Antioxidant action of persulfides and polysulfides against free radical-mediated lipid peroxidation

References

• Niki E, Noguchi N, Tsuchihashi H, et al. Interaction among vitamin C, vitamin E, and beta-carotene. Am J Clin Nutr. 1995;62(6 Suppl):1322S–1326S.
   PubMed Web of Science ®Google Scholar
• Saito Y. Diverse cytoprotective actions of vitamin E isoforms- role as peroxyl radical scavengers and complementary functions with selenoproteins. Free Radic Biol Med. 2021;175:121–129.
   PubMed Web of Science ®Google Scholar
• Winterbourn CC, Hampton MB. Thiol chemistry and specificity in redox signaling. Free Radic Biol Med. 2008;45(5):549–561.
   PubMed Web of Science ®Google Scholar
• Ulrich K, Jakob U. The role of thiols in antioxidant systems. Free Radic Biol Med. 2019;140:14–27.
   PubMed Web of Science ®Google Scholar
• Flohé L, Toppo S, Orian L. The glutathione peroxidase family: discoveries and mechanism. Free Radic Biol Med. 2022;187:113–122.
   PubMed Web of Science ®Google Scholar
• Brigelius-Flohé R, Flohé L. Regulatory phenomena in the glutathione peroxidase superfamily. Antioxid Redox Signal. 2020;33(7):498–516.
   PubMed Web of Science ®Google Scholar
• Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci. 1996;16(3):1066–1071.
   PubMed Web of Science ®Google Scholar
• Ida T, Sawa T, Ihara H, et al. Reactive cysteine persulfides and S-polythiolation regulate oxidative stress and redox signaling. Proc Natl Acad Sci USA. 2014;111(21):7606–7611.
   PubMed Web of Science ®Google Scholar
• Mishanina TV, Libiad M, Banerjee R. Biogenesis of reactive sulfur species for signaling by hydrogen sulfide oxidation pathways. Nat Chem Biol. 2015;11(7):457–464.
   PubMed Web of Science ®Google Scholar
• Álvarez L, Bianco CL, Toscano JP, et al. Chemical biology of hydropersulfides and related species: possible roles in cellular protection and redox signaling. Antioxid Redox Signal. 2017;27(10):622–633.
   PubMed Web of Science ®Google Scholar
• Fukuto JM. The biological/physiological utility of hydropersulfides (RSSH) and related species: what is old is new again. Antioxid Redox Signal. 2022;36(4–6):244–255.
   PubMed Web of Science ®Google Scholar
• Sawa T, Takata T, Matsunaga T, et al. Chemical biology of reactive sulfur species: hydrolysis-driven equilibrium of polysulfides as a determinant of physiological functions. Antioxid Redox Signal. 2022;36(4–6):327–336.
   PubMed Web of Science ®Google Scholar
• Barayeu U, Schilling D, Eid M, et al. Hydropersulfides inhibit lipid peroxidation and ferroptosis by scavenging radicals. Nat Chem Biol. 2023;19(1):28–37.
   PubMed Web of Science ®Google Scholar
• Switzer CH, Fukuto JM. The antioxidant and oxidant properties of hydropersulfides (RSSH) and polysulfide species. Redox Biol. 2022;57:102486.
   PubMed Web of Science ®Google Scholar
• Shieh M, Xu S, Lederberg OL, et al. Detection of sulfane sulfur species in biological systems. Redox Biol. 2022;57:102502.
   PubMed Web of Science ®Google Scholar
• Everett SA, Schoeneich C, Stewart JH, et al. Perthiyl radicals, trisulfide radical ions, and sulfate formation: a combined photolysis and radiolysis study on redox processes with organic di- and trisulfides. J. Phys. Chem. 1992;96(1):306–314.
   Web of Science ®Google Scholar
• Everett SA, Folkes LK, Wardman P, et al. Free-radical repair by a novel perthiol: reversible hydrogen transfer and perthiyl radical formation. Free Radic Res. 1994;20(6):387–400.
   PubMed Web of Science ®Google Scholar
• Everett SA, Wardman P. [5] Perthiols as antioxidants: radical-scavenging and prooxidative mechanisms. In: Lester Packer, editor. Methods in enzymology. London, UK: Academic Press; 1995. p. 55–69. DOI: 10.1016/0076-6879(95)51110-5.
   Google Scholar
• Chauvin J-PR, Griesser M, Pratt DA. Hydropersulfides: H-atom transfer agents par excellence. J Am Chem Soc. 2017;139(18):6484–6493.
   PubMed Web of Science ®Google Scholar
• Poon J-F, Pratt DA. Recent insights on hydrogen atom transfer in the inhibition of hydrocarbon autoxidation. Acc Chem Res. 2018;51(9):1996–2005.
   PubMed Web of Science ®Google Scholar
• Wu Z, Khodade VS, Chauvin J-PR, et al. Hydropersulfides inhibit lipid peroxidation and protect cells from ferroptosis. J Am Chem Soc. 2022;144(34):15825–15837.
   PubMed Web of Science ®Google Scholar
• Chauvin J-PR, Griesser M, Pratt DA. The antioxidant activity of polysulfides: it’s radical!. Chem Sci. 2019;10(19):4999–5010.
   PubMed Web of Science ®Google Scholar
• Niki E. Oxidant-specific biomarkers of oxidative stress. Association with atherosclerosis and implication for antioxidant effects. Free Radic Biol Med. 2018;120:425–440.
   PubMed Web of Science ®Google Scholar
• Sottero B, Rossin D, Poli G, et al. Lipid oxidation products in the pathogenesis of inflammation-related gut diseases. Curr Med Chem. 2018;25(11):1311–1326.
   PubMed Web of Science ®Google Scholar
• Bayır H, Anthonymuthu TS, Tyurina YY, et al. Achieving life through death: redox biology of lipid peroxidation in ferroptosis. Cell Chem Biol. 2020;27(4):387–408.
   PubMed Web of Science ®Google Scholar
• Zilka O, Shah R, Li B, et al. On the mechanism of cytoprotection by ferrostatin-1 and liproxstatin-1 and the role of lipid peroxidation in ferroptotic cell death. ACS Cent Sci. 2017;3(3):232–243.
   PubMed Web of Science ®Google Scholar
• Niki E, Noguchi N. Antioxidant action of vitamin E in vivo as assessed from its reaction products with multiple biological oxidants. Free Radic Res. 2021;55(4):352–363.
   PubMed Web of Science ®Google Scholar
• Niki E. Assessment of antioxidant capacity in vitro and in vivo. Free Radic Biol Med. 2010;49(4):503–515.
   PubMed Web of Science ®Google Scholar
• Frei B, Stocker R, Ames BN. Antioxidant defenses and lipid peroxidation in human blood plasma. Proc Natl Acad Sci USA. 1988;85(24):9748–9752.
   PubMed Web of Science ®Google Scholar
• Niki E, Yoshida Y, Saito Y, et al. Lipid peroxidation: mechanisms, inhibition, and biological effects. Biochem Biophys Res Commun. 2005;338(1):668–676.
   PubMed Web of Science ®Google Scholar
• Umeno A, Morita M, Yoshida Y, et al. Isomer distribution of hydroxyoctadecadienoates (HODE) and hydroxyeicosatetraenoates (HETE) produced in the plasma oxidation mediated by peroxyl radical, peroxynitrite, hypochlorite, 15-lipoxygenase, and singlet oxygen. Arch Biochem Biophys. 2017;635:96–101.
   PubMed Web of Science ®Google Scholar
• Itoh N, Cao J, Chen Z-H, et al. Advantages and limitation of BODIPY as a probe for the evaluation of lipid peroxidation and its inhibition by antioxidants in plasma. Bioorg Med Chem Lett. 2007;17(7):2059–2063.
   PubMed Web of Science ®Google Scholar
• Yin H, Xu L, Porter NA. Free radical lipid peroxidation: mechanisms and analysis. Chem Rev. 2011;111(10):5944–5972.
   PubMed Web of Science ®Google Scholar
• Akasaka K, Suzuki T, Ohrui H, et al. Study on aromatic phosphines for novel fluorometry of hydroperoxides (II) -the determination of lipid hydroperoxides with diphenyl-1-Pyrenylphosphine. Anal Lett. 1987;20(5):797–807.
   Web of Science ®Google Scholar
• Noguchi N, Numano R, Kaneda H, et al. Oxidation of lipids in low density lipoprotein particles. Free Radic Res. 1998;29(1):43–52.
   PubMed Web of Science ®Google Scholar
• Okimotoa Y, Watanabea A, Nikia E, et al. A novel fluorescent probe diphenyl-1-pyrenylphosphine to follow lipid peroxidation in cell membranes. FEBS Lett. 2000;474(2–3):137–140.
   PubMed Web of Science ®Google Scholar
• Takahashi M, Shibata M, Niki E. Estimation of lipid peroxidation of live cells using a fluorescent probe, diphenyl-1-pyrenylphosphine. Free Radic Biol Med. 2001;31(2):164–174.
   PubMed Web of Science ®Google Scholar
• Cerda MM, Hammers MD, Earp MS, et al. Applications of synthetic organic tetrasulfides as H2S donors. Org Lett. 2017;19(9):2314–2317.
   PubMed Web of Science ®Google Scholar
• Takashima M, Horie M, Shichiri M, et al. Assessment of antioxidant capacity for scavenging free radicals in vitro: a rational basis and practical application. Free Radic Biol Med. 2012;52(7):1242–1252.
   PubMed Web of Science ®Google Scholar
• Shi H, Noguchi N, Niki E. Galvinoxyl method for standardizing electron and proton donation activity. Methods Enzymol. 2001;335:157–166.
   PubMed Web of Science ®Google Scholar
• Fukumoto K, Yazaki M, Arisawa M. Rhodium-catalyzed synthesis of peptide polysulfides by insertion of sulfur into unprotected peptide disulfides. Org Lett. 2022;24(44):8176–8179.
   PubMedGoogle Scholar
• Niki E. [3] Free radical initiators as source of water- or lipid-soluble peroxyl radicals. In: Methods in enzymology. London, UK: Academic Press; 1990. p. 100–108. DOI:10.1016/0076-6879(90)86095-D.
   Google Scholar
• Takashima M, Shichiri M, Hagihara Y, et al. Reactivity toward oxygen radicals and antioxidant action of thiol compounds. Biofactors. 2012;38(3):240–248.
   PubMed Web of Science ®Google Scholar
• Niki E. Antioxidant capacity of foods for scavenging reactive oxidants and inhibition of plasma lipid oxidation induced by multiple oxidants. Food Funct. 2016;7(5):2156–2168.
   PubMed Web of Science ®Google Scholar
• Amorati R, Baschieri A, Morroni G, et al. Peroxyl radical reactions in water solution: a gym for proton-coupled electron-transfer theories. Chemistry. 2016;22(23):7924–7934.
   PubMed Web of Science ®Google Scholar
• Hoffmann MR. Kinetics and mechanism of oxidation of hydrogen sulfide by hydrogen peroxide in acidic solution. Environ. Sci. Technol. 1977;11(1):61–66.
   Web of Science ®Google Scholar
• Noguchi N, Yamashita H, Hamahara J, et al. The specificity of lipoxygenase-catalyzed lipid peroxidation and the effects of radical-scavenging antioxidants. Biol Chem. 2002;383(3-4):619–626.
   PubMed Web of Science ®Google Scholar
• Sies H, Stahl W. Vitamins E and C, beta-carotene, and other carotenoids as antioxidants. Am J Clin Nutr. 1995;62(6 Suppl):1315S–1321S.
   PubMed Web of Science ®Google Scholar
• Munday R. Harmful and beneficial effects of organic monosulfides, disulfides, and polysulfides in animals and humans. Chem Res Toxicol. 2012;25(1):47–60.
   PubMed Web of Science ®Google Scholar
• Gotoh N, Noguchi N, Tsuchiya J, et al. Inhibition of oxidation of low density lipoprotein by vitamin E and related compounds. Free Radic Res. 1996;24(2):123–134.
   PubMed Web of Science ®Google Scholar
• Jones DP, Carlson JL, Mody VC, et al. Redox state of glutathione in human plasma. Free Radic Biol Med. 2000;28(4):625–635.
   PubMed Web of Science ®Google Scholar
• Denisov E, Chatgilialoglu C, Shestakov A, et al. Rate constants and transition-state geometry of reactions of alkyl, alkoxyl, and peroxyl radicals with thiols. Int. J. Chem. Kinet. 2009;41(4):284–293.
   Web of Science ®Google Scholar
• Rabenstein DL. Nuclear magnetic resonance studies of the acid-base chemistry of amino acids and peptides. I. Microscopic ionization constants of glutathione and methylmercury-complexed glutathione. J Am Chem Soc 1973;95(9):2797–2803.
   Web of Science ®Google Scholar
• Trujillo M, Alvarez B, Radi R. One- and two-electron oxidation of thiols: mechanisms, kinetics and biological fates. Free Radic Res. 2016;50(2):150–171.
   PubMed Web of Science ®Google Scholar
• Kunath S, Schindeldecker M, De Giacomo A, et al. Prooxidative chain transfer activity by thiol groups in biological systems. Redox Biol. 2020;36:101628.
   PubMed Web of Science ®Google Scholar
• D'Aquino M, Dunster C, Willson RL. Vitamin a and glutathione-mediated free radical damage: competing reactions with polyunsaturated fatty acids and vitamin C. Biochem Biophys Res Commun. 1989;161(3):1199–1203.
   PubMed Web of Science ®Google Scholar
• Schöneich C, Asmus KD, Dillinger U, et al. Thiyl radical attack on polyunsaturated fatty acids: a possible route to lipid peroxidation. Biochem Biophys Res Commun. 1989;161(1):113–120.
   PubMed Web of Science ®Google Scholar
• Schöneich C, Dillinger U, von Bruchhausen F, et al. Oxidation of polyunsaturated fatty acids and lipids through thiyl and sulfonyl radicals: reaction kinetics, and influence of oxygen and structure of thiyl radicals. Arch Biochem Biophys. 1992;292(2):456–467.
   PubMed Web of Science ®Google Scholar
• Moosmann B, Hajieva P. Probing the role of cysteine thiyl radicals in biology: eminently dangerous, difficult to scavenge. Antioxidants. 2022;11(5):885.
   Web of Science ®Google Scholar
• Benson SW. Thermochemistry and kinetics of sulfur-containing molecules and radicals. Chem Rev. 1978;78(1):23–35.
   Web of Science ®Google Scholar
• Bianco CL, Chavez TA, Sosa V, et al. The chemical biology of the persulfide (RSSH)/perthiyl (RSS) redox couple and possible role in biological redox signaling. Free Radic Biol Med. 2016;101:20–31.
   PubMed Web of Science ®Google Scholar
• Chauvin J-PR, Haidasz EA, Griesser M, et al. Polysulfide-1-oxides react with peroxyl radicals as quickly as hindered phenolic antioxidants and do so by a surprising concerted homolytic substitution. Chem Sci. 2016;7(10):6347–6356.
   PubMed Web of Science ®Google Scholar
• Mahoney LR, Mendenhall GD, Ingold KU. Calorimetric and equilibrium studies on some stable nitroxide and iminoxy radicals. Approximate oxygen-hydrogen bond dissociation energies in hydroxylamines and oximes. J Am Chem Soc. 1973;95(26):8610–8614.
   Web of Science ®Google Scholar
• Noguchi N, Damiani E, Greci L, et al. Action of quinolinic and indolinonic aminoxyls as radical-scavenging antioxidants. Chem Phys Lipids. 1999;99(1):11–19.
   PubMed Web of Science ®Google Scholar
• Benchoam D, Semelak JA, Cuevasanta E, et al. Acidity and nucleophilic reactivity of glutathione persulfide. J Biol Chem. 2020;295(46):15466–15481.
   PubMed Web of Science ®Google Scholar
• Koppenol WH, Bounds PL. Signaling by sulfur-containing molecules. Quantitative aspects. Arch Biochem Biophys. 2017;617:3–8.
   PubMed Web of Science ®Google Scholar
• Fukuto JM, Hobbs AJ. A comparison of the chemical biology of hydropersulfides (RSSH) with other protective biological antioxidants and nucleophiles. Nitric Oxide. 2021;107:46–57.
   PubMed Web of Science ®Google Scholar
• Horie T, Murayama T, Mishima T, et al. Protection of liver microsomal membranes from lipid peroxidation by garlic extract. Planta Med. 1989;55(6):506–508.
   PubMedGoogle Scholar
• Horie T, Awazu S, Itakura Y, et al. Identified diallyl polysulfides from an aged garlic extract which protects the membranes from lipid peroxidation. Planta Med. 1992;58(5):468–469.
   PubMed Web of Science ®Google Scholar
• Higuchi O, Tateshita K, Nishimura H. Antioxidative activity of sulfur-containing compounds in allium species for human low-density lipoprotein (LDL) oxidation in vitro. J Agric Food Chem. 2003;51(24):7208–7214.
   PubMed Web of Science ®Google Scholar
• Ndoye Foe FM-C, Tchinang TFK, Nyegue AM, et al. Chemical composition, in vitro antioxidant and anti-inflammatory properties of essential oils of four dietary and medicinal plants from Cameroon. BMC Complement Altern Med. 2016;16:117.
   PubMed Web of Science ®Google Scholar
• Morales-López J, Centeno-Álvarez M, Nieto-Camacho A, et al. Evaluation of antioxidant and hepatoprotective effects of white cabbage essential oil. Pharm Biol. 2017;55(1):233–241.
   PubMed Web of Science ®Google Scholar
• Burton GW, Ingold KU. β-Carotene: an unusual type of lipid antioxidant. Science. 1984;224(4649):569–573.
   PubMed Web of Science ®Google Scholar
• Shibata A, Ishima Y, Ikeda M, et al. Human serum albumin hydropersulfide is a potent reactive oxygen species scavenger in oxidative stress conditions such as chronic kidney disease. Biochem Biophys Res Commun. 2016;479(3):578–583.
   PubMed Web of Science ®Google Scholar
• Pharoah BM, Khodade VS, Eremiev A, et al. Hydropersulfides (RSSH) outperform post-conditioning and other reactive sulfur species in limiting ischemia-reperfusion injury in the isolated mouse heart. Antioxidants. 2022;11(5):1010.
   Web of Science ®Google Scholar
• Khodade VS, Aggarwal SC, Pharoah BM, et al. Alkylsulfenyl thiocarbonates: precursors to hydropersulfides potently attenuate oxidative stress. Chem Sci. 2021;12(23):8252–8259.
   PubMed Web of Science ®Google Scholar
• Sawa T, Ono K, Tsutsuki H, et al. Reactive cysteine persulphides: occurrence, biosynthesis, antioxidant activity, methodologies, and bacterial persulphide signalling. Adv Microb Physiol. 2018;72:1–28.
   PubMed Web of Science ®Google Scholar
• Furne J, Saeed A, Levitt MD. Whole tissue hydrogen sulfide concentrations are orders of magnitude lower than presently accepted values. Am J Physiol Regul Integr Comp Physiol. 2008;295(5):R1479–85.
   PubMed Web of Science ®Google Scholar
• Takata T, Jung M, Matsunaga T, et al. Methods in sulfide and persulfide research. Nitric Oxide. 2021;116:47–64.
   PubMed Web of Science ®Google Scholar
• Brown EM, Bowden NB. Stabilities of three key biological trisulfides with implications for their roles in the release of hydrogen sulfide and bioaccumulation of sulfane sulfur. ACS Omega. 2022;7(13):11440–11451.
   PubMed Web of Science ®Google Scholar
• Amorati R, Lynett PT, Valgimigli L, et al. The reaction of sulfenic acids with peroxyl radicals: insights into the radical-trapping antioxidant activity of plant-derived thiosulfinates. Chemistry. 2012;18(20):6370–6379.
   PubMed Web of Science ®Google Scholar