Oxidatively generated damage to cellular DNA by UVB and UVA radiation

Photochemistry and Photobiology

Volumn 91, Issue 1, 2015, Pages 140-155

  Cadet, Jean ^a,b,c   Douki, Thierry ^a,b   Ravanat, Jean Luc ^a,b  

^a UNIV GRENOBLE ALPES   (France)

^b CEA GRENOBLE   (France)

^c UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

ANIMAL; HUMAN; OXIDATIVE STRESS; RADIATION RESPONSE; ULTRAVIOLET RADIATION;

ANIMALS; DNA; HUMANS; OXIDATIVE STRESS; ULTRAVIOLET RAYS;

EID: 84921469431     PISSN: 00318655     EISSN: 17511097     Source Type: Journal    
DOI: 10.1111/php.12368     Document Type: Review

References (218)

1. Kraemer, K. H., (1997) Sunlight and skin cancer: Another link revealed. Proc. Natl Acad. Sci. USA 94, 11-14.
2. de Gruijl, F. R., H. J. van Kranen, and, L. H. Mullenders, (2001) UV-induced DNA damage, repair, mutations and oncogenic pathways in skin cancer. J. Photochem. Photobiol. B 63, 19-27.
3. de Gruijl, F. R., and, H. Rebel, (2008) Early events in UV carcinogenesis-DNA damage, target cells and mutant p53 foci. Photochem. Photobiol. 84, 382-387.
4. Brash, D. E., J. A. Rudolph, J. A. Simon, A. Lin, G. J. McKenna, H. P. Baden, A. J. Halperin, and, J. Pontén, (1991) A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc. Natl Acad. Sci. USA 88, 10124-11012.
5. Ikehata, H., and, T. Ono, (2011) The mechanisms of UV mutagenesis. J. Radiat. Res. 52, 115-125.
6. Sage, E., P.-M. Girard, and, S. Francesconi, (2012) Unravelling UVA-induced mutagenesis. Photochem. Photobiol. Sci. 11, 74-80.
7. Pfeifer, G. P., and, A. Besaratinia, (2012) UV wavelength-dependent DNA damage and human non-melanoma and melanoma skin cancer. Photochem. Photobiol. Sci. 11, 90-97.
8. Yogianti, F., M. Kunisada, R. Ono, K. Sakumi, Y. Nakabeppu, and, C. Nishigori, (2012) Skin tumours induced by narrowband UVB have higher frequency of p53 mutations than tumours induced by broadband UVB independent of Ogg1 genotype. Mutagenesis 27, 637-643.
9. Mitchell, D. L., D. E. Brash, and, R. S. Nairn, (1990) Rapid repair kinetics of pyrimidine (6-4) pyrimidone photoproducts in human cells are due to excision rather than conformational change. Nucleic Acids Res. 18, 963-971.
10. Mouret, S., M. Charveron, A. Favier, J. Cadet, and, T. Douki, (2008) Differential repair of UVB-induced cyclobutane pyrimidine dimers in cultured human skin cells and whole human skin. DNA Repair (Amst) 7, 704-712.
11. Besaratinia, A., S. I. Kim, and, G. P. Pfeifer, (2008) Rapid repair of UVA-induced oxidized purines and persistence of UVB-induced dipyrimidine lesions determine the mutagenicity of sunlight in mouse cells. FASEB J. 22, 2379-2392.
12. Cadet, J., and, P. Vigny, (1990) The photochemistry of nucleic acids. In Bioorganic Photochemistry: Photochemistry and the Nucleic Acids, Vol. 1, (Edited by, H. Morrison,), pp. 1-272, Wiley and Sons, New York.
13. Taylor, J. S., (1994) Unraveling the molecular pathway from sunlight to skin-cancer. Acc. Chem. Res. 27, 76-82.
14. Cadet, J., S. Mouret, J.-L. Ravanat, and, T. Douki, (2012a) Photoinduced damage to cellular DNA: Direct and photosensitized reactions. Photochem. Photobiol. 88, 1048-1065.
15. Buckel, T. B., A. M. Goldstein, M. C. Fraser, B. Rogers, and, M. A. Tucker, (2006) Recent tanning bed use: A risk factor for melanoma. Arch. Dermatol. 142, 485-488.
16. Ting, W., K. Schultz, N. N. Cac, M. Peterson, and, H. W. Walling, (2007) Tanning bed exposure increases the risk of malignant melanoma. Int. J. Dermatol. 46, 1253-1257.
17. Moan, J., A. C. Porojnicu, and, A. Dahiback, (2008) Ultraviolet radiation and malignant melanoma. Adv. Exp. Med. Biol. 624, 104-116.
18. Noonan, F., M. R. Zaidi, A. Wolnicka-Glubisz, M. R. Anver, J. Bahn, A. Wielgus, J. Cadet, T. Douki, S. Mouret, M. A. Tucker, A. Popratiloff, G. Merlino, and, E. C. De Fabo, (2012) Melanoma induction by ultraviolet A but not ultraviolet B radiation requires melanin pigment. Nat. Commun. 3, 884.
19. Douki, T., A. Reynaud-Angelin, J. Cadet, and, E. Sage, (2003) Bipyrimidine photoproducts rather than oxidative lesions are the main type of DNA damage involved in the genotoxic effect of solar UVA radiation. Biochemistry 42, 9221-9226.
20. Courdavault, S., C. Baudouin, M. Charveron, A. Favier, J. Cadet, and, T. Douki, (2004) Larger yield of cyclobutane dimers than 8-oxo-7,8-dihydroguanine in the DNA of UVA-irradiated human skin cells. Mutat. Res. 556, 135-142.
21. Mouret, S., C. Baudouin, M. Charveron, A. Favier, J. Cadet, and, T. Douki, (2006) Cyclobutane pyrimidine dimers are predominant DNA lesions in whole human skin exposed to UVA radiation. Proc. Natl Acad. Sci. USA 103, 13765-13770.
22. Mouret, S., M.-T. Leccia, J.-L. Bourrain, T. Douki, and, J.-C. Beani, (2011) Individual photosensitivity of human skin and UVA-induced pyrimidine dimers in DNA. J. Invest. Dermatol. 131, 1539-1546.
23. Mouret, S., C. Philippe, J. Gracia-Chantegrel, A. Banyasz, S. Karpati, D. Markovitsi, and, T. Douki, (2010) UVA-induced cyclobutane pyrimidine dimers in DNA: A direct photochemical mechanism? Org. Biomol. Chem. 8, 1706-1711.
24. Banyasz, A., I. Vaya, P. Changenet-Barret, T. Gustavsson, T. Douki, and, D. Markovitsi, (2011) Base pairing enhances fluorescence and favors cyclobutane dimer formation induced upon absorption of UVA radiation by DNA. J. Am. Chem. Soc. 133, 5163-5165.
25. Courdavault, S., C. Baudouin, M. Charveron, B. Canguilhem, A. Favier, J. Cadet, and, T. Douki, (2005) Repair of the three main types of bipyrimidine DNA photoproducts in human keratinocytes exposed to UVB and UVA radiations. DNA Repair (Amst) 4, 836-844.
26. Cadet, J., E. Sage, and, T. Douki, (2005) Ultraviolet radiation mediated damage to cellular DNA. Mutat. Res. 571, 3-17.
27. Cadet, J., T. Douki, and, J.-L. Ravanat, (2008) Oxidatively generated damage to the guanine moiety: Mechanistic aspects and formation in cells. Acc. Chem. Res. 4, 1075-1083.
28. Cadet, J., T. Douki, and, J.-L. Ravanat, (2010) Oxidatively generated base damage to cellular DNA. Free Radic. Biol. Med. 49, 9-21.
29. Cadet, J., J.-L. Ravanat, M. TavernaPorro, H. Menoni, and, D. Angelov, (2012b) Oxidatively generated complex DNA damage: Tandem and clustered lesions. Cancer Lett. 327, 5-15.
30. Cadet, J., and, J. R. Wagner, (2013) DNA base damage by reactive oxygen species, oxidizing agents, and UV radiation. Cold Spring Harb. Perspect. Biol. 5, a012559.
31. Halliday, G. M., (2005) Inflammation, gene mutation and photoimmunosuppression in response to UVR-induced oxidative damage contributes to photocarcinogenesis. Mutat. Res. 571, 107-120.
32. Birch-Machin, M. A., E. V. Russell, and, J. A. Latimer, (2013) Mitochondrial DNA damage as a biomarker for ultraviolet radiation exposure and oxidative stress. Br. J. Dermatol. 169 (Suppl. 2), 9-14.
33. Schneider, L. A., W. Bloch, K. Kopp, A. Hainz, P. Rettberg, M. Wlaschek, G. Horneck, and, K. Scharffetter-Kochanek, (2006) 8-Isoprostane is a dose-related biomarker for photo-oxidative ultraviolet (UV) B damage in vivo: A pilot study with personal UV dosimetry. Br. J. Dermatol. 154, 1147-1154.
34. Yasui, H., T. Hakozaki, A. Date, T. Yoshii, and, H. Sakurai, (2006) Real-time chemiluminescent imaging and detection of reactive oxygen species generated in the UVB-exposed human skin equivalent model. Biochem. Biophys. Res. Commun. 347, 83-88.
35. Hakozaki, T., A. Date, T. Yoshii, S. Toyokuni, H. Yasui, and, H. Sakurai, (2008) Visualization and characterization of UVB-induced reactive oxygen species in a human skin equivalent model. Arch. Dermatol. Res. 300 (Suppl. 1), S51-S56.
36. Schallreuter, K. U., and, J. M. Wood, (2001) Thioredoxin reductase-its role in epidermal redox status. J. Photochem. Photobiol. B 64, 179-184.
37. Kalyanaraman, B., V. Darley-Usmar, K. J. Davies, P. A. Dennery, H. J. Forman, M. B. Grisham, G. E. Mann, K. Moore, L. J. 2nd Roberts, and, H. Ischiropoulos, (2012) Measuring reactive oxygen and nitrogen species with fluorescent probes: Challenges and limitations. Free Radic. Biol. Med. 52, 1-6.
38. Wang, H., and, I. Kochevar, (2005) Involvement of UVB-induced reactive oxygen species in TGF-beta biosynthesis and activation in keratinocytes. Free Radic. Biol. Med. 38, 890-897.
39. Jin, G.-H., Y. Liu, S.-Z. Jin, X. D. Liu, and, S.-Z. Liu, (2007) UVB induced oxidative stress in human keratinocytes and protective effect of antioxidant agents. Radiat. Environ. Biophys. 46, 61-68.
40. Rezvani, H. R., F. Mazurier, M. Cario-Andre, C. Pain, C. Ged, A. Taïeb, and, H. de Verneuil, (2006) Protective effects of catalase overexpression on UVB-induced apoptosis in normal human keratinocytes. J. Biol. Chem. 281, 17999-18007.
41. Horikawa-Miura, M., N. Matsuda, M. Yoshida, Y. Okumara, T. Mori, and, M. Watanabe, (2007) The greater lethality of UVB radiation to cultured human cells is associated with the specific activation of a DNA damage-independent signaling pathway. Radiat. Res. 167, 655-662.
42. Heck, D. E., A. M. Vetrano, T. M. Mariano, and, J. D. Laskin, (2003) UVB light stimu l ates production of reactive oxygen species: Unexpected role for catalase. J. Biol. Chem. 278, 22432-22436.
43. Beak, S. M., Y. S. Lee, and, J. A. Kim, (2004) NADPH oxidase and cyclooxygenase mediate the ultraviolet B-induced generation of reactive oxygen species and activation of nuclear factor-kappaB in HaCaT human keratinocytes. Biochimie 86, 425-429.
44. Bickers, D. R., and, M. Athar, (2006) Oxidative stress in the pathogenesis of skin disease. J. Invest. Dermatol. 126, 2565-2575.
45. Katiyar, S. K., and, S. M. Meeran, (2007) Obesity increases the risk of UV radiation-induced oxidative stress and activation of MAPK and NF-kappaB signaling. Free Radic. Biol. Med. 42, 299-310.
46. Wölfle, U., P. R. Esser, B. Simon-Haarhaus, S. F. Martin, J. Lademann, and, C. M. Schempp, (2011) UVB-induced DNA damage, generation of reactive oxygen species, and inflammation are effectively attenuated by the flavonoid luteolin in vitro and in vivo. Free Radic. Biol. Med. 50, 1081-1093.
47. Yogianti, F., M. Kunisada, E. Nakano, R. Ono, K. Sakumi, S. Oka, Y. Nakabeppu, and, C. Nishigori, (2014) Inhibitory effects of dietary Spirulina platensis on UVB-induced skin inflammatory responses and carcinogenesis. J Invest. Dermatol. 134, 2610-2619.
48. Suschek, C. V., C. Mahotka, O. Schnorr, and, V. Kolb-Bachofen, (2004) UVB radiation-mediated expression of inducible nitric oxide synthase activity and the augmenting role of co-induced TNF-alpha in human skin endothelial cells. J. Invest. Dermatol. 123, 950-957.
49. Katiyar, S. K., and, H. Mukhtar, (2001) Green tea polyphenol (-)-epigallocatechin-3-gallate treatment to mouse skin prevents UVB-induced infiltration of leukocytes, depletion of antigen-presenting cells, and oxidative stress. J. Leukocyte Biol. 69, 719-726.
50. Wiswedel, I., G. Keilhoff, L. Dörner, A. Navarro, R. Böckelmann, B. Bonnekoh, A. Gardemann, and, H. Gollnick, (2007) UVB irradiation-induced impairment of keratinocytes and adaptive responses to oxidative stress. Free Radic. Res. 41, 1017-1027.
51. Anwar, A., M. Gu, S. Brady, L. Qamar, K. Behbakht, Y. G. Shellman, R. Agarwal, D. A. Norris, L. D. Horwitz, and, M. Fujita, (2008) Photoprotective effects of bucillamine against UV-induced damage in an SKH-1 hairless mouse model. Photochem. Photobiol. 84, 477-483.
52. Black, A. T., J. P. Gray, M. P. Sharkarjian, D. L. Laskin, D. E. Heck, and, J. D. Laskin, (2008) Distinct effects of ultraviolet B light on antioxidant expression in undifferentiated and differentiated mouse keratinocytes. Carcinogenesis 29, 219-225.
53. Heck, D. E., D. R. Gerecke, A. M. Vetrano, and, J. D. Laskin, (2004) Solar ultraviolet radiation as a trigger of cell signal transduction. Toxicol. Appl. Pharmacol. 195, 288-297.
54. Dahle, J., O. Kaalhus, T. Stokke, and, E. Kvam, (2005) Bystander effects may modulate ultraviolet A and B radiation-induced delayed mutagenesis. Radiat. Res. 163, 289-295.
55. Dahle, J., E. Kvam, and, T. Stokke, (2006) Bystander effects in UV-induced genomic instability: Antioxidants inhibit delayed mutagenesis induced by ultraviolet A and B radiation. J. Carcinog. 4, 11.
56. Whiteside, J. R., and, T. J. McMillan, (2009) A bystander effect is induced in human cells treated with UVA radiation but not UVB radiation. Radiat. Res. 171, 204-211.
57. Widel, M., A. Krzywon, K. Gajda, M. Skonieczna, and, J. Rzeszowska-Wolny, (2014) Induction of bystander effects by UVA, UVB, and UVC radiation in human fibroblasts and the implication of reactive oxygen species. Free Radic. Biol. Med. 68, 278-287.
58. Danpure, H. J., and, R. M. Tyrrell, (1976) Oxygen-dependence of near UV (365 NM) lethality and the interaction of near UV and X-rays in two mammalian cell lines. Photochem. Photobiol. 23, 171-177.
59. Tyrrell, R. M., (1991) UVA (320-380 nm) radiation as an oxidative stress. In Oxidative Stress: Oxidants and Antioxidants (Edited by, H. Sies,), pp. 57-83. Academic Press, London.
60. Foote, C. S., (1968) Mechanisms of photosensitized oxidation. There are several different types of photosensitized oxidation which may be important in biological systems. Science 162, 963-970.
61. Foote, C. S., (1991) Definition of type I and type II photosensitized oxidation. Photochem. Photobiol. 54, 659.
62. Wondrak, G. T., M. K. Jacboson, and, E. L. Jacobson, (2006) Endogenous UVA-photosensitizers: Mediators of skin photodamage and novel targets for skin photoprotection. Photochem. Photobiol. Sci. 5, 215-237.
63. Misiaszek, R., C. Crean, A. Joffe, N. E. Geacintov, and, V. Shafirovich, (2004) Oxidative DNA damage associated with combination of guanine and superoxide radicals and repair mechanisms via radical trapping. J. Biol. Chem. 279, 32106-32115.
64. Cadet, J., T. Douki, and, J.-L. Ravanat, (2006a) One-electron oxidation of DNA and inflammation processes. Nat. Chem. Biol. 2, 348-349.
65. Cadet, J., and, P. Di Mascio, (2006) Peroxides in biological systems. In Functional Groups in Organic Chemistry-The Chemistry of Peroxides, Vol. 2, (Edited by, Z. Rappoport,), pp. 915-999, Wiley and Sons, New York.
66. Winterbourn, C. C., and, A. J. Kettle, (2003) Radical-radical reactions of superoxide: A potential route to toxicity. Biochem. Biophys. Res. Commun. 305, 729-736.
67. von Sonntag, C., (2006) Free-Radical-Induced DNA Damage and its Repair-A Chemical Perspective. Springer-Verlag, Berlin, Heidelberg, New-York.
68. Das, A. B., T. Nauser, W. H. Koppenol, A. J. Kettle, C. C. Winterbourn, and, P. Nagy, (2014) Rapid reaction of superoxide with insulin-tyrosyl radicals to generate a hydroperoxide with subsequent glutathione addition. Free Radic. Biol. Med. 70, 86-95.
69. Cadet, J., J.-L. Ravanat, G. R. Martinez, M. H. Medeiros, and, P. Di Mascio, (2006b) Singlet oxygen oxidation of isolated and cellular DNA: Product formation and mechanistic insights. Photochem. Photobiol. 82, 1219-1225.
70. Agnez-Lima, L. F., J. T. Melo, A. E. Silva, A. H. Oliveira, A. R. Timoteo, K. M. Lima-Bessa, G. R. Martinez, M. H. Medeiros, P. Di Mascio, R. S. Galhardo, and, C. F. Menck, (2012) DNA damage by singlet oxygen and cellular protective mechanisms. Mutat. Res. 751, 15-28.
71. Lundeen, R. A., and, K. McNeill, (2013) Reactivity differences of combined and free amino acids: Quantifying the relationship between three-dimensional protein structure and singlet oxygen reaction rates. Environ. Sci. Technol. 47, 14215-14223.
72. Frimer, A. A., (1985) Singlet Oxygen. Vol. 1-4, CRC Press, Boca Raton.
73. 2 (1Delta g)] in photosensitized oxidation reactions. Acc. Chem. Res. 39, 797-804.
74. Yasui, H., and, H. Sakurai, (2000) Chemiluminescent detection and imaging of reactive oxygen species in live mouse skin exposed to UVA. Biochem. Biophys. Res. Commun. 269, 131-136.
75. Sakurai, H., H. Yasui, Y. Yamada, H. Nishimura, and, M. Shigemoto, (2005) Detection of reactive oxygen species in the skin of live mice and rats exposed to UVA light: A research review on chemiluminescence and trials for UVA protection. Photochem. Photobiol. Sci. 4, 715-720.
76. Aitken, G. R., J. R. Henderson, S. C. Chang, C. J. McNeil, and, M. A. Birch-Machin, (2007) Direct monitoring of UV-induced free radical generation in HaCaT keratinocytes. Clin. Exp. Dermatol. 32, 722-727.
77. Tyrrell, R. M., and, M. Pidoux, (1989) Singlet oxygen involvement in the inactivation of cultured human fibroblasts by UVA (334 nm, 365 nm) and near-visible (405 nm) radiations. Photochem. Photobiol. 49, 407-412.
78. Briviba, K., L. O. Klotz, and, H. Sies, (1997) Toxic and signaling effects of photochemically or chemically generated singlet oxygen in biological systems. Biol. Chem. 378, 1259-1265.
79. Klotz, L. O., N. J. Holbrook, and, H. Sies, (2001) UVA and singlet oxygen as inducers of cutaneous signaling events. Curr. Probl. Dermatol. 29, 95-113.
80. Klotz, L. O., K. D. Kroncke, and, H. Sies, (2003) Singlet oxygen-induced signaling effects in mammalian cells. Photochem. Photobiol. Sci. 2, 88-94.
81. Triantaphylidès, C., and, M. Havaux, (2009) Singlet oxygen in plants: Production, detoxification and signaling. Trends Plant Sci. 14, 219-228.
82. Gkigkitzis, I., Y. Feng, C. Yang, J. Q. Lu, and, X. H. Hu, (2012) Modeling of oxygen transport and cell killing in type-II photodynamic therapy. Photochem. Photobiol. 88, 969-977.
83. Ruiz-González, R., J. H. White, M. Agut, S. Nonell, and, C. Flors, (2012) A genetically-encoded photosensitiser demonstrates killing of bacteria by purely endogenous singlet oxygen. Photochem. Photobiol. Sci. 11, 1411-1413.
84. Gollmer, A., F. Besostri, T. Breitenbach, and, P. R. Ogilby, (2013) Spatially resolved two-photon irradiation of an intracellular singlet oxygen photosensitizer: Correlating cell response to the site of localized irradiation. Free Radic. Res. 47, 718-730.
85. Grether-Beck, S., S. Olaizola-Horn, H. Schmitt, M. Grewe, A. Jahnke, J. P. Johnson, K. Briviba, H. Sies, and, J. Krutmann, (1996) 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 93, 14586-14591.
86. Tyrrell, R. M., (2000) Role for singlet oxygen in biological effects of ultraviolet A radiation. Methods Enzymol. 319, 290-296.
87. Valencia, A., and, I. E. Kochevar, (2008) Nox1-based NADPH oxidase is the major source of UVA-induced reactive oxygen species in human keratinocytes. J. Invest. Dermatol. 128, 214-222.
88. Belli, R., P. Amerio, L. Brunetti, G. Orlando, P. Toto, G. Proietto, M. Vacca, and, A. Tulli, (2005) Elevated 8-isoprostane levels in basal cell carcino ma and in UVA irradiated skin. Int. J. Immunopathol. Pharmacol. 18, 497-502.
89. Suschek, C., H. Rothe, K. Feshel, J. Enczmann, and, V. Kolb-Bachofen, (1993) Induction of a macrophage-like nitric oxide synthase in cultured rat aortic endothelial cells. IL-1 beta-mediated induction regulated by tumor necrosis factor-alpha and IFN-gamma. J. Immunol. 151, 3283-3291.
90. Mowbray, M., S. McLintock, R. Weerakoon, N. Lomatschinsky, S. Jones, A. G. Rossi, and, R. B. Weller, (2009) Enzyme-independent NO stores in human skin: Quantification and influence of UV radiation. J. Invest. Dermatol. 129, 834-842.
91. Liu, D., B. O. Fernandez, A. Hamilton, N. N. Lang, J. M. Gallagher, D. E. Newby, M. Feelisch, and, R. B. Weller, (2014) UVA irradiation of human skin vasodilates arterial vasculature and lowers blood pressure independently of nitric oxide synthase. J. Invest. Dermatol. 134, 1839-1846.
92. Halliday, G. M., and, S. N. Byrne, (2014) An unexpected role: UVA-induced release of nitric oxide from skin may have unexpected health benefits. J. Invest. Dermatol. 134, 1791-1794.
93. Korytowski, W., M. Zareba, and, A. W. Girotti, (2000) Nitric oxide inhibition of free radical-mediated cholesterol peroxidation in liposomal membranes. Biochemistry 39, 6918-6928.
94. Suschek, C. V., V. Krischel, D. Bruch-Gerharz, D. Berendji, J. Krutmann, and, K.-D. Kröncke, (1999) Nitric oxide fully protects against UVA-induced apoptosis in tight correlation with Bcl-2 up-regulation. J. Biol. Chem. 274, 6130-6137.
95. Suschek, C. V., K. Briviba, D. Bruch-Gerharz, H. Sies, and, K. D. Kröncke, (2001) Even after UVA-exposure will nitric oxide protect cells from reactive oxygen intermediate-mediated apoptosis and necrosis. Cell Death Differ. 8, 515-527.
96. Valencia, A., A. Rajadurai, B. Carle, and, I. E. Kochevar, (2006) 7-Dehydrocholesterol enhances ultraviolet A-induced oxidative stress in keratinocytes: Roles of NADPH oxidase, mitochondria, and lipid rafts. Free Radic. Biol. Med. 41, 1704-1718.
97. Redmond, R. W., A. Rajadurai, D. Udayakumar, E. V. Sviderskaya, and, H. Tsao, (2014) Melanocytes are selectively vulnerable to UVA-mediated bystander oxidative signaling. J. Invest. Dermatol. 134, 1083-1090.
98. Pourzand, C., R. D. Watkin, J. E. Brown, and, R. M. Tyrrell, (1999) Ultraviolet A radiation induces immediate release of iron in human primary skin fibroblasts: The role of ferritin. Proc. Natl Acad. Sci. USA 96, 6751-6756.
99. Mackenzie, E. L., K. Iwasaki, and, Y. Tsuji, (2008) Intracellular iron transport and storage: From molecular mechanisms to health implications. Antioxid. Redox Signal. 10, 997-1030.
100. Aroun, A., J. L. Zhong, R. M. Tyrrell, and, C. Pourzand, (2012) Iron, oxidative stress and the example of solar ultraviolet A radiation. Photochem. Photobiol. Sci. 11, 118-134.
101. Halliwell, B., and, J. M. Gutteridge, (1992) Biologically relevant metal ion-dependent hydroxyl radical generation. FEBS Lett. 307, 108-112.
102. Zhong, J. L., A. Yiakouvaki, P. Holley, R. M. Tyrrell, and, C. Pourzand, (2004) Susceptibility of skin cells to UVA-induced necrotic cell death reflects the intracellular level of labile iron. J. Invest. Dermatol. 123, 771-780.
103. Basu-Modak, S., D. Ali, M. Gordon, T. Polte, A. Yiakouvaki, C. Pourzand, C. Rice-Evans, and, R. M. Tyrrell, (2006) Suppression of UVA-mediated release of labile iron by epicatechin-a link to lysosomal protection. Free Radic. Biol. Med. 41, 1197-1204.
104. Tyrrell, R. M., (2012) Modulation of gene expression by the oxidative stress generated in human skin cells by UVA radiation and the restoration of redox homeostasis. Photochem. Photobiol. Sci. 11, 135-147.
105. Keyse, S. M., and, R. M. Tyrrell, (1989) Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc. Natl Acad. Sci. USA 86, 99-103.
106. Tyrrell, R. M., (2004) Solar ultraviolet A radiation: An oxidizing skin carcinogen that activates heme oxygenase-1. Antioxid. Redox Signal. 6, 835-840.
107. Tyrrell, R. M., and, V. E. Reeve, (2006) Potential protection of skin by acute UVA irradiation-from cellular to animal models. Progr. Biophys. Mol. Biol. 92, 86-91.
108. Kvam, E., V. Hejmadi, S. Ryter, C. Pourzand, and, R. M. Tyrrell, (2000) Heme oxygenase activity causes transient hypersensitivity to oxidative ultraviolet A radiation that depends on release of iron from heme. Free Radic. Biol. Med. 28, 1191-1196.
109. Kielbassa, C., L. Roza, and, B. Epe, (1997) Wavelength dependence of oxidative DNA damage induced by UV and visible light. Carcinogenesis 18, 811-816.
110. Kielbassa, C., and, B. Epe, (2000) DNA damage induced by ultraviolet and visible light and its wavelength dependence. Methods Enzymol. 319, 436-445.
111. Douki, T., D. Perdiz, P. Grof, Z. Kuluncsics, E. Moustacchi, J. Cadet, and, E. Sage, (1999) Oxidation of guanine in cellular DNA by solar UV radiation: Biological role. Photochem. Photobiol. 70, 184-190.
112. Wei, H., Q. Cai, and, M. Lebwohl, (1998) Tamoxifen reduces endogenous and UV light-induced oxidative damage to DNA, lipid and protein in vitro and in vivo. Carcinogenesis 19, 1013-1018.
113. 2 alone or with UVB or UVA irradiation. Photochem. Photobiol. 64, 117-122.
114. Stewart, M. S., G. S. Cameron, and, B. C. Pence, (1996) Antioxidant nutrients protect against UVB-induced oxidative damage to DNA of mouse keratinocytes in culture. J. Invest. Dermatol. 106, 1086-1089.
115. Pelle, E., X. Huang, T. Mammone, K. Marenus, D. Maes, and, K. Frenkel, (2003) Ultraviolet-B-induced oxidative DNA base damage in primary normal human epidermal keratinocytes and inhibition by a hydroxyl radical scavenger. J. Invest. Dermatol. 121, 177-183.
116. Orimo, H., Y. Tokura, R. Hino, and, H. Kasai, (2006) Formation of 8-hydroxy-deoxyguanosine in the DNA of cultured human keratinocytes by clinically used doses of narrowband and broadband ultraviolet B and psoralen plus ultraviolet A. Cancer Sci. 97, 99-105.
117. Garcin, G., T. Douki, P. E. Stoebner, J. Guesnet, A. Guezennec, J. Martinez, J. Cadet, and, L. Meunier, (2007) Cell surface expression of melanocortin-1 receptor on HaCaT keratinocytes and alpha-melanocortin stimulation do not affect the formation and repair of UVB-induced DNA photoproducts. Photochem. Photobiol. Sci. 6, 585-593.
118. Budiyanto, A., M. Ueda, T. Ueda, and, M. Ichihashi, (2002) Formation of cyclobutane pyrimidine dimers and 8-oxo-7,8-dihydro-2deoxyguanosine in mouse and organ-cultured human skin by irradiation with broadband or with narrowband UVB. Photochem. Photobiol. 76, 397-400.
119. Cooke, M. S., R. Olinski, S. Loft, and Members of the European Standards Committee on Urinary (DNA) Lesion Analysis (ESCULA) (2008) Measurement and meaning of oxidatively modified DNA lesions in urine. Cancer Epidemiol. Biomarker Prev. 17, 3-14.
120. Cadet, J., T. Douki, and, J.-L. Ravanat, (2011) Measurement of oxidatively generated base damage in cellular DNA. Mutat. Res. 711, 3-12.
121. Hattori, Y., C. Nishigori, T. Tanaka, K. Uchita, O. Nikaido, T. Osawa, H. Hiai, S. Imamura, and, S. Toyokuni, (1996) 8-Hydroxy-2deoxyguanosine is increased in epidermal cells of hairless mice after chronic ultraviolet B exposure. J. Invest. Dermatol. 107, 733-737.
122. Kusinada, M., K. Sakumi, Y. Tominaga, A. Budiyanto, M. Ueda, M. Ichihashi, Y. Nakabeppu, and, C. Nishigori, (2005) 8-Oxoguanine formation induced by chronic UVB exposure makes Ogg1 knockout mice susceptible to skin carcinogenesis. Cancer Res. 65, 6006-6010.
123. Yang, S., B. J. Misner, R. J. Chiu, and, F. L. Jr Meyskens, (2007) Redox effector factor-1, combined with reactive oxygen species, plays an important role in the transformation of JB6 cells. Carcinogenesis 28, 2382-2390.
124. Struthers, L., R. Patel, J. Clark, and, S. Thomas, (1998) Direct detection of 8-oxodeoxyguanosine and 8-oxoguanine by avidin and its analogues. Anal. Biochem. 255, 20-31.
125. Conners, R., E. Hooley, A.-R. Clarke, S. Thomas, and, L. Brady, (2006) Recognition of oxidatively modified bases within the biotin-binding site of avidin. J. Mol. Biol. 357, 263-274.
126. Javeri, A., J. G. Lyons, X. X. Huang, and, G. M. Halliday, (2011) Downregulation of Cockayne syndrome B protein reduces human 8-oxoguanine DNA glycosylase-1 expression and repair of UV radiation-induced 8-oxo-7,8-dihydro-2deoxyguanosine. Cancer Sci. 102, 1651-1658.
127. Kunisada, M., F. Yogianti, K. Sakumi, R. Ono, Y. Nakabeppu, and, C. Nishigori, (2011) Increased expression of versican in the inflammatory response to UVB- and reactive oxygen species-induced skin tumorigenesis. Am. J. Pathol. 179, 3056-3065.
128. Wulff, B. C., J. S. Schick, J. M. Thomas-Ahner, D. F. Kusewitt, D. B. Yarosh, and, T. M. Oberyszyn, (2008) Topical treatment with OGG1 enzyme affects UVB-induced skin carcinogenesis. Photochem. Photobiol. 84, 317-321.
129. Pouget, J.-P., S. Frelon, J.-L. Ravanat, I. Testard, F. Odin, and, J. Cadet, (2002) Formation of modified DNA bases in cells exposed either to gamma radiation or to high-LET particles. Radiat. Res. 157, 589-595.
130. Douki, T., J.-L. Ravanat, J.-P. Pouget, I. Testard, and, J. Cadet, (2006) Minor contribution of direct ionization to DNA base damage induced by heavy ions. Int. J. Radiat. Biol. 82, 119-127.
131. Samson-Thibault, F., G. S. Madugundu, S. Gao, J. Cadet, and, J. R. Wagner, (2012) Profiling cytosine oxidation in DNA by LC-MS/MS. Chem. Res. Toxicol. 25, 1902-1911.
132. Madugundu, G. S., J. Cadet, and, J. R. Wagner, (2014) Hydroxyl-radical-induced oxidation of 5-methylcytosine in isolated and cellular DNA. Nucleic Acids Res. 42, 7450-7460.
133. Cadet, J., and, J. R. Wagner, (2014) Oxidatively generated base damage to cellular DNA by hydroxyl radical and one-electron oxidants: Similarities and differences. Arch. Biochem. Biophys. 557, 47-54.
134. Boorstein, R. J., T. P. Hilbert, J. Cadet, R. P. Cunningham, and, G. W. Teebor, (1989) UV-induced pyrimidine hydrates in DNA are repaired by bacterial and mammalian DNA glycosylase activities. Biochemistry 28, 6164-6170.
135. Douki, T., G. Vadesne-Bauer, and, J. Cadet, (2002) Formation of 2deoxyuridine hydrates upon exposure of nucleosides to gamma radiation and UVC-irradiation of isolated and cellular DNA. Photochem. Photobiol. Sci. 1, 565-569.
136. Jen, J., D. L. Mitchell, R. P. Cunningham, C. A. Smith, J.-S. Taylor, and, J. E. Cleaver, (1997) Ultraviolet irradiation produces novel endonuclease III-sensitive cytosine photoproducts at dipyrimidine sites. Photochem. Photobiol. 65, 323-329.
137. Souza, L. L., I. R. Edurado, M. Pádula, and, A. C. Leitão, (2006) Endonuclease IV and exonuclease III are involved in the repair and mutagenesis of DNA lesions induced by UVB in Escherichia coli. Mutagenesis 21, 125-129.
138. Garinis, G. A., J. R. Mitchell, M. J. Moorhouse, K. Hanada, H. de Waard, D. Vandeputte, J. Jans, K. Brand, M. Smid, P. van der Spek, J. H. J. Hoeijmakers, R. Kanar, and, G. T. J. van der Horst, (2005) Transcriptome analysis reveals cyclobutane pyrimidine dimers as a major source of UV-induced DNA breaks. EMBO J. 24, 3952-3962.
139. Marti, T. M., E. Hefner, L. Feeney, V. Natale, and, J. E. Cleaver, (2006) H2AX phosphorylation within the G1 phase after UV irradiation depends on nucleotide excision repair and not DNA double-strand breaks. Proc. Natl Acad. Sci. USA 103, 9891-9896.
140. Cleaver, J. E., L. Feeney, and, I. Revet, (2011) Phosphorylated H2Ax is not an unambiguous marker for DNA double-strand breaks. Cell Cycle 10, 3223-3224.
141. Cleaver, J. E., (2011) γH2Ax: Biomarker of damage or functional participant in DNA repair "all that glitters is not gold!". Photochem. Photobiol. 87, 1230-1239.
142. Pfaum, M., C. Kielbassa, M. Garmyn, and, B. Epe, (1998) Oxidative DNA damage induced by visible light in mammalian cells: Extent, inhibition by antioxidants and genotoxic effects. Mutat. Res. 408, 137-146.
143. Burrows, C. J., and, J. G. Muller, (1998) Oxidative nucleobase modifications leading to strand scission. Chem. Rev. 98, 1109-1152.
144. Pogozelski, W. K., and, T. D. Tullius, (1998) Oxidative strand scission of nucleic acids: Routes initiated by hydrogen abstraction from the sugar moiety. Chem. Rev. 98, 1089-1108.
145. Dedon, P. C., (2008) The chemical toxicology of 2-deoxyribose oxidation in DNA. Chem. Res. Toxicol. 21, 206-219.
146. Greenberg, M. M., (2012) The formamidopyrimidines: Purine lesions formed in competition with 8-oxopurines from oxidative stress. Acc. Chem. Res. 45, 588-597.
147. Kasai, H., Z. Yamaizumi, M. Berger, and, J. Cadet, (1992) Photosensitized formation of 7,8-dihydro-8-oxo-2deoxyguanosine (8-hydroxy-2deoxyguanosine) in DNA by riboflavin: A non singlet oxygen mediated reaction. J. Am. Chem. Soc. 114, 9692-9694.
148. Rokhlenko, Y., J. Cadet, N. E. Geacintov, and, V. Shafirovich, (2014) Mechanistic aspects of hydration of guanine radical cations in DNA. J. Am. Chem. Soc. 136, 5956-5962.
149. Cadet, J., J. R. Wagner, V. Shafirovich, and, N. E. Geacintov, (2014) One-electron oxidation reactions of purine and pyrimidine bases in cellular DNA. Int. J. Radiat. Biol. 90, 423-432.
150. Ivanchenko, V. A., E. I. Budowsky, N. A. Simukova, N. S. Vul'fson, A. I. Tishchenko, and, D. B. Askerov, (1977) The photochemistry of purine components of nucleic acids II. Photolysis of deoxyguanosine. Nucleic Acids Res. 4, 955-968.
151. Ravanat, J.-L., S. Sauvaigo, S. Caillat, G. R. Martinez, M. H. Medeiros, P. Di Mascio, A. Favier, and, J. Cadet, (2004a) Singlet oxygen-mediated damage to cellular DNA determined by the comet assay associated with DNA repair enzymes. Biol. Chem. 385, 17-20.
152. Cadet, J., T. Douki, J.-L. Ravanat, and, P. Di Mascio, (2009) Sensitized formation of oxidatively generated damage to cellular DNA by UVA radiation. Photochem. Photobiol. Sci. 8, 903-911.
153. Bishop, S. M., M. Malone, D. Phillips, A. W. Parker, and, M. C. R. Symons, (1994) Singlet oxygen sensitisation by excited state DNA. J. Chem. Soc., Chem. Commun. 871-872.
154. Mohammad, T., and, H. Morrison, (1996) Evidence for the photosensitized formation of singlet oxygen by UVB irradiation of 2deoxyguanosine 5monophosphate. J. Am. Chem. Soc. 118, 1221-1222.
155. Tyrrell, R. M., and, S. M. Keyse, (1990) New trends in photobiology. The interaction of UVA radiation with cultured cells. J. Photochem. Photobiol. B 4, 349-361.
156. de Laat, A., J. C. van der Leun, and, F. R. de Gruijl, (1997) Carcinogenesis induced by UVA (365-nm) radiation: The dose-time dependence of tumor formation in hairless mice. Carcinogenesis 18, 1013-1020.
157. Sander, C. S., H. Chang, F. Hamm, P. Elsner, and, J. J. Thiele, (2004) Role of oxidative stress and the antioxidant network in cutaneous carcinogenesis. Int. J. Dermatol. 43, 326-335.
158. Setlow, R. B., E. Grist, K. Thompson, and, A. D. Woodhead, (1993) Wavelengths effective in induction of malignant melanoma. Proc. Natl Acad. Sci. USA 90, 6666-6670.
159. Wang, S. Q., R. Setlow, M. Berwick, D. Polsky, A. A. Marghoob, A. W. Kopf, and, R. S. Bart, (2001) Ultraviolet A and melanoma: A review. J. Am. Acad. Dermatol. 44, 837-846.
160. Mitchell, D. L., A. A. Fernandez, R. S. Nairn, R. Garcia, L. Paniker, D. Trono, H. D. Thames, and, I. Gimenez-Conti, (2010) Ultraviolet A does not induce melanomas in a Xiphophorus hybrid fish model. Proc. Natl Acad. Sci. USA 107, 9329-9334.
161. Fernandez, A. A., L. Paniker, R. Garcia, and, D. L. Mitchell, (2012) Recent advances in sunlight-induced carcinogenesis using the Xiphophorus melanoma model. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 155, 64-70.
162. Pouget, J.-P., T. Douki, M.-J. Richard, and, J. Cadet, (2000) DNA damage induced in cells by gamma and UVA radiation as measured by HPLC/GC-MS and HPLC-EC and Comet assay. Chem. Res. Toxicol. 13, 541-549.
163. Cortat, B., C. C. Garcia, A. Quinet, A. P. Schuch, K. M. de Lima-Bessa, and, C. F. Menck, (2013) The relative roles of DNA damage induced by UVA irradiation in human cells. Photochem. Photobiol. Sci. 12, 1483-1495.
164. Fisher-Nilsen, A., S. Loft, and, K. G. Jensen, (1993) Effect of ascorbate and 5-aminosalicylic acid on light-induced 8-hydroxydeoxyguanosine formation in V79 Chinese hamster cells. Carcinogenesis 14, 2431-2433.
165. Warmer, W. G., and, R. R. Wei, (1997) In vitro photooxidation of nucleic acids by ultraviolet A radiation. Photochem. Photobiol. 65, 560-563.
166. Kvam, E., and, R. M. Tyrrell, (1997) Induction of oxidative DNA base damage in human skin cells by UV and near visible radiation. Carcinogenesis 18, 2379-2384.
167. Zhang, X., B. S. Rosenstein, Y. Wang, M. Lebwohl, D. L. Mitchell, and, H. Wie, (1997) Induction of 8-oxo-7,8-dihydro-2deoxyguanosine by ultraviolet radiation in calf thymus DNA and HeLa cells. Photochem. Photobiol. 65, 119-124.
168. Duez, P., M. Hanocq, and, J. Dubois, (2001) Photodynamic DNA damage mediated by delta-aminolevulinic acid-induced porphyrins. Carcinogenesis 22, 771-778.
169. Negishi, T., K. Kawai, R. Arakawa, S. Higashi, T. Nakamura, M. Watanabe, H. Kasai, and, K. Fujikawa, (2007) Increased levels of 8-hydroxy-2deoxyguanosine in Drosophila larval DNA after irradiation with 364-nm laser light but not with X-rays. Photochem. Photobiol. 83, 658-663.
170. Besaratinia, A., T. W. Synold, B. Xi, and, G. P. Pfeifer, (2004) G-to-T transversions and small tandem base deletions are the hallmark of mutations induced by ultraviolet a radiation in mammalian cells. Biochemistry 43, 8169-8177.
171. Besaratinia, A., T. W. Synold, H. H. Chen, C. Chang, B. Xi, A. D. Riggs, and, G. P. Pfeifer, (2005) DNA lesions induced by UV A1 and B radiation in human cells: Comparative analyses in the overall genome and in the p53 tumor suppressor gene. Proc. Natl Acad. Sci. USA 102, 10058-10063.
172. Mouret, S., A. Forestier, and, T. Douki, (2012) The specificity of UVA-induced DNA damage in human melanocytes. Photochem. Photobiol. Sci. 11, 155-162.
173. Campalans, A., R. Amouroux, A. Bravard, B. Epe, and, J. P. Radicella, (2007) UVA irradiation induces relocalisation of the DNA repair protein hOGG1 to nuclear speckles. J. Cell Sci. 120, 23-32.
174. Lipinski, L. J., N. Hoehr, S. J. Mazur, G. L. Dianov, S. Sentürker, M. Dizdaroglu, and, V. A. Bohr, (1999) Repair of oxidative DNA base lesions induced by fluorescent light is defective in xeroderma pigmentosum group A cells. Nucleic Acids Res. 27, 3153-3158.
175. Wischermann, K., S. Popp, S. Moshir, K. Scharfetter-Kochanek, M. Wlaschek, F. de Gruijl, W. Hartschuh, R. Greinert, B. Volkmer, A. Faust, A. Rapp, P. Schmezer, and, P. Boukamp, (2008) UVA radiation causes DNA strand breaks, chromosomal aberrations and tumorigenic transformation in HaCaT skin keratinocytes. Oncogene 27, 4269-4280.
176. Wischermann, K., P. Boukamp, and, P. Schmezer, (2007) Improved alkaline comet assay protocol for adherent HaCaT keratinocytes to study UVA-induced DNA damage. Mutat. Res. 630, 122-128.
177. Fell, L. J., N. D. Paul, and, T. J. McMillan, (2002) Role for non-homologous end-joining in the repair of UVA-induced DNA damage. Int. J. Radiat. Biol. 78, 1023-1027.
178. Rapp, A., and, K. O. Greulich, (2004) After double-strand break induction by UV-A, homologous recombination and nonhomologous end joining cooperate at the same DSB if both systems are available. J. Cell Sci. 117, 4935-4945.
179. Limoli, C. K., E. Giedzinski, W. M. Bonner, and, J. E. Cleaver, (2002) UV-induced replication arrest in the xeroderma pigmentosum variant leads to DNA double-strand breaks, gamma-H2AX formation, and Mre11 relocalization. Proc. Natl Acad. Sci. USA 99, 233-238.
180. Rizzo, J. L., J. Dunn, A. Rees, and, T. M. Rünger, (2011) No formation of DNA double-strand breaks and no activation of recombination repair with UVA. J. Invest. Dermatol. 131, 1139-1148.
181. Greinert, R., B. Volkmer, S. Henning, E. W. Ereitbart, K. O. Greulich, M. C. Cardoso, and, A. Rapp, (2012) UVA-induced DNA double-strand breaks result from the repair of clustered oxidative DNA damages. Nucleic Acids Res. 40, 10263-10273.
182. Georgakilas, A. G., P. O'Neill, and, R. D. Stewart, (2013) Induction and repair of clustered DNA lesions: What do we know so far? Radiat. Res. 180, 100-109.
183. Cadet, J., and, T. Douki, (2011) Oxidatively generated damage to DNA by UVA radiation in cells and human skin. J. Invest. Dermatol. 131, 1005-1007.
184. Fang, X., N. Ide, S. I. Higashi, Y. Kamei, T. Toyooka, Y. Ibuki, K. Kawai, H. Kasai, K. Okamoto, S. Arimoto-Kobayashi, and, T. Negishi, (2014) Somatic cell mutations caused by 365 nm LED-UVA due to DNA double-strand breaks through oxidative damage. Photochem. Photobiol. Sci. 13, 1338-1346.
185. Epe, B., (2012) DNA damage spectra induced by photosensitization. Photochem. Photobiol. Sci. 11, 98-106.
186. 18O-labeled singlet oxygen for mechanistic studies. J. Am. Chem. Soc. 122, 10212-10213.
187. 18O]-Peroxides: Synthesis and biological applications. In Functional Groups in Organic Chemistry-The Chemistry of Peroxides, Vol. 3 (Edited by, A. Greer, and, J. F. Liebman,), pp. 769-804. Wiley and Sons, Chichester, UK.
188. Ravanat, J.-L., P. Di Mascio, G. R. Martinez, and, J. Cadet, (2000) Singlet oxygen induces oxidation of cellular DNA. J. Biol. Chem. 275, 40601-40604.
189. Ravanat, J.-L., G. R. Martinez, M. H. G. Medeiros, P. Di Mascio, and, J. Cadet, (2004) Mechanistic aspects of the oxidation of DNA constituents mediated by singlet molecular oxygen. Arch. Biochem. Biophys. 423, 23-30.
190. Di Mascio, P., E. J. Bechara, M. H. Medeiros, K. Briviba, and, H. Sies, (1991) Singlet oxygen induced single-strand breaks in plasmid pBR322 DNA: The enhancing effect of thiols. Biochim. Biophys. Acta 1088, 409-412.
191. Sheu, C., and, C. S. Foote, (1995) Reactivity toward singlet oxygen of a 7,8-dihydro-8-oxoguanosine ("8-hydroxyguanosine") formed by photooxidation of a guanosine derivative. J. Am. Chem. Soc. 117, 6439-6442.
192. Duarte, V., D. Gasparutto, M. Jaquinod, J.-L. Ravanat, and, J. Cadet, (2000) Oxaluric acid as the major product of singlet oxygen-mediated oxidation of 8-oxo-7,8-dihydroguanine in DNA. J. Am. Chem. Soc. 122, 12622-12628.
193. Buchko, G. W., and, J. Cadet, (2006) Identification of the alpha and beta anomers of 1-(2-deoxy-D-erythro-pentofuranosyl)-oxaluric acid at the site of riboflavin-mediated photooxidation of guanine in 2deoxyguanosine and thymidylyl-(35)-2deoxyguanosine. Photochem. Photobiol. 82, 191-199.
194. Otteneder, M. B., C. G. Knutson, J. S. Daniels, M. Hashim, B. C. Crews, R. P. Remmel, H. Wang, C. Rizzo, and, L. J. Marnett, (2006) In vivo oxidative metabolism of a major peroxidation-derived DNA adduct, M1dG. Proc. Natl Acad. Sci. USA 103, 6665-6669.
195. Nair, U., H. Bartsch, and, J. Nair, (2007) Lipid peroxidation-induced DNA damage in cancer-prone inflammatory diseases: A review of published adduct types and levels in humans. Free Radic. Biol. Med. 43, 1109-1120.
196. Blair, I. A., (2008) DNA adducts with lipid peroxidation products. J. Biol. Chem. 283, 15545-15549.
197. Huang, H., I. D. Kozekov, A. Kozekova, H. Wang, R. S. Lloyd, C. J. Rizzo, and, M. P. Stone, (2010a) DNA cross-link induced by trans-4-hydroxynonenal. Environ. Mol. Mutagen. 51, 625-634.
198. Voulgaridou, G. P., I. Anestopoulos, R. Franco, M. I. Panayiotidis, and, A. Pappa, (2011) DNA damage induced by endogenous aldehydes: Current state of knowledge. Mutat. Res. 711, 13-27.
199. Douki, T., F. Odin, S. Caillat, A. Favier, and, J. Cadet, (2004) Predominance of the 1, N2-propano 2deoxyguanosine adduct among 4-hydroxy-2-nonenal-induced DNA lesions. Free Radic. Biol. Med. 37, 62-70.
200. Liu, X., M. A. Lovell, and, B. C. Lynn, (2006) Detection and quantification of endogenous cyclic DNA adducts derived from trans-4-hydroxy-2-nonenal in human brain tissue by isotope dilution capillary liquid chromatography nanoelectrospray tandem mass spectrometry. Chem. Res. Toxicol. 19, 710-718.
201. Medeiros, M. H., (2009) Exocyclic DNA adducts as biomarkers of lipid oxidation and predictors of disease. Challenges in developing sensitive and specific methods for clinical studies. Chem. Res. Toxicol. 22, 419-425.
202. Garcia, C. C., F. P. Freitas, P. Di Mascio, and, M. H. Medeiros, (2010) Ultrasensitive simultaneous quantification of 1, N2-etheno-2deoxyguanosine and 1, N2-propano-2deoxyguanosine in DNA by an online liquid chromatography-electrospray tandem mass spectrometry assay. Chem. Res. Toxicol. 23, 1245-1255.
203. Szabõ, C., H. Ischiropoulos, and, R. Radi, (2007) Peroxynitrite: Biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov. 6, 662-680.
204. Carballal, S., S. Bartesaghi, and, R. Radi, (2014) Kinetic and mechanistic considerations to assess the biological fate of peroxynitrite. Biochim. Biophys. Acta 1840, 768-780.
205. Denicola, A., B. A. Freeman, M. Trujillo, and, R. Radi, (1996) Peroxynitrite reaction with carbon dioxide/bicarbonate: Kinetics and influence on peroxynitrite-mediated oxidations. Arch. Biochem. Biophys. 333, 49-58.
206. Bonini, M. G., R. Radi, G. Ferrer-Sueta, A. M. Ferreira, and, O. Augusto, (1999) Direct EPR detection of the carbonate radical anion produced from peroxynitrite and carbon dioxide. J. Biol. Chem. 274, 10802-10806.
207. Sugiura, H., and, M. Ichinose, (2011) Nitrative stress in inflammatory lung diseases. Nitric Oxide 25, 138-144.
208. Lee, Y. A., B. H. Yun, S. K. Kim, Y. Margolin, P. C. Dedon, N. E. Geacintov, and, V. Shafirovich, (2007) Mechanisms of oxidation of guanine in DNA by carbonate radical anion, a decomposition product of nitrosoperoxycarbonate. Chemistry 13, 4571-4581.
209. Crean, C., Y. Uvaydov, N. E. Geacintov, and, V. Shafirovich, (2008) Oxidation of single-stranded oligonucleotides by carbonate radical anions: Generating intrastrand cross-links between guanine and thymine bases separated by cytosines. Nucleic Acids Res. 36, 742-755.
210. Yun, B. H., N. E. Geacintov, and, V. Shafirovich, (2011) Generation of guanine-thymidine cross-links in DNA by peroxynitrite/carbon dioxide. Chem. Res. Toxicol. 24, 1144-1152.
211. Madugundu, G. S., J. R. Wagner, J. Cadet, K. Kropachev, B. H. Yun, N. E. Geacintov, and, V. Shafirovich, (2013) Generation of guanine-thymine cross-links in human cells by one-electron oxidation mechanisms. Chem. Res. Toxicol. 26, 1031-1033.
212. Silerme, S., L. Bobyk, M. Taverna-Porro, C. Cuier, C. Saint-Pierre, and, J.-L. Ravanat, (2014) DNA-polyamine crosslinks generated upon one electron oxidation of DNA. Chem. Res. Toxicol. 27, 1011-1018.
213. Perrier, S., J. Hau, D. Gasparutto, J. Cadet, A. Favier, and, J.-L. Ravanat, (2006) Characterization of lysine-guanine cross-links upon one-electron oxidation of a guanine-containing oligonucleotide in the presence of a trilysine peptide. J. Am. Chem. Soc. 128, 5703-5710.
214. Brem, R., and, P. Karran, (2012a) Multiple forms of DNA damage caused by UVA photoactivation of DNA 6-thioguanine. Photochem. Photobiol. 88, 5-13.
215. Guerange, Q., A. Kia, D. Frith, and, P. Karran, (2011) Crosslinking of DNA repair and replication proteins to DNA in cells treated with 6-thioguanine and UVA. Nucleic Acids Res. 39, 5057-5066.
216. Brem, R., I. Daehn, and, P. Karran, (2011) Efficient DNA interstrand crosslinking by 6-thioguanine and UVA radiation. DNA Repair (Amst) 10, 869-876.
217. Brem, R., and, P. Karran, (2012b) Oxidation-mediated DNA cross-linking contributes to the toxicity of 6-thioguanine in human cells. Cancer Res. 72, 4787-4795.
218. Ikehata, H., J. Kumagai, T. Ono, and, A. Morita, (2013) Solar-UV-signature mutation prefers TCG to CCG: Extrapolative consideration from UVA1-induced mutation spectra in mouse skin. Photochem. Photobiol. Sci. 12, 1319-1327.