Skip to main content

Persulfidation (S-sulfhydration) and H2S

  • Chapter

Part of the Handbook of Experimental Pharmacology book series (HEP,volume 230)

Abstract

The past decade has witnessed the discovery of hydrogen sulfide (H2S) as a new signalling molecule. Its ability to act as a neurotransmitter, regulator of blood pressure, immunomodulator or anti-apoptotic agent, together with its great pharmacological potential, is now well established. Notwithstanding the growing body of evidence showing the biological roles of H2S, the gap between the macroscopic descriptions and the actual mechanism(s) behind these processes is getting larger. The reactivity towards reactive oxygen and nitrogen species and/or metal centres cannot explain this plethora of biological effects. Therefore, a mechanism involving modification of protein cysteine residues to form protein persulfides is proposed. It is alternatively called S-sulfhydration. Persulfides are not particularly stable and show increased reactivity when compared to free thiols. Detection of protein persulfides is still facing methodological limitations, and mechanisms by which H2S causes this modification are still largely scarce. Persulfidation of protein such as KATP could contribute to H2S-induced vasodilation, while S-sulfhydration of GAPDH and NF-κB inhibits apoptosis. H2S regulates endoplasmic reticulum stress by causing persulfidation of PTP-1B. Several other proteins have been found to be regulated by this posttranslational modification of cysteine. This review article provides a critical overview of the current state of the literature addressing protein S-sulfhydration, with particular emphasis on the challenges and future research directions in this particular field.

Keywords

  • Hydrogen sulfide
  • Polysulfides
  • Sulfenic acids
  • Persulfidation
  • S-sulfhydration
  • S-nitrosation

This is a preview of subscription content, access via your institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • DOI: 10.1007/978-3-319-18144-8_2
  • Chapter length: 31 pages
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
eBook
USD   299.00
Price excludes VAT (USA)
  • ISBN: 978-3-319-18144-8
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
Hardcover Book
USD   379.99
Price excludes VAT (USA)
Fig. 1
Fig. 2
Fig. 3
Fig. 4
Scheme 1
Fig. 5
Fig. 6

References

  • Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16:1066–1071

    CAS  PubMed  Google Scholar 

  • Aggarwal BB, Gupta SC, Kim JH (2012) Historical perspectives on tumor necrosis factor and its superfamily: 25 years later, a golden journey. Blood 119:651–665

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ali MY, Ping CY, Mok YY et al (2006) Regulation of vascular nitric oxide in vitro and in vivo; a new role for endogenous hydrogen sulphide? Br J Pharmacol 149:625–634

    CAS  PubMed Central  PubMed  Google Scholar 

  • Artaud I, Galardon E (2014) A persulfide analogue of the nitrosothiol SNAP: formation, characterization and reactivity. Chembiochem 15:2361–2364

    CAS  PubMed  Google Scholar 

  • Bailey TS, Zakharov LN, Pluth MD (2014) Understanding hydrogen sulfide storage: probing conditions for sulfide release from hydrodisulfides. J Am Chem Soc 136:10573–10576

    CAS  PubMed Central  PubMed  Google Scholar 

  • Blackstone E, Morrison M, Roth MB (2005) H2S induces a suspended animation-like state in mice. Science 308:518

    CAS  PubMed  Google Scholar 

  • Bouillaud F, Blachier F (2011) Mitochondria and sulfide: a very old story of poisoning, feeding, and signaling? Antioxid Redox Signal 15:379–391

    CAS  PubMed  Google Scholar 

  • Broniowska KA, Hogg N (2012) The chemical biology of S-nitrosothiols. Antioxid Redox Signal 17:969–980

    CAS  PubMed Central  PubMed  Google Scholar 

  • Calvert JW, Jha S, Gundewar S et al (2009) Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ Res 105:365–374

    CAS  PubMed Central  PubMed  Google Scholar 

  • Calvert JW, Elston M, Nicholson CK et al (2010) Genetic and pharmacologic hydrogen sulfide therapy attenuates ischemia-induced heart failure in mice. Circulation 122:11–19

    PubMed Central  PubMed  Google Scholar 

  • Carballal S, Radi R, Kirk MC, Barnes S, Freeman BA, Alvarez B (2003) Sulfenic acid formation in human serum albumin by hydrogen peroxide and peroxynitrite. Biochemistry 42:9906–9914

    CAS  PubMed  Google Scholar 

  • Carballal S, Trujillo M, Cuevasanta E et al (2011) Reactivity of hydrogen sulfide with peroxynitrite and other oxidants of biological interest. Free Radic Biol Med 50:196–205

    CAS  PubMed  Google Scholar 

  • Chen W, Liu C, Peng B, Zhao Y, Pacheco A, Xian M (2013) New fluorescent probes for sulfane sulfurs and the application in bioimaging. Chem Sci 4:2892–2896

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chung KK, Thomas B, Li X et al (2004) S-nitrosylation of parkin regulates ubiquitination and compromises parkin’s protective function. Science 304:1328–1331

    CAS  PubMed  Google Scholar 

  • Cohen-Armon M, Visochek L, Rozensal D, Kalal A, Geistrikh I, Klein R, Bendetz-Nezer S, Yao Z, Seger R (2007) DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation. Mol Cell 25:297–308

    CAS  PubMed  Google Scholar 

  • Coletta C, Papapetropoulos A, Erdelyi K et al (2012) Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc Natl Acad Sci USA 109(23):9161–9166

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cuevasanta E, Denicola A, Alvarez B, Moller MN (2012) Solubility and permeation of hydrogen sulfide in lipid membranes. PLoS ONE 7:e34562

    CAS  PubMed Central  PubMed  Google Scholar 

  • D’Amours D, Desnoyers S, D'Silva I, Poirier GG (1999) Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 342:249–268

    PubMed Central  PubMed  Google Scholar 

  • Das TN, Huie RE, Neta P, Padmaja S (1999) Reduction potential of the sulfhydryl radical: pulse radiolysis and laser flash photolysis studies of the formation and reactions of center dot SH and HSSH center dot(-) in aqueous solutions. J Phys Chem A 103:5221–5226

    CAS  Google Scholar 

  • Du J, Huang Y, Yan H et al (2014) Hydrogen sulfide suppresses oxidized low-density lipoprotein (ox-LDL)-stimulated monocyte chemoattractant protein 1 generation from macrophages via the nuclear factor κB (NF-κB) pathway. J Biol Chem 289:9741–9753

    CAS  PubMed Central  PubMed  Google Scholar 

  • Eberhardt M, Dux M, Namer B et al (2014) H2S and NO cooperatively regulate vascular tone by activating a neuroendocrine HNO-TRPA1-CGRP signalling pathway. Nat Commun 5:4381

    CAS  PubMed Central  PubMed  Google Scholar 

  • Filipovic MR, Miljkovic J, Allgäuer A et al (2012a) Biochemical insight into physiological effects of H2S: reaction with peroxynitrite and formation of a new nitric oxide donor, sulfinyl nitrite. Biochem J 441:609–621

    CAS  PubMed  Google Scholar 

  • Filipovic MR, Miljkovic J, Nauser T et al (2012b) Chemical characterization of the smallest S-nitrosothiol, HSNO; cellular cross-talk of H2S and S-nitrosothiols. J Am Chem Soc 134:12016–12027

    CAS  PubMed Central  PubMed  Google Scholar 

  • Filipovic MR, Eberhardt M, Prokopovic V et al (2013) Beyond H2S and NO interplay: hydrogen sulfide and nitroprusside react directly to give nitroxyl (HNO). A new pharmacological source of HNO. J Med Chem 56:1499–1508

    CAS  PubMed  Google Scholar 

  • Flavin M (1962) Microbial transsulfuration: the mechanism of an enzymatic disulfide elimination reaction. J Biol Chem 237:768–777

    CAS  PubMed  Google Scholar 

  • Forrester MT, Foster MW, Benhar M, Stamler JS (2009) Detection of protein S-nitrosylation with the biotin-switch technique. Free Radic Biol Med 46:119–126

    CAS  PubMed Central  PubMed  Google Scholar 

  • Foster MW, Hess DT, Stamler JS (2009) Protein S-nitrosylation in health and disease: a current perspective. Trends Mol Med 15:391–404

    CAS  PubMed Central  PubMed  Google Scholar 

  • Francoleon NE, Carrington SJ, Fukuto JM (2011) The reaction of H2S with oxidized thiols: generation of persulfides and implications to H2S biology. Arch Biochem Biophys 516:146–153

    CAS  PubMed  Google Scholar 

  • Fujii S, Akaike T (2013) Redox signaling by 8-nitro-cyclic guanosine monophosphate: nitric oxide- and reactive oxygen species-derived electrophilic messenger. Antioxid Redox Signal 19:1236–1246

    CAS  PubMed  Google Scholar 

  • Fulton AB (1982) How crowded is the cytoplasm? Cell 30:345–347

    CAS  PubMed  Google Scholar 

  • Giorgio M, Migliaccio E, Orsini F et al (2005) Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122:221–233

    CAS  PubMed  Google Scholar 

  • Greiner R, Palinkas Z, Basell K et al (2013) Polysulfides link H2S to protein thiol oxidation. Antioxid Redox Signal 19:1749–1765

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gupta V, Carroll KS (2014) Sulfenic acid chemistry, detection and cellular lifetime. Biochim Biophys Acta 1840:847–875

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hara MR, Agrawal N, Kim SF et al (2005) S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol 7:665–674

    CAS  PubMed  Google Scholar 

  • Heimer NE (1981) Biologically oriented organic sulfur chemistry. 21. Hydrodisulfide of a penicillamine derivative and related compounds. J Org Chem 46:1374–1377

    CAS  Google Scholar 

  • Herrmann M, Widmann T, Colaianni G, Colucci S, Zallone A, Herrmann W (2005) Increased osteoclast activity in the presence of increased homocysteine concentrations. Clin Chem 51:2348–2353

    CAS  PubMed  Google Scholar 

  • Hess DT, Stamler JS (2012) Regulation by S-nitrosylation of protein post-translational modification. J Biol Chem 287:4411–4418

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hill BC, Woon TC, Nicholls P, Peterson J, Greenwood C, Thomson AJ (1984) Interactions of sulphide and other ligands with cytochrome c oxidase. An electron-paramagnetic-resonance study. Biochem J 224:591–600

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hourihan JM, Kenna JG, Hayes JD (2013) The gasotransmitter hydrogen sulfide induces nrf2-target genes by inactivating the keap1 ubiquitin ligase substrate adaptor through formation of a disulfide bond between cys-226 and cys-613. Antioxid Redox Signal 19:465–481

    CAS  PubMed  Google Scholar 

  • Hybertson BM, Gao B, Bose SK, McCord JM (2011) Oxidative stress in health and disease: the therapeutic potential of Nrf2 activation. Mol Aspects Med 32:234–246

    CAS  PubMed  Google Scholar 

  • Ida T, Sawa T, Ihara H et al (2014) Reactive cysteine persulfides and S-polythiolation regulate oxidative stress and redox signaling. Proc Natl Acad Sci USA 111:7606–7611

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ivanovic-Burmazovic I, Filipovic MR (2012) WO2012/175630

    Google Scholar 

  • Jackson MR, Melideo SL, Jorns MS (2012) Human sulfide:quinone oxidoreductase catalyzes the first step in hydrogen sulfide metabolism and produces a sulfane sulfur metabolite. Biochemistry 51:6804–6815

    CAS  PubMed  Google Scholar 

  • Kabil O, Banerjee R (2014) Enzymology of H2S biogenesis, decay and signaling. Antioxid Redox Signal 20:770–782

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kabil O, Motl N, Banerjee R (2014) H2S and its role in redox signaling. Biochim Biophys Acta. doi:10.1016/j.bbapap.2014.01.002

    PubMed  Google Scholar 

  • Karala AR, Ruddock LW (2007) Does s-methyl methanethiosulfonate trap the thiol-disulfide state of proteins? Antioxid Redox Signal 9:527–531

    CAS  PubMed  Google Scholar 

  • Kaspar JW, Niture SK, Jaiswal AK (2009) Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med 47:1304–1309

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kimura H (2014) Hydrogen sulfide and polysulfides as biological mediators. Molecules 19:16146–16157

    PubMed  Google Scholar 

  • Kimura H, Nagai Y, Umemura K, Kimura Y (2005) Physiological roles of hydrogen sulfide: synaptic modulation, neuroprotection, and smooth muscle relaxation. Antioxid Redox Signal 7:795–803

    CAS  PubMed  Google Scholar 

  • Kimura Y, Mikami Y, Osumi K, Tsugane M, Oka J, Kimura H (2013) Polysulfides are possible H2S-derived signaling molecules in rat brain. FASEB J 27:2451–2457

    CAS  PubMed  Google Scholar 

  • Koenitzer JR, Isbell TS, Patel HD et al (2007) Hydrogen sulfide mediates vasoactivity in an O-2-dependent manner. Am J Physiol Heart Circ Physiol 292:H1953–H1960

    CAS  PubMed  Google Scholar 

  • Kotronarou A, Hoffmann MR (1991) Catalytic autooxidation of hydrogen sulfide in wastewater. Environ Sci Technol 25:1153–1160

    CAS  Google Scholar 

  • Krishnan N, Fu C, Pappin DJ, Tonks NK (2011) H2S-induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Sci Signal 4(203):ra86

    PubMed Central  PubMed  Google Scholar 

  • Kutney GW, Turnbull K (1982) Compounds containing the sulfur-sulfur double bond. Chem Rev 82:333–357

    CAS  Google Scholar 

  • Li L, Bhatia M, Zhu YZ et al (2005) Hydrogen sulfide is a novel mediator of lipopolysaccharide-induced inflammation in the mouse. FASEB J 19:1196–1198

    CAS  PubMed  Google Scholar 

  • Li L, Hsu A, Moore PK (2009) Actions and interactions of nitric oxide, carbon monoxide and hydrogen sulphide in the cardiovascular system and in inflammation–a tale of three gases! Pharmacol Ther 123:386–400

    CAS  PubMed  Google Scholar 

  • Libiad M, Yadav PK, Vitvitsky V, Martinov M, Banerjee R (2014) Organization of the human mitochondrial H2S oxidation pathway. J Biol Chem pii: jbc.M114.602664

    Google Scholar 

  • Lima B, Forrester MT, Hess DT, Stamler JS (2010) S-nitrosylation in cardiovascular signaling. Circ Res 106:633–646

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu C, Chen W, Shi W et al (2014a) Rational design and bioimaging applications of highly selective fluorescence probes for hydrogen polysulfides. J Am Chem Soc 136:7257–7260

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu C, Zhang F, Munske G, Zhang H, Xian M (2014b) Isotope dilution mass spectrometry for the quantification of sulfane sulfurs. Free Radic Biol Med 76C:200–207

    Google Scholar 

  • Liu Y, Yang R, Liu X et al (2014c) Hydrogen sulfide maintains mesenchymal stem cell function and bone homeostasis via regulation of Ca(2+) channel sulfhydration. Cell Stem Cell 15:66–78

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mathai JC, Missner A, Kugler P et al (2009) No facilitator required for membrane transport of hydrogen sulfide. Proc Natl Acad Sci USA 106:16633–16638

    CAS  PubMed Central  PubMed  Google Scholar 

  • Melton LJ 3rd (2003) Adverse outcomes of osteoporotic fractures in the general population. J Bone Miner Res 18:1139–1141

    PubMed  Google Scholar 

  • Mikami Y, Shibuya N, Kimura Y, Nagahara N, Ogasawara Y, Kimura H (2011) Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide. Biochem J 439:479–485

    CAS  PubMed  Google Scholar 

  • Miljkovic JL, Kenkel I, Ivanovic-Burmazovic I, Filipovic MR (2013) Generation of HNO and HSNO from nitrite by heme-iron-catalyzed metabolism with H2S. Angew Chem Int Ed Engl 52:12061–12064

    CAS  PubMed  Google Scholar 

  • Minton AP (1998) Molecular crowding: analysis of effects of high concentrations of inert cosolutes on biochemical equilibria and rates in terms of volume exclusion. Methods Enzymol 295:27–149

    Google Scholar 

  • Módis K, Coletta C, Erdélyi K, Papapetropoulos A, Szabo C (2013) Intramitochondrial hydrogen sulfide production by 3-mercaptopyruvate sulfurtransferase maintains mitochondrial electron flow and supports cellular bioenergetics. FASEB J 27:601–611

    PubMed  Google Scholar 

  • Moore DJ, West AB, Dawson VL, Dawson TM (2005) Molecular pathophysiology of Parkinson’s disease. Annu Rev Neurosci 28:57–87

    CAS  PubMed  Google Scholar 

  • Moriarty-Craige SE, Jones DP (2004) Extracellular thiols and thiol/disulfide redox in metabolism. Annu Rev Nutr 24:481–509

    CAS  PubMed  Google Scholar 

  • Mueller EG (2006) Trafficking in persulfides: delivering sulfur in biosynthetic pathways. Nat Chem Biol 2:185–194

    CAS  PubMed  Google Scholar 

  • Mustafa AK, Gadalla MM, Sen N et al (2009a) H2S signals through protein S-sulfhydration. Sci Signal 2:ra72

    PubMed Central  PubMed  Google Scholar 

  • Mustafa AK, Gadalla MM, Snyder SH (2009b) Signaling by gasotransmitters. Sci Signal 2:re2

    PubMed Central  PubMed  Google Scholar 

  • Mustafa AK, Sikka G, Gazi SK et al (2011) Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels. Circ Res 109:1259–1268

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nagy P, Winterbourn CC (2010) Rapid reaction of hydrogen sulfide with the neutrophil oxidant hypochlorous acid to generate polysulfides. Chem Res Toxicol 23:1541–1543

    CAS  PubMed  Google Scholar 

  • Napetschnig J, Wu H (2013) Molecular basis of NF-κB signaling. Annu Rev Biophys 42:443–468

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nicholls P, Marshall DC, Cooper CE, Wilson MT (2013) Sulfide inhibition of and metabolism by cytochrome c oxidase. Biochem Soc Trans 41:1312–1316

    CAS  PubMed  Google Scholar 

  • Nishida M, Sawa T, Kitajima N et al (2012) Hydrogen sulfide anion regulates redox signaling via electrophile sulfhydration. Nat Chem Biol 8:714–724

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nishida M, Toyama T, Akaike T (2014) Role of 8-nitro-cGMP and its redox regulation in cardiovascular electrophilic signaling. J Mol Cell Cardiol 73:10–17

    CAS  PubMed  Google Scholar 

  • Olson KR (2012) A practical look at the chemistry and biology of hydrogen sulfide. Antioxid Redox Signal 17:32–44

    CAS  PubMed Central  PubMed  Google Scholar 

  • Olson KR, Healy MJ, Qin Z et al (2008) Hydrogen sulfide as an oxygen sensor in trout gill chemoreceptors. Am J Physiol Regul Integr Comp Physiol 295:R669–R680

    CAS  PubMed  Google Scholar 

  • Olson KR, DeLeon ER, Liu F (2014) Controversies and conundrums in hydrogen sulfide biology. Nitric Oxide 41:11–26

    CAS  PubMed  Google Scholar 

  • Ono K, Akaike T, Sawa T et al (2014) Redox chemistry and chemical biology of H2S, hydropersulfides, and derived species: implications of their possible biological activity and utility. Free Radic Biol Med. doi:10.1016/j.freeradbiomed.2014.09.007

    PubMed  Google Scholar 

  • Pálinkás Z, Furtmüller PG, Nagy A et al (2014) Interactions of hydrogen sulfide with myeloperoxidase. Br J Pharmacol. doi:10.1111/bph.12769

    PubMed  Google Scholar 

  • Pan J, Carroll KS (2013) Persulfide reactivity in the detection of protein S-sulfhydration. ACS Chem Biol 8:1110–1116

    CAS  PubMed Central  PubMed  Google Scholar 

  • Papapetropoulos A, Pyriochou A, Altaany Z et al (2009) Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc Natl Acad Sci USA 106:21972–21977

    CAS  PubMed Central  PubMed  Google Scholar 

  • Park CM, Macinkovic I, Filipovic MR, Xian M (2015) Use of the “Tag-Switch” method for the detection of protein S-Sulfhydration. Methods Enzymol. doi:10.1016/bs.mie.2014.11.033

    Google Scholar 

  • Parsons LB, Walton JH (1921) Preparation and properties of the persulfides of hydrogen. J Am Chem Soc 43:2539–2548

    Google Scholar 

  • Paul BD, Snyder SH (2012) H2S signalling through protein sulfhydration and beyond. Nat Rev Mol Cell Biol 13:499–507

    CAS  PubMed  Google Scholar 

  • Paulsen CE, Carroll KS (2013) Cysteine-mediated redox signaling: chemistry, biology, and tools for discovery. Chem Rev 113:4633–4679

    CAS  PubMed Central  PubMed  Google Scholar 

  • Paulsen CE, Truong TH, Garcia FJ et al (2011) Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat Chem Biol 8:57–64

    PubMed Central  PubMed  Google Scholar 

  • Peaper DR, Wearsch PA, Cresswell P (2005) Tapasin and ERp57 form a stable disulfide-linked dimer within the MHC class I peptide-loading complex. EMBO J 24:3613–3623

    CAS  PubMed Central  PubMed  Google Scholar 

  • Peng YJ, Nanduri J, Raghuraman G et al (2010) H2S mediates O2 sensing in the carotid body. Proc Natl Acad Sci USA 107:10719–10724

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pietri R, Lewis A, León RG et al (2009) Factors controlling the reactivity of hydrogen sulfide with hemeproteins. Biochemistry 48:4881–4894

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pittenge MF, Mackay AM, Beck SC et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147

    Google Scholar 

  • Poynton RA, Hampton MB (2014) Peroxiredoxins as biomarkers of oxidative stress. Biochim Biophys Acta 1840:906–912

    CAS  PubMed  Google Scholar 

  • Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71–74

    CAS  PubMed  Google Scholar 

  • Reynolds JD, Bennett KM, Cina AJ et al (2013) S-nitrosylation therapy to improve oxygen delivery of banked blood. Proc Natl Acad Sci USA 110:11529–11534

    CAS  PubMed Central  PubMed  Google Scholar 

  • Riahi S, Rowley CN (2014) Why can hydrogen sulfide permeate cell membranes? J Am Chem Soc 136:15111–15113

    CAS  PubMed  Google Scholar 

  • Ríos-González BB, Román-Morales EM, Pietri R, López-Garriga J (2014) Hydrogen sulfide activation in hemeproteins: the sulfheme scenario. J Inorg Biochem 133:78–86

    PubMed Central  PubMed  Google Scholar 

  • Sen N, Paul BD, Gadalla MM et al (2012) Hydrogen sulfide-linked sulfhydration of NF-κB mediates its antiapoptotic actions. Mol Cell 45:13–24

    CAS  PubMed Central  PubMed  Google Scholar 

  • Seth D, Stamler JS (2011) The SNO-proteome: causation and classifications. Curr Opin Chem Biol 15:129–136

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shulman JM, De Jager PL, Feany MB (2011) Parkinson’s disease: genetics and pathogenesis. Annu Rev Pathol 6:193–222

    CAS  PubMed  Google Scholar 

  • Sparatore A, Perrino E, Tazzari V et al (2008) Pharmacological profile of a novel H2S-releasing aspirin. Free Radic Biol Med 46:586–592

    PubMed  Google Scholar 

  • Steudel R, Drozdova Y, Miaskiewicz K, Hertwig RH, Koch W (1997) How unstable are thiosulfoxides? An ab initio MO study of various disulfanes RSSR (R = H, Me, Pr, All), their branched isomers R2SS, and the related transition states. J Am Chem Soc 119:1990–1996

    CAS  Google Scholar 

  • Szabó C, Papapetropoulos A (2011) Hydrogen sulphide and angiogenesis: mechanisms and applications. Br J Pharmacol 164:853–865

    PubMed Central  PubMed  Google Scholar 

  • Szczesny B, Módis K, Yanagi K et al (2014) AP39, a novel mitochondria-targeted hydrogen sulfide donor, stimulates cellular bioenergetics, exerts cytoprotective effects and protects against the loss of mitochondrial DNA integrity in oxidatively stressed endothelial cells in vitro. Nitric Oxide 41:120–130

    CAS  PubMed Central  PubMed  Google Scholar 

  • Talipov MR, Timerghazin QK (2013) Protein control of S-nitrosothiol reactivity: interplay of antagonistic resonance structures. J Phys Chem B 117:1827–1837

    CAS  PubMed  Google Scholar 

  • Terzić V, Padovani D, Balland V, Artauda I, Galardon E (2014) Electrophilic sulfhydration of 8-nitro-cGMP involves sulfane sulfur. Org Biomol Chem 12:5360–5364

    PubMed  Google Scholar 

  • van Montfort RL, Congreve M, Tisi D, Carr R, Jhoti H (2003) Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423:773–777

    PubMed  Google Scholar 

  • Vandiver MS, Paul BD, Xu R et al (2013) Sulfhydration mediates neuroprotective actions of parkin. Nat Commun 4:1626

    PubMed Central  PubMed  Google Scholar 

  • Vitvitsky V, Kabil O, Banerjee R (2012) High turnover rates for hydrogen sulfide allow for rapid regulation of its tissue concentrations. Antioxid Redox Signal 17:22–31

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wakabayashi N, Dinkova-Kostova AT, Holtzclaw WD, Kang MI, Kobayashi A, Yamamoto M, Kensler TW, Talalay P (2004) Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proc Natl Acad Sci U S A 101:2040–2045

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang R (2002) Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16:1792–1808

    CAS  PubMed  Google Scholar 

  • Wedmann R, Bertlein S, Macinkovic I, Boeltz S, Miljkovic J, Munoz L, Herrmann M, Filipovic MR (2014) Working with “H2S”: facts and apparent artifacts. Nitric Oxide 41:85–96

    CAS  PubMed  Google Scholar 

  • Whiteman M, Winyard PG (2011) Hydrogen sulfide and inflammation: the good, the bad, the ugly and the promising. Expert Rev Clin Pharmacol 4:13–32

    CAS  PubMed  Google Scholar 

  • Whiteman M, Li L, Kostetski I et al (2006) Evidence for the formation of a novel nitrosothiol from the gaseous mediators nitric oxide and hydrogen sulphide. Biochem Biophys Res Commun 343:303–310

    CAS  PubMed  Google Scholar 

  • Wood JL (1987) Sulfane sulfur. Methods Enzymol 143:25–29

    CAS  PubMed  Google Scholar 

  • Xie ZZ, Shi MM, Xie L et al (2014) Sulfhydration of p66Shc at cysteine59 mediates the antioxidant effect of hydrogen sulfide. Antioxid Redox Signal. doi:10.1089/ars.2013.5604

    PubMed Central  Google Scholar 

  • Xu L, Eu JP, Meissner G, Stamler JS (1998) Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science 279:234–237

    CAS  PubMed  Google Scholar 

  • Xu ZS, Wang XY, Xiao DM, Hu LF, Lu M, Wu ZY, Bian JS (2011) Hydrogen sulfide protects MC3T3-E1 osteoblastic cells against H2O2-induced oxidative damage-implications for the treatment of osteoporosis. Free Radic Biol Med 50(10):1314–23

    CAS  PubMed  Google Scholar 

  • Yadav PK, Yamada K, Chiku T, Koutmos M, Banerjee R (2013) Structure and kinetic analysis of H2S production by human mercaptopyruvate sulfurtransferase. J Biol Chem 288:20002–200013

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang G, Wu L, Jiang B et al (2008) H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 322:587–590

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang G, Zhao K, Ju Y et al (2013) Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2. Antioxid Redox Signal 18:1906–1919

    CAS  PubMed  Google Scholar 

  • Yang J, Gupta V, Carroll KS, Liebler DC (2014) Site-specific mapping and quantification of protein S-sulphenylation in cells. Nat Commun 5:4776

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yong QC, Hu LF, Wang S, Huang D, Bian JS (2010) Hydrogen sulfide interacts with nitric oxide in the heart: possible involvement of nitroxyl. Cardiovasc Res 88:482–491

    CAS  PubMed  Google Scholar 

  • Yong QC, Cheong JL, Hua F et al (2011) Regulation of heart function by endogenous gaseous mediators-crosstalk between nitric oxide and hydrogen sulfide. Antioxid Redox Signal 14:2081–2091

    CAS  PubMed  Google Scholar 

  • Yoshida T, Inoue R, Morii T et al (2006) Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat Chem Biol 2:596–607

    CAS  PubMed  Google Scholar 

  • Zhang D, Macinkovic I, Devarie-Baez NO et al (2014) Detection of protein S-sulfhydration by a tag-switch technique. Angew Chem Int Ed Engl 53:575–581

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao Y, Bhushan S, Yang C et al (2013) Controllable hydrogen sulfide donors and their activity against myocardial ischemia-reperfusion injury. ACS Chem Biol 8:1283–1290

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao K, Ju Y, Li S, Altaany Z, Wang R, Yang G (2014) S-sulfhydration of MEK1 leads to PARP-1 activation and DNA damage repair. EMBO Rep 15:792–800

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhou Z, von Wantoch Rekowski M, Coletta C et al (2012) Thioglycine and L-thiovaline: biologically active H2S-donors. Bioorg Med Chem 20:2675–2678

    CAS  PubMed  Google Scholar 

Download references

Acknowledgement

The author is grateful to professors Ivana Ivanovic-Burmazovic, Jon Fukuto and Ruma Banerjee for the helpful discussion. This work is supported by the FAU Erlangen-Nuremberg intramural grant within Emerging Fields Initiative (MRIC).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Milos R. Filipovic .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and Permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Filipovic, M.R. (2015). Persulfidation (S-sulfhydration) and H2S. In: Moore, P., Whiteman, M. (eds) Chemistry, Biochemistry and Pharmacology of Hydrogen Sulfide. Handbook of Experimental Pharmacology, vol 230. Springer, Cham. https://doi.org/10.1007/978-3-319-18144-8_2

Download citation