Reactive cysteine persulfides and S-polythiolation regulate oxidative stress and redox signaling

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 21, 2014, Pages 7606-7611

  Ida, Tomoaki ^a   Sawa, Tomohiro ^a,b   Ihara, Hideshi ^c   Tsuchiya, Yukihiro ^d   Watanabe, Yasuo ^d   Kumagai, Yoshito ^e   Suematsu, Makoto ^f   Motohashi, Hozumi ^g   Fujii, Shigemoto ^a   Matsunaga, Tetsuro ^a   Yamamoto, Masayuki ^a   Ono, Katsuhiko ^h   Devarie Baez, Nelmi O ⁱ   Xian, Ming ⁱ   Fukuto, Jon M ^h   Akaike, Takaaki ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c Osaka Prefecture University   (Japan)

^d SHOWA PHARMACEUTICAL UNIVERSITY   (Japan)

^e UNIVERSITY OF TSUKUBA   (Japan)

^f KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^g TOHOKU UNIVERSITY   (Japan)

^h SONOMA STATE UNIVERSITY   (United States)

ⁱ WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Electrophilic signaling; Hydrogen sulfide; Polysulfidomics; Thiol redox

Indexed keywords

8 NITROGUANOSINE 3',5' CYCLIC MONOPHOSPHATE; ANTIOXIDANT; CYSTATHIONINE BETA SYNTHASE; CYSTATHIONINE GAMMA LYASE; CYSTEINE DERIVATIVE; CYSTEINE HYDROPERSULFIDE DERIVATIVE; CYTOPROTECTIVE AGENT; DISULFIDE; GLUTATHIONE; GLUTATHIONE DISULFIDE; GUANOSINE DERIVATIVE; HYDROGEN PEROXIDE; HYDROGEN SULFIDE; REACTIVE SULFUR SPECIES; RIBONUCLEOTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BIOLOGICAL ACTIVITY; CELL PROTECTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEGRADATION KINETICS; ELECTROPHILICITY; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; LIMIT OF QUANTITATION; MAMMAL CELL; MOUSE; NONHUMAN; NUCLEOPHILICITY; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN METABOLISM; REGULATORY MECHANISM; S POLYTHIOLATION;

ELECTROPHILIC SIGNALING; HYDROGEN SULFIDE; POLYSULFIDOMICS; THIOL REDOX;

ANIMALS; CHROMATOGRAPHY, LIQUID; CYCLIC GMP; CYSTATHIONINE BETA-SYNTHASE; CYSTATHIONINE GAMMA-LYASE; CYSTEINE; DISULFIDES; HUMANS; HYDROGEN PEROXIDE; MICE; OXIDATION-REDUCTION; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; SULFHYDRYL COMPOUNDS; TANDEM MASS SPECTROMETRY;

EID: 84901659489     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1321232111     Document Type: Article

References (27)

1. Toohey JI (2011) Sulfur signaling: Is the agent sulfide or sulfane? Anal Biochem 413(1): 1-7.
2. Nishida M, et al. (2012) Hydrogen sulfide anion regulates redox signaling via elec-trophile sulfhydration. Nat Chem Biol 8(8):714-724.
3. Iciek M, Włodek L (2001) Biosynthesis and biological properties of compounds containing highly reactive, reduced sulfane sulfur. Pol J Pharmacol 53(3):215-225.
4. Paulsen CE, Carroll KS (2013) Cysteine-mediated redox signaling: Chemistry, biology, and tools for discovery. Chem Rev 113(7):4633-4679.
5. Fukuto JM, et al. (2012) Small molecule signaling agents: The integrated chemistry and biochemistry of nitrogen oxides, oxides of carbon, dioxygen, hydrogen sulfide, and their derived species. Chem Res Toxicol 25(4):769-793.
6. Mueller EG (2006) Trafficking in persulfides: Delivering sulfur in biosynthetic pathways. Nat Chem Biol 2(4):185-194.
7. 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(34):6804-6815.
8. Yamanishi T, Tuboi S (1981) The mechanism of the L-cystine cleavage reaction catalyzed by rat liver γ-cystathionase. J Biochem 89(6):1913-1921.
9. Kabil O, Banerjee R (2010) Redox biochemistry of hydrogen sulfide. J Biol Chem 285(29):21903-21907.
10. Chen W, et al. (2013) New fluorescent probes for sulfane sulfurs and the application in bioimaging. Chem Sci 4(7):2892-2896.
11. Meister A (1988) Glutathione metabolism and its selective modification. J Biol Chem 263(33):17205-17208. (Pubitemid 19029311)
12. Hyde R, Taylor PM, Hundal HS (2003) Amino acid transporters: Roles in amino acid sensing and signalling in animal cells. Biochem J 373(Pt 1):1-18. (Pubitemid 36819495)
13. Conrad M, Sato H (2012) The oxidative stress-inducible cystine/glutamate antiporter, system x (c) (-): Cystine supplier and beyond. Amino Acids 42(1):231-246.
14. Zhang D, Devarie-Baez NO, Li Q, Lancaster JR, Jr., Xian M (2012) Methylsulfonyl ben-zothiazole (MSBT): A selective protein thiol blocking reagent. Org Lett 14(13):3396-3399.
15. Francoleon NE, Carrington SJ, Fukuto JM (2011) The reaction of H(2)S with oxidized thiols: Generation of persulfides and implications to H(2)S biology. Arch Biochem Bi-ophys 516(2):146-153.
16. Sawa T, et al. (2007) Protein S-guanylation by the biological signal 8-nitroguanosine 3′, 5′-cyclic monophosphate. Nat Chem Biol 3(11):727-735. (Pubitemid 47609113)
17. Akaike T, Nishida M, Fujii S (2013) Regulation of redox signalling by an electrophilic cyclic nucleotide. J Biochem 153(2):131-138.
18. Kawamura S, Otsuji Y, Nakabayashi T, Kitao T, Tsurugi J (1965) Aralkyl hydrodisulfides. IV. The reaction of benzylhydrodisulfide with several nucleophiles. J Org Chem 30(8):2711-2714.
19. Moutiez M, et al. (1994) Reduction of a trisulfide derivative of glutathione by glu-tathione reductase. Biochem Biophys Res Commun 202(3):1380-1386. (Pubitemid 24265920)
20. Stipanuk MH (1986) Metabolism of sulfur-containing amino acids. Annu Rev Nutr 6: 179-209.
21. Greiner R, et al. (2013) Polysulfides link H2S to protein thiol oxidation. Antioxid Redox Signal 19(15):1749-1765.
22. Sen N, et al. (2012) Hydrogen sulfide-linked sulfhydration of NF-κB mediates its an-tiapoptotic actions. Mol Cell 45(1):13-24.
23. Kimura Y, et al. (2013) Polysulfides are possible H2S-derived signaling molecules in rat brain. FASEB J 27(6):2451-2457.
24. Mustafa AK, et al. (2009) H2S signals through protein S-sulfhydration. Sci Signal 2(96):ra72.
25. Pan J, Carroll KS (2013) Persulfide reactivity in the detection of protein s-sulfhydra-tion. ACS Chem Biol 8(6):1110-1116.
26. Hayes JD, Flanagan JU, Jowsey IR (2005) Glutathione transferases. Annu Rev Pharmacol Toxicol 45:51-88. (Pubitemid 40261798)
27. Schopfer FJ, Cipollina C, Freeman BA (2011) Formation and signaling actions of elec-trophilic lipids. Chem Rev 111(10):5997-6021.