How super is supersulfide?: Reconsidering persulfide reactivity in cellular biology

Redox Biology - Tập 67 - Trang 102899 - 2023
Christopher H. Switzer1
1Department of Molecular and Cell Biology, University of Leicester, Leicester, LE1 7RH, United Kingdom

Tài liệu tham khảo

Beauchamp, 1984, A critical review of the literature on hydrogen sulfide toxicity, CRC Crit. Rev. Toxicol., 13, 25, 10.3109/10408448409029321 Truong, 2006, Molecular mechanisms of hydrogen sulfide toxicity, Drug Metabol. Rev., 38, 733, 10.1080/03602530600959607 Kimura, 2012, Hydrogen sulfide is a signaling molecule and a cytoprotectant, Antioxidants Redox Signal., 17, 45, 10.1089/ars.2011.4345 Nishida, 2012, Hydrogen sulfide anion regulates redox signaling via electrophile sulfhydration, Nat. Chem. Biol., 8, 714, 10.1038/nchembio.1018 Gemici, 2015, Chapter nine - anti-inflammatory and cytoprotective properties of hydrogen sulfide, vol. 555, 169 Giovinazzo, 2021, Hydrogen sulfide is neuroprotective in Alzheimer's disease by sulfhydrating GSK3β and inhibiting Tau hyperphosphorylation, Proc. Natl. Acad. Sci. USA, 118, 10.1073/pnas.2017225118 Furne, 2008, Whole tissue hydrogen sulfide concentrations are orders of magnitude lower than presently accepted values, Am. J. Physiol. Regul. Integr. Comp. Physiol., 295, R1479, 10.1152/ajpregu.90566.2008 Fu, 2012, Hydrogen sulfide (H2S) metabolism in mitochondria and its regulatory role in energy production, Proc. Natl. Acad. Sci. USA, 109, 2943, 10.1073/pnas.1115634109 Szabo, 2014, Regulation of mitochondrial bioenergetic function by hydrogen sulfide. Part I. Biochemical and physiological mechanisms, Br. J. Pharmacol., 171, 2099, 10.1111/bph.12369 Petersen, 1977, The effect of inhibitors on the oxygen kinetics of cytochrome c oxidase, Biochim. Biophys. Acta Bioenerg., 460, 299, 10.1016/0005-2728(77)90216-X Hill, 1984, Interactions of sulphide and other ligands with cytochrome c oxidase. An electron-paramagnetic-resonance study, Biochem. J., 224, 591, 10.1042/bj2240591 Switzer, 2023, SOD1 is an essential H(2)S detoxifying enzyme, Proc. Natl. Acad. Sci. U. S. A., 120, 10.1073/pnas.2205044120 Landry, 2021, Hydrogen sulfide oxidation by sulfide quinone oxidoreductase, Chembiochem, 22, 949, 10.1002/cbic.202000661 Cuevasanta, 2015, Reaction of hydrogen sulfide with disulfide and sulfenic acid to form the strongly nucleophilic persulfide, J. Biol. Chem., 290, 26866, 10.1074/jbc.M115.672816 Paul, 2012, H2S signalling through protein sulfhydration and beyond, Nat. Rev. Mol. Cell Biol., 13, 499, 10.1038/nrm3391 Millikin, 2016, The chemical biology of protein hydropersulfides: studies of a possible protective function of biological hydropersulfide generation, Free Radic. Biol. Med., 97, 136, 10.1016/j.freeradbiomed.2016.05.013 Ono, 2014, Redox chemistry and chemical biology of H2S, hydropersulfides, and derived species: implications of their possible biological activity and utility, Free Radic. Biol. Med., 77, 82, 10.1016/j.freeradbiomed.2014.09.007 Akaike, 2017, Cysteinyl-tRNA synthetase governs cysteine polysulfidation and mitochondrial bioenergetics, Nat. Commun., 8, 1177, 10.1038/s41467-017-01311-y Zainol Abidin, 2023, Synthesis of sulfides and persulfides is not impeded by disruption of three canonical enzymes in sulfur metabolism, Antioxidants, 12, 868, 10.3390/antiox12040868 Kumagai, 2017, Environmental electrophiles: protein adducts, modulation of redox signaling, and interaction with persulfides/polysulfides, Chem. Res. Toxicol., 30, 203, 10.1021/acs.chemrestox.6b00326 Zhang, 2023, Redox regulation of xenobiotics by reactive sulfur and supersulfide species, Antioxidants Redox Signal., 10.1089/ars.2022.0172 Dang, 2022, A novel anti-inflammatory role links the CARS2 locus to protection from coronary artery disease, Atherosclerosis, 348, 8, 10.1016/j.atherosclerosis.2022.03.024 Matsunaga, 2023, Supersulphides provide airway protection in viral and chronic lung diseases, Nat. Commun., 14, 4476, 10.1038/s41467-023-40182-4 Wiedemann, 2020, Cysteines and disulfide bonds as structure-forming units: insights from different domains of life and the potential for characterization by NMR, Front. Chem., 8, 10.3389/fchem.2020.00280 Perri, 2016, The unfolded protein response and the role of protein disulfide isomerase in neurodegeneration, Front. Cell Dev. Biol., 3, 10.3389/fcell.2015.00080 Wang, 2020, Hydrogen sulfide plays an important protective role through influencing endoplasmic reticulum stress in diseases, Int. J. Biol. Sci., 16, 264, 10.7150/ijbs.38143 Benchoam, 2020, Acidity and nucleophilic reactivity of glutathione persulfide, J. Biol. Chem., 295, 15466, 10.1074/jbc.RA120.014728 Cuevasanta, 2022, Possible molecular basis of the biochemical effects of cysteine-derived persulfides, Front. Mol. Biosci., 9, 10.3389/fmolb.2022.975988 Fukuto, 2018, Biological hydropersulfides and related polysulfides – a new concept and perspective in redox biology, FEBS (Fed. Eur. Biochem. Soc.) Lett., 592, 2140, 10.1002/1873-3468.13090 Edwards, 1962, The factors determining nucleophilic reactivities, J. Am. Chem. Soc., 84, 16, 10.1021/ja00860a005 Hansen, 2021, Origin of the α-effect in SN2 reactions, Angew. Chem. Int. Ed., 60, 20840, 10.1002/anie.202106053 Henderson, 2020, Cysteine trisulfide protects E. coli from electrophile-induced death through the generation of cysteine hydropersulfide, Chem. Res. Toxicol., 33, 678, 10.1021/acs.chemrestox.9b00494 Park, 2015, Persulfides: current knowledge and challenges in chemistry and chemical biology, Mol. Biosyst., 11, 1775, 10.1039/C5MB00216H S. Kasamatsu et al., Supersulfide catalysis for nitric oxide and aldehyde metabolism. Sci. Adv. 9, eadg8631. Heppner, 2018, Cysteine perthiosulfenic acid (Cys-SSOH): a novel intermediate in thiol-based redox signaling?, Redox Biol., 14, 379, 10.1016/j.redox.2017.10.006 Wu, 2022, Hydropersulfides inhibit lipid peroxidation and protect cells from ferroptosis, J. Am. Chem. Soc., 144, 15825, 10.1021/jacs.2c06804 Barayeu, 2023, Hydropersulfides inhibit lipid peroxidation and ferroptosis by scavenging radicals, Nat. Chem. Biol., 19, 28, 10.1038/s41589-022-01145-w Kaneko, 2022, Antioxidant action of persulfides and polysulfides against free radical-mediated lipid peroxidation, Free Radic. Res., 56, 677, 10.1080/10715762.2023.2165918 Switzer, 2022, The antioxidant and oxidant properties of hydropersulfides (RSSH) and polysulfide species, Redox Biol., 57, 10.1016/j.redox.2022.102486 Bianco, 2016, The chemical biology of the persulfide (RSSH)/perthiyl (RSS·) redox couple and possible role in biological redox signaling, Free Radic. Biol. Med., 101, 20, 10.1016/j.freeradbiomed.2016.09.020 Gray, 1961, Isoelectronic principle, thermochemistry, and reactivity of related free radicals, Nature, 191, 1357, 10.1038/1911357a0 Girotti, 2013, Generation and reactivity of lipid hydroperoxides in biological systems Allison, 1976, Formation and reactions of sulfenic acids in proteins, Accounts Chem. Res., 9, 293, 10.1021/ar50104a003 Greiner, 2013, Polysulfides link H2S to protein thiol oxidation, Antioxidants Redox Signal., 19, 1749, 10.1089/ars.2012.5041 Lin, 2003, The oxidative damage theory of aging, Clin. Neurosci. Res., 2, 305, 10.1016/S1566-2772(03)00007-0 Baba, 2018, Role of thiols in oxidative stress, Curr. Opin. Toxicol., 7, 133, 10.1016/j.cotox.2018.03.005 Eaton, 2006, Protein thiol oxidation in health and disease: techniques for measuring disulfides and related modifications in complex protein mixtures, Free Radic. Biol. Med., 40, 1889, 10.1016/j.freeradbiomed.2005.12.037 Finkel, 2000, Oxidative stress and the biology of ageing, Nature, 408, 239, 10.1038/35041687 Calabrese, 2007, Biological stress response terminology: integrating the concepts of adaptive response and preconditioning stress within a hormetic dose–response framework, Toxicol. Appl. Pharmacol., 222, 122, 10.1016/j.taap.2007.02.015 Calabrese, 2003, Toxicology rethinks its central belief, Nature, 421, 691, 10.1038/421691a Griffiths, 2023, Cysteine hydropersulfide reduces lipid peroxidation and protects against myocardial ischaemia-reperfusion injury - are endogenous persulfides mediators of ischaemic preconditioning?, Redox Biol., 60, 10.1016/j.redox.2023.102605 Parvez, 2018, Redox signaling by reactive electrophiles and oxidants, Chem. Rev., 118, 8798, 10.1021/acs.chemrev.7b00698 Calabrese, 2010, Cellular stress responses, the hormesis paradigm, and vitagenes: novel targets for therapeutic intervention in neurodegenerative disorders, Antioxidants Redox Signal., 13, 1763, 10.1089/ars.2009.3074 Mantha, 2010, Cadmium-induced hormetic effect in differentiated Caco-2 cells: ERK and p38 activation without cell proliferation stimulation, J. Cell. Physiol., 224, 250, 10.1002/jcp.22128 Goto, 2009, Hormetic effects of reactive oxygen species by exercise: a view from animal studies for successful aging in human Sies, 2017, Radiation hormesis: the link to nanomolar hydrogen peroxide, Antioxidants Redox Signal., 27, 596, 10.1089/ars.2017.7233 Prysyazhna, 2019, Blood pressure–lowering by the antioxidant resveratrol is counterintuitively mediated by oxidation of cGMP-dependent protein kinase, Circulation, 140, 126, 10.1161/CIRCULATIONAHA.118.037398 Calabrese, 2010, Resveratrol commonly displays hormesis: occurrence and biomedical significance, Hum. Exp. Toxicol., 29, 980, 10.1177/0960327110383625 Rainey, 2015, Curcumin hormesis mediates a cross-talk between autophagy and cell death, Cell Death Dis., 6, e2003, 10.1038/cddis.2015.343 Pal, 2016, Hormetic potential of sulforaphane (SFN) in switching cells' fate towards survival or death, Mini-Rev. Med. Chem., 16, 980, 10.2174/1389557516666151120115027 Sthijns, 2014, Adaptation to acrolein through upregulating the protection by glutathione in human bronchial epithelial cells: the materialization of the hormesis concept, Biochem. Biophys. Res. Commun., 446, 1029, 10.1016/j.bbrc.2014.03.081 Switzer, 2021, Cysteine trisulfide oxidizes protein thiols and induces electrophilic stress in human cells, Redox Biol., 47, 10.1016/j.redox.2021.102155 Forman, 2014, Para-hormesis: an innovative mechanism for the health protection brought by antioxidants in wine, Nutr. Aging, 2, 117, 10.3233/NUA-130033 Olson, 2015, The role of hydrogen sulfide in evolution and the evolution of hydrogen sulfide in metabolism and signaling, Physiology, 31, 60, 10.1152/physiol.00024.2015 Ida, 2014, Reactive cysteine persulfides and S-polythiolation regulate oxidative stress and redox signaling, Proc. Natl. Acad. Sci. USA, 111, 7606, 10.1073/pnas.1321232111