Q-site inhibitor induced ROS production of mitochondrial complex II is attenuated by TCA cycle dicarboxylates

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1827, Issue 10, 2013, Pages 1156-1164

  Siebels, Ilka ^a   Dröse, Stefan ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

Atpenin A5; Complex II; Dicarboxylates; Mitochondria; Reactive oxygen species (ROS); Succinate:ubiquinone oxidoreductase

Indexed keywords

ALPHA TOCOPHEROL SUCCINATE; ATPENIN B; DICARBOXYLIC ACID; HYDROGEN PEROXIDE; OXYGEN RADICAL; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); SUCCINIC ACID; SUPEROXIDE;

ARTICLE; BINDING SITE; CITRIC ACID CYCLE; COW; ENZYME ACTIVITY; HEART MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION REACTION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RESPIRATORY CHAIN; SUBMITOCHONDRIAL PARTICLE;

BOVINAE; MAMMALIA;

EID: 84884593391     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2013.06.005     Document Type: Article

References (62)

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, 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. 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, C.C. Winterbourn, Unraveling the biological roles of reactive oxygen species, Cell Metab. 13 (2011) 361-366.
5. T. Finkel, Signal transduction by mitochondrial oxidants, J. Biol. Chem. 287 (2012) 4434-4440.
6. S. Dröse, U. Brandt, Molecular mechanisms of superoxide production by the mitochondrial respiratory chain, Adv. Exp. Med. Biol. 748 (2012) 145-169.
7. 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.
8. T.V. Votyakova, I.J. Reynolds, Δm-Dependent and -independent production of reactive oxygen species by rat brain mitochondria, J. Neurochem. 79 (2001) 266-277. (Pubitemid 32988942)
9. Y. Liu, G. Fiskum, D. Schubert, Generation of reactive oxygen species by the mitochondrial electron transport chain, J. Neurochem. 80 (2002) 780-787. (Pubitemid 34809230)
10. A.J. Lambert, 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)
11. F. Zoccarato, L. Cavallini, S. Bortolami, A. Alexandre, Succinate modulation of H2O2 release at NADH:ubiquinone oxidoreductase (complex I) in brain mitochondria, Biochem. J. 406 (2007) 125-129. (Pubitemid 47264742)
12. F.L. Muller, Y.H. Liu, M.A. Abdul-Ghani, M.S. Lustgarten, A. Bhattacharya, Y.C. Jang, 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)
13. S. Dröse, P.J. Hanley, U. Brandt, Ambivalent effects of diazoxide on mitochondrial ROS production at respiratory chain complexes I and III, Biochim. Biophys. Acta 1790 (2009) 558-565.
14. S. Dröse, L. Bleier, 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.
15. S. Dröse, U. Brandt, The mechanism of mitochondrial superoxide production by the cytochrome bc1 complex, J. Biol. Chem. 283 (2008) 21649-21654.
16. L. Bleier, S.Dröse, Superoxide generation by complex III: frommechanistic rationales to functional consequences, Biochim. Biophys. Acta (2013), http://dx.doi.org/ 10.1016/j.bbabio.2012.12.002.
17. J. St Pierre, J.A. Buckingham, S.J. Roebuck, 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)
18. Q. Chen, E.J. Vazquez, S. Moghaddas, C.L. Hoppel, E.J. Lesnefsky, Production of reactive oxygen species by mitochondria: central role of complex III, J. Biol. Chem. 278 (2003) 36027-36031. (Pubitemid 37139922)
19. T.M. Iverson, E. Maklashina, G. Cecchini, Structural basis for malfunction in complex II, J. Biol. Chem. 287 (2012) 35430-35438.
20. T. Ishii, M. Miyazawa, H. Onouchi, K. Yasuda, P.S. Hartman, N. Ishii, Model animals for the study of oxidative stress from complex II, Biochim. Biophys. Acta 1827 (2013) 588-597.
21. A.S. Hoekstra, J.P. Bayley, The role of complex II in disease, Biochim. Biophys. Acta 1827 (2013) 543-551.
22. C. Bardella, P.J. Pollard, I. Tomlinson, SDH mutations in cancer, Biochim. Biophys. Acta 1807 (2011) 1432-1443.
23. B.E. Baysal, Mitochondrial complex II and genomic imprinting in inheritance of paraganglioma tumors, Biochim. Biophys. Acta 1827 (2013) 573-577.
24. S.J. Ralph, R. Moreno-Sanchez, J. Neuzil, S. Rodriguez-Enriquez, Inhibitors of succinate:quinone reductase/complex II regulate production of mitochondrial reactive oxygen species and protect normal cells from ischemic damage but induce specific cancer cell death, Pharm. Res. 28 (2011) 2695-2730.
25. K. Kluckova, A. Bezawork-Geleta, J. Rohlena, L. Dong, J. Neuzil, Mitochondrial complex II, a novel target for anti-cancer agents, Biochim. Biophys. Acta 1827 (2013) 552-564.
26. G. Cecchini, Function and structure of complex II of the respiratory chain, Annu. Rev. Biochem. 72 (2003) 77-109. (Pubitemid 36930442)
27. T.M. Iverson, Catalytic mechanisms of complex II enzymes: a structural perspective, Biochim. Biophys. Acta 1827 (2013) 648-657.
28. J.A. Imlay, A metabolic enzyme that rapidly produces superoxide, fumarate reductase of Escherichia coli, J. Biol. Chem. 270 (1995) 19767-19777.
29. K.R. Messner, J.A. Imlay, Mechanism of superoxide and hydrogen peroxide formation by fumarate reductase, succinate dehydrogenase, and aspartate oxidase, J. Biol. Chem. 277 (2002) 42563-42571.
30. C.L. Quinlan, A.L. Orr, I.V. Perevoshchikova, J.R. Treberg, B.A. Ackrell, 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.
31. S. Dröse, U. Brandt, P.J. Hanley, K+-independent actions of diazoxide question the role of inner membrane KATP channels in mitochondrial cytoprotective signaling, J. Biol. Chem. 281 (2006) 23733-23739. (Pubitemid 44274148)
32. T.V. Votyakova, I.J. Reynolds, Detection of hydrogen peroxide with Amplex Red: interference by NADH and reduced glutathione auto-oxidation, Arch. Biochem. Biophys. 431 (2004) 138-144. (Pubitemid 39349367)
33. S. Dröse, A. Galkin, U. Brandt, Measurement of superoxide formation by mitochondrial complex I of Yarrowia lipolytica, Methods Enzymol. 456 (2009) 475-490.
34. M.J. Zhou, Z.J. Diwu, N. PanchukVoloshina, R.P. Haugland, A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases, Anal. Biochem. 253 (1997) 162-168. (Pubitemid 27508167)
35. A. Azzi, C. Montecucco, C. Richter, The use of acetylated ferricytochrome c for the detection of superoxide radicals produced in biological membranes, Biochem. Biophys. Res. Commun. 65 (1975) 597-603.
36. A. Stroh, O. Anderka, K. Pfeiffer, T. Yagi, M. Finel, B. Ludwig, H. Schägger, Assembly of respiratory complexes I, III, and IV into NADH oxidase supercomplex stabilizes complex I in Paracoccus denitrificans, J. Biol. Chem. 279 (2004) 5000-5007.
37. G. von Jagow, T.A. Link, Use of specific inhibitors on the mitochondrial bc1 complex, Methods Enzymol. 126 (1986) 253-271.
38. H. Miyadera, K. Shiomi, H. Ui, Y. Yamaguchi, R. Masuma, H. Tomoda, H. Miyoshi, A. Osanai, K. Kita, S. Omura, Atpenins, potent and specific inhibitors of mitochondrial complex II (succinate-ubiquinone oxidoreductase), Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 473-477. (Pubitemid 36126075)
39. R. Horsefield, V. Yankovskaya, G. Sexton, W. Whittingham, K. Shiomi, S. Omura, B. Byrne, G. Cecchini, S. Iwata, Structural and computational analysis of the quinone-binding site of complex II (succinate-ubiquinone oxidoreductase) - a mechanism of electron transfer and proton conduction during ubiquinone reduction, J. Biol. Chem. 281 (2006) 7309-7316. (Pubitemid 43847499)
40. V.G. Grivennikova, E.V. Gavrikova, A.A. Timoshin, A.D. Vinogradov, Fumarate reductase activity of bovine heart succinate-ubiquinone reductase. New assay system and overall properties of the reaction, Biochim. Biophys. Acta 1140 (1993) 282-292. (Pubitemid 23015693)
41. R.M. Hollingworth, K.I. Ahammadsahib, G. Gadelhak, J.L. McLaughlin, New inhibitors of complex I of the mitochondrial electron transport chain with activity as pesticides, Biochem. Soc. Trans. 22 (1994) 230-233. (Pubitemid 24072425)
42. F.L. Muller, A.G. Roberts, M.K. Bowman, D.M. Kramer, Architecture of the Qo site of the cytochrome bc1 complex probed by superoxide production, Biochemistry 42 (2003) 6493-6499. (Pubitemid 36665824)
43. B.H.J. Bielski, D.E. Cabelli, R.L. Arudi, A.B. Ross, Reactivity of HO2/O2 - radicals in aqueous solution, J. Phys. Chem. Ref. Data 14 (1985) 1041-1100.
44. M. Gutman, E.B. Kearney, T.P. Singer, Control of succinate dehydrogenase in mitochondria, Biochemistry 10 (1971) 4763-4770.
45. E.B. Kearney, B.A.C. Ackrell, M. Mayr, Tightly bound oxalacetate and activation of succinate dehydrogenase, Biochem. Biophys. Res. Commun. 49 (1972) 1115-1121.
46. B.A.C. Ackrell, E.B. Kearney, M. Mayr, Studies on succinate- dehydrogenase. 24. Role of oxalacetate in regulation of mammalian succinate-dehydrogenase, J. Biol. Chem. 249 (1974) 2021-2027.
47. Y.O. Belikova, A.B. Kotlyar, A.D. Vinogradov, Oxidation of malate by the mitochondrial succinate-ubiquinone reductase, Biochim. Biophys. Acta 936 (1988) 1-9.
48. 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, J. Neuzil, α-Tocopheryl succinate induces apoptosis by targeting ubiquinone-binding sites in mitochondrial respiratory complex II, Oncogene 27 (2008) 4324-4335. (Pubitemid 352010000)
49. L.F. Dong, V.J.A. Jameson, D. Tilly, L. Prochazka, J. Rohlena, K. Valis, J. Truksa, R. Zobalova, E. Mandavian, K. Kluckova, M. Stantic, J. Stursa, R. Freeman, P.K. Witting, E. Norberg, J. Goodwin, B.A. Salvatore, J. Novotna, J. Turanek, M. Ledvina, P. Hozak, B. Zhivotovsky, M.J. Coster, S.J. Ralph, R.A.J. Smith, J. Neuzil, Mitochondrial targeting of α-tocopheryl succinate enhances its pro-apoptotic efficacy: a new paradigm for effective cancer therapy, Free Radic. Biol. Med. 50 (2011) 1546-1555.
50. L.F. Dong, V.J.A. Jameson, D. Tilly, J. Cerny, E. Mahdavian, A. Marin-Hernandez, L. Hernandez-Esquivel, S. Rodriguez-Enriquez, J. Stursa, P.K. Witting, B. Stantic, J. Rohlena, J. Truksa, K. Kluckova, J.C. Dyason, M. Ledvina, B.A. Salvatore, R. Moreno-Sanchez, M.J. Coster, S.J. Ralph, R.A.J. Smith, J. Neuzil, Mitochondrial targeting of vitamin E succinate enhances its pro-apoptotic and anti-cancer activity via mitochondrial complex II, J. Biol. Chem. 286 (2011) 3717-3728.
51. J. Guo, 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)
52. S.S.W. Szeto, S.N. Reinke, B.D. Sykes, B.D. Lemire, Ubiquinone-binding sitemutations in the Saccharomyces cerevisiae succinate dehydrogenase generate superoxide and lead to the accumulation of succinate, J. Biol. Chem. 282 (2007) 27518-27526. (Pubitemid 47501935)
53. M.P. Paranagama, K. Sakamoto, H. Amino, M. Awano, H. Miyoshi, 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.
54. N. Senoo-Matsuda, K. Yasuda, M. Tsuda, T. Ohkubo, S. Yoshimura, H. Nakazawa, P.S. Hartman, N. Ishii, A defect in the cytochrome b large subunit in complex II causes both superoxide anion overproduction and abnormal energy metabolism in Caenorhabditis elegans, J. Biol. Chem. 276 (2001) 41553-41558.
55. J.Z. Huang, B.D. Lemire, Mutations in the C. elegans succinate dehydrogenase iron- sulfur subunit promote superoxide generation and premature aging, J. Mol. Biol. 387 (2009) 559-569.
56. T. Ishii, M. Miyazawa, A. Onodera, K. Yasuda, N. Kawabe, M. Kirinashizawa, S. Yoshimura, N. Maruyama, P.S. Hartman, N. Ishii, Mitochondrial reactive oxygen species generation by the SDHC V69E mutation causes low birth weight and neonatal growth retardation, Mitochondrion 11 (2011) 155-165.
57. K.M. Owens, N. Aykin-Burns, D. Dayal, M.C. Coleman, F.E. Domann, D.R. Spitz, Genomic instability induced by mutant succinate dehydrogenase subunit D (SDHD) is mediated by O2 - and H2O2, Free Radic. Biol. Med. 52 (2012) 160-166.
58. V. Yankovskaya, R. Horsefield, S. Tornroth, C. Luna-Chavez, C. Leger, B. Byrne, G. Cecchini, S. Iwata, Architecture of succinate dehydrogenase and reactive oxygen species generation, Science 299 (2003) 700-704. (Pubitemid 36159483)
59. S. Hoyer, C. Krier, Ischemia and the aging brain - studies on glucose and energy-metabolism in rat cerebral-cortex, Neurobiol. Aging 7 (1986) 23-29. (Pubitemid 16153126)
60. R.J. Wiesner, P. Rosen, M.K. Grieshaber, Pathways of succinate formation and their contribution to improvement of cardiac-function in the hypoxic rat-heart, Biochem. Med. Metab. Biol. 40 (1988) 19-34.
61. K. Brockmann, A. Bjornstad, P. Dechent, C.G. Korenke, J. Smeitink, J.M.F. Trijbels, S. Athanassopoulos, R. Villagran, O.H. Skjeldal, E. Wilichowski, J. Frahm, F. Hanefeld, Succinate in dystrophic white matter: a proton magnetic resonance spectroscopy finding characteristic for complex II deficiency, Ann. Neurol. 52 (2002) 38-46. (Pubitemid 34693741)
62. A.A. Starkov, The role of mitochondria in reactive oxygen species metabolism and signaling, Ann. N. Y. Acad. Sci. 1147 (2008) 37-52.