Reduction of hydrophilic ubiquinones by the flavin in mitochondrial NADH:ubiquinone oxidoreductase (complex I) and production of reactive oxygen species

Biochemistry

Volumn 48, Issue 9, 2009, Pages 2053-2062

  King, Martin S ^a   Sharpley, Mark S ^a,b   Hirst, Judy ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITES; BOVINE HEARTS; COFACTOR; COVALENTLY BOUNDS; FLAVIN MONONUCLEOTIDE; FRIEDREICH'S ATAXIAS; INTRA-MOLECULAR ELECTRON TRANSFERS; IRON-SULFUR CLUSTERS; MECHANISTIC STUDIES; MEMBRANE-BOUND ENZYMES; MITOCHONDRIAL NADH; NADH OXIDATIONS; NATURAL SUBSTRATES; NON ENERGIES; OXIDOREDUCTASE; PROTON TRANSLOCATIONS; REACTIVE OXYGEN SPECIES; REDOX CYCLING; SEMIQUINONES; SUPEROXIDE RADICALS; TRANSDUCING; UBIQUINONE;

COENZYMES; ENZYMES; FREE RADICAL REACTIONS; HYDROGEN; HYDROGEN PEROXIDE; HYDROPHILICITY; IRON COMPOUNDS; MOLECULAR OXYGEN; OXIDATION; PROTON TRANSFER; REDOX REACTIONS; SULFUR;

PLANTS (BOTANY);

HYDROGEN PEROXIDE; IDEBENONE; QUERCETIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SEMIQUINONE; UBIDECARENONE; UBIQUINONE;

ARTICLE; ELECTRON TRANSPORT; ENERGY TRANSFER; ENZYME KINETICS; ISOLATION PROCEDURE; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; STOICHIOMETRY;

ALGORITHMS; ANIMALS; CATTLE; CYTOCHROMES C; ELECTRON TRANSPORT COMPLEX I; FLAVINS; HYDROGEN PEROXIDE; KINETICS; MITOCHONDRIA, LIVER; NAD; OXIDATION-REDUCTION; OXYGEN; REACTIVE OXYGEN SPECIES; ROTENONE; UBIQUINONE; UNCOUPLING AGENTS; WATER;

BOVINAE;

EID: 64549096768     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi802282h     Document Type: Article

References (56)

1. Brandt, U. (2006) Energy converting NADH:quinone oxidoreduc-tase (complex I). Annu. Rev. Biochem. 75, 69-92.
2. Hirst, J. (2005) Energy transduction by respiratory complex I: An evaluation of current knowledge. Biochem. Soc. Trans. 33, 525-529.
3. Carroll, J., Fearnley, I. M., Skehel, M., Shannon, R. J., Hirst, J., and Walker, J. E. (2006) Bovine complex I is a complex of 45 different subunits. J. Biol. Chem. 281, 32124-32121.
4. Hirst, J., Carroll, J., Fearnley, I. M., Shannon, R. J., and Walker, J. E. (2003) The nuclear encoded subunits of complex I from bovine heart mitochondria. Biochim. Biovhys. Acta 1604, 135-150.
5. Yakovlev, G., Reda, T., and Hirst, J. (2007) Reevaluating the relationship between EPR spectra and enzyme structure for the iron-sulfur clusters in NADH:quinone oxidoreductase. Proc. Natl. Acad. Sci. U.S.A. 104, 12720-12725.
6. Sazanov, L. A., and Hinchliffe, P. (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311, 1430-1436.
7. Ragan, C. I. (1978) The role of phospholipids in the reduction of ubiquinone analogues by the mitochondrial reduced nicotinamide-adenine dinucleotide-ubiquinone oxidoreductase complex. Biochem. J. 172, 539-547.
8. + pump by exogenous quinones in intact mitochondria. J. Biol. Chem. 257, 4106-4113.
9. Estornell, E., Fato, R., Pallotti, F., and Lenaz, G (1993) Assay conditions for the mitochondrial NADHxoenzyme Q oxidoreductase. FEBS Lett. 332, 127-131.
10. Degli Esposti, M., Ngo, A., McMullen, G. L., GheUi, A., Sparla, F., Benelli, B., Ratta, M., and Linnane, A. W. (1996) The specificity of mitochondrial complex I for ubiquinones. Biochem. J. 313, 327-334.
11. Fato, R., Estornell, E., Di Bernardo, S., Pallotti, F., Castelli, G. P., and Lenaz, G. (1996) Steady-state kinetics of the reduction of coenzyme Q analogues by complex I (NADH:ubiquinone oxidoreductase) in bovine heart mitochondria and submitochondrial particles. Biochemistry 35, 2705-2716.
12. Lenaz, G (1998) Quinone specificity of complex I. Biochim. Biovhys. Acta 1364, 207-221.
13. Tocilescu, M. A., Fendel, U., Zwicker, K., Kerscher, S., and Brandt, U. (2007) Exploring the ubiquinone binding cavity of respiratory complex I. J. Biol. Chem. 282, 29514-29520.
14. Miyoshi, H. (1998) Structure-activity relationships of some complex I inhibitors. Biochim. Biovhys. Acta 1364, 236-244.
15. Degli Esposti, M. (1998) Inhibitors of NADH-ubiquinone reductase: An overview. Biochim. Biovhys. Acta 1364, 222-235.
16. Darrouzet, E., Issartel, J. P., Lunardi, J., and Dupuis, A. (1998) The 49-kDa subunit of NADH-ubiquinone oxidoreductase (complex I) is involved in the binding of piericidin and rotenone, two quinone-related inhibitors. FEBS Lett. 431, 34-38.
17. Schuler, F., Yano, T., Di Bernardo, S., Yagi, T., Yankovskaya, V., Singer, T. P., and Casida, J. E. (1999) NADH-quinone oxidoreductase: PSST subunit couples electron transfer from iron-sulfur cluster N2 to quinone. Proc. Natl. Acad. Sci. U.S.A. 96, 4149-4153.
18. 3H]dihydrorotenone. FEBS Lett. 219, 108-113.
19. Murai, M., Ishihara, A., Nishioka, T., Yagi, T, and Miyoshi, H. (2007) The ND1 subunit constructs the inhibitor binding domain in bovine heart mitochondrial complex I. Biochemistry 46, 6409-6416.
20. Nakamaru-Ogiso, E., Sakamoto, K., Matsuno-Yagi, A., Miyoshi. H, and Yagi, T. (2003) The ND5 subunit was labeled by a photoaffinity analogue of fenpyroximate in bovine mitochondrial complex I. Biochemistry 42, 746-754.
21. Schatz, G, and Racker, E. (1966) Partial resolution of the enzymes catalyzing oxidative phosphorylation. VII. Oxidative phosphorylation in the diphosphopyridine nucleotide-cytochrome b segments of the respiratory chain: Assay and properties in submitochondrial particles. J. Biol. Chem. 241, 1429-1438.
22. Zickermann, V., Bostina, M., Hunte, C., Ruiz, T, Radermacher, M., and Brandt, U. (2003) Functional implications from an unexpected position of the 49-kDa subunit of NADH ubiquinone oxidoreductase. J. Biol. Chem. 278, 29072-29078.
23. Tormo, J. R., and Estornell, E. (2000) New evidence for the multiplicity of ubiquinone- and inhibitor-binding sites in the mitochondrial complex I. Arch. Biochem. Biovhys. 381, 241-246.
24. Degli Esposti, M., Ngo, A., Ghelli, A., Benelli, B., Carelli, V., McLennan, H, and Linnane, A. W. (1996) The interaction of Q analogs, particularly hydroxydecyl benzoquinone (idebenone), with the respiratory complexes of heart mitochondria. Arch. Biochem. Biovhys. 330, 395-400.
25. Genova, M. L., Ventura, B., Guiuliano, G, Bovina, C., Formiggini, G., Castelli, G. P., and Lenaz, G. (2001) The site of production of superoxide radical in mitochondrial complex I is not a bound semiquinone but presumably iron-sulfur cluster N2. FEBS Lett. 505, 364-368.
26. Cenas, N. K., Bironaite, D. A., and Kulys, J. J. (1991) On the mechanism of rotenone-insensitive reduction of quinones by mitochondrial NADH ubiquinone reductase. FEBS Lett. 284, 192-194.
27. Pandolfo, M. (2008) Drug insight: Antioxidant therapy in inherited ataxias. Nat. Clin. Pract. Neurol. 4, 86-96.
28. Sharpley, M. S., Shannon, R. J., Draghi, F., and Hirst, J. (2006) Interactions between phospholipids and NADH ubiquinone oxidoreductase (complex I) from bovine mitochondria. Biochemistry 45, 241-248.
29. Fearnley, I. M., Carroll, J., Shannon, R. J., Runswick, M. J., Walker, J. E., and Hirst, J. (2001) GRIM-19, a cell death regulatory gene product, is a subunit of bovine mitochondrial NADH:ubiquinone oxidoreductase (complex I). J. Biol. Chem. 276, 38345-38348.
30. II-DTPA, a very low potential reductant. Biochemistry 47, 8885-8893.
31. Kotlyar, A. B., and Vinogradov, A. D. (1990) Slow active/inactive transition of the mitochondrial NADH-ubiquinone reductase. Biochim. Biovhys. Acta 1019, 151-158.
32. Rauchová, H., Drahota, Z., Bergamini, C, Fato, R., and Lenaz, G. (2008) Modification of respiratory-chain enzyme activities in brown adipose tissue mitochondria by idebenone (hydroxydecyl-ubiquinone). J. BioenerQ. Biomembr. 40, 85-93.
33. Yakovlev, G., and Hirst, J. (2007) Transhydrogenation reactions catalyzed by mitochondrial NADH-ubiquinone oxidoreductase (complex I). Biochemistry 46, 14250-14258.
34. + oxidation-reduction state. Biochem. J. 368, 545-553.
35. 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.
36. Votyakova, T. V., and Reynolds, I. J. (2004) Detection of hydrogen peroxide with amplex red: Interference by NADH and reduced glutathione auto-oxidation. Arch. Biochem. Biovhys. 431, 138-144.
37. 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. Biovhys. Res. Com-mun. 65, 597-603.
38. 1 binding site of bovine heart NADH:oenzyme Q oxidoreductase. J. Bioen-ere. Biomembr. 34, 89-94.
39. Jauslin, M. L., Wirth, T., Meier, T., and Schoumacher, F. (2002) A cellular model for Friedreich Ataxia reveals small-molecule glutathione peroxidase mimetics as novel treatment strategy. Hum. Mol. Genet. 11, 3055-3063.
40. Minakami, S., Ringler, R. L., and Singer, T. P. (1962) Studies on the respiratory chain-linked dihydrodiphosphopyridine nucleotide dehydrogenase. J. Biol. Chem. 237, 569-576.
41. Helfenbaum, L., Ngo, A., Ghelli, A., Linnane, A. W., and Degli Esposti, M. (1997) Proton pumping of mitochondrial complex I: Differential activation by analogs of ubiquinone. J. BioenerQ. Biomembr. 29, 71-80.
42. Winterbourn, C. C. (1981) Cytochrome c reduction by semiquinone radicals can be directly inhibited by superoxide dismutase. Arch. Biochem. Biovhys. 209, 159-167.
43. Calkin, A., and Brandt, U. (2005) Superoxide radical formation by pure complex I (NADH:ubiquinone oxidoreductase) from Yarrowia lipolytica. J. Biol. Chem. 280, 30129-30135.
44. Eschemann, A., Calkin, A., Oettmeier, W., Brandt, U., and Kerscher, S. (2005) HDQ (l-hydroxy-2-dodecyl-4(lH)quinolone), a high affinity inhibitor for mitochondrial alternative NADH dehydrogenase: Evidence for a ping-pong mechanism. J. Biol. Chem. 280, 3138-3142.
45. Sled, V. D., Rudnitzky, N. I., Hatefi, Y., and Ohnishi, T. (1994) Thermodynamic analysis of flavin in mitochondrial NADH: ubiquinone oxidoreductase (complex I). Biochemistry 33, 10069-10075.
46. Deller, S., Macheroux, P., and Sollner, S. (2008) Flavin-dependent quinone reductases. Cell. Mol. Life Sci. 65, 141-160.
47. Faig, M., Bianchet, M. A., Talalay, P., Chen, S., Winski, S., Ross, D., and Amzel, L. M. (2000) Structures of recombinant human and mouse NAD(P)H:quinone oxidoreductases: Species comparison and structural changes with substrate binding and release. Proc. Natl. Acad. Sci. U.S.A. 97, 3177-3182.
48. Ragan, C. I., and Racker, E. (1973) Resolution and reconstitution of the mitochondrial electron transfer system. IV. The reconstitution of rotenone-sensitive reduced nicotinamide adenine dinucleotide-ubiquinone reductase from reduced nicotinamide adenine dinucle-otide dehydrogenase and phospholipids. J. Biol. Chem. 248, 6876-6884.
49. Fry, M., and Green, D. E. (1981) Cardiolipin requirement for electron transfer in complex I and III of the mitochondrial respiratory chain. J. Biol. Chem. 256, 1874-1880.
50. Dröse, S., Zwicker, K., and Brandt, U. (2002) Full recovery of the NADH:ubiquinone activity of complex I (NADH:ubiquinone oxidoreductase) from Yarrowia lipolytica by the addition of phospholipids. Biochim. Biovhys. Acta 1556, 65-72.
51. Clint, J. H. (1974) Micellization of mixed nonionic surface active agents. J. Chem. Soc. 71, 1327-1334.
52. Holland, P. M., and Rubingh, D. N. (1983) Nonideal multicom-ponent mixed micelle model. J. Phys. Chem. 87, 1984-1990.
53. Sakamoto, K., Miyoshi, H., Ohshima, M., Kuwabara, K., Kano, K., Akagi, T., Mogi, T., and Iwamura, H. (1998) Role of the isoprenyl tail of ubiquinone in reaction with respiratory enzymes: Studies with bovine heart mitochondrial complex I and Escherichia coli bo-type ubiquinol oxidase. Biochemistry 37, 15106-15113.
54. Berthiaume, J. M., and Wallace, K. B. (2007) Adriamycin-induced oxidative mitochondrial cardiotoxicity. Cell Biol. Toxicol. 23, 15-25.
55. Cochemé, H. M., and Murphy, M. P. (2008) Complex I is the major site of mitochondrial superoxide production by paraquat. J. Biol. Chem. 283, 1786-1798.
56. Greenamyre, J. T., and Hastings, T. G. (2004) Parkinson's: Divergent causes, convergent mechanisms. Science 304. 1120-1122. BI802282H