H2S: A Novel Gasotransmitter that Signals by Sulfhydration

Trends in Biochemical Sciences

Volumn 40, Issue 11, 2015, Pages 687-700

  Paul, Bindu D ^a   Snyder, Solomon H ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cysteine; Gasotransmitter; Hydrogen sulfide; Sulfhydration

Indexed keywords

ENDOTHELIUM DERIVED RELAXING FACTOR; GASOTRANSMITTER; HEME OXYGENASE 2; HYDROGEN SULFIDE; MALEIMIDE; MITOCHONDRIAL DNA; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; THIOMESYLIC ACID METHYL ESTER;

BIOASSAY; BIOSYNTHESIS; CELL FUNCTION; CHEMICAL MODIFICATION; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; MODIFIED BIOTIN SWITCH ASSAY; NITROSYLATION; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTON TRANSPORT; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SULFHYDRATION; UNFOLDED PROTEIN RESPONSE; METABOLISM;

GASOTRANSMITTERS; HYDROGEN SULFIDE; SIGNAL TRANSDUCTION;

EID: 84945930415     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2015.08.007     Document Type: Review

References (86)

1. 2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 2008, 322:587-590.
2. 2S signalling through protein sulfhydration and beyond. Nat. Rev. Mol. Cell Biol. 2012, 13:499-507.
3. Shibuya N., et al. A novel pathway for the production of hydrogen sulfide from D-cysteine in mammalian cells. Nat. Commun. 2013, 4:1366.
4. Wang R. Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol. Rev. 2012, 92:791-896.
5. 2S signaling in the brain and peripheral tissues. Antiox. Redox Signal. 2015, 22:411-423.
6. Sen N., et al. Hydrogen sulfide-linked sulfhydration of NF-kappaB mediates its antiapoptotic actions. Mol. Cell 2012, 45:13-24.
7. 2S production in lipopolysaccharide-treated macrophages. Cell. Mol. Life Sci. 2010, 67:1119-1132.
8. Kaneko Y., et al. Glucose-induced production of hydrogen sulfide may protect the pancreatic beta-cells from apoptotic cell death by high glucose. FEBS Lett. 2009, 583:377-382.
9. Hine C., et al. Endogenous hydrogen sulfide production is essential for dietary restriction benefits. Cell 2015, 160:132-144.
10. 2S-Induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Sci. Signal. 2011, 4:ra86.
11. Finkelstein J.D., et al. Activation of cystathionine synthase by adenosylmethionine and adenosylethionine. Biochem. Biophys. Res. Commun. 1975, 66:81-87.
12. Ereno-Orbea J., et al. Structural insight into the molecular mechanism of allosteric activation of human cystathionine beta-synthase by S-adenosylmethionine. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:E3845-E3852.
13. Morikawa T., et al. Hypoxic regulation of the cerebral microcirculation is mediated by a carbon monoxide-sensitive hydrogen sulfide pathway. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:1293-1298.
14. Hishiki T., et al. Carbon monoxide: impact on remethylation/transsulfuration metabolism and its pathophysiologic implications. J. Mol. Med. 2012, 90:245-254.
15. Vicente J.B., et al. NO* binds human cystathionine beta-synthase quickly and tightly. J. Biol. Chem. 2014, 289:8579-8587.
16. Kabil O., et al. Reversible heme-dependent regulation of human cystathionine beta-synthase by a flavoprotein oxidoreductase. Biochemistry 2011, 50:8261-8263.
17. Enokido Y., et al. Cystathionine beta-synthase, a key enzyme for homocysteine metabolism, is preferentially expressed in the radial glia/astrocyte lineage of developing mouse CNS. FASEB J. 2005, 19:1854-1856.
18. Shibuya N., et al. 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid. Redox Signal. 2009, 11:703-714.
19. Kimura H. Hydrogen sulfide: its production, release and functions. Amino Acids 2011, 41:113-121.
20. Ishigami M., et al. A source of hydrogen sulfide and a mechanism of its release in the brain. Antioxid. Redox Signal. 2009, 11:205-214.
21. Mikami Y., et al. Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide. Biochem. J. 2011, 439:479-485.
22. Carbonero F., et al. Microbial pathways in colonic sulfur metabolism and links with health and disease. Front. Physiol. 2012, 3:448.
23. Pfennig N., Widdel F. The bacteria of the sulphur cycle. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 1982, 298:433-441.
24. Linden D.R. Hydrogen sulfide signaling in the gastrointestinal tract. Antioxid. Redox Signal. 2014, 20:818-830.
25. 2S signals through protein S-sulfhydration. Sci. Signal. 2009, 2:ra72.
26. Stamler J.S., et al. S-Nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:444-448.
27. Marino S.M., Gladyshev V.N. Redox biology: computational approaches to the investigation of functional cysteine residues. Antioxid. Redox Signal. 2011, 15:135-146.
28. 2S to protein thiol oxidation. Antioxid. Redox Signal. 2013, 19:1749-1765.
29. Poole L.B., Nelson K.J. Discovering mechanisms of signaling-mediated cysteine oxidation. Curr. Opin. Chem. Biol. 2008, 12:18-24.
30. Klomsiri C., et al. Cysteine-based redox switches in enzymes. Antioxid. Redox Signal. 2011, 14:1065-1077.
31. Finkel T. From sulfenylation to sulfhydration: what a thiolate needs to tolerate. Sci. Signal. 2012, 5:pe10.
32. Ohno K., et al. Endogenous S-sulfhydration of PTEN helps protect against modification by nitric oxide. Biochem. Biophys. Res. Commun. 2015, 456:245-249.
33. 2S biology. Arch. Biochem. Biophys. 2011, 516:146-153.
34. Zhang D., et al. Detection of protein S-sulfhydration by a tag-switch technique. Angew. Chem. 2014, 53:575-581.
35. Nagy P., Winterbourn C.C. Rapid reaction of hydrogen sulfide with the neutrophil oxidant hypochlorous acid to generate polysulfides. Chem. Res. Toxicol. 2010, 23:1541-1543.
36. 2S-derived signaling molecules in rat brain. FASEB J. 2013, 27:2451-2457.
37. Jaffrey S.R., Snyder S.H. The biotin switch method for the detection of S-nitrosylated proteins. Sci. STKE 2001, 2001:pl1.
38. Jaffrey S.R., et al. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat. Cell Biol. 2001, 3:193-197.
39. Paul B.D., Snyder S.H. Protein sulfhydration. Methods Enzymol. 2015, 555:79-90.
40. Pan J., Carroll K.S. Persulfide reactivity in the detection of protein S-sulfhydration. ACS Chem. Biol. 2013, 8:1110-1116.
41. Reisz J.A., et al. Thiol-blocking electrophiles interfere with labeling and detection of protein sulfenic acids. FEBS J. 2013, 280:6150-6161.
42. Park C.M., et al. Use of the 'tag-switch' method for the detection of protein S-sulfhydration. Meth. Enzymol. 2015, 555:39-56.
43. Pietri R., et al. Hydrogen sulfide and hemeproteins: knowledge and mysteries. Antioxid. Redox Signal. 2011, 15:393-404.
44. Ishii I., et al. Cystathionine gamma-lyase-deficient mice require dietary cysteine to protect against acute lethal myopathy and oxidative injury. J. Biol. Chem. 2010, 285:26358-26368.
45. Mustafa A.K., et al. Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels. Circ. Res. 2011, 109:1259-1268.
46. Hughes M.N., et al. Making and working with hydrogen sulfide: the chemistry and generation of hydrogen sulfide in vitro and its measurement in vivo: a review. Free Radic. Biol. Med. 2009, 47:1346-1353.
47. Nishida M., et al. Hydrogen sulfide anion regulates redox signaling via electrophile sulfhydration. Nat. Chem. Biol. 2012, 8:714-724.
48. Ida T., et al. Reactive cysteine persulfides and S-polythiolation regulate oxidative stress and redox signaling. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:7606-7611.
49. 2S induces a suspended animation-like state in mice. Science 2005, 308:518.
50. Modis K., et al. Intramitochondrial hydrogen sulfide production by 3-mercaptopyruvate sulfurtransferase maintains mitochondrial electron flow and supports cellular bioenergetics. FASEB J. 2013, 27:601-611.
51. Szabo C., et al. Tumor-derived hydrogen sulfide, produced by cystathionine-beta-synthase, stimulates bioenergetics, cell proliferation, and angiogenesis in colon cancer. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:12474-12479.
52. Modis K., et al. Hydrogen sulfide-mediated stimulation of mitochondrial electron transport involves inhibition of the mitochondrial phosphodiesterase 2A, elevation of cAMP and activation of protein kinase A. Biochem. Pharmacol. 2013, 86:1311-1319.
53. 2S) metabolism in mitochondria and its regulatory role in energy production. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:2943-2948.
54. Teng H., et al. Oxygen-sensitive mitochondrial accumulation of cystathionine beta-synthase mediated by Lon protease. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:12679-12684.
55. Li S., Yang G. Hydrogen sulfide maintains mitochondrial DNA replication via demethylation of TFAM. Antioxid. Redox Signal. 2015, 23:630-642.
56. Hildebrandt T.M., Grieshaber M.K. Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria. FEBS J. 2008, 275:3352-3361.
57. Bartholomew T.C., et al. Oxidation of sodium sulphide by rat liver, lungs and kidney. Biochem. Pharmacol. 1980, 29:2431-2437.
58. Furne J., et al. Oxidation of hydrogen sulfide and methanethiol to thiosulfate by rat tissues: a specialized function of the colonic mucosa. Biochem. Pharmacol. 2001, 62:255-259.
59. Curtis C.G., et al. Detoxication of sodium 35 S-sulphide in the rat. Biochem. Pharmacol. 1972, 21:2313-2321.
60. Libiad M., et al. Organization of the human mitochondrial hydrogen sulfide oxidation pathway. J. Biol. Chem. 2014, 289:30901-30910.
61. Dickhout J.G., et al. Integrated stress response modulates cellular redox state via induction of cystathionine gamma-lyase: cross-talk between integrated stress response and thiol metabolism. J. Biol. Chem. 2012, 287:7603-7614.
62. Calvert J.W., et al. Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ. Res. 2009, 105:365-374.
63. Hayes J.D., Dinkova-Kostova A.T. The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends Biochem. Sci. 2014, 39:199-218.
64. Yang G., et al. Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2. Antioxid. Redox Signal. 2013, 18:1906-1919.
65. Kabil H., et al. Increased transsulfuration mediates longevity and dietary restriction in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:16831-16836.
66. Abe K., Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J. Neurosci. 1996, 16:1066-1071.
67. Xuan A., et al. Hydrogen sulfide attenuates spatial memory impairment and hippocampal neuroinflammation in beta-amyloid rat model of Alzheimer's disease. J. Neuroinflamm. 2012, 9:202.
68. Kimura Y., Kimura H. Hydrogen sulfide protects neurons from oxidative stress. FASEB J. 2004, 18:1165-1167.
69. Vandiver M.S., et al. Sulfhydration mediates neuroprotective actions of parkin. Nat. Commun. 2013, 4:1626.
70. Paul B.D., et al. Cystathionine gamma-lyase deficiency mediates neurodegeneration in Huntington's disease. Nature 2014, 509:96-100.
71. Paul B.D., Snyder S.H. Neurodegeneration in Huntington's disease involves loss of cystathionine gamma-lyase. Cell Cycle 2014, 13:2491-2493.
72. Ishii I., et al. Murine cystathionine gamma-lyase: complete cDNA and genomic sequences, promoter activity, tissue distribution and developmental expression. Biochem. J. 2004, 381:113-123.
73. Mir S., et al. Cytokine-induced GAPDH sulfhydration affects PSD95 degradation and memory. Mol. Cell 2014, 56:786-795.
74. Kamoun P., et al. Endogenous hydrogen sulfide overproduction in Down syndrome. Am. J. Med. Genet. A 2003, 116A:310-311.
75. Ichinohe A., et al. Cystathionine beta-synthase is enriched in the brains of Down's patients. Biochem. Biophys. Res. Commun. 2005, 338:1547-1550.
76. Aroca A., et al. S-Sulfhydration: a new post-translational modification in plant systems. Plant Physiol. 2015, 168:334-342.
77. Alvarez C., et al. An O-acetylserine(thiol)lyase homolog with L-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol. 2010, 152:656-669.
78. Calderwood A., Kopriva S. Hydrogen sulfide in plants: from dissipation of excess sulfur to signaling molecule. Nitric Oxide 2014, 41:72-78.
79. Hancock J.T., Whiteman M. Hydrogen sulfide and cell signaling: team player or referee?. Plant Physiol. 2014, 78:37-42.
80. Hara M.R., et al. S-Nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat. Cell Biol. 2005, 7:665-674.
81. Chung K.K., et al. S-Nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 2004, 304:1328-1331.
82. Zhao K., et al. S-Sulfhydration of MEK1 leads to PARP-1 activation and DNA damage repair. EMBO Rep. 2014, 15:792-800.
83. de Beus M.D., et al. Modification of cysteine 111 in Cu/Zn superoxide dismutase results in altered spectroscopic and biophysical properties. Protein Sci. 2004, 13:1347-1355.
84. Xie Z.Z., et al. Sulfhydration of p66Shc at cysteine59 mediates the antioxidant effect of hydrogen sulfide. Antioxid. Redox Signal. 2014, 21:2531-2542.
85. Zhao K., et al. Hydrogen sulfide represses androgen receptor transactivation by targeting at the second zinc finger module. J. Biol. Chem. 2014, 289:20824-20835.
86. 2+ channel sulfhydration. Cell Stem Cell 2014, 15:66-78.