 (2006). https://doi.org/10.1039/b504573h

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