Photosensitized reactions of oxidative damage to biomolecules: role in genotoxic and cytotoxic processes
https://doi.org/10.55959/MSU0137-0952-16-79-3-1
Abstract
Photosensitized oxidation reactions of biomolecules such as lipids, proteins, DNA initiate cytotoxic and genotoxic processes that are mediated by endogenous sensitizers under effect of ultraviolet radiation in the range A (UVA, 320–400 nm) on living systems. The photosensitization reactions are oxygen-dependent and depending upon primary mechanism are divided into type I and type II. Type I reactions involve electron transfer between photoexcited sensitizer and biomolecule with the formation of radical states. The interaction of radical cation of biomolecule with oxygen leads to the production of its final oxidation products, and electron transfer between radical anion of sensitizer and oxygen generates superoxide anion radical (O2•−) with following production of H2O2 and the highly reactive hydroxyl radical (•OH). In contrast to radical mechanism of type I reactions, primary mechanism of type II reactions involves energy transfer from photoexcited sensitizer to oxygen (O2) that leads to the formation of singlet oxygen (1O2, 1Δg), which is much more reactive in relation to biomolecule oxidation than O2. Current knowledge on mechanisms of initial stages of the type I and type II reactions as well as their involvement in the oxidized degradation of biomolecules such as DNA, proteins and lipids are expounded in detail in present review. Sensitized properties of pterins, riboflavin and protoporphyrin IX with characteristic peculiarities of action of each of these photosensitizers are also considered. The considerable attention is given to processes of photosensitized damage to DNA and discussing the role of different DNA photoproducts in initiating genotoxic processes including carcinogenesis in human skin.
Keywords
photosensitized reactions,
oxidized degradation of biomolecules,
DNA photoproducts,
genotoxic processes,
cellular photosensitizers,
UVA photons
Supporting agencies: This study was performed under the state assignment of Moscow State University, project number 121032500058-7.
About the Author
G. Ya. Fraikin
Lomonosov Moscow State University
Russian Federation
Russian Federation
Department of Biophysics, Biological Faculty
Leninskiye Gory, 1–12, Moscow, 119234
References
1. Baptista M.S., Cadet J., Greer A., Thomas A.H. Photosensitization reactions of biomolecules: definition, targets and mechanisms. Photochem. Photobiol. 2021;97(6):1456–1483.
2. Pfeifer G.P., Besaratinia A. UV wavelength- dependent DNA damage and human non-melanoma and melanoma skin cancer. Photochem. Photobiol. Sci. 2012;11(1):90–97.
3. Fraikin G.Ya., Belenikina N.S., Rubin A.B. Damaging and defense processes induced in plant cells by UVB radiation. Biol. Bull. 2018;45(6):519–527.
4. Markovitsi D., Sage E., Lewis F.D., Davies J. Interaction of UV radiation with DNA. Photochem. Photobiol. Sci. 2013;12(8):1256–1258.
5. Cadet J., Douki T. Formation of UV-induced DNA damage contributing to skin cancer development. Photochem. Photobiol. Sci. 2018;17(12):1816–1841.
6. Mullenders L.H.F. Solar UV damage to cellular DNA: from mechanisms to biological effects. Photochem. Photobiol. Sci. 2018;17(12):1842–1852.
7. Johann to Berens P., Molinier J. Formation and recognition of UV-induced DNA damage within genome complexity. Int. J. Mol. Sci. 2020;21(18):6689.
8. Frances-Monerris A., Hognon C., Miranda M.A., Lhiaubet-Vallet V., Monari A. Triplet photosensitization mechanism of thymine by an oxidized nucleobase: from a dimeric model to DNA environment. Phys. Chem. Chem. Phys. 2018;20(40):25666–25675.
9. Gontcharov J., Liu L., Pilles B.M., Carell T., Schreier W.J., Zinth W. Triplet-induced lesion formation at CpT and TpC sites in DNA. Chem. Eur. J. 2019;25(66):15164–15172.
10. Laustriat G. Molecular mechanisms of photosensitization. Biochimie. 1986;68(6):771–778.
11. Baptista M.S., Cadet J., Di Mascio P., Ghogare A.A., Greer A., Hamblin M.R., Lorente C., Nunez S.C., Ribeiro M.S., Thomas A.H., Vignoni M., Yoshimura T.M. Type I and type II photosensitized oxidation reactions: guidelines and mechanistic pathways. Photochem. Photobiol. 2017;93(4):912–919.
12. Krasnovsky A.A., Jr. Photodynamic action and singlet oxygen. Biophysics. 2004;49(2):289–306.
13. Fraikin G.Ya. Photosensory and signaling properties of cryptochromes. Moscow Univ. Biol. Sci. Bull. 2022;71(2):54–63.
14. Fraikin G.Ya., Strakhovskaya M.G., Rubin A.B. Biological photoreceptors of light-dependent regulatory processes. Biochemistry (Mosc.). 2013;78(11):1238–1253.
15. Vechtomova Y.L., Telegina T.A., Kritsky M.S. Evolution of proteins of the DNA photolyase/cryptochrome family. Biochemistry (Mosc.). 2020;85(Suppl.1):S131–S153.
16. Fuentes-Lemus E., Mariotti M., Reyes J., Leinisch F., Hagglund P., Silva E., Davies M.J., Lopez- Alarcon C. Photooxidation of lysozyme triggered by riboflavin is O2-dependent, occurs via mixed type 1 and type 2 pathways, and results in inactivation, site-specific damage and intra-and inter-molecular cross-links. Free. Radic. Biol. Med. 2020;152:61–73.
17. Perrier S., Hau J., Gasparutto D., Cadet J., Favier A., Ravanat J.-L. Characterization of lysine-guanine cross-links upon one-electron oxidation of a guaninecontaining oligonucleotide in the presence of a trilysine peptide. J. Am. Chem. Soc. 2006;128(17):5703–5710.
18. Chan C.H., Monari A., Ravanat J.-L., Dumont E. Probing interaction of a trilysine peptide with DNA underlying formation of guanine-lysine cross-links: Insights from molecular dynamics. Phys. Chem. Chem. Phys. 2019;21(42):23418–23424.
19. Di Mascio P., Martinez G.R., Miyamoto S., Ronsein G.E., Medeiros M.H.G., Cadet J. Singlet molecular oxygen reactions with nucleic acids, lipids, and proteins. Chem. Rev. 2019;119(3):2043–2086.
20. Ravanat J.-L., Dumont E. Reactivity of singlet oxygen with DNA, an update. Photochem. Photobiol. 2022;98(3):564–571.
21. Girotti A.W. Photosensitized oxidation of membrane lipids. J. Photochem. Photobiol. B: Biol. 2001;63(1–3):103–113.
22. Oliveros E., Dantola M.L., Vignoni M., Thomas A.H., Lorente C. Production and quenching of reactive oxygen species by pterin derivatives, an intriguing class of biomolecules. Pure Appl. Chem. 2011;83(4):801–811.
23. Buglak A.A., Telegina T.A., Lyudnikova T.A., Vechtomova Y.L., Kritsky M.S. Photooxidation of tetrahydrobiopterin under UV irradiation: possible pathways and mechanisms. Photochem. Photobiol. 2014;90(5):1017–1026.
24. Buglak A.A., Telegina T.A., Vechtomova Y.L., Kritsky M.S. Autooxidation and photooxidation of tetrahydrobiopterin: a theoretical study. Free Radic. Res. 2021;55(5):499–509.
25. Thomas A.H., Lorente C., Capparelli A.L., Martinez C.G., Braun A.M., Oliveros E. Singlet oxygen (1Δg) production by pterin derivatives in aqueous solutions. Photochem. Photobiol. Sci. 2003;2(3):245–250.
26. Lorente C., Serrano M.P., Vignoni M., Dantola M.L., Thomas A.H. A model to understand type I oxidations of biomolecules photosensitized by pterins. J. Photochem. Photobiol. 2021;7:100045.
27. Serrano M.P., Lorente C., Vieyra F.E.M., Borsarelli C.D., Thomas A.H. Photosensitizing properties of biopterin and its photoproducts using 2ʹ-deoxyguanosine 5ʹ-monophosphate as an oxidizable target. Phys. Chem. Chem. Phys. 2012;14(33):11657–11665.
28. Serrano M.P., Lorente C., Borsarelli C.D., Thomas A.H. Unraveling the degradation mechanism of purine nucleotides photosensitized by pterins: the role of charge-transfer steps. ChemPhysChem. 2015;16(10):2244–2252.
29. Serrano M.P., Vignoni M., Lorente C., Vicendo P., Oliveros E., Thomas A.H. Thymidine radical formation via one-electron transfer oxidation photoinduced by pterin: mechanism and products characterization. Free Radic. Biol. Med. 2016;96:418–431.
30. Estebanez S., Lorente C., Tosato M.G., Miranda M.A., Marin M.L., Lhiaubet-Vallet V., Thomas A.H. Photochemical formation of a fluorescent thymidine–pterin adduct in DNA. Dyes Pigm. 2019;160:624–632.
31. Cadet J., Douki T., Ravanat J.-L. Oxidatevely generated damage to cellular DNA by UVB and UVA radiation. Photochem. Photobiol. 2015;91(1):140–155.
32. Cadet J., Davies K.J.A., Medeiros M.H., Di Mascio P., Wagner J.R. Formation and repair of oxidatively generated damage in cellular DNA. Free Radic. Biol. Med. 2017;107:13–34.
33. Shumarina A.O., Strakhovskaya M.G., Turovetskii V.B., Fraikin G.Ya. Photodynamic damage to yeast subcellular organelles induced by elevated levels of endogenous protoporphyrin IX. Microbiology. 2003;72(4):434–437.
34. Fraikin G.Ya., Strakhovskaya M.G., Rubin A.B. The role of membrane-bound porphyrin-type compound as endogenous sensitizer in photodynamic damage to yeast plasma membranes. J. Photochem. Photobiol. B: Biol. 1996;34(2–3):129–135.
35. Strakhovskaya M.G., Shumarina A.O., Fraikin G.Ya., Rubin A.B. Fluorescence photobleaching of endogenous protoporphyrin IX in Saccharomyces cerevisiae cells. Biophysics. 2002;47(5):791–796.
36. Blair I.A. DNA adducts with lipid peroxidation products. J. Biol. Chem. 2008;283(23):15545–15549.
37. Selby C.P., Lindsey-Boltz L.A. Li W., Sancar A. Molecular mechanisms of transcription-coupled repair. Annu. Rev. Biochem. 2023;92:115–144.
38. Panigrahi A., Vemuri H., Aggarwal M., Pitta K., Krishnan M. Sequence specificity, energetic and mechanism of mismatch recognition by DNA damage sensing protein Rad4/XPC. Nucleic Acids Res. 2020;48(5):2246–2257.
39. Xu J., Lahiri I., Wang W., Wier A., Cianfrocco M.A., Chong J., Hare A.A., Dervan P.B., DiMaio F., Leschziner A.E., Wang D. Structural basis for the initiation of eukaryotic transcription-coupled DNA repair. Nature. 2017;551(7682):653–657.
40. Mei Kwei J.S., Kuraoka I., Horibata K., Ubukata M., Kobatake E., Iwai S., Handa H., Tanaka K. Blockage of RNA polymerase II at a cyclobutane pyrimidine dimer and 6-4 photoproduct. Biochem. Biophys. Res. Commun. 2004;320(4):1133–1138.
41. Brueckner F., Hennecke U., Carell T., Cramer P. CPD damage recognition by transcribing RNA polymerase II. Science. 2007;315(5813):859–862.
42. Walmacq C., Cheung A.C.M., Kireeva M.L., Lubkowska L., Ye C., Gotte D., Strathern J.N., Carell T., Cramer P., Kashlev M. Mechanism of translesion transcription by RNA polymerase II and its role in cellular resistance to DNA damage. Mol. Cell. 2012;46(1):18–29.
43. Tkachev V., Menshchikova E., Zenkov N.K. Mechanism of the Nrf2/Keap 1/ARE signaling system. Biochemistry (Mosc.). 2011;76(4):407–422.
44. Tekutskaya Е.E., Il’chenko G.P., Dorohova A.S., Malyshko V.V., Baryshev M.G., Dzhimak S.S. 8-Oxoguanine-DNA-glycosylase gene polymorphism and the effects of an alternating magnetic field on the sensitivity of peripheral blood. Front. Biosci. (Landmark Ed.). 2023;28(10):252.
45. Tewari A., Grage M.M.L., Harrison G.I., Sarkany R., Young A.R. UVA1 is skin deep: molecular and clinical implications. Photochem. Photobiol. Sci. 2013;12(1):95–103.
46. Halliday G.M., Cadet J. Itʹs all about position: the basal layer of human epidermis is particularly susceptible to different types of sunlight-induced DNA damage. J. Invest. Dermatol. 2012;132(2):265–267.
47. Delinasios G.J., Karbaschi M., Cooke M.S., Young A.R. Vitamin E inhibits the UVA1 induction of “light” and “dark” cyclobutane pyrimidine dimers, and oxidatively generated DNA damage, in keratinocytes. Sci. Rep. 2018;8(1):423.
48. Lawrence K.P., Douki T., Sarkany R.P.E., Acker S., Herzog B., Young A.R. The UV/Visible radiation boundary region (385–405 nm) damages skin cells and induces “dark” cyclobutane pyrimidine dimers in human skin in vivo. Sci. Rep. 2018;8(1):12722.
49. Mouret S., Forestier A., Douki T. The specificity of UVA-induced DNA damage in human melanocytes. Photochem. Photobiol. Sci. 2012;11(1):155–162.
50. Noonan F., Zaidi M.R., Wolnicka–Glubisz A., Anver M.R., Bahn J., Wielgus A., Cadet J., Douki T., Mouret S., Tucker M.A., Popratiloff A., Merlino G., De Fabo E.C. Melanoma induction by UVA but not UVB radiation requires melanin. Nat. Commun. 2012;3(1):884.
51. Premi S., Wallisch S., Mano C.M., Weiner A.B., Bacchiocchi N., Wakamatsu K., Bechara E.J., Halaban R., Douki T., Brash D.E. Photochemistry. Chemiexcitation of melanin derivatives induces DNA photoproducts long after UV exposure. Science. 2015;347(6224):842–847.
52. Premi S., Brash D.E. Chemical excitation of electrons: a dark path to melanoma. DNA Repair (Amst.). 2016;44:169–177.
53. Premi S., Brash D.E. Unanticipated role of melanin in causing carcinogenic cyclobutane pyrimidine dimers. Mol. Cell. Oncol. 2016;3(1):e1033588.
54. Fajuyigbe D., Douki T., van Dijk A., Sarkany R.P.E., Young A.R. Dark cyclobutane pyrimidine dimers are formed in the epidermis of Fizpatrick skin types I/II and VI in vivo after exposure to solar-simulated radiation. Pigment Cell Melanoma Res. 2021;34(3):575–584.
Review
For citations:
Fraikin G.Ya. Photosensitized reactions of oxidative damage to biomolecules: role in genotoxic and cytotoxic processes. Vestnik Moskovskogo universiteta. Seriya 16. Biologiya. 2024;79(3):167-183. (In Russ.) https://doi.org/10.55959/MSU0137-0952-16-79-3-1
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