Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions

Journal of Biological Chemistry

Volumn 287, Issue 32, 2012, Pages 27255-27264

  Quinlan, Casey L ^a   Orr, Adam L ^a   Perevoshchikova, Irina V ^a   Treberg, Jason R ^b   Ackrell, Brian A ^a   Brand, Martin D ^a  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRON TRANSPORT CHAIN; EXPERIMENTAL EVIDENCE; FORWARD REACTIONS; FUMARATES; HIGH RATE; INTACT CELLS; KREBS CYCLE; MALONATES; MITOCHONDRIAL COMPLEX; RAT SKELETAL MUSCLE; REACTIVE OXYGEN SPECIES; REDUCTION STATE; RESPIRATORY COMPLEX; REVERSE REACTIONS; SUBSTRATE OXIDATION; SUPEROXIDES; UBIQUINONE;

OXYGEN;

MITOCHONDRIA;

ATPENIN A5; ATPENIN B; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; CORTICOTROPIN RELEASING FACTOR RECEPTOR 2; FLAVOPROTEIN; FUMARIC ACID; G PROTEIN COUPLED RECEPTOR; MYXOTHIAZOL; QUERCETIN; REACTIVE OXYGEN METABOLITE; ROTENONE; SUCCINIC ACID; SUPEROXIDE; UBIQUINONE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; BIOGENESIS; ENZYME SUBSTRATE; FEMALE; MITOCHONDRION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; RAT; RESPIRATORY CHAIN; SKELETAL MUSCLE;

ELECTRON TRANSPORT COMPLEX II; HYDROGEN PEROXIDE; MITOCHONDRIA; REACTIVE OXYGEN SPECIES;

RATTUS;

EID: 84864540083     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.374629     Document Type: Article

References (51)

1. Bunik, V. I., and Sievers, C. (2002) Inactivation of the 2-oxo acid dehydrogenase complexes upon generation of intrinsic radical species. Eur. J. Biochem. 269, 5004-5015 (Pubitemid 35279014)
2. Tretter, L., and Adam-Vizi, V. (2004) Generation of reactive oxygen species in the reaction catalyzed by α-ketoglutarate dehydrogenase. J. Neurosci. 24, 7771-7778 (Pubitemid 39215680)
3. Grivennikova, V. G., Kareyeva, A. V., and Vinogradov, A. D. (2010) What are the sources of hydrogen peroxide production by heart mitochondria? Biochim. Biophys. Acta 1797, 939-944
4. Adam-Vizi, V. (2005) Production of reactive oxygen species in brain mitochondria: contribution by electron transport chain and non-electron transport chain sources. Antioxid. Redox. Signal. 7, 1140-1149
5. 2 production by membrane potential and NAD(P)H redox state. J. Neurochem. 86, 1101-1107
6. Murphy, M. P. (2009) How mitochondria produce reactive oxygen species. Biochem. J. 417, 1-13
7. Brand, M. D. (2010) The sites and topology of mitochondrial superoxide production. Exp. Gerontol. 45, 466-472
8. Quinlan, C. L., Treberg, J. R., and Brand, M. D. (2011) Mechanisms of free radical production and their relationship to the aging process, The Handbook of the Biology of Aging, pp. 45-59, Academic Press
9. Dröse, S., and Brandt, U. (2008) The mechanism of mitochondrial superoxide production by the cytochrome bc1 complex. J. Biol. Chem. 283, 21649-21654
10. Kussmaul, L., and Hirst, J. (2006) The mechanism of superoxide production by NADH:ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. Proc. Natl. Acad. Sci. U.S.A. 103, 7607-7612
11. Ackrell, B. A., Kearney, E. B., and Edmondson, D. (1975) Mechanism of the reductive activation of succinate dehydrogenase. J. Biol. Chem. 250, 7114-7119
12. Quinlan, C. L., Gerencser, A. A., Treberg, J. R., and Brand, M. D. (2011) The mechanism of superoxide production by the antimycin-inhibited mitochondrial Q-cycle. J. Biol. Chem. 286, 31361-31372
13. Treberg, J. R., Quinlan, C. L., and Brand, M. D. (2010) Hydrogen peroxide efflux from muscle mitochondria underestimates matrix superoxide production - a correction using glutathione depletion. FEBS J. 277, 2766-2778
14. St-Pierre, J., Buckingham, J. A., Roebuck, S. J., and Brand, M. D. (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277, 44784-44790 (Pubitemid 36159072)
15. Ackrell, B. A. (2002) Cytopathies involving mitochondrial complex II. Mol. Aspects Med., 23, 369-384
16. Sun, F., Huo, X., Zhai, Y., Wang, A., Xu, J., Su, D., Bartlam, M., and Rao, Z. (2005) Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121, 1043-1057 (Pubitemid 40884395)
17. Gutman, M., Kearney, E. B., and Singer, T. P. (1971) Control of succinate dehydrogenase in mitochondria. Biochemistry 10, 4763-4770
18. Ackrell, B. A., Kearney, E. B., and Singer, T. P. (1978) Mammalian succinate dehydrogenase. Methods Enzymol. 53, 466-483
19. Merli, A., Capaldi, R. A., Ackrell, B. A., and Kearney, E. B. (1979) Arrangement of complex II (succinate-ubiquinone reductase) in the mitochondrial inner membrane. Biochemistry 18, 1393-1400
20. Cecchini, G. (2003) Function and structure of complex II of the respiratory chain. Annu. Rev. Biochem. 72, 77-109
21. Yu, L., Xu, J. X., Haley, P. E., and Yu, C. A. (1987) Properties of bovine heart mitochondrial cytochrome b560. J. Biol. Chem. 262, 1137-1143 (Pubitemid 17028425)
22. Imlay, J. A. (1995) A metabolic enzyme that rapidly produces superoxide, fumarate reductase of Escherichia coli. J. Biol. Chem. 270, 19767-19777
23. Paranagama, M. P., Sakamoto, K., Amino, H., Awano, M., Miyoshi, H., and Kita, K. (2010) Contribution of the FAD and quinone binding sites to the production of reactive oxygen species from Ascaris suum mitochondrial complex II. Mitochondrion 10, 158-165
24. Messner, K. R., and Imlay, J. A. (2002) Mechanism of superoxide and hydrogen peroxide formation by fumarate reductase, succinate dehydrogenase, and aspartate oxidase. J. Biol. Chem. 277, 42563-42571 (Pubitemid 35285624)
25. Guo, J., and Lemire, B. D. (2003) The ubiquinone-binding site of the Saccharomyces cerevisiae succinate-ubiquinone oxidoreductase is a source of superoxide. J. Biol. Chem. 278, 47629-47635 (Pubitemid 37523207)
26. Zhao, Z., Rothery, R. A., and Weiner, J. H. (2006) Effects of site-directed mutations in Escherichia coli succinate dehydrogenase on the enzyme activity and production of superoxide radicals. Biochem. Cell Biol. 84, 1013-1021 (Pubitemid 46450700)
27. Szeto, S. S., Reinke, S. N., Sykes, B. D., and Lemire, B. D. (2007) Ubiquinone-binding site mutations in the Saccharomyces cerevisiae succinate dehydrogenase generate superoxide and lead to the accumulation of succinate. J. Biol. Chem. 282, 27518-27526 (Pubitemid 47501935)
28. Messner, K. R., and Imlay, J. A. (1999) The identification of primary sites of superoxide and hydrogen peroxide formation in the aerobic respiratory chain and sulfite reductase complex of Escherichia coli. J. Biol. Chem. 274, 10119-10128
29. Yankovskaya, V., Horsefield, R., Törnroth, S., Luna-Chavez, C., Miyoshi, H., Léger, C., Byrne, B., Cecchini, G., and Iwata, S. (2003) Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299, 700-704 (Pubitemid 36159483)
30. Zhang, L., Yu, L., and Yu, C. A. (1998) Generation of superoxide anion by succinate-cytochrome c reductase from bovine heart mitochondria. J. Biol. Chem. 273, 33972-33976 (Pubitemid 29008862)
31. Bardella, C., Pollard, P. J., and Tomlinson, I. (2011) SDH mutations in cancer. Biochim. Biophys. Acta 1807, 1432-1443
32. Ishii, T., Yasuda, K., Akatsuka, A., Hino, O., Hartman, P. S., and Ishii, N. (2005) A mutation in the SDHC gene of complex II increases oxidative stress, resulting in apoptosis and tumorigenesis. Cancer Res. 65, 203-209 (Pubitemid 40070811)
33. Guzy, R. D., Sharma, B., Bell, E., Chandel, N. S., and Schumacker, P. T. (2008) Loss of the SdhB, but not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxia-inducible factor activation and tumorigenesis. Mol. Cell Biol. 28, 718-731
34. Affourtit, C., Quinlan, C. L., and Brand, M. D. (2012) Measurement of proton leak and electron leak in isolated mitochondria. Methods Mol. Biol. 810, 165-182
35. Chappell, J. B., and Perry, S. V. (1954) Biochemical and osmotic properties of skeletal muscle mitochondria. Nature 173, 1094-1095
36. Azzi, A., Montecucco, C., and Richter, C. (1975) The use of acetylated ferricytochrome c for the detection of superoxide radicals produced in biological membranes. Biochem. Biophys. Res. Commun. 65, 597- 603
37. Hatefi, Y., and Stiggall, D. L. (1978) Preparation and properties of succinate: ubiquinone oxidoreductase (complex II). Methods Enzymol. 53, 21-27
38. Palmieri, F., Prezioso, G., Quagliariello, E., and Klingenberg, M. (1971) Kinetic study of the dicarboxylate carrier in rat liver mitochondria. Eur. J. Biochem. 22, 66-74
39. Boveris, A., Oshino, N., and Chance, B. (1972) The cellular production of hydrogen peroxide. Biochem. J. 128, 617-630
40. 2 formation by rat heart mitochondria on substrate availability and donor age. J. Bioenerg. Biomembr. 29, 89-95
41. Lambert, A. J., and Brand, M. D. (2004) Superoxide production by NADH:ubiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane. Biochem. J. 382, 511-517 (Pubitemid 39243917)
42. Treberg, J. R., Quinlan, C. L., and Brand, M. D. (2011) Evidence for two sites of superoxide production by mitochondrial NADH-ubiquinone oxidoreductase (complex I). J. Biol. Chem. 286, 27103-27110
43. Belikova, Y. O., Kotlyar, A. B., and Vinogradov, A. D. (1988) Oxidation of malate by the mitochondrial succinate-ubiquinone reductase. Biochim. Biophys. Acta, 936, 1-9
44. Miyadera, H., Shiomi, K., Ui, H., Yamaguchi, Y., Masuma, R., Tomoda, H., Miyoshi, H., Osanai, A., Kita, K., and Omura, S. (2003) Atpenins, potent and specific inhibitors of mitochondrial complex II (succinate-ubiquinone oxidoreductase). Proc. Natl. Acad. Sci. U.S.A. 100, 473-477 (Pubitemid 36126075)
45. Ramsay, R. R., Ackrell, B. A., Coles, C. J., Singer, T. P., White, G. A., and Thorn, G. D. (1981) Reaction site of carboxanilides and of thenoyltrifluoroacetone in complex II. Proc. Natl. Acad. Sci. U.S.A. 78, 825-828 (Pubitemid 11159518)
46. Mowery, P. C., Steenkamp, D. J., Ackrell, A. C., Singer, T. P., and White, G. A. (1977) Inhibition of mammalian succinate dehydrogenase by carboxins. Arch. Biochem. Biophys. 178, 495-506 (Pubitemid 8041846)
47. Hirst, J., Sucheta, A., Ackrell, B. A., and Armstrong, F. A. (1996) Electrocatalytic voltammetry of succinate dehydrogenase: direct quantification of the catalytic properties of a complex electron-transport enzyme. J. Am. Chem. Soc. 118, 5031-5038 (Pubitemid 26200977)
48. Drahota, Z., Chowdhury, S. K., Floryk, D., Mrácek, T., Wilhelm, J., Rauchová, H., Lenaz, G., and Houstek, J. (2002) Glycerophosphate- dependent hydrogen peroxide production by brown adipose tissue mitochondria and its activation by ferricyanide. J. Bioenerg. Biomembr. 34, 105-113 (Pubitemid 34477973)
49. Miwa, S., St-Pierre, J., Partridge, L., and Brand, M. D. (2003) Superoxide and hydrogen peroxide production by Drosophila mitochondria. Free Radic. Biol. Med. 35, 938-948 (Pubitemid 37211448)
50. Miwa, S., and Brand, M. D. (2005) The topology of superoxide production by complex III and glycerol-3-phosphate dehydrogenase in Drosophila mitochondria. Biochim. Biophys. Acta 1709, 214-219 (Pubitemid 41254214)
51. Bonomi, F., Pagani, S., Cerletti, P., and Giori, C. (1983) Modification of the thermodynamic properties of the electron-transferring groups in mitochondrial succinate dehydrogenase upon binding of succinate. Eur. J. Biochem. 134, 439-445