Mitochondrial respiratory chain complexes as sources and targets of thiol-based redox-regulation

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1844, Issue 8, 2014, Pages 1344-1354

  Dröse, Stefan ^a   Brandt, Ulrich ^b,c   Wittig, Ilka ^c  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

Active deactive transition; Mitochondria; Reactive oxygen species (ROS); Redox proteomics; Respiratory chain complex; S nitrosylation

Indexed keywords

MITOCHONDRIAL PROTEIN; REACTIVE OXYGEN METABOLITE; SUCCINATE DEHYDROGENASE (UBIQUINONE); THIOL;

CELL ORGANELLE; HUMAN; MITOCHONDRION; OXIDATION REDUCTION REACTION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEOMICS; RESPIRATORY CHAIN; REVIEW;

ACTIVE/DEACTIVE TRANSITION; MITOCHONDRIA; REACTIVE OXYGEN SPECIES (ROS); REDOX PROTEOMICS; RESPIRATORY CHAIN COMPLEX; S-NITROSYLATION;

ANIMALS; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX I; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SULFHYDRYL COMPOUNDS;

EID: 84902242573     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2014.02.006     Document Type: Review

References (170)

1. M.P. Murphy How mitochondria produce reactive oxygen species Biochem. J. 417 2009 1 13
2. A.J. Kowaltowski, N.C. Souza-Pinto, R.F. Castilho, and A.E. Vercesi Mitochondria and reactive oxygen species Free Radic. Biol. Med. 47 2009 333 343
3. M.D. Brand The sites and topology of mitochondrial superoxide production Exp. Gerontol. 45 2010 466 472
4. S. Dröse, and U. Brandt Molecular mechanisms of superoxide production by the mitochondrial respiratory chain Adv. Exp. Med. Biol. 748 2012 145 169
5. A.I. Andreyev, Y.E. Kushnareva, and A.A. Starkov Mitochondrial metabolism of reactive oxygen species Biochemistry (Mosc) 70 2005 200 214 (Pubitemid 40512329)
6. A.A. Starkov The role of mitochondria in reactive oxygen species metabolism and signaling Ann. N. Y. Acad. Sci. 1147 2008 37 52
7. A.G. Cox, C.C. Winterbourn, and M.B. Hampton Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling Biochem. J. 425 2010 313 325
8. M.P. Murphy Mitochondrial thiols in antioxidant protection and redox signaling: distinct roles for glutathionylation and other thiol modifications Antioxid. Redox Signal. 16 2012 476 495
9. T.R. Figueira, M.H. Barros, A.A. Camargo, R.F. Castilho, J.C.B. Ferreira, A.J. Kowaltowski, F.E. Sluse, N.C. Souza-Pinto, and A.E. Vercesi Mitochondria as a source of reactive oxygen and nitrogen species: from molecular mechanisms to human health Antioxid. Redox Signal. 18 2013 2029 2074
10. M.T. Lin, and M.F. Beal Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases Nature 443 2006 787 795 (Pubitemid 44622683)
11. F. Weinberg, and N.S. Chandel Reactive oxygen species-dependent signaling regulates cancer Cell. Mol. Life Sci. 66 2009 3663 3673
12. D.C. Wallace Mitochondria and cancer Nat. Rev. Cancer 12 2012 685 698
13. A.P. Halestrap, S.J. Clarke, and I. Khaliulin The role of mitochondria in protection of the heart by preconditioning Biochim. Biophys. Acta 1767 2007 1007 1031 (Pubitemid 47101788)
14. D.M. Yellon, and D.J. Hausenloy Mechanisms of disease: myocardial reperfusion injury N. Engl. J. Med. 357 2007 1121 1135
15. R.B. Hamanaka, and N.S. Chandel Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes Trends Biochem. Sci. 35 2010 505 513
16. M.P. Murphy, A. Holmgren, N.G. Larsson, B. Halliwell, C.J. Chang, B. Kalyanaraman, S.G. Rhee, P.J. Thornalley, L. Partridge, D. Gems, T. Nystrom, V. Belousov, P.T. Schumacker, and C.C. Winterbourn Unraveling the biological roles of reactive oxygen species Cell Metab. 13 2011 361 366
17. T. Finkel Signal transduction by mitochondrial oxidants J. Biol. Chem. 287 2012 4434 4440
18. C.C. Winterbourn, and M.B. Hampton Thiol chemistry and specificity in redox signaling Free Radic. Biol. Med. 45 2008 549 561
19. N. Brandes, S. Schmitt, and U. Jakob Thiol-based redox switches in eukaryotic proteins Antioxid. Redox Signal. 11 2009 997 1014
20. Y.M. Go, and D.P. Jones The redox proteome J. Biol. Chem. 288 2013 26512 26520
21. m-Dependent and -independent production of reactive oxygen species by rat brain mitochondria J. Neurochem. 79 2001 266 277 (Pubitemid 32988942)
22. A.J. Lambert, and M.D. Brand Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I) J. Biol. Chem. 279 2004 39414 39420 (Pubitemid 39258206)
23. A.J. Lambert, and M.D. Brand Superoxide production by NADH:ubiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane Biochem. J. 382 2004 511 517 (Pubitemid 39243917)
24. A. Galkin, and U. Brandt Superoxide radical formation by pure complex I (NADH:ubiquinone oxidoreductase) from Yarrowia lipolytica J. Biol. Chem. 280 2005 30129 30135 (Pubitemid 41216190)
25. L. Kussmaul, and J. Hirst The mechanism of superoxide production by NADH:ubiquinone oxidoreductase (complex I) from bovine heart mitochondria Proc. Natl. Acad. Sci. U. S. A. 103 2006 7607 7612
26. F.L. Muller, Y.H. Liu, M.A. Abdul-Ghani, M.S. Lustgarten, A. Bhattacharya, Y.C. Jang, and H. Van Remmen High rates of superoxide production in skeletal-muscle mitochondria respiring on both complex I- and complex II-linked substrates Biochem. J. 409 2008 491 499 (Pubitemid 351184967)
27. C.L. Quinlan, A.L. Orr, I.V. Perevoshchikova, J.R. Treberg, B.A. Ackrell, and M.D. Brand Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions J. Biol. Chem. 287 2012 27255 27264
28. S. Dröse Differential effects of complex II on mitochondrial ROS production and their relation to cardioprotective pre- and postconditioning Biochim. Biophys. Acta 1827 2013 578 587
29. I. Siebels, and S. Dröse Q-site inhibitor induced ROS production of mitochondrial complex II is attenuated by TCA cycle dicarboxylates Biochim. Biophys. Acta 1827 2013 1156 1164
30. 1 complex Biochemistry 41 2002 7866 7874 (Pubitemid 34655151)
31. 1 complex J. Biol. Chem. 283 2008 21649 21654
32. 1. Implications for the mechanism of superoxide production Biochim. Biophys. Acta 1797 2010 1820 1827
33. L. Bleier, and S. Dröse Superoxide generation by complex III: from mechanistic rationales to functional consequences Biochim. Biophys. Acta 1827 2013 1320 1331
34. P. Lanciano, B. Khalfaoui-Hassani, N. Selamoglu, A. Ghelli, M. Rugolo, and F. Daldal Molecular mechanisms of superoxide production by complex III: a bacterial versus human mitochondrial comparative case study Biochim. Biophys. Acta 1827 2013 1332 1339
35. D.V. Dibrova, D.A. Cherepanov, M.Y. Galperin, V.P. Skulachev, and A.Y. Mulkidjanian Evolution of cytochrome bc complexes: from membrane-anchored dehydrogenases of ancient bacteria to triggers of apoptosis in vertebrates Biochim. Biophys. Acta 1827 2013 1407 1427
36. Y.R. Chen, C.L. Chen, D.R. Pfeiffer, and J.L. Zweier Mitochondrial complex II in the post-ischemic heart - oxidative injury and the role of protein S-glutathionylation J. Biol. Chem. 282 2007 32640 32654 (Pubitemid 350159288)
37. C.L. Chen, S. Varadhara, P.P. Kaumaya, J.L. Zweier, and Y.R. Chen Oxidative modification with protein tyrosine nitration occurs following deglutathiolation of the 70 kDa flavoprotein of mitochondrial complex II is associated with loss of electron transfer activity in the post-ischemic myocardium Circulation 118 2008 S273
38. T.R. Hurd, R. Requejo, A. Filipovska, S. Brown, T.A. Prime, A.J. Robinson, I.M. Fearnley, and M.P. Murphy 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. 283 2008 24801 24815
39. S.R. Danielson, and J.K. Andersen Oxidative and nitrative protein modifications in Parkinson's disease Free Radic. Biol. Med. 44 2008 1787 1794
40. J.F. Chen, C.L. Chen, S. Rawale, C.A. Chen, J.L. Zweier, P.T.P. Kaumaya, and Y.R. Chen Peptide-based antibodies against glutathione-binding domains suppress superoxide production mediated by mitochondrial complex I J. Biol. Chem. 285 2010 3168 3180
41. V. Kumar, T. Kleffmann, M.B. Hampton, M.B. Cannell, and C.C. Winterbourn Redox proteomics of thiol proteins in mouse heart during ischemia/reperfusion using ICAT reagents and mass spectrometry Free Radic. Biol. Med. 58 2013 109 117
42. T.A. Prime, F.H. Blaikie, C. Evans, S.M. Nadtochiy, A.M. James, C.C. Dahm, D.A. Vitturi, R.P. Patel, C.R. Hiley, I. Abakumova, R. Requejo, E.T. Chouchani, T.R. Hurd, J.F. Garvey, C.T. Taylor, P.S. Brookes, R.A.J. Smith, and M.P. Murphy A mitochondria-targeted S-nitrosothiol modulates respiration, nitrosates thiols, and protects against ischemia-reperfusion injury Proc. Natl. Acad. Sci. U. S. A. 106 2009 10764 10769
43. E.T. Chouchani, C. Methner, S.M. Nadtochiy, A. Logan, V.R. Pell, S.J. Ding, A.M. James, H.M. Cocheme, J. Reinhold, K.S. Lilley, L. Partridge, I.M. Fearnley, A.J. Robinson, R.C. Hartley, R.A.J. Smith, T. Krieg, P.S. Brookes, and M.P. Murphy Cardioprotection by S-nitrosation of a cysteine switch on mitochondrial complex I Nat. Med. 19 2013 753 759
44. J.M. Herrmann, and J. Riemer Mitochondrial disulfide relay: redox-regulated protein import into the intermembrane space J. Biol. Chem. 287 2012 4426 4433
45. T.G. Frey, and C.A. Mannella The internal structure of mitochondria Trends Biochem. Sci. 25 2000 319 324
46. C.A. Mannella The relevance of mitochondrial membrane topology to mitochondrial function Biochim. Biophys. Acta 1762 2006 140 147 (Pubitemid 43006021)
47. J.M. Herrmann, and J. Riemer The intermembrane space of mitochondria Antioxid. Redox Signal. 13 2010 1341 1358
48. H. Schägger, and K. Pfeiffer Supercomplexes in the respiratory chains of yeast and mammalian mitochondria EMBO J. 19 2000 1777 1783 (Pubitemid 30204389)
49. K.M. Davies, M. Strauss, B. Daum, J. Kief, H.D. Osiewacz, A. Rycovska, V. Zickermann, and W. Kühlbrandt Macromolecular organization of ATP synthase and complex I in whole mitochondria Proc. Natl. Acad. Sci. U. S. A. 108 2011 14121 14126
50. K.M. Davies, C. Anselmi, I. Wittig, J.D. Faraldo-Gomez, and W. Kuhlbrandt Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae Proc. Natl. Acad. Sci. U. S. A. 109 2012 13602 13607
51. K.M. Davies, and B. Daum Role of cryo-ET in membrane bioenergetics research Biochem. Soc. Trans. 41 2013 1227 1234
52. J.J. Hu, L.X. Dong, and C.E. Outten The redox environment in the mitochondrial intermembrane space is maintained separately from the cytosol and matrix J. Biol. Chem. 283 2008 29126 29134
53. E.M. Hanschmann, J.R. Godoy, C. Berndt, C. Hudemann, and C.H. Lillig Thioredoxins, glutaredoxins, and peroxiredoxins-molecular mechanisms and health significance: from cofactors to antioxidants to redox signaling Antioxid. Redox Signal. 19 2013 1539 1605
54. Y.M. Go, and D.P. Jones Redox compartmentalization in eukaryotic cells Biochim. Biophys. Acta 1780 2008 1271 1290
55. J. Garcia, D. Han, H. Sancheti, L.P. Yap, N. Kaplowitz, and E. Cadenas Regulation of mitochondrial glutathione redox status and protein glutathionylation by respiratory substrates J. Biol. Chem. 285 2010 39646 39654
56. F.Q. Schafer, and G.R. Buettner Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple Free Radic. Biol. Med. 30 2001 1191 1212 (Pubitemid 32463931)
57. O.W. Griffith, and A. Meister Origin and turnover of mitochondrial glutathione Proc. Natl. Acad. Sci. U. S. A. 82 1985 4668 4672 (Pubitemid 16239624)
58. M. Mari, A. Morales, A. Colell, C. Garcia-Ruiz, and J.C. Fernandez-Checa Mitochondrial glutathione, a key survival antioxidant Antioxid. Redox Signal. 11 2009 2685 2700
59. I. Rebrin, and R.S. Sohal Comparison of thiol redox state of mitochondria and homogenates of various tissues between two strains of mice with different longevities Exp. Gerontol. 39 2004 1513 1519 (Pubitemid 39410551)
60. M. Kemp, Y.M. Go, and D.P. Jones Nonequilibrium thermodynamics of thiol/disulfide redox systems: a perspective on redox systems biology Free Radic. Biol. Med. 44 2008 921 937
61. A.R. Cardoso, B. Chausse, F.M. da Cunha, L.A. Luevano-Martinez, T.B.M. Marazzi, P.S. Pessoa, B.B. Queliconi, and A.J. Kowaltowski Mitochondrial compartmentalization of redox processes Free Radic. Biol. Med. 52 2012 2201 2208
62. J. Rydström Mitochondrial NADPH, transhydrogenase and disease Biochim. Biophys. Acta 1757 2006 721 726 (Pubitemid 43993846)
63. L.A. Sazanov, and J.B. Jackson Proton-translocating transhydrogenase and NAD-linked and NADP-linked isocitrate dehydrogenases operate in a substrate cycle which contributes to fine regulation of the tricarboxylic-acid cycle activity in mitochondria FEBS Lett. 344 1994 109 116
64. +-dependent isocitrate dehydrogenase J. Biol. Chem. 276 2001 16168 16176
65. +/NADPH in cellular functions and cell death: regulation and biological consequences Antioxid. Redox Signal. 10 2008 179 206
66. J. Rydström Energy-linked nicotinamide nucleotide transhydrogenase - properties of proton-translocating and ATP-driven transhydrogenase reconstituted from synthetic phospholipids and purified transhydrogenase from beef-heart mitochondria J. Biol. Chem. 254 1979 8611 8619
67. 2 + J. Biol. Chem. 279 2004 4166 4174 (Pubitemid 38199002)
68. 2 removal in brain mitochondria via the thioredoxin/peroxiredoxin system J. Biol. Chem. 285 2010 27850 27858
69. J.R. Treberg, C.L. Quinlan, and M.D. Brand Hydrogen peroxide efflux from muscle mitochondria underestimates matrix superoxide production - a correction using glutathione depletion FEBS J. 277 2010 2766 2778
70. 2 emission from isolated heart mitochondria J. Biol. Chem. 286 2011 33669 33677
71. 2 emission: an experimental-computational study J. Gen. Physiol. 139 2012 479 491
72. R. Requejo, T.R. Hurd, N.J. Costa, and M.P. Murphy Cysteine residues exposed on protein surfaces are the dominant intramitochondrial thiol and may protect against oxidative damage FEBS J. 277 2010 1465 1480
73. C.C. Winterbourn Reconciling the chemistry and biology of reactive oxygen species Nat. Chem. Biol. 4 2008 278 286 (Pubitemid 351550893)
74. T.R. Hurd, N.J. Costa, C.C. Dahm, S.M. Beer, S.E. Brown, A. Filipovska, and M.P. Murphy Glutathionylation of mitochondrial proteins Antioxid. Redox Signal. 7 2005 999 1010 (Pubitemid 40967150)
75. A.V. Peskin, and C.C. Winterbourn Kinetics of the reactions of hypochlorous acid and amino acid chloramines with thiols, methionine, and ascorbate Free Radic. Biol. Med. 30 2001 572 579 (Pubitemid 32162964)
76. K. Kojer, M. Bien, H. Gangel, B. Morgan, T.P. Dick, and J. Riemer Glutathione redox potential in the mitochondrial intermembrane space is linked to the cytosol and impacts the Mia40 redox state EMBO J. 31 2012 3169 3182
77. U. Brandt Energy converting NADH: quinone oxidoreductase (complex I) Annu. Rev. Biochem. 75 2006 69 92 (Pubitemid 44118026)
78. H. Angerer, K. Zwicker, Z. Wumaier, L. Sokolova, H. Heide, M. Steger, S. Kaiser, E. Nubel, B. Brutschy, M. Radermacher, U. Brandt, and V. Zickermann A scaffold of accessory subunits links the peripheral arm and the distal proton pumping module of mitochondrial complex I Biochem. J. 437 2011 279 288
79. N. Mesecke, N. Terziyska, C. Kozany, F. Baumann, W. Neupert, K. Hell, and J.M. Herrmann A disulfide relay system in the intermembrane space of mitochondria that mediates protein import Cell 121 2005 1059 1069 (Pubitemid 40884396)
80. M. Bien, M. Fischer, S. Longen, J.M. Herrmann, and J. Riemer Oxidative protein folding in the intermembrane space of mitochondria Biochim. Biophys. Acta 1797 2010 109
81. A.A. Starkov, G. Fiskum, C. Chinopoulos, B.J. Lorenzo, S.E. Browne, M.S. Patel, and M.F. Beal Mitochondrial α-ketoglutarate dehydrogenase complex generates reactive oxygen species J. Neurosci. 24 2004 7779 7788 (Pubitemid 39215681)
82. T. Mracek, Z. Drahota, and J. Houstek The function and the role of the mitochondrial glycerol-3-phosphate dehydrogenase in mammalian tissues Biochim. Biophys. Acta 1827 2013 401 410
83. T. Mracek, E. Holzerova, Z. Drahota, N. Kovarova, M. Vrbacky, P. Jesina, and J. Houstek ROS generation and multiple forms of mammalian mitochondrial glycerol-3-phosphate dehydrogenase Biochim. Biophys. Acta 1837 2014 98 111
84. S. Dröse, P.J. Hanley, and U. Brandt Ambivalent effects of diazoxide on mitochondrial ROS production at respiratory chain complexes I and III Biochim. Biophys. Acta 1790 2009 558 565
85. S. Dröse, L. Bleier, and U. Brandt A common mechanism links differently acting complex II inhibitors to cardioprotection: modulation of mitochondrial reactive oxygen species production Mol. Pharmacol. 79 2011 814 822
86. H.J. Forman, M. Maiorino, and F. Ursini Signaling functions of reactive oxygen species Biochemistry 49 2010 835 842
87. J. St Pierre, J.A. Buckingham, S.J. Roebuck, and M.D. Brand Topology of superoxide production from different sites in the mitochondrial electron transport chain J. Biol. Chem. 277 2002 44784 44790 (Pubitemid 36159072)
88. F.L. Muller, Y.H. Liu, and H. Van Remmen Complex III releases superoxide to both sides of the inner mitochondrial membrane J. Biol. Chem. 279 2004 49064 49073 (Pubitemid 39625788)
89. Q. Chen, E.J. Vazquez, S. Moghaddas, C.L. Hoppel, and E.J. Lesnefsky Production of reactive oxygen species by mitochondria: central role of complex III J. Biol. Chem. 278 2003 36027 36031 (Pubitemid 37139922)
90. V.G. Grivennikova, and A.D. Vinogradov Generation of superoxide by the mitochondrial complex I Biochim. Biophys. Acta 1757 2006 553 561 (Pubitemid 43993849)
91. K.R. Pryde, and J. Hirst Superoxide is produced by the reduced flavin in mitochondrial complex I J. Biol. Chem. 286 2011 18056 18065
92. J.R. Treberg, C.L. Quinlan, and M.D. Brand Evidence for two sites of superoxide production by mitochondrial NADH-ubiquinone oxidoreductase (complex I) J. Biol. Chem. 286 2011 27103 27110
93. C. Hunte, V. Zickermann, and U. Brandt Functional modules and structural basis of conformational coupling in mitochondrial complex I Science 329 2010 448 451
94. 1 complex probed by superoxide production Biochemistry 42 2003 6493 6499 (Pubitemid 36665824)
95. o site for reaction with oxygen Biochemistry 47 2008 12365 12370
96. 1 Biochemistry 52 2013 6388 6395
97. J. Guo, and B.D. Lemire The ubiquinone-binding site of the Saccharomyces cerevisiae succinate-ubiquinone oxidoreductase is a source of superoxide J. Biol. Chem. 278 2003 47629 47635 (Pubitemid 37523207)
98. S.S.W. Szeto, S.N. Reinke, B.D. Sykes, and B.D. Lemire Ubiquinone-binding site mutations in the Saccharomyces cerevisiae succinate dehydrogenase generate superoxide and lead to the accumulation of succinate J. Biol. Chem. 282 2007 27518 27526 (Pubitemid 47501935)
99. M.P. Paranagama, K. Sakamoto, H. Amino, M. Awano, H. Miyoshi, and K. Kita Contribution of the FAD and quinone binding sites to the production of reactive oxygen species from Ascaris suum mitochondrial complex II Mitochondrion 10 2010 158 165
100. V. Kumar, T.D. Calamaras, D. Haeussler, W.S. Colucci, R.A. Cohen, M.E. Mccomb, D. Pimentel, and M.M. Bachschmid Cardiovascular redox and ox stress proteomics Antioxid. Redox Signal. 17 2012 1528 1559
101. A. Bachi, I. Dalle-Donne, and A. Scaloni Redox proteomics: chemical principles, methodological approaches and biological/biomedical promises Chem. Rev. 113 2013 596 698
102. E.T. Chouchani, A.M. James, I.M. Fearnley, K.S. Lilley, and M.P. Murphy Proteomic approaches to the characterization of protein thiol modification Curr. Opin. Chem. Biol. 15 2011 120 128
103. R.E. Hansen, and J.R. Winther An introduction to methods for analyzing thiols and disulfides: reactions, reagents, and practical considerations Anal. Biochem. 394 2009 147 158
104. P. Eaton Protein thiol oxidation in health and disease: techniques for measuring disulfides and related modifications in complex protein mixtures Free Radic. Biol. Med. 40 2006 1889 1899 (Pubitemid 43744434)
105. L.K. Rogers, B.L. Leinweber, and C.V. Smith Detection of reversible protein thiol modifications in tissues Anal. Biochem. 358 2006 171 184 (Pubitemid 44573080)
106. J. Ying, N. Clavreul, M. Sethuraman, T. Adachi, and R.A. Cohen Thiol oxidation in signaling and response to stress: detection and quantification of physiological and pathophysiological thiol modifications Free Radic. Biol. Med. 43 2007 1099 1108 (Pubitemid 47374443)
107. R. Charles, T. Jayawardhana, and P. Eaton Gel-based methods in redox proteomics Biochim. Biophys. Acta 1840 2014 830 837
108. A. Galkin, B. Meyer, I. Wittig, M. Karas, H. Schagger, A. Vinogradov, and U. Brandt Identification of the mitochondrial ND3 subunit as a structural component involved in the active/deactive enzyme transition of respiratory complex I J. Biol. Chem. 283 2008 20907 20913
109. P.H. O'Farrell High-resolution 2-dimensional electrophoresis of proteins J. Biol. Chem. 250 1975 4007 4021
110. J.W. Baty, M.B. Hampton, and C.C. Winterbourn Detection of oxidant sensitive thiol proteins by fluorescence labeling and two-dimensional electrophoresis Proteomics 2 2002 1261 1266
111. T.R. Hurd, T.A. Prime, M.E. Harbour, K.S. Lilley, and M.P. Murphy Detection of reactive oxygen species-sensitive thiol proteins by redox difference gel electrophoresis - implications for mitochondrial redox signaling J. Biol. Chem. 282 2007 22040 22051 (Pubitemid 47195755)
112. M. Unlu, M.E. Morgan, and J.S. Minden Difference gel electrophoresis: a single gel method for detecting changes in protein extracts Electrophoresis 18 1997 2071 2077 (Pubitemid 27501267)
113. E.T. Chouchani, T.R. Hurd, S.M. Nadtochiy, P.S. Brookes, I.M. Fearnley, K.S. Lilley, R.A.J. Smith, and M.P. Murphy Identification of S-nitrosated mitochondrial proteins by S-nitrosothiol difference in gel electrophoresis (SNO-DIGE): implications for the regulation of mitochondrial function by reversible S-nitrosation Biochem. J. 430 2010 49 59
114. R. Scheving, I. Wittig, H. Heide, B. Albuquerque, M. Steger, U. Brandt, and I. Tegeder Protein S-nitrosylation and denitrosylation in the mouse spinal cord upon injury of the sciatic nerve J. Proteome 75 2012 3987 4004
115. J.M. Held, S.R. Danielson, J.B. Behring, C. Atsriku, D.J. Britton, R.L. Puckett, B. Schilling, J. Campisi, C.C. Benz, and B.W. Gibson Targeted quantitation of site-specific cysteine oxidation in endogenous proteins using a differential alkylation and multiple reaction monitoring mass spectrometry approach Mol. Cell. Proteomics 9 2010 1400 1410
116. S.R. Jaffrey, H. Erdjument-Bromage, C.D. Ferris, P. Tempst, and S.H. Snyder Protein S-nitrosylation: a physiological signal for neuronal nitric oxide Nat. Cell Biol. 3 2001 193 197 (Pubitemid 32118373)
117. G. Hao, B. Derakhshan, L. Shi, F. Campagne, and S.S. Gross SNOSID, a proteomic method for identification of cysteine S-nitrosylation sites in complex protein mixtures Proc. Natl. Acad. Sci. U. S. A. 103 2006 1012 1017 (Pubitemid 43212213)
118. L.B. Poole, C. Klomsiri, S.A. Knaggs, C.M. Furdui, K.J. Nelson, M.J. Thomas, J.S. Fetrow, L.W. Daniel, and S.B. King Fluorescent and affinity-based tools to detect cysteine sulfenic acid formation in proteins Bioconjug. Chem. 18 2007 2004 2017 (Pubitemid 350220002)
119. R.L. Charles, E. Schroder, G. May, P. Free, P.R.J. Gaffney, R. Wait, S. Begum, R.J. Heads, and P. Eaton Protein sulfenation as a redox sensor - proteomics studies using a novel biotinylated dimedone analogue Mol. Cell. Proteomics 6 2007 1473 1484 (Pubitemid 47506161)
120. V. Gupta, and K.S. Carroll Sulfenic acid chemistry, detection and cellular lifetime Biochim. Biophys. Acta 1840 2014 847 875
121. Y. Shiio, and R. Aebersold Quantitative proteome analysis using isotope-coded affinity tags and mass spectrometry Nat. Protoc. 1 2006 139 145
122. M. Sethuraman, M.E. Mccomb, H. Huang, S.Q. Huang, T. Heibeck, C.E. Costello, and R.A. Cohen Isotope-coded affinity tag (ICAT) approach to redox proteomics: identification and quantitation of oxidant-sensitive cysteine thiols in complex protein mixtures J. Proteome Res. 3 2004 1228 1233 (Pubitemid 40040377)
123. M. Sethuraman, M.E. Mccomb, T. Heibeck, C.E. Costello, and R.A. Cohen Isotope-coded affinity tag approach to identify and quantify oxidant-sensitive protein thiols Mol. Cell. Proteomics 3 2004 273 278 (Pubitemid 38714283)
124. L.I. Leichert, F. Gehrke, H.V. Gudiseva, T. Blackwell, M. Ilbert, A.K. Walker, J.R. Strahler, P.C. Andrews, and U. Jakob Quantifying changes in the thiol redox proteome upon oxidative stress in vivo Proc. Natl. Acad. Sci. U. S. A. 105 2008 8197 8202 (Pubitemid 351904734)
125. N. Brandes, D. Reichmann, H. Tienson, L.I. Leichere, and U. Jakob Using quantitative redox proteomics to dissect the yeast redoxome J. Biol. Chem. 286 2011 41893 41903
126. C. Lindemann, and L.I. Leichert Quantitative redox proteomics: the NOxICAT method Methods Mol. Biol. 893 2012 387 403
127. D. Knoefler, M. Thamsen, M. Koniczek, N.J. Niemuth, A.K. Diederich, and U. Jakob Quantitative in vivo redox sensors uncover oxidative stress as an early event in life Mol. Cell 47 2012 767 776
128. 2-oxidized proteins J. Proteome 74 2011 2476 2486
129. P. Martinez-Acedo, E. Nunez, F.J. Gomez, M. Moreno, E. Ramos, A. Izquierdo-Alvarez, E. Miro-Casas, R. Mesa, P. Rodriguez, A. Martinez-Ruiz, D.G. Dorado, S. Lamas, and J. Vazquez A novel strategy for global analysis of the dynamic thiol redox proteome Mol. Cell. Proteomics 11 2012 800 813
130. H. Heide, L. Bleier, M. Steger, J. Ackermann, S. Dröse, B. Schwamb, M. Zornig, A.S. Reichert, I. Koch, I. Wittig, and U. Brandt Complexome profiling identifies TMEM126B as a component of the mitochondrial complex I assembly complex Cell Metab. 16 2012 538 549
131. A.C. Nulton-Persson, D.W. Starke, J.J. Mieyal, and L.I. Szweda Reversible inactivation of alpha-ketoglutarate dehydrogenase in response to alterations in the mitochondrial glutathione status Biochemistry 42 2003 4235 4242 (Pubitemid 36418317)
132. M.A.B. Applegate, K.M. Humphries, and L.I. Szweda Reversible inhibition of alpha-ketoglutarate dehydrogenase by hydrogen peroxide: glutathionylation and protection of lipoic acid Biochemistry 47 2008 473 478
133. A.L. Mclain, P.J. Cormier, M. Kinter, and L.I. Szweda Glutathionylation of alpha-ketoglutarate dehydrogenase: the chemical nature and relative susceptibility of the cofactor lipoic acid to modification Free Radic. Biol. Med. 61 2013 161 169
134. J. Engelhard, B.E. Christian, L. Weingarten, G. Kuntz, L.L. Spremulli, and T.P. Dick In situ kinetic trapping reveals a fingerprint of reversible protein thiol oxidation in the mitochondrial matrix Free Radic. Biol. Med. 50 2011 1234 1241
135. A.P. Halestrap, K.Y. Woodfield, and C.P. Connern Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase J. Biol. Chem. 272 1997 3346 3354
136. S.M. Davidson, D.M. Yellon, M.P. Murphy, and M.R. Duchen Slow calcium waves and redox changes precede mitochondrial permeability transition pore opening in the intact heart during hypoxia and reoxygenation Cardiovasc. Res. 93 2012 445 453
137. A.W.C. Leung, and A.P. Halestrap Recent progress in elucidating the molecular mechanism of the mitochondrial permeability transition pore Biochim. Biophys. Acta 1777 2008 946 952
138. V. Giorgio, S. von Stockum, M. Antoniel, A. Fabbro, F. Fogolari, M. Forte, G.D. Glick, V. Petronilli, M. Zoratti, I. Szabo, G. Lippe, and P. Bernardi Dimers of mitochondrial ATP synthase form the permeability transition pore Proc. Natl. Acad. Sci. U. S. A. 110 2013 5887 5892
139. M.J. Kohr, J.H. Sun, A. Aponte, G.H. Wang, M. Gucek, E. Murphy, and C. Steenbergen Simultaneous measurement of protein oxidation and S-nitrosylation during preconditioning and ischemia/reperfusion injury with resin-assisted capture Circ. Res. 108 2011 (418-U50)
140. T.T. Nguyen, M.V. Stevens, M. Kohr, C. Steenbergen, M.N. Sack, and E. Murphy Cysteine 203 of cyclophilin D is critical for cyclophilin D activation of the mitochondrial permeability transition pore J. Biol. Chem. 286 2011 40184 40192
141. R.J. Mailloux, A. Fu, C. Robson-Doucette, E.M. Allister, M.B. Wheeler, R. Screaton, and M.E. Harper Glutathionylation state of uncoupling protein-2 and the control of glucose-stimulated insulin secretion J. Biol. Chem. 287 2012
142. R.J. Mailloux, J.Y. Xuan, B. Beauchamp, L.D. Jui, M. Lou, and M.E. Harper Glutaredoxin-2 is required to control proton leak through uncoupling protein-3 J. Biol. Chem. 288 2013 8365 8379
143. R.J. Mailloux, S.L. McBride, and M.E. Harper Unearthing the secrets of mitochondrial ROS and glutathione in bioenergetics Trends Biochem. Sci. 38 2013 592 602
144. J.H. Sun, M. Morgan, R.F. Shen, C. Steenbergen, and E. Murphy Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport Circ. Res. 101 2007 1155 1163 (Pubitemid 350146442)
145. E.R. Taylor, F. Hurrell, R.J. Shannon, T.K. Lin, J. Hirst, and M.P. Murphy Reversible glutathionylation of complex I increases mitochondrial superoxide formation J. Biol. Chem. 278 2003 19603 19610 (Pubitemid 36799143)
146. L.S. Burwell, S.M. Nadtochiy, A.J. Tompkins, S. Young, and P.S. Brookes Direct evidence for S-nitrosation of mitochondrial complex I Biochem. J. 394 2006 627 634
147. C.C. Dahm, K. Moore, and M.P. Murphy Persistent S-nitrosation of complex I and other mitochondrial membrane proteins by S-nitrosothiols but not nitric oxide or peroxynitrite - implications for the interaction of nitric oxide with mitochondria J. Biol. Chem. 281 2006 10056 10065 (Pubitemid 43864540)
148. C.L. Chen, L.W. Zhang, A. Yeh, C.A. Chen, K.B. Green-Church, J.L. Zweier, and Y.R. Chen Site-specific S-glutathiolation of mitochondrial NADH ubiquinone reductase Biochemistry 46 2007 5754 5765 (Pubitemid 46764124)
149. L. Zhang, H. Xu, C.L. Chen, K.B. Green-Church, M.A. Freitas, and Y.R. Chen Mass spectrometry profiles superoxide-induced intramolecular disulfide in the FMN-binding subunit of mitochondrial complex I J. Am. Soc. Mass Spectrom. 19 2008 1875 1886
150. P.T. Kang, L.W. Zhang, C.L. Chen, J.F. Chen, K.B. Green, and Y.R. Chen Protein thiyl radical mediates S-glutathionylation of complex I Free Radic. Biol. Med. 53 2012 962 973
151. A.B. Kotlyar, and A.D. Vinogradov Slow active/inactive transition of the mitochondrial NADH-ubiquinone reductase Biochim. Biophys. Acta 1019 1990 151 158
152. E. Maklashina, A.B. Kotlyar, and G. Cecchini Active/de-active transition of respiratory complex I in bacteria, fungi, and animals Biochim. Biophys. Acta 1606 2003 95 103 (Pubitemid 37267873)
153. 2 + ions on the slow active/inactive transition of the mitochondrial NADH-ubiquinone reductase Biochim. Biophys. Acta 1098 1992 144 150
154. E.V. Gavrikova, and A.D. Vinogradov Active/de-active state transition of the mitochondrial complex I as revealed by specific sulfhydryl group labeling FEBS Lett. 455 1999 36 40 (Pubitemid 29322777)
155. E. Maklashina, Y. Sher, H.Z. Zhou, M.O. Gray, J.S. Karliner, and G. Cecchini Effect of anoxia/reperfusion on the reversible active/de-active transition of NADH-ubiquinone oxidoreductase (complex I) in rat heart Biochim. Biophys. Acta 1556 2002 6 12 (Pubitemid 35283893)
156. A. Galkin, and S. Moncada S-nitrosation of mitochondrial complex I depends on its structural conformation J. Biol. Chem. 2007 37748 37753
157. A. Galkin, A.Y. Abramov, N. Frakich, M.R. Duchen, and S. Moncada Lack of oxygen deactivates mitochondrial complex I - implications for ischemic injury? J. Biol. Chem. 284 2009 36055 36061
158. R. Baradaran, J.M. Berrisford, G.S. Minhas, and L.A. Sazanov Crystal structure of the entire respiratory complex I Nature 494 2013 443 448
159. S. Kerscher, S. Dröse, K. Zwicker, V. Zickermann, and U. Brandt Yarrowia lipolytica, a yeast genetic system to study mitochondrial complex I Biochim. Biophys. Acta 1555 2002 83 91 (Pubitemid 35246010)
160. M.A. Tocilescu, U. Fendel, K. Zwicker, S. Kerscher, and U. Brandt Exploring the ubiquinone binding cavity of respiratory complex I J. Biol. Chem. 282 2007 29514 29520 (Pubitemid 350043352)
161. H. Angerer, H.R. Nasiri, V. Niedergesass, S. Kerscher, H. Schwalbe, and U. Brandt Tracing the tail of ubiquinone in mitochondrial complex I Biochim. Biophys. Acta 1817 2012 1776 1784
162. M. Ciano, M. Fuszard, H. Heide, C.H. Botting, and A. Galkin Conformation-specific crosslinking of mitochondrial complex I FEBS Lett. 587 2013 867 872
163. I.M. Fearnley, and J.E. Walker Conservation of sequences of subunits of mitochondrial complex I and their relationships with other proteins Biochim. Biophys. Acta 1140 1992 105 134
164. U. Schulte, V. Haupt, A. Abelmann, W. Fecke, B. Brors, T. Rasmussen, T. Friedrich, and H. Weiss A reductase/isomerase subunit of mitochondrial NADH:ubiquinone oxidoreductase (complex I) carries an NADPH and is involved in the biogenesis of the complex J. Mol. Biol. 292 1999 569 580 (Pubitemid 29457319)
165. A. Abdrakhmanova, K. Zwicker, S. Kerscher, V. Zickermann, and U. Brandt Tight binding of NADPH to the 39-kDa subunit of complex I is not required for catalytic activity but stabilizes the multiprotein complex Biochim. Biophys. Acta 1757 2006 1676 1682 (Pubitemid 44841959)
166. C.L. Chen, J.F. Chen, S. Rawale, S. Varadharaj, P.P.T. Kaumaya, J.L. Zweier, and Y.R. Chen Protein tyrosine nitration of the flavin subunit is associated with oxidative modification of mitochondrial complex II in the post-ischemic myocardium J. Biol. Chem. 283 2008 27991 28003
167. L.W. Zhang, C.L. Chen, P.T. Kang, V. Garg, K.L. Hu, K.B. Green-Church, and Y.R. Chen Peroxynitrite-mediated oxidative modifications of complex II: relevance in myocardial infarction Biochemistry 49 2010 2529 2539
168. M. Fratelli, H. Demol, M. Puype, S. Casagrande, I. Eberini, M. Salmona, V. Bonetto, M. Mengozzi, F. Duffieux, E. Miclet, A. Bachi, J. Vandekerckhove, E. Gianazza, and P. Ghezzi Identification by redox proteomics of glutathionylated proteins in oxidatively stressed human T lymphocytes Proc. Natl. Acad. Sci. U. S. A. 99 2002 3505 3510 (Pubitemid 34252138)
169. M. Fratelli, H. Demol, M. Puype, S. Casagrande, P. Villa, I. Eberini, J. Vandekerckhove, E. Gianazza, and P. Ghezzi Identification of proteins undergoing glutathionylation in oxidatively stressed hepatocytes and hepatoma cells Proteomics 3 2003 1154 1161 (Pubitemid 36929537)
170. Brown, and Borutaite There is no evidence that mitochondria are the main source of reactive oxygen species in mammalian cells Mitochondrion 12 2003 1 4