Formation of reactive oxygen species by human and bacterial pyruvate and 2-oxoglutarate dehydrogenase multienzyme complexes reconstituted from recombinant components

Free Radical Biology and Medicine

Volumn 89, Issue , 2015, Pages 642-650

  Ambrus, Attila ^a   Nemeria, Natalia S ^b   Torocsik, Beata ^a   Tretter, Laszlo ^a   Nilsson, Mattias ^a   Jordan, Frank ^a   Adam Vizi, Vera ^b  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

2 oxoglutarate dehydrogenase complex; Alpha ketoglutarate dehydrogenase complex; E3 deficiency; Oxidative stress; Pyruvate dehydrogenase complex; Reactive oxygen species

Indexed keywords

ADENOSINE DIPHOSPHATE; CALCIUM ION; CYTOCHROME C; MULTIENZYME COMPLEX; OXOGLUTARATE DEHYDROGENASE; PYRUVIC ACID; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SUPEROXIDE; RECOMBINANT PROTEIN;

ACIDOSIS; ARTICLE; CATALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PURIFICATION; ENZYME RECONSTITUTION; ESCHERICHIA COLI; GENE MUTATION; HUMAN; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; REDUCTION; STOICHIOMETRY; METABOLISM;

ESCHERICHIA COLI; HUMANS; KETOGLUTARATE DEHYDROGENASE COMPLEX; MULTIENZYME COMPLEXES; PYRUVIC ACID; REACTIVE OXYGEN SPECIES; RECOMBINANT PROTEINS;

EID: 84944391651     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.10.001     Document Type: Article

References (119)

1. V. Massey The composition of the ketoglutarate dehydrogenase complex Biochim. Biophys. Acta 38 1960 447 460
2. L.J. Reed Multienzyme complexes Acc. Chem. Res. 7 1974 40 46
3. R.N. Perham Domains, motifs, and linkers in 2-oxo acid dehydrogenase multienzyme complexes - a paradigm in the design of a multifunctional protein Biochemistry 30 1991 8501 8512
4. K.F.R. Sheu, and J.P. Blass The alpha-ketoglutarate dehydrogenase complex Oxidative/Energy Metabolism in Neurodegenerative Disorders 1999 61 78 New York: New York Acad Sciences
5. G.E. Gibson, L.C.H. Park, K.-F.R. Sheu, J.P. Blass, and N.Y. Calingasan The [alpha]-ketoglutarate dehydrogenase complex in neurodegeneration Neurochem. Int. 36 2000 97 112
6. M.S. Patel, N.S. Nemeria, W. Furey, and F. Jordan The Pyruvate Dehydrogenase Complexes: Structure-based Function and Regulation J. Biol. Chem. 289 2014 16615 16623
7. A.A. Starkov, G. Fiskum, C. Chinopoulos, B.J. Lorenzo, S.E. Browne, M.S. Patel, and M.F. Beal Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species J. Neurosci. 24 2004 7779 7788
8. L. Tretter, and V. Adam-Vizi Generation of reactive oxygen species in the reaction catalyzed by alpha-ketoglutarate dehydrogenase J. Neurosci. 24 2004 7771 7778
9. N.E. Babady, Y.P. Pang, O. Elpeleg, and G. Isaya Cryptic proteolytic activity of dihydrolipoamide dehydrogenase Proc. Natl. Acad. Sci. USA 104 2007 6158 6163
10. T.K. Tyagi, P. Ponnan, P. Singh, S. Bansal, A. Batra, F. Collin, F. Guillonneau, D. Jore, S.A. Patkar, R.K. Saxena, V.S. Parmar, R.C. Rastogi, and H.G. Raj Moonlighting protein in Starkeyomyces koorchalomoides: Characterization of dihydrolipoamide dehydrogenase as a protein acetyltransferase utilizing acetoxycoumarin as the acetyl group donor Biochimie 91 2009 868 875
11. K.H. Fisher-Wellman, L.A.A. Gilliam, C.T. Lin, B.L. Cathey, D.S. Lark, and P.D. Neufer Mitochondrial glutathione depletion reveals a novel role for the pyruvate dehydrogenase complex as a key H2O2-emitting source under conditions of nutrient overload Free Radic. Biol. Med. 65 2013 1201 1208
12. N.S. Nemeria, A. Ambrus, H. Patel, G. Gerfen, V. Adam-Vizi, L. Tretter, J. Zhou, J. Wang, and F. Jordan Human 2-Oxoglutarate Dehydrogenase Complex E1 Component Forms a Thiamin-derived Radical by Aerobic Oxidation of the Enamine Intermediate J. Biol. Chem. 289 2014 29859 29873
13. C.L. Quinlan, R.L. Goncalves, M. Hey-Mogensen, N. Yadava, V.I. Bunik, and M.D. Brand The 2-oxoacid dehydrogenase complexes in mitochondria can produce superoxide/hydrogen peroxide at much higher rates than complex I J Biol Chem 289 2014 8312 8325
14. A.A. Starkov An update on the role of mitochondrial alpha-ketoglutarate dehydrogenase in oxidative stress Molecular and Cellular Neuroscience 55 2013 13 16
15. V. Adam-Vizi, and L. Tretter The role of mitochondrial dehydrogenases in the generation of oxidative stress Neurochem. Int. 62 2013 757 763
16. A. Berg, and A. deKok 2-oxo acid dehydrogenase multienzyme complexes. The central role of the lipoyl domain Biol. Chem. 378 1997 617 634
17. J.R. Guest, M.G. Darlison, M.E. Spencer, and P.E. Stephens Cloning and sequence analysis of the pyruvate and 2-oxoglutarate dehydrogenase complex genes of Escherichia coli Biochem. Soc. Trans. 12 1984 220 223
18. K. Koike Cloning, structure, chromosomal localization and promoter analysis of human 2-oxoglutarate dehydrogenase gene Biochimica Et Biophysica Acta-Protein Structure and Molecular Enzymology 1385 1998 373 384
19. K. Koike, S. Ohta, Y. Urata, Y. Kagawa, and M. Koike Cloning and sequencing of cDNAs encoding alpha-subunits and beta-subunits of human pyruvate dehydrogenase Proc. Natl. Acad. Sci. USA 85 1988 41 45
20. T.J. Thekkumkara, B.W. Jesse, L. Ho, C. Raefsky, R.A. Pepin, A.A. Javed, G. Pons, and M.S. Patel Isolation of a cDNA clone for the dihydrolipoamide acetyltransferase component of the human liver pyruvate dehydrogenase complex Biochem. Biophys. Res. Commun. 145 1987 903 907
21. K. Nakano, C. Takase, T. Sakamoto, S. Nakagawa, J. Inazawa, S. Ohta, and S. Matuda Isolation, characterization and structural organization of the gene and pseudogene for the dihydrolipoamide succinyltransferase component of the human 2-oxoglutarate dehydrogenase complex Eur. J. Biochem. 224 1994 179 189
22. G. Otulakowski, B.H. Robinson, and H.F. Willard Gene for lipoamide dehydrogenase maps to human chromosome 7 Somatic Cell and Molecular Genetics 14 1988 411 414
23. J.P. Brown, and R.N. Perham An amino acid sequence in the active site of lipoamide dehydrogenase from the 2-oxoglutarate dehydrogenase complex of E. coli (Crookes strain) FEBS Letters 26 1972 221 224
24. F.H. Pettit, and L.J. Reed Alpha-keto acid dehydrogenase complexes. 8. Comparison of dihydrolipoyl dehydrogenases from pyruvate and alpha-ketoglutarate dehydrogenase complexes of Escherichia coli Proc. Natl. Acad. Sci. USA 58 1967 1126 1130
25. L.J. Reed, and M.L. Hackert Structure-function relationships in dihydrolipoamide acyltransferases J. Biol. Chem. 265 1990 8971 8974
26. F.M. Huennekens, R.E. Basford, and B.W. Gabrio An oxidase for reduced diphosphopyridine nucleotide J. Biol. Chem. 213 1955 951 967
27. A. Ambrus, L. Tretter, and V. Adam-Vizi Inhibition of the alpha-ketoglutarate dehydrogenase-mediated reactive oxygen species generation by lipoic acid J. Neurochem. 109 2009 222 229
28. L. Tretter, and V. Adam-Vizi Alpha-ketoglutarate dehydrogenase: a target and generator of oxidative stress Philos. Trans. R. Soc. B-Biol. Sci 360 2005 2335 2345
29. V. Adam-Vizi Production of reactive oxygen species in brain mitochondria: Contribution by electron transport chain and non-electron transport chain sources Antioxid. Redox Signal. 7 2005 1140 1149
30. V. Adam-Vizi, and C. Chinopoulos Bioenergetics and the formation of mitochondrial reactive oxygen species Trends in Pharmacological Sciences 27 2006 639 645
31. E.B. Tahara, M.H. Barros, G.A. Oliveira, L.E.S. Netto, and A.J. Kowaltowski Dihydrolipoyl dehydrogenase as a source of reactive oxygen species inhibited by caloric restriction and involved in Saccharomyces cerevisiae aging Faseb J 21 2007 274 283
32. V.I. Bunik, J.V. Schloss, J.T. Pinto, G.E. Gibson, and A.J.L. Cooper Enzyme-catalyzed side reactions with molecular oxygen may contribute to cell signaling and neurodegenerative diseases Neurochem. Res. 32 2007 871 891
33. G. Zundorf, S. Kahlert, V.I. Bunik, and G. Reiser Alpha-ketoglutarate dehydrogenase contributes to production of reactive oxygen species in glutamate-stimulated hippocampal neurons in situ Neuroscience 158 2009 610 616
34. A. Graf, M. Kabysheva, E. Klimuk, L. Trofimova, T. Dunaeva, G. Zundorf, S. Kahlert, G. Reiser, T. Storozhevykh, V. Pinelis, N. Sokolova, and V. Bunik Role of 2-oxoglutarate dehydrogenase in brain pathologies involving glutamate neurotoxicity J. Mol. Catal. B-Enzym. 61 2009 80 87
35. A.A. Starkov, and V. Adam-Vizi Calcium and mitochondrial reactive oxygen species generation: how to read the facts J. Alzheim. Dis 20 2010 S413 S426
36. G.E. Gibson, A. Starkov, J.P. Blass, R.R. Ratan, and M.F. Beal Cause and consequence: Mitochondrial dysfunction initiates and propagates neuronal dysfunction, neuronal death and behavioral abnormalities in age-associated neurodegenerative diseases Biochim. Biophys. Acta-Mol. Basis Dis 1802 2010 122 134
37. A. Ambrus, B. Torocsik, L. Tretter, O. Ozohanics, and V. Adam-Vizi Stimulation of reactive oxygen species generation by disease-causing mutations of lipoamide dehydrogenase Hum. Mol. Genet. 20 2011 2984 2995
38. C. Chinopoulos, L. Tretter, and V. Adam-Vizi Depolarization of In Situ Mitochondria Due to Hydrogen Peroxide-Induced Oxidative Stress in Nerve Terminals J. Neurochem. 73 1999 220 228
39. L. Tretter, and V. Adam-Vizi Inhibition of Krebs cycle enzymes by hydrogen peroxide: A key role of alpha-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress J. Neurosci. 20 2000 8972 8979
40. A.C. Nulton-Persson, and L.I. Szweda Modulation of mitochondrial function by hydrogen peroxide J. Biol. Chem. 276 2001 23357 23361
41. M.J. Kumar, D.G. Nicholls, and J.K. Andersen Oxidative alpha-ketoglutarate dehydrogenase inhibition via subtle elevations in monoamine oxidase B levels results in loss of spare respiratory capacity - Implications for Parkinson's disease J. Biol. Chem. 278 2003 46432 46439
42. A. Ambrus, and V. Adam-Vizi Molecular dynamics study of the structural basis of dysfunction and the modulation of reactive oxygen species generation by pathogenic mutants of human dihydrolipoamide dehydrogenase Arch. Biochem. Biophys. 538 2013 145 155
43. V. Vereczki, E. Martin, R.E. Rosenthal, P.R. Hof, G.E. Hoffman, and G. Fiskum Normoxic resuscitation after cardiac arrest protects against hippocampal oxidative stress, metabolic dysfunction, and neuronal death J. Cereb. Blood Flow Metab. 26 2006 821 835
44. N.D. Contreras, and C.C. Vasquez Tellurite-induced carbonylation of the Escherichia coli pyruvate dehydrogenase multienzyme complex Archives of Microbiology 192 2010 969 973
45. R.A. Vaubel, P. Rustin, and G. Isaya Mutations in the Dimer Interface of Dihydrolipoamide Dehydrogenase Promote Site-specific Oxidative Damages in Yeast and Human Cells J. Biol. Chem. 286 2011 40232 40245
46. N.L. Klyachko, V.A. Shchedrina, A.V. Efimov, S.V. Kazakov, I.G. Gazaryan, B.S. Kristal, and A.M. Brown pH-dependent substrate preference of pig heart lipoamide dehydrogenase varies with oligomeric state - Response to mitochondrial matrix acidification J. Biol. Chem. 280 2005 16106 16114
47. I.G. Gazaryan, B.F. Krasnikov, G.A. Ashby, R.N.F. Thorneley, B.S. Kristal, and A. Brown M.Zinc is a potent inhibitor of thiol oxidoreductase activity and stimulates reactive oxygen species production by lipoamide dehydrogenase J. Biol. Chem. 277 2002 10064 10072
48. Y. Bando, and K. Aki Mechanisms of generation of oxygen radicals and reductive mobilization of ferritin iron by lipoamide dehydrogenase J. Biochem. 109 1991 450 454
49. V. Massey, S. Strickland, S.G. Mayhew, L.G. Howell, P.C. Engel, R.G. Matthews, M. Schuman, and P.A. Sullivan The production of superoxide anion radicals in the reaction of reduced flavins and flavoproteins with molecular oxygen Biochem. Biophys. Res. Commun. 36 1969 891 897
50. A. Ambrus, R. Mizsei, and V. Adam-Vizi Structural alterations by five disease-causing mutations in the low-pH conformation of human dihydrolipoamide dehydrogenase (hLADH) analyzed by molecular dynamics - Implications in functional loss and modulation of reactive oxygen species generation by pathogenic hLADH forms Biochem. Biophys. Reports 2 2015 50 56
51. S.C. Quinonez, S.M. Leber, D.M. Martin, J.G. Thoene, and J.K. Bedoyan Leigh Syndrome in a Girl With a Novel DLD Mutation Causing E3 Deficiency Pediatr. Neurol. 48 2013 67 72
52. R.A.W. Frank, C.W.M. Kay, J. Hirsi, and B.F. Luisi Off-pathway, oxygen-dependent thiamine radical in the Krebs cycle J. Am. Chem. Soc. 130 2008 1662 1668
53. G.H. Reed, S.W. Ragsdale, and S.O. Mansoorabadi Radical reactions of thiamin pyrophosphate in 2-oxoacid oxidoreductases Biochimica Et Biophysica Acta-Proteins and Proteomics 1824 2012 1291 1298
54. L.J. Reed, and R.M. Oliver The multienzyme alpha-keto acid dehydrogenase complexes Brookhaven Symp. Biol. 21 1968 397 412
55. J.D. Erfle, and F. Sauer The inhibitory effects of acyl-coenzyme A esters on the pyruvate and a-oxoglutarate dehydrogenase complexes Biochim. Biophys. Acta 178 1969 441 452
56. L.L. Poulsen, and R.T. Wedding Purification and properties of the a-ketoglutarate dehydrogenase complex of cauliflower mitochondria J. Biol. Chem. 245 1970 5709 5717
57. A. Constantinescu, U. Pick, G.J. Handelman, N. Haramaki, D. Han, M. Podda, H.J. Tritschler, and L. Packer Reduction and transport of lipoic acid by human erythrocytes Biochem. Pharmacol. 50 1995 253 261
58. L.J. Yan, N. Thangthaeng, N. Sumien, and M.J. Forster Serum Dihydrolipoamide Dehydrogenase Is a Labile Enzyme J Biochem Pharmacol Res 1 2013 30 42
59. C. Mottley, and R.P. Mason Sulfur-centered radical formation from the antioxidant dihydrolipoic acid J. Biol. Chem. 276 2001 42677 42683
60. N. Nemeria, A. Volkov, A. Brown, J. Yi, L. Zipper, J.R. Guest, and F. Jordan Systematic study of the six cysteines of the E1 subunit of the pyruvate dehydrogenase multienzyme complex from Escherichia coli: None is essential for activity Biochemistry 37 1998 911 922
61. J. Song, Y.H. Park, N. Nemeria, S. Kale, L. Kakalis, and F. Jordan Nuclear magnetic resonance evidence for the role of the flexible regions of the E1 component of the pyruvate dehydrogenase complex from gram-negative bacteria J. Biol. Chem. 285 2010 4680 4694
62. W. Wei, H. Li, N. Nemeria, and F. Jordan Expression and purification of the dihydrolipoamide acetyltransferase and dihydrolipoamide dehydrogenase subunits of the Escherichia coli pyruvate dehydrogenase multienzyme complex: a mass spectrometric assay for reductive acetylation of dihydrolipoamide acetyltransferase Protein Expr. Purif. 28 2003 140 150
63. D.J. Shim, N.S. Nemeria, A. Balakrishnan, H. Patel, J. Song, J.J. Wang, F. Jordan, and E.T. Farinas Assignment of Function to Histidines 260 and 298 by Engineering the E1 Component of the Escherichia coli 2-Oxoglutarate Dehydrogenase Complex; Substitutions That Lead to Acceptance of Substrates Lacking the 5-Carboxyl Group Biochemistry 50 2011 7705 7709
64. L.G. Korotchkina, M.M. Tucker, T.J. Thekkumkara, K.T. Madhusudhan, G. Pons, H.J. Kim, and M.S. Patel Overexpression and characterization of human tetrameric pyruvate dehydrogenase and its individual subunits Protein Expr. Purif. 6 1995 79 90
65. L.G. Korotchkina, and M.S. Patel Probing the mechanism of inactivation of human pyruvate dehydrogenase by phosphorylation of three sites J. Biol. Chem. 276 2001 5731 5738
66. D.Q. Yang, J.S. Song, T. Wagenknecht, and T.E. Roche Assembly and full functionality of recombinantly expressed dihydrolipoyl acetyltransferase component of the human pyruvate dehydrogenase complex J. Biol. Chem. 272 1997 6361 6369
67. R.A. Harris, M.M. BowkerKinley, P.F. Wu, J.J. Jeng, and K.M. Popov Dihydrolipoamide dehydrogenase-binding protein of the human pyruvate dehydrogenase complex - DNA-derived amino acid sequence, expression, and reconstitution of the pyruvate dehydrogenase complex J. Biol. Chem. 272 1997 19746 19751
68. A. Ambrus, B. Torocsik, and V. Adam-Vizi Periplasmic cold expression and one-step purification of human dihydrolipoamide dehydrogenase Protein Expr. Purif. 63 2009 50 57
69. A. Balakrishnan, N.S. Nemeria, S. Chakraborty, L. Kakalis, and F. Jordan Determination of pre-steady-state constants on the Escherichia coli pyruvate dehydrogenase complex reveals that loop movement controls the rate-limiting step J. Am. Chem. Soc. 134 2012 18644 18655
70. J.Z. Yi, N. Nemeria, A. McNally, F. Jordan, R.S. Machado, and J.R. Guest Effect of substitutions in the thiamin diphosphate-magnesium fold on the activation of the pyruvate dehydrogenase complex from Escherichia coli by cofactors and substrate J. Biol. Chem. 271 1996 33192 33200
71. H. Saumweber, R. Binder, and H. Bisswanger Pyruvate dehydrogenase component of the pyruvate dehydrogenase complex from Escherichia coli K-12 - purification and characterization Eur. J. Biochem. 114 1981 407 411
72. N. Nemeria, Y. Yan, Z. Zhang, A.M. Brown, P. Arjunan, W. Furey, J.R. Guest, and F. Jordan Inhibition of the Escherichia coli pyruvate dehydrogenase complex E1 subunit and its tyrosine 177 variants by thiamin 2-thiazolone and thiamin 2-thiothiazolone diphosphates - Evidence for reversible tight-binding inhibition J. Biol. Chem. 276 2001 45969 45978
73. S.C. Gupta, and E.E. Dekker Evidence for the identity and some comparative properties of alpha-ketoglutarate and 2-keto-4-hydroxyglutarate dehydrogenase activity J. Biol. Chem. 255 1980 1107 1112
74. M. Hirashima, T. Hayakawa, and M. Koike Mammalian alpha-keto acid dehydrogenase complexes. II. An improved procedure for the preparation of 2-oxoglutarate dehydrogenase complex from pig heart muscle J. Biol. Chem. 242 1967 902 907
75. M. Hamada, K. Koike, Y. Nakaula, T. Hiraoka, and M. Koike A kinetic study of the alpha-keto acid dehydrogenase complexes from pig heart mitochondria J. Biochem. 77 1975 1047 1056
76. R.G. Hansford Control of mitochondrial substrate oxidation Curr. Top. Bioenerg 10 1980 217 278
77. Y.V. Kiselevsky, S.A. Ostrovtsova, and S.A. Strumilo Kinetic characterization of the pyruvate and oxoglutarate dehydrogenase complexes from human heart Acta Biochim Pol 37 1990 135 139
78. F. Seifert, R. Golbik, J. Brauer, H. Lilie, K. Schroder-Tittmann, E. Hinze, L.G. Korotchkina, M.S. Patel, and K. Tittmann Direct kinetic evidence for half-of-the-sites reactivity in the E1 component of the human pyruvate dehydrogenase multienzyme complex through alternating sites cofactor activation Biochemistry 45 2006 12775 12785
79. V.O. Popov, I.G. Gazaryan, A.M. Egorov, and I.V. Berezin NAD-dependent hydrogenase from the hydrogen-oxidizing bacterium Alcaligenes Eutrophus Z1 - kinetic studies of the NADH-dehydrogenase activity Biochim. Biophys. Acta 827 1985 466 471
80. L.A. Mayo, and J.T. Curnutte KInetic microplate assay for superoxide production by neutrophils and other phagocytic cells Method Enzymol 186 1990 567 575
81. A. Azzi, C. Montecucco, and C. Richter Use of acetylated ferricytochrome c for detection of superoxide radicals produced in biological membranes Biochem. Biophys. Res. Commun. 65 1975 597 603
82. J.M. McCord, and I. Fridovich The reduction of cytochrome c by milk xantine oxidase J. Biol. Chem. 243 1968 5753 5760
83. G.M. Rosen, E. Finkelstein, and E.J. Rauckman A method for the detection of superoxide in biological systems Arch. Biochem. Biophys. 215 1982 367 378
84. J.M. Cameron, V. Levandovskiy, N. MacKay, J. Raiman, D.L. Renaud, J.T.R. Clarke, A. Feigenbaum, O. Elpeleg, and B.H. Robinson Novel mutations in dihydrolipoamide dehydrogenase deficiency in two cousins with borderline-normal PDH complex activity Am. J. Med. Genet. A 140A 2006 1542 1552
85. C.A. Brautigam, J.L. Chuang, D.R. Tomchick, M. Machius, and D.T. Chuang Crystal structure of human dihydrolipoamide dehydrogenase: NAD(+)/NADH binding and the structural basis of disease-causing mutations J. Mol. Biol. 350 2005 543 552
86. V. Massey Activation of molecular oxygen by flavins and flavoproteins J. Biol. Chem. 269 1994 22459 22462
87. L. Tretter, and A. Ambrus Measurement of ROS homeostasis in isolated mitochondria Methods Enzymol 547 2014 199 223
88. V.I. Bunik, and C. Sievers Inactivation of the 2-oxo acid dehydrogenase complexes upon generation of intrinsic radical species Eur. J. Biochem. 269 2002 5004 5015
89. Starkov, A.A. The Role of Mitochondria in Reactive Oxygen Species Metabolism and Signaling. In: Gibson, G. E.; Ratan, R. R.; Beal, M. F., eds. Mitochondria and Oxidative Stress in Neurodegenerative Disorders; 2008: 37-52.
90. W. Droge, and H.M. Schipper Oxidative stress and aberrant signaling in aging and cognitive decline Aging Cell 6 2007 361 370
91. L. Tretter, I. Sipos, and V. Adam-Vizi Initiation of neuronal damage by complex I deficiency and oxidative stress in Parkinson's disease Neurochem. Res. 29 2004 569 577
92. G.E. Gibson, A.E. Kingsbury, H. Xu, J.G. Lindsay, S. Daniel, O.J.F. Foster, A.J. Lees, and J.P. Blass Deficits in a tricarboxylic acid cycle enzyme in brains from patients with Parkinson's disease Neurochem. Int. 43 2003 129 135
93. Brookes, P.S., ed.Mitochondrial production of oxidants and their role in the regulation of cellular processes. 2007.
94. D. Martinvalet, P.C. Zhu, and J. Lieberman Granzyme A induces caspase-independent mitochondrial damage, a required first step for apoptosis Immunity 22 2005 355 370
95. C. Chinopoulos, and V. Adam-Vizi Calcium, mitochondria and oxidative stress in neuronal pathology - Novel aspects of an enduring theme Febs J. 273 2006 433 450
96. J.C.K. Lai, J.M. Walsh, S.C. Dennis, and J.B. Clark Synaptic and non-synaptic mitochondria from rat brain isolation and characterization J. Neurochem. 28 1977 625 631
97. J.P. Blass Metabolic alterations common to neural and non-neural cells in Alzheimer's disease Hippocampus 13 1993 45 54
98. H.L. Willems, T.F. de Kort, F.J. Trijbels, L.A. Monnens, and J.H. Veerkamp Determination of pyruvate oxidation rate and citric acid cycle activity in intact human leukocytes and fibroblasts Clinical Chemistry 24 1978 200 203
99. 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
100. H.R. McLennan, and M. Degli Esposti The contribution of mitochondrial respiratory complexes to the production of reactive oxygen species J Bioenerg Biomembr 32 2000 153 162
101. I. Siebels, and S. Drose Q-site inhibitor induced ROS production of mitochondrial complex II is attenuated by TCA cycle dicarboxylates Biochim Biophys Acta 1827 2013 1156 1164
102. G. Lakaschus, and M. Loffler Differential susceptibility of dihydroorotate dehydrogenase/oxidase to Brequinar Sodium (NSC 368 390) in vitro Biochem Pharmacol 43 1992 1025 1030
103. A.Y. Andreyev, Y.E. Kushnareva, A.N. Murphy, A.A. Starkov, and R.O.S. Mitochondrial metabolism: 10 Years later Biochemistry-Moscow 80 2015 517 531
104. L. Tretter, and V. Adam-Vizi Moderate dependence of ROS formation on Delta psi m in isolated brain mitochondria supported by NADH-linked substrates Neurochem. Res. 32 2007 569 575
105. L. Tretter, and V. Adam-Vizi Uncoupling is without an effect on the production of reactive oxygen species by in situ synaptic mitochondria J. Neurochem. 103 2007 1864 1871
106. L. Tretter, and V. Adam-Vizi High Ca2+ load promotes Hydrogen peroxide generation via activation of alpha-glycerophosphate dehydrogenase in brain mitochondria Free Radic. Biol. Med. 53 2012 2119 2130
107. L. Tretter, B. Liktor, and V. Adam-Vizi Dual effect of pyruvate in isolated nerve terminals: Generation of reactive oxygen species and protection of aconitase Neurochem. Res. 30 2005 1331 1338
108. L. Tretter, D. Mayer-Takacs, and V. Adam-Vizi The effect of bovine serum albumin on the membrane potential and reactive oxygen species generation in succinate-supported isolated brain mitochondria Neurochem. Int. 50 2007 139 147
109. L. Tretter, K. Takacs, V. Hegedus, and V. Adam-Vizi Characteristics of alpha-glycerophosphate-evoked H2O2 generation in brain mitochondria J. Neurochem. 100 2007 650 663
110. L. Tretter, K. Takacs, K. Kover, and V. Adam-Vizi Stimulation of H2O2 generation by calcium in brain mitochondria respiring on alpha-glycerophosphate J. Neurosci. Res. 85 2007 3471 3479
111. Q.L. Shi, H.L. Chen, H. Xu, and G.E. Gibson Reduction in the E2k subunit of the alpha-ketoglutarate dehydrogenase complex has effects independent of complex activity J. Biol. Chem. 280 2005 10888 10896
112. G.E. Gibson, H. Zhang, K.F.R. Sheu, N. Bogdanovich, J.G. Lindsay, L. Lannfelt, M. Vestling, and R. Cowburn F. alpha-ketoglutarate dehydrogenase in Alzheimer brains bearing the APP670/671 mutation Ann. Neurol. 44 1998 676 681
113. M. Cruts, H. Backhovens, G. Vangassen, J. Theuns, S.Y. Wang, A. Wehnert, C.M. Vanduijn, T. Karlsson, A. Hofman, R. Adolfsson, J.J. Martin, and C. Vanbroeckhoven Mutation analysis of the chromosome 14q24.3 dihydrolipoyl succinyltransferase (dlst) gene in patients with early-onset Alzheimer-disease Neuroscience Letters 199 1995 73 77
114. M. Dumont, D.J. Ho, N.Y. Calingasan, H. Xu, G. Gibson, and M.F. Beal Mitochondrial dihydrolipoyl succinyltransferase deficiency accelerates amyloid pathology and memory deficit in a transgenic mouse model of amyloid deposition Free Radic. Biol. Med. 47 2009 1019 1027
115. M.D. Diaz-Munoz, S.E. Bell, K. Fairfax, E. Monzon-Casanova, A.F. Cunningham, M. Gonzalez-Porta, S.R. Andrews, V.I. Bunik, K. Zarnack, T. Curk, W.A. Heggermont, S. Heymans, G.E. Gibson, D.L. Kontoyiannis, J. Ule, and M. Turner The RNA-binding protein HuR is essential for the B cell antibody response Nature Immunology 16 2015 415 425
116. A. Shaag, A. Saada, I. Berger, H. Mandel, A. Joseph, A. Feigenbaum, and O.N. Elpeleg Molecular basis of lipoamide dehydrogenase deficiency in Ashkenazi Jews Am. J. Med. Genet. 82 1999 177 182
117. Y.S. Hong, S.H. Korman, J. Lee, P. Ghoshal, Q. Qu, V. Barash, S. Kang, S. Oh, M. Kwon, A. Gutman, A. Rachmel, and M.S. Patel Identification of a common mutation (Gly194Cys) in both Arab Moslem and Ashkenazi Jewish patients with dihydrolipoamide dehydrogenase (E3) deficiency: Possible beneficial effect of vitamin therapy J. Inherit. Metab. Dis. 26 2003 816 818
118. E. Shany, A. Saada, D. Landau, A. Shaag, E. Hershkovitz, and O.N. Elpeleg Lipoamide dehydrogenase deficiency due to a novel mutation in the interface domain Biochem. Biophys. Res. Commun. 262 1999 163 166
119. C.A. Brautigam, R.M. Wynn, J.L. Chuang, M. Machius, D.R. Tomchick, and D.T. Chuang Structural insight into interactions between dihydrolipoamide dehydrogenase (E3) and E3 binding protein of human pyruvate dehydrogenase complex Structure 14 2006 611 621