Redox regulation of mitochondrial function with emphasis on cysteine oxidation reactions

Redox Biology

Volumn 2, Issue 1, 2014, Pages 123-139

  Mailloux, Ryan J ^a,b   Jin, Xiaolei ^b   Willmore, William G ^a  

^a CARLETON UNIVERSITY   (Canada)

^b TOXICOLOGY RESEARCH DIVISION   (Canada)

Author keywords

Mitochondria; Redox; S glutathionylation; S nitrosylation; S oxidation

Indexed keywords

CYSTEINE; REACTIVE OXYGEN METABOLITE;

ANIMAL; HUMAN; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; APOPTOSIS; ENZYME METABOLISM; METABOLIC REGULATION; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; NITROSYLATION; NONHUMAN; NUTRIENT; OXIDATIVE PHOSPHORYLATION; PROTEIN SYNTHESIS; REVIEW; S GLUTATHIONYLATION; SIGNAL TRANSDUCTION; SULFENYLATION; SULFINYLATION;

ANIMALS; CYSTEINE; HUMANS; MITOCHONDRIA; OXIDATION-REDUCTION;

EID: 84892575903     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2013.12.011     Document Type: Review

References (221)

1. Brown G.C., Borutaite V. There is no evidence that mitochondria are the main source of reactive oxygen species in mammalian cells. Mitochondrion 2012, 12:1-4.
2. Fernie A.R., Carrari F., Sweetlove L.J. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr. Opin. Plant Biol. 2004, 7:254-261.
3. Baradaran R., Berrisford J.M., Minhas G.S., Sazanov L.A. Crystal structure of the entire respiratory complex I. Nature 2013, 494:443-448.
4. Quinlan C.L., Orr A.L., Perevoshchikova I.V., Treberg J.R., Ackrell B.A., Brand M.D. Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. J. Biol. Chem. 2012, 287:27255-27264.
5. Khutornenko A.A., Roudko V.V., Chernyak B.V., Vartapetian A.B., Chumakov P.M., Evstafieva A.G. Pyrimidine biosynthesis links mitochondrial respiration to the p53 pathway. Proc. Natl. Acad. Sci. USA 2010, 107:12828-12833.
6. Zhang J., Frerman F.E., Kim J.J. Structure of electron transfer flavoprotein-ubiquinone oxidoreductase and electron transfer to the mitochondrial ubiquinone pool. Proc. Natl. Acad. Sci. USA 2006, 103:16212-16217.
7. Orr A.L., Quinlan C.L., Perevoshchikova I.V., Brand M.D. A refined analysis of superoxide production by mitochondrial sn-glycerol 3-phosphate dehydrogenase. J. Biol. Chem. 2012, 287:42921-42935.
8. Brand M.D., Nicholls D.G. Assessing mitochondrial dysfunction in cells. Biochem. J. 2011, 435:297-312.
9. Mailloux R.J., Harper M.E. Uncoupling proteins and the control of mitochondrial reactive oxygen species production. Free Radic. Biol. Med. 2011, 51:1106-1115.
10. Mailloux R.J., McBride S.L., Harper M.E. Unearthing the secrets of mitochondrial ROS and glutathione in bioenergetics. Trends Biochem. Sci. 2013, 38:592-632.
11. Starkov A.A., Fiskum G., Chinopoulos C., Lorenzo B.J., Browne S.E., Patel M.S., Beal M.F. Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species. J. Neurosci.: Off. J. Soc. Neurosci. 2004, 24:7779-7788.
12. Quinlan C.L., Perevoshchikova I.V., Hey-Mogensen M., Orr A.L., Brand M.D. Sites of reactive oxygen species generation by mitochondria oxidizing different substrates. Redox Biol. 2013, 1:304-312.
13. Guzy R.D., Hoyos B., Robin E., Chen H., Liu L., Mansfield K.D., Simon M.C., Hammerling U., Schumacker P.T. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab. 2005, 1:401-408.
14. Tormos K.V., Anso E., Hamanaka R.B., Eisenbart J., Joseph J., Kalyanaraman B., Chandel N.S. Mitochondrial complex III ROS regulate adipocyte differentiation. Cell Metab. 2011, 14:537-544.
15. Loh K., Deng H., Fukushima A., Cai X., Boivin B., Galic S., Bruce C., Shields B.J., Skiba B., Ooms L.M., Stepto N., Wu B., Mitchell C.A., Tonks N.K., Watt M.J., Febbraio M.A., Crack P.J., Andrikopoulos S., Tiganis T. Reactive oxygen species enhance insulin sensitivity. Cell Metab. 2009, 10:260-272.
16. Mailloux R.J., Fu A., Robson-Doucette C., Allister E.M., Wheeler M.B., Screaton R., Harper M.E. Glutathionylation state of uncoupling protein-2 and the control of glucose-stimulated insulin secretion. J. Biol. Chem. 2012, 287:39673-39685.
17. Hamanaka R.B., Chandel N.S. Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends Biochem. Sci. 2010, 35:505-513.
18. Lillig C.H., Berndt C., Vergnolle O., Lonn M.E., Hudemann C., Bill E., Holmgren A. Characterization of human glutaredoxin 2 as iron-sulfur protein: a possible role as redox sensor. Proc. Natl. Acad. Sci. USA 2005, 102:8168-8173.
19. James A.M., Collins Y., Logan A., Murphy M.P. Mitochondrial oxidative stress and the metabolic syndrome. Trends Endocrinol. Metab. 2012, 23:429-434.
20. Wang W., Fang H., Groom L., Cheng A., Zhang W., Liu J., Wang X., Li K., Han P., Zheng M., Yin J., Mattson M.P., Kao J.P., Lakatta E.G., Sheu S.S., Ouyang K., Chen J., Dirksen R.T., Cheng H. Superoxide flashes in single mitochondria. Cell 2008, 134:279-290.
21. Schwarzlander M., Logan D.C., Fricker M.D., Sweetlove L.J. The circularly permuted yellow fluorescent protein cpYFP that has been used as a superoxide probe is highly responsive to pH but not superoxide in mitochondria: implications for the existence of superoxide 'flashes'. Biochem. J. 2011, 437:381-387.
22. Schwarzlander M., Murphy M.P., Duchen M.R., Logan D.C., Fricker M.D., Halestrap A.P., Muller F.L., Rizzuto R., Dick T.P., Meyer A.J., Sweetlove L.J. Mitochondrial 'flashes': a radical concept repHined. Trends Cell Biol. 2012, 22:503-508.
23. Murphy M.P. Mitochondrial thiols in antioxidant protection and redox signaling: distinct roles for glutathionylation and other thiol modifications. Antioxid. Redox Signal. 2012, 16:476-495.
24. Mailloux R.J., Lemire J., Appanna V.D. Hepatic response to aluminum toxicity: dyslipidemia and liver diseases. Exp. Cell Res. 2011, 317:2231-2238.
25. Pacher P., Schulz R., Liaudet L., Szabo C. Nitrosative stress and pharmacological modulation of heart failure. Trends Pharmacol. Sci. 2005, 26:302-310.
26. Lane N. Evolution. The costs of breathing. Science 2011, 334:184-185.
27. Korshunov S.S., Skulachev V.P., Starkov A.A. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 1997, 416:15-18.
28. Mailloux R.J., Dumouchel T., Aguer C., Dekemp R., Beanlands R., Harper M.E. Hexokinase II acts through UCP3 to suppress mitochondrial reactive oxygen species production and maintain aerobic respiration. Biochem. J. 2011, 437:301-311.
29. Lenaz G. The mitochondrial production of reactive oxygen species: mechanisms and implications in human pathology. IUBMB Life 2001, 52:159-164.
30. Pouvreau S. Superoxide flashes in mouse skeletal muscle are produced by discrete arrays of active mitochondria operating coherently. PLoS One 2010, 5:e13035.
31. Lee I., Bender E., Kadenbach B. Control of mitochondrial membrane potential and ROS formation by reversible phosphorylation of cytochrome c oxidase. Mol. Cell. Biochem. 2002, 234-235:63-70.
32. Hue L., Taegtmeyer H. The Randle cycle revisited: a new head for an old hat. Am. J. Physiol. Endocrinol. Metab. 2009, 297:E578-E591.
33. Scherz-Shouval R., Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem. Sci. 2011, 36:30-38.
34. St-Pierre J., Drori S., Uldry M., Silvaggi J.M., Rhee J., Jager S., Handschin C., Zheng K., Lin J., Yang W., Simon D.K., Bachoo R., Spiegelman B.M. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 2006, 127:397-408.
35. Maranzana E., Barbero G., Falasca A.I., Lenaz G., Genova M.L. Mitochondrial respiratory supercomplex association limits production of reactive oxygen species from Complex I. Antioxid. Redox Signal. 2013, 19:1469-1480.
36. Hurd T.R., Costa N.J., Dahm C.C., Beer S.M., Brown S.E., Filipovska A., Murphy M.P. Glutathionylation of mitochondrial proteins. Antioxid. Redox Signal. 2005, 7:999-1010.
37. Piantadosi C.A. Regulation of mitochondrial processes by protein S-nitrosylation. Biochim. Biophys. Acta 2012, 1820:712-721.
38. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
39. Mailloux R.J., Harper M.E. Mitochondrial proticity and ROS signaling: lessons from the uncoupling proteins. Trends Endocrinol. Metab. 2012, 23:451-458.
40. Sena L.A., Chandel N.S. Physiological roles of mitochondrial reactive oxygen species. Mol. Cell 2012, 48:158-167.
41. Huang B., Chen S.C., Wang D.L. Shear flow increases S-nitrosylation of proteins in endothelial cells. Cardiovasc. Res. 2009, 83:536-546.
42. Lindahl M., Mata-Cabana A., Kieselbach T. The disulfide proteome and other reactive cysteine proteomes: analysis and functional significance. Antioxid. Redox Signal. 2011, 14:2581-2642.
43. Grek C., Zhang J., Manevich Y., Townsend D.M., Tew K.D. Causes and consequences of cysteine S-glutathionylation. J. Biol. Chem. 2013, 72:2383-2393.
44. Chepelev N.L., Willmore W.G. Regulation of iron pathways in response to hypoxia. Free Radic. Biol. Med. 2011, 50:645-666.
45. Stewart M.D., Igumenova T.I. Reactive cysteine in the structural Zn(2+) site of the C1B domain from PKCalpha. Biochemistry 2012, 51:7263-7277.
46. Lill R. Function and biogenesis of iron-sulphur proteins. Nature 2009, 460:831-838.
47. Velan B., Grosfeld H., Kronman C., Leitner M., Gozes Y., Lazar A., Flashner Y., Marcus D., Cohen S., Shafferman A. The effect of elimination of intersubunit disulfide bonds on the activity, assembly, and secretion of recombinant human acetylcholinesterase. Expression of acetylcholinesterase Cys-580-Ala mutant. J. Biol. Chem. 1991, 266:23977-23984.
48. Lo Conte M., Carroll K.S. The redox biochemistry of protein sulfenylation and sulfinylation. J. Biol. Chem. 2013, 288:26480-26488.
49. Winterbourn C.C., Hampton M.B. Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 2008, 45:549-561.
50. Smith R.E., MacQuarrie R. The role of cysteine residues in the catalytic activity of glycerol-3-phosphate dehydrogenase. Biochim. Biophys. Acta 1979, 567:269-277.
51. Kortemme T., Creighton T.E. Ionisation of cysteine residues at the termini of model alpha-helical peptides. Relevance to unusual thiol pKa values in proteins of the thioredoxin family. J. Mol. Biol. 1995, 253:799-812.
52. Gallogly M.M., Starke D.W., Mieyal J.J. Mechanistic and kinetic details of catalysis of thiol-disulfide exchange by glutaredoxins and potential mechanisms of regulation. Antioxid. Redox Signal. 2009, 11:1059-1081.
53. Stroher E., Millar A.H. The biological roles of glutaredoxins. Biochem. J. 2012, 446:333-348.
54. Cox A.G., Winterbourn C.C., Hampton M.B. Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochem. J. 2010, 425:313-325.
55. Lo Conte M., Carroll K.S. The redox biochemistry of protein sulfenylation and sulfinylation. J. Biol. Chem. 2013, 288:26480-26488.
56. Paulsen C.E., Carroll K.S. Cysteine-mediated redox signaling: chemistry, biology, and tools for discovery. Chem. Rev. 2013, 113:4633-4679.
57. Go Y.M., Jones D.P. Redox compartmentalization in eukaryotic cells. Biochim. Biophys. Acta 2008, 1780:1273-1290.
58. Kemp M., Go Y.M., Jones D.P. Nonequilibrium thermodynamics of thiol/disulfide redox systems: a perspective on redox systems biology. Free Radic. Biol. Med. 2008, 44:921-937.
59. Requejo R., Hurd T.R., Costa N.J., Murphy M.P. Cysteine residues exposed on protein surfaces are the dominant intramitochondrial thiol and may protect against oxidative damage. FEBS J. 2010, 277:1465-1480.
60. Brown G.C. Nitric oxide and mitochondria. Front. Biosci.: J. Virtual Lib. 2007, 12:1024-1033.
61. Roos G., Messens J. Protein sulfenic acid formation: from cellular damage to redox regulation. Free Radic. Biol. Med. 2011, 51:314-326.
62. Peskin A.V., Low F.M., Paton L.N., Maghzal G.J., Hampton M.B., Winterbourn C.C. The high reactivity of peroxiredoxin 2 with H(2)O(2) is not reflected in its reaction with other oxidants and thiol reagents. J. Biol. Chem. 2007, 282:11885-11892.
63. Hall A., Parsonage D., Poole L.B., Karplus P.A. Structural evidence that peroxiredoxin catalytic power is based on transition-state stabilization. J. Mol. Biol. 2010, 402:194-209.
64. Enami S., Hoffmann M.R., Colussi A.J. Simultaneous detection of cysteine sulfenate, sulfinate, and sulfonate during cysteine interfacial ozonolysis. J. Phys. Chem. B 2009, 113:9356-9358.
65. McGrath A.J., Garrett G.E., Valgimigli L., Pratt D.A. The redox chemistry of sulfenic acids. J. Am. Chem. Soc. 2010, 132:16759-16761.
66. Hugo M., Turell L., Manta B., Botti H., Monteiro G., Netto L.E., Alvarez B., Radi R., Trujillo M. Thiol and sulfenic acid oxidation of AhpE, the one-cysteine peroxiredoxin from Mycobacterium tuberculosis: kinetics, acidity constants, and conformational dynamics. Biochemistry 2009, 48:9416-9426.
67. 2-induced oxidative stress in nerve terminals. Ann. N. Y. Acad. Sci. 1999, 893:412-416.
68. Applegate M.A., Humphries K.M., Szweda L.I. Reversible inhibition of alpha-ketoglutarate dehydrogenase by hydrogen peroxide: glutathionylation and protection of lipoic acid. Biochemistry 2008, 47:473-478.
69. Hurd T.R., Requejo R., Filipovska A., Brown S., Prime T.A., Robinson A.J., Fearnley I.M., Murphy M.P. Complex I within oxidatively stressed bovine heart mitochondria is glutathionylated on Cys-531 and Cys-704 of the 75-kDa subunit: potential role of CYS residues in decreasing oxidative damage. J. Biol. Chem. 2008, 283:24801-24815.
70. McStay G.P., Clarke S.J., Halestrap A.P. Role of critical thiol groups on the matrix surface of the adenine nucleotide translocase in the mechanism of the mitochondrial permeability transition pore. Biochem. J. 2002, 367:541-548.
71. Nelson K.J., Klomsiri C., Codreanu S.G., Soito L., Liebler D.C., Rogers L.C., Daniel L.W., Poole L.B. Use of dimedone-based chemical probes for sulfenic acid detection methods to visualize and identify labeled proteins. Methods Enzymol. 2010, 473:95-115.
72. Hutson S.M., Poole L.B., Coles S., Conway M.E. Redox regulation and trapping sulfenic acid in the peroxide-sensitive human mitochondrial branched chain aminotransferase. Methods Mol. Biol. 2008, 476:139-152.
73. Cocheme H.M., Kelso G.F., James A.M., Ross M.F., Trnka J., Mahendiran T., Asin-Cayuela J., Blaikie F.H., Manas A.R., Porteous C.M., Adlam V.J., Smith R.A., Murphy M.P. Mitochondrial targeting of quinones: therapeutic implications. Mitochondrion 2007, 7(Suppl):S94-S102.
74. Reily C., Mitchell T., Chacko B.K., Benavides G., Murphy M.P., Darley-Usmar V. Mitochondrially targeted compounds and their impact on cellular bioenergetics. Redox Biol. 2013, 1:86-93.
75. Bindoli A., Fukuto J.M., Forman H.J. Thiol chemistry in peroxidase catalysis and redox signaling. Antioxid. Redox Signal. 2008, 10:1549-1564.
76. 2 in red blood cells. Antioxid. Redox Signal. 2010, 12:1235-1246.
77. Lowther W.T., Haynes A.C. Reduction of cysteine sulfinic acid in eukaryotic, typical 2-Cys peroxiredoxins by sulfiredoxin. Antioxid. Redox Signal. 2011, 15:99-109.
78. Hamann M., Zhang T., Hendrich S., Thomas J.A. Quantitation of protein sulfinic and sulfonic acid, irreversibly oxidized protein cysteine sites in cellular proteins. Methods Enzymol. 2002, 348:146-156.
79. Chevallet M., Wagner E., Luche S., van Dorsselaer A., Leize-Wagner E., Rabilloud T. Regeneration of peroxiredoxins during recovery after oxidative stress: only some overoxidized peroxiredoxins can be reduced during recovery after oxidative stress. J. Biol. Chem. 2003, 278:37146-37153.
80. Canet-Aviles R.M., Wilson M.A., Miller D.W., Ahmad R., McLendon C., Bandyopadhyay S., Baptista M.J., Ringe D., Petsko G.A., Cookson M.R. The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc. Natl. Acad. Sci. USA 2004, 101:9103-9108.
81. Woo H.A., Yim S.H., Shin D.H., Kang D., Yu D.Y., Rhee S.G. Inactivation of peroxiredoxin I by phosphorylation allows localized H(2)O(2) accumulation for cell signaling. Cell 2010, 140:517-528.
82. Noh Y.H., Baek J.Y., Jeong W., Rhee S.G., Chang T.S. Sulfiredoxin translocation into mitochondria plays a crucial role in reducing hyperoxidized peroxiredoxin III. J. Biol. Chem. 2009, 284:8470-8477.
83. Peskin A.V., Dickerhof N., Poynton R.A., Paton L.N., Pace P.E., Hampton M.B., Winterbourn C.C. Hyperoxidation of peroxiredoxins 2 and 3: rate constants for the reactions of the sulfenic acid of the peroxidatic cysteine. J. Biol. Chem. 2013, 288:14170-14177.
84. Lo Conte M., Carroll K.S. Chemoselective ligation of sulfinic acids with aryl-nitroso compounds. Angew. Chem. Int. Ed. Engl. 2012, 51:6502-6505.
85. Beer S.M., Taylor E.R., Brown S.E., Dahm C.C., Costa N.J., Runswick M.J., Murphy M.P. Glutaredoxin 2 catalyzes the reversible oxidation and glutathionylation of mitochondrial membrane thiol proteins: implications for mitochondrial redox regulation and antioxidant DEFENSE. J. Biol. Chem. 2004, 279:47939-47951.
86. Mailloux R.J., Xuan J.Y., Beauchamp B., Jui L., Lou M., Harper M.E. Glutaredoxin-2 is required to control proton leak through uncoupling protein-3. J. Biol. Chem. 2013, 288:8365-8379.
87. Mailloux R.J., Seifert E.L., Bouillaud F., Aguer C., Collins S., Harper M.E. Glutathionylation acts as a control switch for uncoupling proteins UCP2 and UCP3. J. Biol. Chem. 2011, 286:21865-21875.
88. Gutscher M., Pauleau A.L., Marty L., Brach T., Wabnitz G.H., Samstag Y., Meyer A.J., Dick T.P. Real-time imaging of the intracellular glutathione redox potential. Nat. Methods 2008, 5:553-559.
89. Dalle-Donne I., Rossi R., Giustarini D., Colombo R., Milzani A. S-glutathionylation in protein redox regulation. Free Radic. Biol. Med. 2007, 43:883-898.
90. Gallogly M.M., Mieyal J.J. Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress. Curr. Opin. Pharmacol. 2007, 7:381-391.
91. Kang P.T., Zhang L., Chen C.L., Chen J., Green K.B., Chen Y.R. Protein thiyl radical mediates S-glutathionylation of complex I. Free Radic. Biol. Med. 2012, 53:962-973.
92. Ziegler D.M. Role of reversible oxidation-reduction of enzyme thiols-disulfides in metabolic regulation. Annu. Rev. Biochem. 1985, 54:305-329.
93. Mailloux R.J., Adjeitey C.N., Xuan J.Y., Harper M.E. Crucial yet divergent roles of mitochondrial redox state in skeletal muscle vs. brown adipose tissue energetics. Faseb J. 2012, 26:363-375.
94. Deponte M. Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim. Biophys. Acta 2013, 1830:3217-3266.
95. Gladyshev V.N., Liu A., Novoselov S.V., Krysan K., Sun Q.A., Kryukov V.M., Kryukov G.V., Lou M.F. Identification and characterization of a new mammalian glutaredoxin (thioltransferase), Grx2. J. Biol. Chem. 2001, 276:30374-30380.
96. Lundberg M., Johansson C., Chandra J., Enoksson M., Jacobsson G., Ljung J., Johansson M., Holmgren A. Cloning and expression of a novel human glutaredoxin (Grx2) with mitochondrial and nuclear isoforms. J. Biol. Chem. 2001, 276:26269-26275.
97. Mitra S., Elliott S.J. Oxidative disassembly of the [2Fe-2S] cluster of human Grx2 and redox regulation in the mitochondria. Biochemistry 2009, 48:3813-3815.
98. Qi W., Cowan J.A. Mechanism of glutaredoxin-ISU [2Fe-2S] cluster exchange. Chem. Commun. (Camb) 2011, 47:4989-4991.
99. Klaus A., Zorman S., Berthier A., Polge C., Ramirez S., Michelland S., Seve M., Vertommen D., Rider M., Lentze N., Auerbach D., Schlattner U. Glutathione S-transferases interact with AMP-activated protein kinase: evidence for S-glutathionylation and activation in vitro. PLoS One 2013, 8:e62497.
100. Raza H. Dual localization of glutathione S-transferase in the cytosol and mitochondria: implications in oxidative stress, toxicity and disease. FEBS J. 2011, 278:4243-4251.
101. Knowles R.G., Moncada S. Nitric oxide as a signal in blood vessels. Trends Biochem. Sci. 1992, 17:399-402.
102. *: the structure of the SNO moiety in "S-Nitrosohemoglobin", a possible NO reservoir and transporter. J. Am. Chem. Soc. 2006, 128:1422-1423.
103. Ford E., Hughes M.N., Wardman P. Kinetics of the reactions of nitrogen dioxide with glutathione, cysteine, and uric acid at physiological pH. Free Radic. Biol. Med. 2002, 32:1314-1323.
104. Sun J., Steenbergen C., Murphy E. S-nitrosylation: NO-related redox signaling to protect against oxidative stress. Antioxid. Redox Signal. 2006, 8:1693-1705.
105. Bates T.E., Loesch A., Burnstock G., Clark J.B. Immunocytochemical evidence for a mitochondrially located nitric oxide synthase in brain and liver. Biochem. Biophys. Res. Commun. 1995, 213:896-900.
106. Brown G.C., Borutaite V. Nitric oxide and mitochondrial respiration in the heart. Cardiovasc. Res. 2007, 75:283-290.
107. Freeman B.A., Baker P.R., Schopfer F.J., Woodcock S.R., Napolitano A., d'Ischia M. Nitro-fatty acid formation and signaling. J. Biol. Chem. 2008, 283:15515-15519.
108. Chouchani E.T., Methner C., Nadtochiy S.M., Logan A., Pell V.R., Ding S., James A.M., Cocheme H.M., Reinhold J., Lilley K.S., Partridge L., Fearnley I.M., Robinson A.J., Hartley R.C., Smith R.A., Krieg T., Brookes P.S., Murphy M.P. Cardioprotection by S-nitrosation of a cysteine switch on mitochondrial complex I. Nat. Med. 2013, 19:753-759.
109. Doulias P.T., Tenopoulou M., Greene J.L., Raju K., Ischiropoulos H. Nitric oxide regulates mitochondrial fatty acid metabolism through reversible protein S-nitrosylation. Sci. Signal. 2013, 6:rs1.
110. Nguyen T.T., Stevens M.V., Kohr M., Steenbergen C., Sack M.N., Murphy E. Cysteine 203 of cyclophilin D is critical for cyclophilin D activation of the mitochondrial permeability transition pore. J. Biol. Chem. 2011, 286:40184-40192.
111. Piantadosi C.A., Tatro L.G., Whorton A.R. Nitric oxide and differential effects of ATP on mitochondrial permeability transition. Nitric Oxide: Biol. Chem./Off. J. Nitric Oxide Soc. 2002, 6:45-60.
112. Chinta S.J., Andersen J.K. Nitrosylation and nitration of mitochondrial complex I in Parkinson's disease. Free Radic. Res. 2011, 45:53-58.
113. Kwong L.K., Sohal R.S. Substrate and site specificity of hydrogen peroxide generation in mouse mitochondria. Arch. Biochem. Biophys. 1998, 350:118-126.
114. Kushnareva Y., Murphy A.N., Andreyev A. Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+ oxidation-reduction state. Biochem. J. 2002, 368:545-553.
115. Aon M.A., Cortassa S., Maack C., O'Rourke B. Sequential opening of mitochondrial ion channels as a function of glutathione redox thiol status. J. Biol. Chem. 2007, 282:21889-21900.
116. de la Asuncion J.G., Millan A., Pla R., Bruseghini L., Esteras A., Pallardo F.V., Sastre J., Vina J. Mitochondrial glutathione oxidation correlates with age-associated oxidative damage to mitochondrial DNA. Faseb J. 1996, 10:333-338.
117. Bulteau A.L., Lundberg K.C., Ikeda-Saito M., Isaya G., Szweda L.I. Reversible redox-dependent modulation of mitochondrial aconitase and proteolytic activity during in vivo cardiac ischemia/reperfusion. Proc. Natl. Acad. Sci. USA 2005, 102:5987-5991.
118. Mailloux R.J., Hamel R., Appanna V.D. Aluminum toxicity elicits a dysfunctional TCA cycle and succinate accumulation in hepatocytes. J. Biochem. Mol. Toxicol. 2006, 20:198-208.
119. Kil I.S., Park J.W. Regulation of mitochondrial NADP+-dependent isocitrate dehydrogenase activity by glutathionylation. J. Biol. Chem. 2005, 280:10846-10854.
120. McLain A.L., Cormier P.J., Kinter M., Szweda L.I. Glutathionylation of alpha-ketoglutarate dehydrogenase: the chemical nature and relative susceptibility of the cofactor lipoic acid to modification. Free Radic. Biol. Med. 2013, 61C:161-169.
121. McLain A.L., Szweda P.A., Szweda L.I. alpha-Ketoglutarate dehydrogenase: a mitochondrial redox sensor. Free Radic. Res. 2011, 45:29-36.
122. Yan L.J., Sumien N., Thangthaeng N., Forster M.J. Reversible inactivation of dihydrolipoamide dehydrogenase by mitochondrial hydrogen peroxide. Free Radic. Res. 2013, 47:123-133.
123. Chen Y.R., Chen C.L., Pfeiffer D.R., Zweier J.L. Mitochondrial complex II in the post-ischemic heart: oxidative injury and the role of protein S-glutathionylation. J. Biol. Chem. 2007, 282:32640-32654.
124. Giangregorio N., Palmieri F., Indiveri C. Glutathione controls the redox state of the mitochondrial carnitine/acylcarnitine carrier Cys residues by glutathionylation. Biochim. Biophys. Acta 2013, 1830:5299-5304.
125. Wu H., Lin L., Giblin F., Ho Y.S., Lou M.F. Glutaredoxin 2 knockout increases sensitivity to oxidative stress in mouse lens epithelial cells. Free Radic. Biol. Med. 2011, 51:2108-2117.
126. Hill B.G., Higdon A.N., Dranka B.P., Darley-Usmar V.M. Regulation of vascular smooth muscle cell bioenergetic function by protein glutathiolation. Biochim. Biophys. Acta 2010, 1797:285-295.
127. Pfefferle A., Mailloux R.J., Adjeitey C.N., Harper M.E. Glutathionylation of UCP2 sensitizes drug resistant leukemia cells to chemotherapeutics. Biochim. Biophys. Acta 2013, 1833:80-89.
128. Baffy G., Derdak Z., Robson S.C. Mitochondrial recoupling: a novel therapeutic strategy for cancer?. Br. J. Cancer. 2011, 105:469-474.
129. Diotte N.M., Xiong Y., Gao J., Chua B.H., Ho Y.S. Attenuation of doxorubicin-induced cardiac injury by mitochondrial glutaredoxin 2. Biochim. Biophys. Acta 2009, 1793:427-438.
130. Taylor E.R., Hurrell F., Shannon R.J., Lin T.K., Hirst J., Murphy M.P. Reversible glutathionylation of complex I increases mitochondrial superoxide formation. J. Biol. Chem. 2003, 278:19603-19610.
131. Tretter L., Adam-Vizi V. Inhibition of Krebs cycle enzymes by hydrogen peroxide: a key role of [alpha]-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress. J. Neurosci.: Off. J. Soc. Neurosci. 2000, 20:8972-8979.
132. Gibson G.E., Park L.C., Sheu K.F., Blass J.P., Calingasan N.Y. The alpha-ketoglutarate dehydrogenase complex in neurodegeneration. Neurochem. Int. 2000, 36:97-112.
133. Wang S.B., Murray C.I., Chung H.S., Van Eyk J.E. Redox regulation of mitochondrial ATP synthase. Trends Cardiovasc. Med. 2013, 23:14-18.
134. Garcia J., Han D., Sancheti H., Yap L.P., Kaplowitz N., Cadenas E. Regulation of mitochondrial glutathione redox status and protein glutathionylation by respiratory substrates. J. Biol. Chem. 2010, 285:39646-39654.
135. Liesa M., Shirihai O.S. Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab. 2013, 17:491-506.
136. Chan D.C. Mitochondria: dynamic organelles in disease, aging, and development. Cell 2006, 125:1241-1252.
137. Shutt T., Geoffrion M., Milne R., McBride H.M. The intracellular redox state is a core determinant of mitochondrial fusion. EMBO Rep. 2012, 13:909-915.
138. Redpath C.J., Bou Khalil M., Drozdzal G., Radisic M., McBride H.M. Mitochondrial hyperfusion during oxidative stress is coupled to a dysregulation in calcium handling within a C2C12 cell model. PLoS One 2013, 8:e69165.
139. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
140. Kowaltowski A.J., Castilho R.F., Vercesi A.E. Mitochondrial permeability transition and oxidative stress. FEBS Lett. 2001, 495:12-15.
141. Halestrap A.P., Brenner C. The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and key player in cell death. Curr. Med. Chem. 2003, 10:1507-1525.
142. Kowaltowski A.J., Castilho R.F., Vercesi A.E. Ca(2+)-induced mitochondrial membrane permeabilization: role of coenzyme Q redox state. Am. J. Physiol. 1995, 269:C141-C147.
143. 2+ ions. A proposed model for phosphate-stimulated lipid peroxidation. J. Biol. Chem. 1996, 271:2929-2934.
144. Kowaltowski A.J., Netto L.E., Vercesi A.E. The thiol-specific antioxidant enzyme prevents mitochondrial permeability transition. Evidence for the participation of reactive oxygen species in this mechanism. J. Biol. Chem. 1998, 273:12766-12769.
145. Yin F., Sancheti H., Cadenas E. Mitochondrial thiols in the regulation of cell death pathways. Antioxid. Redox Signal. 2012, 17:1714-1727.
146. Halestrap A.P. A pore way to die: the role of mitochondria in reperfusion injury and cardioprotection. Biochem. Soc. Trans. 2010, 38:841-860.
147. Queiroga C.S., Almeida A.S., Martel C., Brenner C., Alves P.M., Vieira H.L. Glutathionylation of adenine nucleotide translocase induced by carbon monoxide prevents mitochondrial membrane permeabilization and apoptosis. J. Biol. Chem. 2010, 285:17077-17088.
148. Leung A.W., Varanyuwatana P., Halestrap A.P. The mitochondrial phosphate carrier interacts with cyclophilin D and may play a key role in the permeability transition. J. Biol. Chem. 2008, 283:26312-26323.
149. Varanyuwatana P., Halestrap A.P. The roles of phosphate and the phosphate carrier in the mitochondrial permeability transition pore. Mitochondrion 2012, 12:120-125.
150. Giorgio V., von Stockum S., Antoniel M., Fabbro A., Fogolari F., Forte M., Glick G.D., Petronilli V., Zoratti M., Szabo I., Lippe G., Bernardi P. Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc. Natl. Acad. Sci. USA 2013, 110:5887-5892.
151. Sanchez G., Fernandez C., Montecinos L., Domenech R.J., Donoso P. Preconditioning tachycardia decreases the activity of the mitochondrial permeability transition pore in the dog heart. Biochem. Biophys. Res. Commun. 2011, 410:916-921.
152. Baines C.P., Kaiser R.A., Purcell N.H., Blair N.S., Osinska H., Hambleton M.A., Brunskill E.W., Sayen M.R., Gottlieb R.A., Dorn G.W., Robbins J., Molkentin J.D. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005, 434:658-662.
153. Nakagawa T., Shimizu S., Watanabe T., Yamaguchi O., Otsu K., Yamagata H., Inohara H., Kubo T., Tsujimoto Y. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 2005, 434:652-658.
154. Kokoszka J.E., Waymire K.G., Levy S.E., Sligh J.E., Cai J., Jones D.P., MacGregor G.R., Wallace D.C. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 2004, 427:461-465.
155. Ambrosio G., Zweier J.L., Flaherty J.T. The relationship between oxygen radical generation and impairment of myocardial energy metabolism following post-ischemic reperfusion. J. Mol. Cell. Cardiol. 1991, 23:1359-1374.
156. Zweier J.L., Flaherty J.T., Weisfeldt M.L. Direct measurement of free radical generation following reperfusion of ischemic myocardium. Proc. Natl. Acad. Sci. USA 1987, 84:1404-1407.
157. Bolli R., Marban E. Molecular and cellular mechanisms of myocardial stunning. Physiol. Rev. 1999, 79:609-634.
158. Tompkins A.J., Burwell L.S., Digerness S.B., Zaragoza C., Holman W.L., Brookes P.S. Mitochondrial dysfunction in cardiac ischemia-reperfusion injury: ROS from complex I, without inhibition. Biochim. Biophys. Acta 2006, 1762:223-231.
159. Lesnefsky E.J., Moghaddas S., Tandler B., Kerner J., Hoppel C.L. Mitochondrial dysfunction in cardiac disease: ischemia-reperfusion, aging, and heart failure. J. Mol. Cell. Cardiol. 2001, 33:1065-1089.
160. Rouslin W. Mitochondrial complexes I, II, III, IV, and V in myocardial ischemia and autolysis. Am. J. Physiol. 1983, 244:H743-H748.
161. Kumar V., Kleffmann T., Hampton M.B., Cannell M.B., Winterbourn C.C. Redox proteomics of thiol proteins in mouse heart during ischemia/reperfusion using ICAT reagents and mass spectrometry. Free Radic. Biol. Med. 2013, 58:109-117.
162. Liu B., Tewari A.K., Zhang L., Green-Church K.B., Zweier J.L., Chen Y.R., He G. Proteomic analysis of protein tyrosine nitration after ischemia reperfusion injury: mitochondria as the major target. Biochim. Biophys. Acta 2009, 1794:476-485.
163. Zhao X., Chen Y.R., He G., Zhang A., Druhan L.J., Strauch A.R., Zweier J.L. Endothelial nitric oxide synthase (NOS3) knockout decreases NOS2 induction, limiting hyperoxygenation and conferring protection in the postischemic heart. Am. J. Physiol. Heart Circ. Physiol. 2007, 292:H1541-H1550.
164. Zhao X., He G., Chen Y.R., Pandian R.P., Kuppusamy P., Zweier J.L. Endothelium-derived nitric oxide regulates postischemic myocardial oxygenation and oxygen consumption by modulation of mitochondrial electron transport. Circulation 2005, 111:2966-2972.
165. Zhang L., Chen C.L., Kang P.T., Garg V., Hu K., Green-Church K.B., Chen Y.R. Peroxynitrite-mediated oxidative modifications of complex II: relevance in myocardial infarction. Biochemistry 2010, 49:2529-2539.
166. Burwell L.S., Nadtochiy S.M., Tompkins A.J., Young S., Brookes P.S. Direct evidence for S-nitrosation of mitochondrial complex I. Biochem. J. 2006, 394:627-634.
167. Poderoso J.J., Carreras M.C., Lisdero C., Riobo N., Schopfer F., Boveris A. Nitric oxide inhibits electron transfer and increases superoxide radical production in rat heart mitochondria and submitochondrial particles. Arch. Biochem. Biophys. 1996, 328:85-92.
168. *) signaling pathway, and the transduction of nitrosative to oxidative cell signals: an alternative function for cytochrome C oxidase. Free Radic. Biol. Med. 2002, 32:370-374.
169. Chen Q., Vazquez E.J., Moghaddas S., Hoppel C.L., Lesnefsky E.J. Production of reactive oxygen species by mitochondria: central role of complex III. J. Biol. Chem. 2003, 278:36027-36031.
170. Zweier J.L., Chen C.A., Talukder M.A. Cardiac resynchronization therapy and reverse molecular remodeling: importance of mitochondrial redox signaling. Circ. Res. 2011, 109:716-719.
171. Chen C.A., Wang T.Y., Varadharaj S., Reyes L.A., Hemann C., Talukder M.A., Chen Y.R., Druhan L.J., Zweier J.L. S-glutathionylation uncouples eNOS and regulates its cellular and vascular function. Nature 2010, 468:1115-1118.
172. Rolo A.P., Palmeira C.M. Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicol. Appl. Pharmacol. 2006, 212:167-178.
173. Anderson E.J., Rodriguez E., Anderson C.A., Thayne K., Chitwood W.R., Kypson A.P. Increased propensity for cell death in diabetic human heart is mediated by mitochondrial-dependent pathways. Am. J. Physiol. Heart Circ. Physiol. 2011, 300:H118-H124.
174. Williamson C.L., Dabkowski E.R., Baseler W.A., Croston T.L., Alway S.E., Hollander J.M. Enhanced apoptotic propensity in diabetic cardiac mitochondria: influence of subcellular spatial location. Am. J. Physiol. Heart Circ. Physiol. 2010, 298:H633-H642.
175. Sanchez-Gomez F.J., Espinosa-Diez C., Dubey M., Dikshit M., Lamas S. S-glutathionylation: relevance in diabetes and potential role as a biomarker. Biol. Chem. 2013, 394:1263-1280.
176. Bournat J.C., Brown C.W. Mitochondrial dysfunction in obesity. Curr. Opin. Endocrinol. Diabetes Obes. 2010, 17:446-452.
177. Picklo M.J., Idso J.P., Jackson M.I. S-Glutathionylation of hepatic and visceral adipose proteins decreases in obese rats. Obesity (Silver Spring) 2013, 21:297-305.
178. Harper M.E., Green K., Brand M.D. The efficiency of cellular energy transduction and its implications for obesity. Annu. Rev. Nutr. 2008, 28:13-33.
179. Lazarin Mde O., Ishii-Iwamoto E.L., Yamamoto N.S., Constantin R.P., Garcia R.F., da Costa C.E., Vitoriano Ade S., de Oliveira M.C., Salgueiro-Pagadigorria C.L. Liver mitochondrial function and redox status in an experimental model of non-alcoholic fatty liver disease induced by monosodium L-glutamate in rats. Exp. Mol. Pathol. 2011, 91:687-694.
180. Blatnik M., Thorpe S.R., Baynes J.W. Succination of proteins by fumarate: mechanism of inactivation of glyceraldehyde-3-phosphate dehydrogenase in diabetes. Ann. N. Y. Acad. Sci. 2008, 1126:272-275.
181. Frizzell N., Lima M., Baynes J.W. Succination of proteins in diabetes. Free Radic. Res. 2011, 45:101-109.
182. Nagai R., Brock J.W., Blatnik M., Baatz J.E., Bethard J., Walla M.D., Thorpe S.R., Baynes J.W., Frizzell N. Succination of protein thiols during adipocyte maturation: a biomarker of mitochondrial stress. J. Biol. Chem. 2007, 282:34219-34228.
183. Frizzell N., Thomas S.A., Carson J.A., Baynes J.W. Mitochondrial stress causes increased succination of proteins in adipocytes in response to glucotoxicity. Biochem. J. 2012, 445:247-254.
184. Ternette N., Yang M., Laroyia M., Kitagawa M., O'Flaherty L., Wolhulter K., Igarashi K., Saito K., Kato K., Fischer R., Berquand A., Kessler B.M., Lappin T., Frizzell N., Soga T., Adam J., Pollard P.J. Inhibition of mitochondrial aconitase by succination in fumarate hydratase deficiency. Cell Rep. 2013, 3:689-700.
185. Sabens Liedhegner E.A., Gao X.H., Mieyal J.J. Mechanisms of altered redox regulation in neurodegenerative diseases-focus on S-glutathionylation. Antioxid. Redox Signal. 2012, 16:543-566.
186. Ansari M.A., Scheff S.W. Oxidative stress in the progression of Alzheimer disease in the frontal cortex. J. Neuropathol. Exp. Neurol. 2010, 69:155-167.
187. Jenner P., Dexter D.T., Sian J., Schapira A.H., Marsden C.D. Oxidative stress as a cause of nigral cell death in Parkinson's disease and incidental Lewy body disease. The Royal Kings and Queens Parkinson's Disease Research Group. Ann. Neurol. 1992, 32(Suppl:):S82-S87.
188. Sian J., Dexter D.T., Lees A.J., Daniel S., Agid Y., Javoy-Agid F., Jenner P., Marsden C.D. Alterations in glutathione levels in Parkinson's disease and other neurodegenerative disorders affecting basal ganglia. Ann. Neurol. 1994, 36:348-355.
189. Schulz J.B., Lindenau J., Seyfried J., Dichgans J. Glutathione, oxidative stress and neurodegeneration. Eur. J. Biochem./FEBS 2000, 267:4904-4911.
190. Lee D.W., Kaur D., Chinta S.J., Rajagopalan S., Andersen J.K. A disruption in iron-sulfur center biogenesis via inhibition of mitochondrial dithiol glutaredoxin 2 may contribute to mitochondrial and cellular iron dysregulation in mammalian glutathione-depleted dopaminergic cells: implications for Parkinson's disease. Antioxid. Redox Signal. 2009, 11:2083-2094.
191. Calabrese V., Scapagnini G., Ravagna A., Bella R., Butterfield D.A., Calvani M., Pennisi G., Giuffrida Stella A.M. Disruption of thiol homeostasis and nitrosative stress in the cerebrospinal fluid of patients with active multiple sclerosis: evidence for a protective role of acetylcarnitine. Neurochem. Res. 2003, 28:1321-1328.
192. Akterin S., Cowburn R.F., Miranda-Vizuete A., Jimenez A., Bogdanovic N., Winblad B., Cedazo-Minguez A. Involvement of glutaredoxin-1 and thioredoxin-1 in beta-amyloid toxicity and Alzheimer's disease. Cell Death Differ. 2006, 13:1454-1465.
193. Kenchappa R.S., Ravindranath V. Glutaredoxin is essential for maintenance of brain mitochondrial complex I: studies with MPTP. Faseb J. 2003, 17:717-719.
194. Dinoto L., Deture M.A., Purich D.L. Structural insights into Alzheimer filament assembly pathways based on site-directed mutagenesis and S-glutathionylation of three-repeat neuronal Tau protein. Microsc. Res. Tech. 2005, 67:156-163.
195. Chinta S.J., Andersen J.K. Reversible inhibition of mitochondrial complex I activity following chronic dopaminergic glutathione depletion in vitro: implications for Parkinson's disease. Free Radic. Biol. Med. 2006, 41:1442-1448.
196. Hsu M., Srinivas B., Kumar J., Subramanian R., Andersen J. Glutathione depletion resulting in selective mitochondrial complex I inhibition in dopaminergic cells is via an NO-mediated pathway not involving peroxynitrite: implications for Parkinson's disease. J. Neurochem. 2005, 92:1091-1103.
197. Nakamura T., Lipton S.A. Redox modulation by S-nitrosylation contributes to protein misfolding, mitochondrial dynamics, and neuronal synaptic damage in neurodegenerative diseases. Cell Death Differ. 2011, 18:1478-1486.
198. Uehara T., Nakamura T., Yao D., Shi Z.Q., Gu Z., Ma Y., Masliah E., Nomura Y., Lipton S.A. S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 2006, 441:513-517.
199. Cho D.H., Nakamura T., Fang J., Cieplak P., Godzik A., Gu Z., Lipton S.A. S-nitrosylation of Drp1 mediates beta-amyloid-related mitochondrial fission and neuronal injury. Science 2009, 324:102-105.
200. Van Laar V.S., Berman S.B. Mitochondrial dynamics in Parkinson's disease. Exp. Neurol. 2009, 218:247-256.
201. Chen H., Chan D.C. Mitochondrial dynamics-fusion, fission, movement, and mitophagy--in neurodegenerative diseases. Hum. Mol. Genet. 2009, 18:R169-R176.
202. Bossy B., Petrilli A., Klinglmayr E., Chen J., Lutz-Meindl U., Knott A.B., Masliah E., Schwarzenbacher R., Bossy-Wetzel E. S-Nitrosylation of DRP1 does not affect enzymatic activity and is not specific to Alzheimer's disease. J. Alzheimer's Dis.: JAD 2010, 20(Suppl 2):S513-S526.
203. Moosmann B. Respiratory chain cysteine and methionine usage indicate a causal role for thiyl radicals in aging. Exp. Gerontol. 2011, 46:164-169.
204. Schindeldecker M., Stark M., Behl C., Moosmann B. Differential cysteine depletion in respiratory chain complexes enables the distinction of longevity from aerobicity. Mech. Ageing Dev. 2011, 132:171-179.
205. Held J.M., Gibson B.W. Regulatory control or oxidative damage? Proteomic approaches to interrogate the role of cysteine oxidation status in biological processes. Mol. Cell. Proteomics: MCP 2012, 11(R111):013037.
206. Butterfield D.A., Perluigi M., Reed T., Muharib T., Hughes C.P., Robinson R.A., Sultana R. Redox proteomics in selected neurodegenerative disorders: from its infancy to future applications. Antioxid. Redox Signal. 2012, 17:1610-1655.
207. Go Y.M., Jones D.P. Cysteine/cystine redox signaling in cardiovascular disease. Free Radic. Biol. Med. 2011, 50:495-509.
208. Martinez Banaclocha M. N-acetylcysteine elicited increase in complex I activity in synaptic mitochondria from aged mice: implications for treatment of Parkinson's disease. Brain Res. 2000, 859:173-175.
209. Rebrin I., Sohal R.S. Comparison of thiol redox state of mitochondria and homogenates of various tissues between two strains of mice with different longevities. Exp. Gerontol. 2004, 39:1513-1519.
210. Musicco C., Capelli V., Pesce V., Timperio A.M., Calvani M., Mosconi L., Zolla L., Cantatore P., Gadaleta M.N. Accumulation of overoxidized Peroxiredoxin III in aged rat liver mitochondria. Biochim. Biophys. Acta 2009, 1787:890-896.
211. Cai Z., Yan L.J. Protein oxidative modifications: beneficial roles in disease and health. J. Biochem. Pharmacol. Res. 2013, 1:15-26.
212. Droge W. The plasma redox state and ageing. Ageing Res. Rev. 2002, 1:257-278.
213. Velu C.S., Niture S.K., Doneanu C.E., Pattabiraman N., Srivenugopal K.S. Human p53 is inhibited by glutathionylation of cysteines present in the proximal DNA-binding domain during oxidative stress. Biochemistry 2007, 46:7765-7780.
214. 2+/calmodulin-dependent protein kinase I by S-glutathionylation of the active-site cysteine residue. FEBS Lett. 2010, 584:2478-2484.
215. Nakamura T., Tu S., Akhtar M.W., Sunico C.R., Okamoto S., Lipton S.A. Aberrant protein s-nitrosylation in neurodegenerative diseases. Neuron 2013, 78:596-614.
216. Schulman I.H., Hare J.M. Regulation of cardiovascular cellular processes by S-nitrosylation. Biochim. Biophys. Acta 2012, 1820:752-762.
217. Kaneki M., Shimizu N., Yamada D., Chang K. Nitrosative stress and pathogenesis of insulin resistance. Antioxid. Redox Signal. 2007, 9:319-329.
218. Cooper A.J., Pinto J.T., Callery P.S. Reversible and irreversible protein glutathionylation: biological and clinical aspects. Expert Opin. Drug Metab. Toxicol. 2011, 7:891-910.
219. Newman J.C., He W., Verdin E. Mitochondrial protein acylation and intermediary metabolism: regulation by sirtuins and implications for metabolic disease. J. Biol. Chem. 2012, 287:42436-42443.
220. Bouillaud F., Blachier F. Mitochondria and sulfide: a very old story of poisoning, feeding, and signaling?. Antioxid. Redox Signal. 2011, 15:379-391.
221. Szabo C., Ransy C., Modis K., Andriamihaja M., Murghes B., Coletta C., Olah G., Yanagi K., Bouillaud F. Regulation of mitochondrial bioenergetic function by hydrogen sulfide. Part I. Biochemical and physiological mechanisms. Br. J. Pharmacol. 2013, 221. 10.1111/bph.12369.