Differential susceptibility of mitochondrial complex II to inhibition by oxaloacetate in brain and heart

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1857, Issue 9, 2016, Pages 1561-1568

  Stepanova, Anna ^a,b   Shurubor, Yevgeniya ^c   Valsecchi, Federica ^c   Manfredi, Giovanni ^c   Galkin, Alexander ^a,c  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b KOL TSOV INSTITUTE OF DEVELOPMENTAL BIOLOGY   (Russian Federation)

^c FEIL FAMILY BRAIN AND MIND RESEARCH INSTITUTE   (United States)

Author keywords

Ischemia; Krebs cycle; Mitochondrial complex II; Oxaloacetate; Succinate dehydrogenase

Indexed keywords

ASPARTATE AMINOTRANSFERASE ISOENZYME 1; CYTOCHROME C OXIDASE; MALONIC ACID; OXALOACETIC ACID; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN MITOCHONDRION; CELL ISOLATION; CITRIC ACID CYCLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HEART MITOCHONDRION; HEART MUSCLE ISCHEMIA; MALE; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSAMINATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; CARDIAC MUSCLE; ENZYMOLOGY; METABOLISM; MITOCHONDRION;

ANIMALS; BRAIN; ELECTRON TRANSPORT COMPLEX II; MICE; MITOCHONDRIA; MYOCARDIUM; OXALOACETIC ACID; SUCCINATE DEHYDROGENASE;

EID: 84975474583     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2016.06.002     Document Type: Article

References (69)

1. F. Sun, X. Huo, Y. Zhai, A. Wang, J. Xu, D. Su, M. Bartlam, and Z. Rao Crystal structure of mitochondrial respiratory membrane protein complex II Cell 121 2005 1043 1057
2. C. Hagerhall Succinate: quinone oxidoreductases - variations on a conserved theme Biochim. Biophys. Acta 1320 1997 107 141
3. P. Bernath, E.B. Kearney, and T.P. Singer Studies on succinic dehydrogenase. II. Isolation and properties of the dehydrogenase from beef heart J. Biol. Chem. 223 1956 599 613
4. E.B. Kearney, B.A. Ackrell, and M. Mayr Tightly bound oxalacetate and the activation of succinate dehydrogenase Biochem. Biophys. Res. Commun. 49 1972 1115 1121
5. A. Priegnitz, O.N. Brzhevskaya, and L. Wojtczak Tight binding of oxaloacetate to succinate dehydrogenase Biochem. Biophys. Res. Commun. 51 1973 1034 1041
6. B.A. Ackrell, E.B. Kearney, and M. Mayr Role of oxalacetate in the regulation of mammalian succinate dehydrogenase J. Biol. Chem. 249 1974 2021 2027
7. A.B. Kotlyar, and A.D. Vinogradov Interaction of the membrane-bound succinate dehydrogenase with substrate and competitive inhibitors Biochim. Biophys. Acta 784 1984 24 34
8. E. Maklashina, A.B. Kotlyar, J.S. Karliner, and G. Cecchini Effect of oxygen on activation state of complex I and lack of oxaloacetate inhibition of complex II in Langendorff perfused rat heart FEBS Lett. 556 2004 64 68
9. M. Gutman, E.B. Kearney, and T.P. Singer Control of succinate dehydrogenase in mitochondria Biochemistry 10 1971 4763 4770
10. A.D. Vinogradov, D. Winter, and T.E. King The binding site for oxaloacetate on succinate dehydrogenase Biochem. Biophys. Res. Commun. 49 1972 441 444
11. 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
12. L.W. Finley, W. Haas, V. squiret-Dumas, D.C. Wallace, V. Procaccio, S.P. Gygi, and M.C. Haigis Succinate dehydrogenase is a direct target of sirtuin 3 deacetylase activity PLoS One 6 2011 e23295
13. H. Cimen, M.J. Han, Y. Yang, Q. Tong, H. Koc, and E.C. Koc Regulation of succinate dehydrogenase activity by SIRT3 in mammalian mitochondria Biochemistry 49 2010 304 311
14. K.S. Hewitson, B.M. Lienard, M.A. McDonough, I.J. Clifton, D. Butler, A.S. Soares, N.J. Oldham, L.A. McNeill, and C.J. Schofield Structural and mechanistic studies on the inhibition of the hypoxia-inducible transcription factor hydroxylases by tricarboxylic acid cycle intermediates J. Biol. Chem. 282 2007 3293 3301
15. L.F. Dong, P. Low, J.C. Dyason, X.F. Wang, L. Prochazka, P.K. Witting, R. Freeman, E. Swettenham, K. Valis, J. Liu, R. Zobalova, J. Turanek, D.R. Spitz, F.E. Domann, I.E. Scheffler, S.J. Ralph, and J. Neuzil Alpha-tocopheryl succinate induces apoptosis by targeting ubiquinone-binding sites in mitochondrial respiratory complex II Oncogene 27 2008 4324 4335
16. T. Albayrak, V. Scherhammer, N. Schoenfeld, E. Braziulis, T. Mund, M.K.A. Bauer, I.E. Scheffler, and S. Grimm The tumor suppressor cybL, a component of the respiratory chain, mediates apoptosis induction Mol. Biol. Cell 14 2003 3082 3096
17. J. Favier, L. Amar, and A.P. Gimenez-Roqueplo Paraganglioma and phaeochromocytoma: from genetics to personalized medicine Nat. Rev. Endocrinol. 11 2015 101 111
18. M.A. Selak, S.M. Armour, E.D. MacKenzie, H. Boulahbel, D.G. Watson, K.D. Mansfield, Y. Pan, M.C. Simon, C.B. Thompson, and E. Gottlieb Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase Cancer Cell 7 2005 77 85
19. A. King, M.A. Selak, and E. Gottlieb Succinate dehydrogenase and fumarate hydratase: linking mitochondrial dysfunction and cancer Oncogene 25 2006 4675 4682
20. E. Mills, and L.A. O'Neill Succinate: a metabolic signal in inflammation Trends Cell Biol. 24 2014 313 320
21. S.E. Browne, A.C. Bowling, U. MacGarvey, M.J. Baik, S.C. Berger, M.M. Muqit, E.D. Bird, and M.F. Beal Oxidative damage and metabolic dysfunction in Huntington's disease: selective vulnerability of the basal ganglia Ann. Neurol. 41 1997 646 653
22. E.T. Chouchani, V.R. Pell, E. Gaude, D. Aksentijevic, S.Y. Sundier, E.L. Robb, A. Logan, S.M. Nadtochiy, E.N. Ord, A.C. Smith, F. Eyassu, R. Shirley, C.H. Hu, A.J. Dare, A.M. James, S. Rogatti, R.C. Hartley, S. Eaton, A.S. Costa, P.S. Brookes, S.M. Davidson, M.R. Duchen, K. Saeb-Parsy, M.J. Shattock, A.J. Robinson, L.M. Work, C. Frezza, T. Krieg, and M.P. Murphy Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS Nature 515 2014 431 435
23. R.F. Villa, A. Gorini, and S. Hoyer Effect of ageing and ischemia on enzymatic activities linked to Krebs' cycle, electron transfer chain, glutamate and aminoacids metabolism of free and intrasynaptic mitochondria of cerebral cortex Neurochem. Res. 34 2009 2102 2116
24. A.M. Walters, G.A. Porter Jr., and P.S. Brookes Mitochondria as a drug target in ischemic heart disease and cardiomyopathy Circ. Res. 111 2012 1222 1236
25. M. Lu, L. Zhou, W.C. Stanley, M.E. Cabrera, G.M. Saidel, and X. Yu Role of the malate-aspartate shuttle on the metabolic response to myocardial ischemia J. Theor. Biol. 254 2008 466 475
26. O. Pisarenko, I. Studneva, V. Khlopkov, E. Solomatina, and E. Ruuge An assessment of anaerobic metabolism during ischemia and reperfusion in isolated Guinea pig heart Biochim. Biophys. Acta 934 1988 55 63
27. K.J. Peuhkurinen, T.E. Takala, E.M. Nuutinen, and I.E. Hassinen Tricarboxylic acid cycle metabolites during ischemia in isolated perfused rat heart Am. J. Phys. 244 1983 H281 H288
28. N. Gorenkova, E. Robinson, D. Grieve, and A. Galkin Conformational change of mitochondrial complex I increases ROS sensitivity during ischaemia Antioxid. Redox Signal. 19 2013 1459 1468
29. V.D. Sled, and A.D. Vinogradov Kinetics of the mitochondrial NADH-ubiquinone oxidoreductase interaction with hexaammineruthenium(III) Biochim. Biophys. Acta 1141 1993 262 268
30. A.B. Kotlyar, and A.D. Vinogradov Slow active/inactive transition of the mitochondrial NADH-ubiquinone reductase Biochim. Biophys. Acta 1019 1990 151 158
31. M. Babot, A. Birch, P. Labarbuta, and A. Galkin Characterisation of the active/de-active transition of mitochondrial complex I Biochim. Biophys. Acta 1837 2014 1083 1092
32. 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
33. E. Estornell, R. Fato, F. Pallotti, and G. Lenaz Assay conditions for the mitochondrial NADH:coenzyme Q oxidoreductase FEBS Lett. 332 1993 127 131
34. B.A. Ackrell, E.B. Kearney, and T.P. Singer Mammalian succinate dehydrogenase Methods Enzymol. 53 1978 466 483
35. S.S. Tate, A.K. Grzybowski, and S.P. Datta 265. The acid dissociations of the keto and enol isomers of oxaloacetic acid at 25[degree] J. Chem. Soc. Resumed 1964 1372 1380
36. V. Rhein, X. Song, A. Wiesner, L.M. Ittner, G. Baysang, F. Meier, L. Ozmen, H. Bluethmann, S. Drose, U. Brandt, E. Savaskan, C. Czech, J. Gotz, and A. Eckert Amyloid-beta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's disease mice Proc. Natl. Acad. Sci. U. S. A. 106 2009 20057 20062
37. 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
38. M. Gutman The effect of opposing effectors on activation level of succinate dehydrogenase: equilibrium and kinetic studies Biochemistry 15 1976 1342 1348
39. E. Tomitsuka, H. Hirawake, Y. Goto, M. Taniwaki, S. Harada, and K. Kita Direct evidence for two distinct forms of the flavoprotein subunit of human mitochondrial complex II (succinate-ubiquinone reductase) J. Biochem. 134 2003 191 195
40. C. Sakai, E. Tomitsuka, M. Miyagishi, S. Harada, and K. Kita Type II Fp of human mitochondrial respiratory complex II and its role in adaptation to hypoxia and nutrition-deprived conditions Mitochondrion 13 2013 602 609
41. N. Satoh, C. Yokoyama, N. Itamura, Y. Miyajima-Nakano, and H. Hisatomi Alternative splicing isoform in succinate dehydrogenase complex, subunit C causes downregulation of succinate-coenzyme Q oxidoreductase activity in mitochondria Oncol. Lett. 9 2015 330 334
42. M. Gutman Modulation of mitochondrial succinate dehydrogenase activity, mechanism and function Mol. Cell. Biochem. 20 1978 41 60
43. L.S. Kappen, J.D. Brodie, and P. Nicholls Fast and slow inhibitors of Ox heart succinate dehydrogenase: action of oxaloacetate and its fluoro analogues Biochem. Soc. Trans. 1 1973 877 880
44. C.E. Frohman, J.M. Orten, and A.H. Smith Chromatographic determination of the acids of the citric acid cycle in tissues J. Biol. Chem. 193 1951 277 283
45. J. Folbergrova, B. Ljunggren, K. Norberg, and B.K. Siesjo Influence of complete ischemia on glycolytic metabolites, citric acid cycle intermediates, and associated amino acids in the rat cerebral cortex Brain Res. 80 1974 265 279
46. H. Taegtmeyer Metabolic responses to cardiac hypoxia. Increased production of succinate by rabbit papillary muscles Circ. Res. 43 1978 808 815
47. S. Hoyer, and C. Krier Ischemia and aging brain. Studies on glucose and energy metabolism in rat cerebral cortex Neurobiol. Aging 7 1986 23 29
48. O.I. Pisarenko, E.S. Solomatina, and I.M. Studneva The role of amino acid catabolism in the formation of the tricarboxylic acid cycle intermediates and ammonia in anoxic rat heart Biochim. Biophys. Acta 885 1986 154 161
49. A.I. Amaral, T.W. Meisingset, M.R. Kotter, and U. Sonnewald Metabolic aspects of neuron-oligodendrocyte-astrocyte interactions Front. Endocrinol. (Lausanne) 4 2013 54
50. D.R. Sanadi, and A.L. Fluharty On the mechanism of oxidative phosphorylation. VII. The energy-requiring reduction of pyridine nucleotide by succinate and the energy-yielding oxidation of reduced pyridine nucleotide by fumarate Biochemistry 2 1963 523 528
51. M.A. Wilson, and J. Cascarano The energy-yielding oxidation of NADH by fumarate in submitochondrial particles of rat tissues Biochim. Biophys. Acta 216 1970 54 62
52. L. Hardy, J.B. Clark, V.M. Darley-Usmar, D.R. Smith, and D. Stone Reoxygenation-dependent decrease in mitochondrial NADH:CoQ reductase (complex I) activity in the hypoxic/reoxygenated rat heart Biochem. J. 274 Pt 1 1991 133 137
53. A.J. Tompkins, L.S. Burwell, S.B. Digerness, C. Zaragoza, W.L. Holman, and P.S. Brookes Mitochondrial dysfunction in cardiac ischemia-reperfusion injury: ROS from complex I, without inhibition Biochim. Biophys. Acta 1762 2006 223 231
54. A.P. Wojtovich, and P.S. Brookes The endogenous mitochondrial complex II inhibitor malonate regulates mitochondrial ATP-sensitive potassium channels: implications for ischemic preconditioning Biochim. Biophys. Acta 1777 2008 882 889
55. E.T. Chouchani, C. Methner, S.M. Nadtochiy, A. Logan, V.R. Pell, S. 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. 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
56. C. Armstrong, and J.F. Staples The role of succinate dehydrogenase and oxaloacetate in metabolic suppression during hibernation and arousal J. Comp. Physiol. B. 180 2010 775 783
57. T. Bourgeron, P. Rustin, D. Chretien, M. Birch-Machin, M. Bourgeois, E. Viegas-Pequignot, A. Munnich, and A. Rotig Mutation of a nuclear succinate dehydrogenase gene results in mitochondrial respiratory chain deficiency Nat. Genet. 11 1995 144 149
58. W.P. Zeylemaker, A.D. Klaasse, and E.C. Slater Studies on succinate dehydrogenase. V. Inhibition by oxaloacetate Biochim. Biophys. Acta 191 1969 229 238
59. L. Wojtczak, A.B. Wojtczak, and L. Ernster The inhibition of succinate dehydrogenase by oxaloacetate Biochim. Biophys. Acta 191 1969 10 21
60. A.D. Vinogradov Catalytic properties of the mitochondrial NADH-ubiquinone oxidoreductase (complex I) and the pseudo-reversible active/inactive enzyme transition Biochim. Biophys. Acta 1364 1998 169 185
61. D.M. Ferber, B. Moy, and R.J. Maier Bradyrhizobium japonicum hydrogen-ubiquinone oxidoreductase activity: quinone specificity, inhibition by quinone analogs, and evidence for separate sites of electron acceptor reactivity Biochim. Biophys. Acta 1229 1995 334 346
62. J.T. Jarrett, S. Huang, and R.G. Matthews Methionine synthase exists in two distinct conformations that differ in reactivity toward methyltetrahydrofolate, adenosylmethionine, and flavodoxin Biochemistry 37 1998 5372 5382
63. V. Massey, B. Curti, and H. Ganther A temperature-dependent conformational change in D-amino acid oxidase and its effect on catalysis J. Biol. Chem. 241 1966 2347 2357
64. E. Cadenas, and A. Boveris Enhancement of hydrogen peroxide formation by protophores and ionophores in antimycin-supplemented mitochondria Biochem. J. 188 1980 31 37
65. S. Drose, 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
66. 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
67. M.D. Moser, S. Matsuzaki, and K.M. Humphries Inhibition of succinate-linked respiration and complex II activity by hydrogen peroxide Arch. Biochem. Biophys. 488 2009 69 75
68. C. Eng, M. Kiuru, M.J. Fernandez, and L.A. Aaltonen A role for mitochondrial enzymes in inherited neoplasia and beyond Nat. Rev. Cancer 3 2003 193 202
69. M. Degli Esposti Assessing functional integrity of mitochondria in vitro and in vivo Methods Cell Biol. 65 2001 75 96