It is well known that biological systems, such as microorganisms, plants, and animals, including human beings, form spontaneous electronically excited species through oxidative metabolic processes. Though the mechanism responsible for the formation of electronically excited species is still not clearly understood, several lines of evidence suggest that reactive oxygen species (ROS) are involved in the formation of electronically excited species. This review attempts to describe the role of ROS in the formation of electronically excited species during oxidative metabolic processes. Briefly, the oxidation of biomolecules, such as lipids, proteins, and nucleic acids by ROS initiates a cascade of reactions that leads to the formation of triplet excited carbonyls formed by the decomposition of cyclic (1,2-dioxetane) and linear (tetroxide) high-energy intermediates. When chromophores are in proximity to triplet excited carbonyls, the triplet-singlet and triplet-triplet energy transfers from triplet excited carbonyls to chromophores result in the formation of singlet and triplet excited chromophores, respectively. Alternatively, when molecular oxygen is present, the triplet-singlet energy transfer from triplet excited carbonyls to molecular oxygen initiates the formation of singlet oxygen. Understanding the mechanism of the formation of electronically excited species allows us to use electronically excited species as a marker for oxidative metabolic processes in cells.

Department of Biophysics Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Šlechtitelů 27 783 71 Olomouc Czech Republic

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Halliwell B., Gutteridge J.M.C. Free Radical in Biology and Medicine. Oxford University Press; New York, NY, USA: 2007. p. 704.

Halliwell B. Free radicals and antioxidants-Quo vadis? Trends Pharmacol. Sci. 2011;32:125–130. doi: 10.1016/j.tips.2010.12.002. PubMed DOI

Hawkins C.L., Davies M.J. Generation and propagation of radical reactions on proteins. Biochim. Biophys. Acta Bioenerget. 2001;1504:196–219. doi: 10.1016/S0005-2728(00)00252-8. PubMed DOI

Tulah A.S., Birch-Machin M.A. Stressed out mitochondria: The role of mitochondria in ageing and cancer focussing on strategies and opportunities in human skin. Mitochondrion. 2013;13:444–453. doi: 10.1016/j.mito.2012.11.007. PubMed DOI

Kroeller-Schoen S., Steven S., Kossmann S., Scholz A., Daub S., Oelze M., Xia N., Hausding M., Mikhed Y., Zinssius E., et al. Molecular Mechanisms of the Crosstalk Between Mitochondria and NADPH Oxidase Through Reactive Oxygen Species-Studies in White Blood Cells and in Animal Models. Antioxid. Redox Signal. 2014;20:247–266. doi: 10.1089/ars.2012.4953. PubMed DOI PMC

Radi R. Peroxynitrite, a Stealthy Biological Oxidant. J. Biol. Chem. 2013;288:26464–26472. doi: 10.1074/jbc.R113.472936. PubMed DOI PMC

Bartesaghi S., Radi R. Fundamentals on the biochemistry of peroxynitrite and protein tyrosine nitration. Redox Biol. 2018;14:618–625. doi: 10.1016/j.redox.2017.09.009. PubMed DOI PMC

Radi R. Oxygen radicals, nitric oxide, and peroxynitrite: Redox pathways in molecular medicine. Proc. Natl. Acad. Sci. USA. 2018;115:5839–5848. doi: 10.1073/pnas.1804932115. PubMed DOI PMC

Gutteridge J.M.C., Halliwell B. Free radicals and antioxidants in the year 2000—A historical look to the future. Ann. N. Y. Acad. Sci. 2000;899:136–147. doi: 10.1111/j.1749-6632.2000.tb06182.x. PubMed DOI

Halliwell B., Gutteridge J.M.C. The definition and measurement of antioxidants in biological systems. Free Radic. Biol. Med. 1995;18:125–126. doi: 10.1016/0891-5849(95)91457-3. PubMed DOI

Hellemans L., Corstjens H., Neven A., Declercq L., Maes D. Antioxidant enzyme activity in human stratum corneum shows seasonal variation with an age-dependent recovery. J. Investig. Dermatol. 2003;120:434–439. doi: 10.1046/j.1523-1747.2003.12056.x. PubMed DOI

Auf Dem Keller U., Kumin A., Braun S., Werner S. Reactive oxygen species and their detoxification in healing skin wounds. J. Investig. Dermatol. Symp. Proc. 2006;11:106–111. doi: 10.1038/sj.jidsymp.5650001. PubMed DOI

Darvin M.E., Patzelt A., Knorr F., Blume-Peytavi U., Sterry W., Lademann J. One-year study on the variation of carotenoid antioxidant substances in living human skin: Influence of dietary supplementation and stress factors. J. Biomed. Opt. 2008;13:044028. doi: 10.1117/1.2952076. PubMed DOI

Tiwari S., Mishra P.C. Urocanic acid as an efficient hydroxyl radical scavenger: A quantum theoretical study. J. Mol. Model. 2011;17:59–72. doi: 10.1007/s00894-010-0699-3. PubMed DOI

Linton S., Davies M.J., Dean R.T. Protein oxidation and ageing. Exp. Gerontol. 2001;36:1503–1518. doi: 10.1016/S0531-5565(01)00136-X. PubMed DOI

Celaje J.A., Zhang D., Guerrero A.M., Selke M. Chemistry of trans-Resveratrol with Singlet Oxygen: 2+2 Addition, 4+2 Addition, and Formation of the Phytoalexin Moracin M. Org. Lett. 2011;13:4846–4849. doi: 10.1021/ol201922u. PubMed DOI

Jacobson M.D. Reactive oxygen species and programmed cell death. Trends Biochem. Sci. 1996;21:83–86. doi: 10.1016/S0968-0004(96)20008-8. PubMed DOI

Bennett M.F., Robinson M.K., Baron E.D., Cooper K.D. Skin immune systems and inflammation: Protector of the skin or promoter of aging? J. Investig. Dermatol. Symp. Proc. 2008;13:15–19. doi: 10.1038/jidsymp.2008.3. PubMed DOI

Cilento G., Adam W. From free radicals to electronically excited species. Free Radic. Biol. Med. 1995;19:103–114. doi: 10.1016/0891-5849(95)00002-F. PubMed DOI

Mano C.M., Prado F.M., Massari J., Ronsein G.E., Martinez G.R., Miyamoto S., Cadet J., Sies H., Medeiros M.H.G., Bechara E.J.H., et al. Excited singlet molecular O-2 ((1)Delta g) is generated enzymatically from excited carbonyls in the dark. Sci. Rep. 2014;4:5938. doi: 10.1038/srep05938. PubMed DOI PMC

Cifra M., Pospíšil P. Ultra-weak photon emission from biological samples: Definition, mechanisms, properties, detection and applications. J. Photochem. Photobiol. B Biol. 2014;139:2–10. doi: 10.1016/j.jphotobiol.2014.02.009. PubMed DOI

Prasad A., Pospisil P. Towards the two-dimensional imaging of spontaneous ultra-weak photon emission from microbial, plant and animal cells. Sci. Rep. 2013;3:1211. doi: 10.1038/srep01211. PubMed DOI PMC

Madl P., Verwanger T., Geppert M., Scholkmann F. Oscillations of ultra-weak photon emission from cancer and non-cancer cells stressed by culture medium change and TNF-alpha. Sci. Rep. 2017;7:11249. doi: 10.1038/s41598-017-10949-z. PubMed DOI PMC

Rac M., Sedlarova M., Pospisil P. The formation of electronically excited species in the human multiple myeloma cell suspension. Sci. Rep. 2015;5:8882. doi: 10.1038/srep08882. PubMed DOI PMC

He M., van Wijk E., van Wietmarschen H., Wang M., Sun M.M., Koval S., van Wijk R., Hankemeier T., van der Greef J. Spontaneous ultra-weak photon emission in correlation to inflammatory metabolism and oxidative stress in a mouse model of collagen-induced arthritis. J. Photochem. Photobiol. B. 2017;168:98–106. doi: 10.1016/j.jphotobiol.2016.12.036. PubMed DOI

Prasad A., Ferretti U., Sedlarova M., Pospisil P. Singlet oxygen production in Chlamydomonas reinhardtii under heat stress. Sci. Rep. 2016;6:13. doi: 10.1038/srep20094. PubMed DOI PMC

Usui S., Tada M., Kobayashi M. Non-invasive visualization of physiological changes of insects during metamorphosis based on biophoton emission imaging. Sci. Rep. 2019;9:7. doi: 10.1038/s41598-019-45007-3. PubMed DOI PMC

Van Wijk R., Van Wijk E. Ultraweak Photon Emission from Human Body. Springer; Boston, MA, USA: 2005. pp. 173–184.

Biesalski H.K., Obermueller-Jevic U.C. UV light, beta-carotene and human skin-Beneficial and potentially harmful effects. Arch. Biochem. Biophys. 2001;389:1–6. doi: 10.1006/abbi.2001.2313. PubMed DOI

Hao O.Y., Stamatas G., Saliou C., Kollias N. A chemiluminescence study of UVA-induced oxidative stress in human skin in vivo. J. Investig. Dermatol. 2004;122:1020–1029. PubMed

Rattan S.I.S., Fernandes R.A., Demirovic D., Dymek B., Lima C.F. Heat stress and hormetin-induced hormesis in human cells: Effects on aging, wound healing, angiogenesis, and differentiation. Dose-response. 2009;7:90–103. doi: 10.2203/dose-response.08-014.Rattan. PubMed DOI PMC

Kobayashi M., Kikuchi D., Okamura H. Imaging of Ultraweak Spontaneous Photon Emission from Human Body Displaying Diurnal Rhythm. PLoS ONE. 2009;4:e6256. doi: 10.1371/journal.pone.0006256. PubMed DOI PMC

Prasad A., Pospisil P. Linoleic Acid-Induced Ultra-Weak Photon Emission from Chlamydomonas reinhardtii as a Tool for Monitoring of Lipid Peroxidation in the Cell Membranes. PLoS ONE. 2011;6:e22345. doi: 10.1371/journal.pone.0022345. PubMed DOI PMC

Prasad A., Pospisil P. Two-dimensional imaging of spontaneous ultra-weak photon emission from the human skin: Role of reactive oxygen species. J. Biophotonics. 2011;4:840–849. doi: 10.1002/jbio.201100073. PubMed DOI

Rastogi A., Pospíšil P. Production of hydrogen peroxide and hydroxyl radical in potato tuber during the necrotrophic phase of hemibiotrophic pathogen Phytophthora infestans infection. J. Photochem. Photobiol. B Biol. 2012;117:202–206. doi: 10.1016/j.jphotobiol.2012.10.001. PubMed DOI

Burgos R.C.R., Schoeman J.C., van Winden L.J., Cervinkova K., Ramautar R., Van Wijk E.P.A., Cifra M., Berger R., Hankemeier T., van der Greef J. Ultra-weak photon emission as a dynamic tool for monitoring oxidative stress metabolism. Sci. Rep. 2017;7:1229. doi: 10.1038/s41598-017-01229-x. PubMed DOI PMC

Kamal A.M., Komatsu S. Proteins involved in biophoton emission and flooding-stress responses in soybean under light and dark conditions. Mol. Biol. Rep. 2016;43:73–89. doi: 10.1007/s11033-015-3940-4. PubMed DOI

Cadenas E., Arad I.D., Boveris A., Fisher A.B., Chance B. Partial Spectral-Analysis of the Hydroperoxide-Induced Chemi-Luminescence of the Perfused Lung. FEBS Lett. 1980;111:413–418. doi: 10.1016/0014-5793(80)80839-8. PubMed DOI

Van Wijk R., Ackerman J.M., Van Wijk E.P.A. Color filters and human photon emission: Implications for auriculomedicine. Explor. J. Sci. Heal. 2005;1:102–108. doi: 10.1016/j.explore.2004.12.003. PubMed DOI

Cadenas E., Wefers H., Sies H. Low-Level Chemi-Luminescence of Isolated Hepatocytes. Eur. J. Biochem. 1981;119:531–536. doi: 10.1111/j.1432-1033.1981.tb05640.x. PubMed DOI

Mathew B.G., Roy D. Weak luminescence from the frozen-thawed root tips of Cicer arietinum L. J. Photochem. Photobiol. B Biol. 1992;12:141–150. doi: 10.1016/1011-1344(92)85003-D. DOI

Pospíšil P., Prasad A., Rác M. Role of reactive oxygen species in ultra-weak photon emission in biological systems. J. Photochem. Photobiol. B Biol. 2014;139:11–23. doi: 10.1016/j.jphotobiol.2014.02.008. PubMed DOI

Han D., Williams E., Cadenas E. Mitochondrial respiratory chain-dependent generation of superoxide anion and its release into the intermembrane space. Biochem. J. 2001;353:411–416. doi: 10.1042/bj3530411. PubMed DOI PMC

Auchere F., Rusnak F. What is the ultimate fate of superoxide anion in vivo? J. Biol. Inorg. Chem. 2002;7:664–667. doi: 10.1007/s00775-002-0362-2. PubMed DOI

Pospisil P. Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim. Biophys. Acta Bioenerget. 2012;1817:218–231. doi: 10.1016/j.bbabio.2011.05.017. PubMed DOI

Asada K. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 2006;141:391–396. doi: 10.1104/pp.106.082040. PubMed DOI PMC

Barber M.J., Kay C.J. Superoxide production during reduction of molecular oxygen by assimilatory nitrate reductase. Arch. Biochem. Biophys. 1996;326:227–232. doi: 10.1006/abbi.1996.0069. PubMed DOI

Lambert A.J., Brand M.D. Superoxide production by NADH: Ubiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane. Biochem. J. 2004;382:511–517. doi: 10.1042/BJ20040485. PubMed DOI PMC

Wood P.M. The potential diagram for oxygen at PH-7. Biochem. J. 1988;253:287–289. doi: 10.1042/bj2530287. PubMed DOI PMC

Aikens J., Dix T.A. Perhydroxyl radical (HOO.) initiated lipid-peroxidation-the role of fatty acid hydroperoxide. J. Biol. Chem. 1991;266:15091–15098. PubMed

Gebicki J.M., Bielski B.H.J. Comparison of the capacities of the perhydroxyl and the speroxide radicals to initiate chain oxidation of linoleic acid. J. Am. Chem. Soc. 1981;103:7020–7022. doi: 10.1021/ja00413a066. DOI

Winterbourn C.C., Kettle A.J. Radical-radical reactions of superoxide: A potential route to toxicity. Biochem. Biophys. Res. Commun. 2003;305:729–736. doi: 10.1016/S0006-291X(03)00810-6. PubMed DOI

Barbouti A., Doulias P.T., Zhu B.Z., Frei B., Galaris D. Intracellular iron, but not copper, plays a critical role in hydrogen peroxide-induced DNA damage. Free Radical Biol. Med. 2001;31:490–498. doi: 10.1016/S0891-5849(01)00608-6. PubMed DOI

Dahlgren C., Karlsson A., Bylund J. Measurement of respiratory burst products generated by professional phagocytes. Methods Mol. Biol. 2007;412:349–363. PubMed

Daithankar V.N., Wang W., Trujillo J.R., Thorpe C. Flavin-linked Erv-family sulfhydryl oxidases release superoxide anion during catalytic turnover. BioChemistry. 2012;51:265–272. doi: 10.1021/bi201672h. PubMed DOI PMC

Wood P.M. The 2 Redox Potentials for Oxygen Reduction to Superoxide. Trends Biochem. Sci. 1987;12:250–251. doi: 10.1016/0968-0004(87)90123-X. DOI

Culotta V.C., Yang M., O’Halloran T.V. Activation of superoxide dismutases: Putting the metal to the pedal. Biochim. Biophysica Acta-Mol. Cell Res. 2006;1763:747–758. doi: 10.1016/j.bbamcr.2006.05.003. PubMed DOI PMC

Halliwell B., Clement M.V., Long L.H. Hydrogen peroxide in the human body. FEBS Lett. 2000;486:10–13. doi: 10.1016/S0014-5793(00)02197-9. PubMed DOI

Kale R., Hebert A.E., Frankel L.K., Sallans L., Bricker T.M., Pospíšil P. Amino acid oxidation of the D1 and D2 proteins by oxygen radicals during photoinhibition of Photosystem II. Proc. Natl. Acad. Sci. USA. 2017;114:2988–2993. doi: 10.1073/pnas.1618922114. PubMed DOI PMC

Hoffmann M.E., Meneghini R. Action of hydrogen peroxide on human fibroblast in culture. PhotoChem. Photobiol. 1979;30:151–155. doi: 10.1111/j.1751-1097.1979.tb07128.x. PubMed DOI

Stadtman E.R., Levine R.L. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids. 2003;25:207–218. doi: 10.1007/s00726-003-0011-2. PubMed DOI

Kim Y.H., Berry A.H., Spencer D.S., Stites W.E. Comparing the effect on protein stability of methionine oxidation versus mutagenesis: Steps toward engineering oxidative resistance in proteins. Protein Eng. 2001;14:343–347. doi: 10.1093/protein/14.5.343. PubMed DOI

Ashby M.T., Nagy P. On the kinetics and mechanism of the reaction of cysteine and hydrogen peroxide in aqueous solution-Commentary. J. Pharm. Sci. 2006;95:15–18. doi: 10.1002/jps.20521. PubMed DOI

Winterbourn C.C. Toxicity of iron and hydrogen peroxide: The Fenton reaction. Toxicol. Lett. 1995;82–83:969–974. doi: 10.1016/0378-4274(95)03532-X. PubMed DOI

Prousek J. Fenton chemistry in biology and medicine. Pure Appl. Chem. 2007;79:2325–2338. doi: 10.1351/pac200779122325. DOI

Buettner G.R. The pecking order of free-radicals and antioxidants-lipid-peroxidation, alpha-tocopherol, and ascorbate. Arch. BioChem. Biophys. 1993;300:535–543. doi: 10.1006/abbi.1993.1074. PubMed DOI

Pierre J.L., Fontecave M. Iron and activated oxygen species in biology: The basic chemistry. Biometals. 1999;12:195–199. doi: 10.1023/A:1009252919854. PubMed DOI

Bresgen N., Jaksch H., Lacher H., Ohlenschlager I., Uchida K., Eckl P.M. Iron-mediated oxidative stress plays an essential role in ferritin-induced cell death. Free Radic. Biol. Med. 2010;48:1347–1357. doi: 10.1016/j.freeradbiomed.2010.02.019. PubMed DOI

Waldo G.S., Wright E., Whang Z.H., Briat J.F., Theil E.C., Sayers D.E. Formation of the ferritin iron mineral occurs in plastids-an X-ray-absorption spectroscopy study. Plant Physiol. 1995;109:797–802. doi: 10.1104/pp.109.3.797. PubMed DOI PMC

Koppenol W.H., Butler J., Vanleeuwen J.W. Haber-Weiss Cycle. PhotoChem. Photobiol. 1978;28:655–660. doi: 10.1111/j.1751-1097.1978.tb06989.x. DOI

Pospíšil P. Production of reactive oxygen species by photosystem II. Biochim. Biophysica Acta-Bioenerget. 2009;1787:1151–1160. doi: 10.1016/j.bbabio.2009.05.005. PubMed DOI

Stadtman E.R. Oxidation of free amino-acids and amino-acid-residues in proteins by radiolysis and by meral-catalyzed reactions. Annu. Rev. BioChem. 1993;62:797–821. doi: 10.1146/annurev.bi.62.070193.004053. PubMed DOI

Aust A.E., Eveleigh J.F. Mechanisms of DNA oxidation. Proc. Soc. Exp. Biol. Med. 1999;222:246–252. doi: 10.1046/j.1525-1373.1999.d01-141.x. PubMed DOI

Balasubramanian B., Pogozelski W.K., Tullius T.D. DNA strand breaking by the hydroxyl radical is governed by the accessible surface areas of the hydrogen atoms of the DNA backbone. Proc. Natl. Acad. Sci. USA. 1998;95:9738–9743. doi: 10.1073/pnas.95.17.9738. PubMed DOI PMC

Pogozelski W.K., Tullius T.D. Oxidative strand scission of nucleic acids: Routes initiated by hydrogen abstraction from the sugar moiety. Chem. Rev. 1998;98:1089–1107. doi: 10.1021/cr960437i. PubMed DOI

Henle E.S., Linn S. Formation, prevention, and repair of DNA damage by iron hydrogen peroxide. J. Biol. Chem. 1997;272:19095–19098. doi: 10.1074/jbc.272.31.19095. PubMed DOI

Halliwell B., Aruoma O.I. DNA damage by oxygen-derived species-its mechanism and measurement in mammalian systems. FEBS Lett. 1991;281:9–19. doi: 10.1016/0014-5793(91)80347-6. PubMed DOI

Ogilby P.R. Singlet oxygen: There is indeed something new under the sun. Chem. Soc. Rev. 2010;39:3181–3209. doi: 10.1039/b926014p. PubMed DOI

DeRosa M.C., Crutchley R.J. Photosensitized singlet oxygen and its applications. Coord. Chem. Rev. 2002;233:351–371. doi: 10.1016/S0010-8545(02)00034-6. DOI

Adam W., Cilento G. Chemical and Biology Generation of Excited States. Academic Press; New York, NY, USA: 1982.

Adam W., Kazakov D.V., Kazakov V.P. Singlet-oxygen chemiluminescence in peroxide reactions. Chem. Rev. 2005;105:3371–3387. doi: 10.1021/cr0300035. PubMed DOI

Stratton S.P., Liebler D.C. Determination of singlet oxygen-specific versus radical-mediated lipid peroxidation in photosensitized oxidation of lipid bilayers: Effect of beta-carotene and alpha-tocopherol. BioChemistry. 1997;36:12911–12920. doi: 10.1021/bi9708646. PubMed DOI

Gracanin M., Hawkins C.L., Pattison D.I., Davies M.J. Singlet-oxygen-mediated amino acid and protein oxidation: Formation of tryptophan peroxides and decomposition products. Free Radic. Biol. Med. 2009;47:92–102. doi: 10.1016/j.freeradbiomed.2009.04.015. PubMed DOI

Pryor W.A., Stanley J.P., Blair E., Cullen G.B. Autoxidation of polyunsaturated fatty-acids. 1. effect of ozone on autoxidation of neat methyl linoleate and methyl linolenate. Arch. Environ. Health. 1976;31:201–210. doi: 10.1080/00039896.1976.10667220. PubMed DOI

D’Ambrosio P., Tonucci L., d’Alessandro N., Morvillo A., Sortino S., Bressan M. Water-Soluble Transition-Metal-Phthalocyanines as Singlet Oxygen Photosensitizers in Ene Reactions. Eur. J. Inorg. Chem. 2011;2011:503–509. doi: 10.1002/ejic.201000784. DOI

Griesbeck A.G., de Kiff A. A New Directing Mode for Singlet Oxygen Ene Reactions: The Vinylogous Gem Effect Enables a O-1(2) Domino Ene/ 4+2 Process. Org. Lett. 2013;15:2073–2075. doi: 10.1021/ol4009602. PubMed DOI

Ravanat J.L., Di Mascio P., Martinez G.R., Medeiros M.H.G., Cadet J. Singlet oxygen induces oxidation of cellular DNA. J. Biol. Chem. 2000;275:40601–40604. doi: 10.1074/jbc.M006681200. PubMed DOI

Tsunoda H., Kudo T., Masaki Y., Ohkubo A., Seio K., Sekine M. Biochemistry behavior of N-oxidized cytosine and adenine bases in DNA polymerase-mediated primer extension reactions. Nucleic Acids Res. 2011;39:2995–3004. doi: 10.1093/nar/gkq914. PubMed DOI PMC

Nguyen K.V., Muller J.G., Burrows C.J. Oxidation of 9-beta-D-ribofuranosyl uric acid by one-electron oxidants versus singlet oxygen and its implications for the oxidation of 8-oxo-7,8-dihydroguanosine. Tetrahedron Lett. 2011;52:2176–2180. doi: 10.1016/j.tetlet.2010.11.123. DOI

Kang P., Foote C.S. Formation of transient intermediates in low-temperature photosensitized oxidation of an 8-C-13-guanosine derivative. J. Am. Chem. Soc. 2002;124:4865–4873. doi: 10.1021/ja012038x. PubMed DOI

Prat F., Houk K.N., Foote C.S. Effect of guanine stacking on the oxidation of 8-oxoguanine in B-DNA. J. Am. Chem. Soc. 1998;120:845–846. doi: 10.1021/ja972331q. DOI

Hatz S., Poulsen L., Ogilby P.R. Time-resolved singlet oxygen phosphorescence measurements from photosensitized experiments in single cells: Effects of oxygen diffusion and oxygen concentration. PhotoChem. Photobiol. 2008;84:1284–1290. doi: 10.1111/j.1751-1097.2008.00359.x. PubMed DOI

Da Silva E.F.F., Pedersen B.W., Breitenbach T., Toftegaard R., Kuimova M.K., Arnaut L.G., Ogilby P.R. Irradiation-and Sensitizer-Dependent Changes in the Lifetime of Intracellular Singlet Oxygen Produced in a Photosensitized Process. J. Phys. Chem. B. 2012;116:445–461. doi: 10.1021/jp206739y. PubMed DOI

Breitenbach T., Kuimova M.K., Gbur P., Hatz S., Schack N.B., Pedersen B.W., Lambert J.D.C., Poulsen L., Ogilby P.R. Photosensitized production of singlet oxygen: Spatially-resolved optical studies in single cells. Photochem. PhotoBiol. Sci. 2009;8:442–452. doi: 10.1039/B809049A. PubMed DOI

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;119:2043–2086. doi: 10.1021/acs.chemrev.8b00554. PubMed DOI

Girotti A.W. Lipid hydroperoxide generation, turnover, and effector action in biological systems. J. Lipid Res. 1998;39:1529–1542. PubMed

Leach A.G., Houk K.N., Foote C.S. Theoretical Prediction of a Perepoxide Intermediate for the Reaction of Singlet Oxygen with trans-Cyclooctene Contrasts with the Two-Step No-Intermediate Ene Reaction for Acyclic Alkenes. J. Org. Chem. 2008;73:8511–8519. doi: 10.1021/jo8016154. PubMed DOI

Dean R.T., Gieseg S., Davies M.J. Reactive Species and Their Accumulation on Radical-Damaged Proteins. Trends Biochem. Sci. 1993;18:437–441. doi: 10.1016/0968-0004(93)90145-D. PubMed DOI

Simpson J.A., Narita S., Gieseg S., Gebicki S., Gebicki J.M., Dean R.T. Long-lived reactive species on free-radical-damaged proteins. Biochem. J. 1992;282:621–624. doi: 10.1042/bj2820621. PubMed DOI PMC

Greer A., Vassilikogiannakis G., Lee K.C., Koffas T.S., Nahm K., Foote C.S. Reaction of singlet oxygen with trans-4-propenylanisole. Formation of 2+2 products with added acid. J. Org. Chem. 2000;65:6876–6878. doi: 10.1021/jo991576d. PubMed DOI

Fedorova G.F., Trofimov A.V., Vasil’ev R.F., Veprintsev T.L. Peroxy-radical-mediated chemiluminescence: Mechanistic diversity and fundamentals for antioxidant assay. Arkivoc. 2007;8:163–215. doi: 10.1002/chin.200709275. DOI

Uemi M., Ronsein G.E., Miyamoto S., Medeiros M.H.G., Di Mascio P. Generation of Cholesterol Carboxyaldehyde by the Reaction of Singlet Molecular Oxygen O-2 ((1)Delta(g)) as Well as Ozone with Cholesterol. Chem. Res. Toxicol. 2009;22:875–884. doi: 10.1021/tx800447b. PubMed DOI

Clennan E.L. New mechanistic and synthetic aspects of singlet oxygen chemistry. Tetrahedron. 2000;56:9151–9179. doi: 10.1016/S0040-4020(00)00794-8. DOI

Adam W., Bosio S.G., Turro N.J. Highly diastereoselective dioxetane formation in the photooxygenation of enecarbamates with an oxazolidinone chiral auxiliary: Steric control in the 2+2 cycloaddition of singlet oxygen through conformational alignment. J. Am. Chem. Soc. 2002;124:8814–8815. doi: 10.1021/ja026815k. PubMed DOI

Clennan E.L., Pace A. Advances in singlet oxygen chemistry. Tetrahedron. 2005;61:6665–6691. doi: 10.1016/j.tet.2005.04.017. DOI

Corey E.J., Wang Z. Conversion of arachidonic acid to the prostaglandin endoperoxide PGG(2), a chemical analog of the biosynthetic-pathway. Tetrahedron Lett. 1994;35:539–542. doi: 10.1016/S0040-4039(00)75832-1. DOI

Miyamoto S., Rettori D., Augusto O., Martinez G.R., Medeiros M.H.G., Di Mascio P. Linoleic acid hydroperoxide reacts with hypochlorite generating peroxyl radical intermediates and singlet oxygen. Free Radic. Biol. Med. 2004;37:S16. PubMed PMC

Prado F.M., Oliveira M.C.B., Miyamoto S., Martinez G.R., Medeiros M.H.G., Ronsein G.E., Di Mascio P. Thymine hydroperoxide as a potential source of singlet molecular oxygen in DNA. Free Radic. Biol. Med. 2009;47:401–409. doi: 10.1016/j.freeradbiomed.2009.05.001. PubMed DOI

Russell G.A. Deuterium-isotope Effects in the Autoxidation of Aralkyl Hydrocarbons. Mechanism of the Interaction of Peroxy Radicals. J. Am. Chem. Soc. 1957;79:3871–3877. doi: 10.1021/ja01571a068. DOI

Miyamoto S., Martinez G.R., Medeiros M.H.G., Di Mascio P. Singlet molecular oxygen generated by biological hydroperoxides. J. PhotoChem. Photobiol. B Biol. 2014;139:24–33. doi: 10.1016/j.jphotobiol.2014.03.028. PubMed DOI

Miyamoto S., Di Mascio P. Lipid Hydroperoxides as a Source of Singlet Molecular Oxygen. In: Kato Y., editor. Lipid Hydroperoxide-Derived Modification of Biomolecules. Volume 77. Springer; Berlin/Heidelberg, Germany: 2014. pp. 3–20. PubMed

Cadenas E., Sies H. Methods in Enzymology. Academic Press; Cambridge, MA, USA: 2000. Formation of electronically excited states during the oxidation of arachidonic acid by prostaglandin endoperoxide synthase. PubMed

Hall R., Chamulitrat W., Takahashi N., Chignell C., Mason R. Detection of Singlet oxygem phosphorescence during chloroperoxidase-catalyzed decomposition of ethyl hydroperoxide. J. Biol. Chem. 1989;264:7900–7906. PubMed

Howard J.A., Ingold K.U. Absolute rate constants for hydrocarbon autooxidation.V. Hydroperoxy radical in chain propagation and termination. Can. J. Chem. 1967;45:785–792. doi: 10.1139/v67-131. DOI

Cilento G., Nascimento A. Generation of electronically excited triplet species at the cellular level: A potential source of genotoxicity. Toxicol. Lett. 1993;67:17–28. doi: 10.1016/0378-4274(93)90043-W. PubMed DOI

Boveris A., Cadenas E., Reiter R., Filipkowski M., Nakase Y., Chance B. Organ Chemi-Luminescence-Non-Invasive Assay for Oxidative Radical Reactions. Proc. Natl. Acad. Sci. USA. 1980;77:347–351. doi: 10.1073/pnas.77.1.347. PubMed DOI PMC

Bennett M., Mehta M., Grant M. Biophoton imaging: A nondestructive method for assaying R gene responses. Mol. Plant-Microbe Interact. 2005;18:95–102. doi: 10.1094/MPMI-18-0095. PubMed DOI

Darmanyan A.P., Foote C.S. Solvent effects on singlet oxygen yield from N,PI-asterisk and PI,PI-asterisk triplet carbonyl compounds. J. Phys. Chem. 1993;97:5032–5035. doi: 10.1021/j100121a029. DOI

Mansfield J.W. Biophoton distress flares signal the onset of the hypersensitive reaction. Trends Plant Sci. 2005;10:307–309. doi: 10.1016/j.tplants.2005.05.007. PubMed DOI

Niu E.P., Mau A.W.H., Ghiggino K.P. Dye-Sensitized Photooxidation of Anthracene and Its Derivatives in Nafion Membrane. Aust. J. Chem. 1991;44:695–704. doi: 10.1071/CH9910695. DOI

Cilento G., Adam W. Photochemistry and Photobiology without Light. PhotoChem. Photobiol. 1988;48:361–368. doi: 10.1111/j.1751-1097.1988.tb02835.x. PubMed DOI

Kopecky K.R., Mumford C. Luminescence in thermal decomposition of 3,3,4-trimethyl-1,2-dioxetane. Can. J. Chem. 1969;47:709. doi: 10.1139/v69-114. DOI

Cilento G., Debaptista C., Brunetti I.L. Triplet carbonyls: From photophysics to biochemistry. J. Mol. Struct. 1994;324:45–48. doi: 10.1016/0022-2860(94)08225-1. DOI

Kopecky K.R., Filby J.E. Yields of excited-states from thermolysis of some 1,2-dioxetanes. Can. J. Chem. 1979;57:283–288. doi: 10.1139/v79-047. DOI

Turro N.J., Lechtken P. Biacetyl sensitized decomposition of tetramethyl-1,2-dioxetane-example of anti-Stokes sensitization involving a masked excited state. Tetrahedron Lett. 1973;14:565–568. doi: 10.1016/S0040-4039(01)95847-2. DOI

Matsumoto M. Advanced chemistry of dioxetane-based chemiluminescent substrates originating from bioluminescence. J. Photochem. Photobiol. C. 2004;5:27–53. doi: 10.1016/j.jphotochemrev.2004.02.001. DOI

Richardson W.H., Anderegg J.H., Price M.E., Tappen W.A., Oneal H.E. Kinetics and mechanisms of thermal decomposition of triphenyl-1,1,2-dioxetane. J. Org. Chem. 1978;43:2236–2242. doi: 10.1021/jo00405a031. DOI

Akasaka T., Fukuoka K., Ando W. A 3-methylene-1,2-dioxetane as a possible chemiluminescent intermediate in singlet oxygenation of allene. Bull. Chem. Soc. Jpn. 1989;62:1367–1369. doi: 10.1246/bcsj.62.1367. DOI

Baumstark A.L., Anderson S.L., Sapp C.J., Vasquez P.C. Thermolysis of 3-alkyl-3-methyl-1,2-dioxetanes: Activation parameters and chemiexcitation yields. Heteroat. Chem. 2001;12:176–179. doi: 10.1002/hc.1028. DOI

Nery A.L.P., Weiss D., Catalani L.H., Baader W.J. Studies on the intramolecular electron transfer catalyzed thermolysis of 1,2-dioxetanes. Tetrahedron. 2000;56:5317–5327. doi: 10.1016/S0040-4020(00)00457-9. DOI

Carey F., Sundberg R. Advanced Organic Chemisty Part A Structure and Mechanisms. Plenum Press; New York, NY, USA: 1984. p. 1199.

Miyamoto S., Ronsein G.E., Prado F.M., Uemi M., Correa T.C., Toma I.N., Bertolucci A., Oliveira M.C.B., Motta F.D., Medeiros M.H.G., et al. Biological hydroperoxides and singlet molecular oxygen generation. IUBMB Life. 2007;59:322–331. doi: 10.1080/15216540701242508. PubMed DOI

Vacher M., Galvan I.F., Ding B.W., Schramm S., Berraud-Pache R., Naumov P., Ferre N., Liu Y.J., Navizet I., Roca-Sanjuan D., et al. Chemi-and Bioluminescence of Cyclic Peroxides. Chem. Rev. 2018;118:6927–6974. doi: 10.1021/acs.chemrev.7b00649. PubMed DOI

Augusto O., Cilento G. Dark Excitation of Chlorophyll. PhotoChem. Photobiol. 1979;30:191–193. doi: 10.1111/j.1751-1097.1979.tb07135.x. DOI

Bohne C., Campa A., Cilento G., Nassi L., Villablanca M. Chlorophyll-an efficient detector of electronically excited species in Biochem. systems. Anal. BioChem. 1986;155:1–9. doi: 10.1016/0003-2697(86)90215-0. PubMed DOI

Campa A., Nassi L., Cilento G. Triplet Energy-Transfer to Chloroplasts from Peroxidase-Generated Excited Aliphatic-Aldehydes. PhotoChem. Photobiol. 1984;40:127–131. doi: 10.1111/j.1751-1097.1984.tb04563.x. DOI

Marder J.B., Droppa M., Caspi V., Raskin V.I., Horvath G. Light-independent thermoluminescence from thylakoids of greening barley leaves. Evidence for involvement of oxygen radicals and free chlorophyll. Physiol. Plant. 1998;104:713–719. doi: 10.1034/j.1399-3054.1998.1040428.x. DOI

Porcal G., Bertolotti S.G., Previtah C.M., Encinas M.V. Electron transfer quenching of singlet and triplet excited states of flavins and lumichrome by aromatic and aliphatic electron donors. Phys. Chem. Chem. Phys. 2003;5:4123–4128. doi: 10.1039/b306945a. DOI

Krasnovsky A.A., Neverov K.V., Egorov S.Y., Roeder B., Levald T. Photophysical Studies of Pheophorbide-a and Pheophytin-a Phosphorescence and Photo-Sensitized Singlet Oxygen Luminescence. J. Photochem. Photobiol. B. 1990;5:245–254. doi: 10.1016/1011-1344(90)80009-M. PubMed DOI

Ortega-Ojeda F., Calcerrada M., Ferrero A., Campos J., Garcia-Ruiz C. Measuring the Human Ultra-Weak Photon Emission Distribution Using an Electron-Multiplying, Charge-Coupled Device as a Sensor. Sensors. 2018;18:1152. doi: 10.3390/s18041152. PubMed DOI PMC

Tsuchida K., Iwasa T., Kobayashi M. Noninvasive imaging of UV-induced oxidative stress in human skin using ultra-weak photon emission. J. Investig. Dermatol. 2018;138:B20. doi: 10.1016/j.jid.2018.06.124. DOI

Kobayashi M., Iwasa T., Tada M. Polychromatic spectral pattern analysis of ultra-weak photon emissions from a human body. J. Photochem. Photobiol. B. 2016;159:186–190. doi: 10.1016/j.jphotobiol.2016.03.037. PubMed DOI

Prasad A., Balukova A., Pospisil P. Triplet Excited Carbonyls and Singlet Oxygen Formation During Oxidative Radical Reaction in Skin. Front. Physiol. 2018;9:1109. doi: 10.3389/fphys.2018.01109. PubMed DOI PMC

Hideg E., Inaba H. Biophoton Emission (Ultraweak Photoemission) from Dark Adapted Spinach-Chloroplasts. PhotoChem. Photobiol. 1991;53:137–142. doi: 10.1111/j.1751-1097.1991.tb08479.x. DOI

Kalaji H.M., Goltsev V., Bosa K., Allakhverdiev S.I., Strasser R.J., Govindjee Experimental in vivo measurements of light emission in plants: A perspective dedicated to David Walker. Photosynth. Res. 2012;114:69–96. doi: 10.1007/s11120-012-9780-3. PubMed DOI

Kellogg R.E. Mechanism of chemiluminescence from peroxy radicals. J. Am. Chem. Soc. 1969;91:5433–5436. doi: 10.1021/ja01048a005. DOI

Niu Q.J., Mendenhall G.D. Yields of singlet molecular oxygen from peroxyl radical termination. J. Am. Chem. Soc. 1992;114:165–172. doi: 10.1021/ja00027a024. DOI

Kanofsky J.R. Singlet oxygen production from the peroxidase catalyzed formation of styrene glutathione adducts. Biochem. Biophys. Res. Commun. 1989;159:1051–1054. doi: 10.1016/0006-291X(89)92215-8. PubMed DOI

Sun S., Bao Z., Ma H., Zhang D., Zheng X. Singlet oxygen generation from the decomposition of alpha-linolenic acid hydroperoxide by cytochrome c and lactoperoxidase. BioChemstry. 2007;46:6668–6673. doi: 10.1021/bi700178u. PubMed DOI

Koh E., Fluhr R. Singlet oxygen detection in biological systems: Uses and limitations. Plant Signal. Behav. 2016;11:e1192742. doi: 10.1080/15592324.2016.1192742. PubMed DOI PMC

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