Production of reactive oxygen species by complex I (NADH:ubiquinone oxidoreductase) from Escherichia coli and comparison to the enzyme from mitochondria

Biochemistry

Volumn 47, Issue 12, 2008, Pages 3964-3971

  Esterházy, Daria ^a,b   King, Martin S ^a   Yakovlev, Gregory ^a   Hirst, Judy ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEXATION; ESCHERICHIA COLI; MITOCHONDRIA; OXIDATIVE STRESS; PATHOLOGY; REACTION RATES;

MITOCHONDRIAL COMPLEXES; MITOCHONDRIAL ENZYMES; PATHOLOGICAL EFFECTS; REACTIVE OXYGEN SPECIES;

ENZYMES;

FLAVINE MONONUCLEOTIDE; HYDROETHIDINE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUPEROXIDE;

ARTICLE; COW; ENZYME ANALYSIS; ESCHERICHIA COLI; MITOCHONDRION; OXIDATION; PRIORITY JOURNAL; REDUCTION;

ANIMALS; CATTLE; ELECTRON TRANSPORT COMPLEX I; ESCHERICHIA COLI; HYDROGEN PEROXIDE; MITOCHONDRIA, HEART; OXIDATION-REDUCTION; OXYGEN; REACTIVE OXYGEN SPECIES; SUPEROXIDES;

BACTERIA (MICROORGANISMS); BOVINAE; ESCHERICHIA COLI;

EID: 41149100550     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi702243b     Document Type: Article

References (49)

1. Hirst, J. (2005) Energy transduction by respiratory complex I - An evaluation of current knowledge. Biochem. Soc. Trans. 33, 525-529.
2. Brandt, U. (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annu. Rev. Biochem. 75, 69-92.
3. Sazanov, L. A. (2007) Respiratory complex I: Mechanistic and structural insights provided by the crystal structure of the hydrophilic domain. Biochemistry 46, 2275-2288.
4. Raha, S., and Robinson, B. H. (2000) Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem. Sci. 25, 502-508.
5. m- dependent and -independent production of reactive oxygen species by rat brain mitochondria. J. Neurochem. 79, 266-277.
6. Brand, M. D., Affourtit, C., Esteves, T. C., Green, K., Lambert, A. J., Miwa, S., Pakay, J. L., and Parker, N. (2004) Mitochondrial superoxide: Production, biological effects, and activation of uncoupling proteins. Free Radical Biol. Med. 37, 755-767.
7. Balaban, R. S., Nemoto, S., and Finkel, T. (2005) Mitochondria, oxidants, and aging. Cell 120, 483-495.
8. Wallace, D. C. (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging and cancer: A dawn for evolutionary medicine. Annu. Rev. Genet. 39, 359-407.
9. Lin, M. T., and Beal, M. F. (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787-795.
10. Perier, C., Tieu, K., Guégan, C., Caspersen, C., Jackson-Lewis, V., Carelli, V., Martinuzzi, A., Hirano, M., Przedborski, S., and Vila, M. (2005) Complex I deficiency primes Bax-dependent neuronal apoptosis through mitochondrial oxidative damage. Proc. Natl. Acad. Sci. U.S.A. 102, 19126-19131.
11. Adam-Vizi, V., and Chinopoulos, C. (2006) Bioenergetics and the formation of mitochondrial reactive oxygen species. Trends Pharmacol. Sci. 27, 639-645.
12. Yadava, N., and Nicholls, D. G. (2007) Spare respiratory capacity rather than oxidative stress regulates glutamate excitotoxicity after partial respiratory inhibition of mitochondrial complex I with rotenone. J. Neurosci. 27, 7310-7317.
13. Koopman, W. J. H., Verkaart, S., Visch, H. J., van Emst-de Vries, S., Nijtmans, L. G. J., Smeitink, J. A. M., and Willems, P. H. G. M. (2007) Human NADH:ubiquinone oxidoreductase deficiency: Radical changes in mitochondrial morphology? Am. J. Physiol. Cell Physiol. 293, C22-C29.
14. 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.
15. Galkin, A., and Brandt, U. (2005) Superoxide radical formation by pure complex I (NADH:ubiquinone oxidoreductase) from Yarrowia lipolytica. J. Biol. Chem. 280, 30129-30135.
16. + oxidation-reduction state. Biochem. J. 368, 545-553.
17. Liu, Y., Fiskum, G., and Schubert, D. (2002) Generation of reactive Oxygen species by the mitochondrial electron transport chain. J. Neurochem. 80, 780-787.
18. 2 production by membrane potential and NAD-(P)H redox state. J. Neurochem. 86, 1101-1107.
19. Kudin, A. P., Bimpong-Buta, N. Y.-B., Vielhaber, S., Elger, C. E., and Kunz, W. S. (2004) Characterisation of superoxide-producing sites in isolated brain mitochondria. J. Biol. Chem. 279, 4127-4135.
20. Lambert, A. J., and Brand, M. D. (2004) Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I). J. Biol. Chem. 279, 39414-39420.
21. Nf) and the interaction with cluster N2: New insight into the energy-coupled electron transfer in complex I. Biochemistry 44, 1744-1754.
22. Leif, H., Sled, V. D., Ohnishi, T., Weiss, H., and Friedrich, T. (1995) Isolation and characterization of the proton-translocating NADH:ubiquinone oxidoreductase from Escherichia coli. Eur. J. Biochem. 230, 538-548.
23. Ohnishi, T. (1998) Iron - sulfur clusters/semiquinones in complex I. Biochim. Biophys. Acta 1364, 186-206.
24. Zu, Y., Di Bernardo, S., Yagi, T., and Hirst, J. (2002) Redox properties of the [2Fe-2S] center in the 24 kDa (NQO2) subunit of NADH:ubiquinone oxidoreductase (complex I). Biochemistry 41, 10056-10069.
25. 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.
26. Massey, V. (1994) Activation of molecular oxygen by flavins and flavoproteins. J. Biol. Chem. 269, 22459-22462.
27. Klinman, J. P. (2001) Life as aerobes: Are there simple rules for activation of dioxygen by enzymes? J. Biol. Inorg. Chem. 6, 1-13.
28. Mattevi, A. (2006) To be or not to be an oxidase: Challenging the oxygen reactivity of flavoenzymes. Trends Biochem. Sci. 31, 276-283.
29. Sazanov, L. A., and Hinchliffe, P. (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311, 1430-1436.
30. Sazanov, L. A., Carroll, J., Holt, P., Toime, L., and Fearnley, I. M. (2003) A role for native lipids in the stabilization and two-dimensional crystallization of the Escherichia coli NADH-ubiquinone oxidoreductase (complex I). J. Biol. Chem. 278, 19483-19491.
31. Sherwood, S., and Hirst, J. (2006) Investigation of the mechanism of proton translocation by NADH:ubiquinone oxidoreductase (complex I) from bovine heart mitochondria: Does the enzyme operate by a Q-cycle mechanism? Biochem. J. 400, 541-550.
32. Burch, H. B. (1957) Fluorimetric assay of FAD, FMN and riboflavin. Methods Enzymol. 3, 960-962.
33. Ukeda, H., Shimamura, T., Tsubouchi, M., Harada, Y., Nakai, Y., and Sawamura, M. (2002) Spectrophotometric assay of superoxide anion formed in Maillard reaction based on highly water-soluble tetrazolium salt. Anal. Sci. 18, 1151-1154.
34. .-. Free Radical Biol. Med. 15, 447-451.
35. Lucas, M., and Solano, F. (1992) Coelenterazine is a superoxide anion-sensitive chemiluminescent probe: Its usefulness in the assay of respiratory burst in neutrophils. Anal. Biochem. 206, 273-277.
36. Robinson, K. M., Janes, M. S., Pehar, M., Monette, J. S., Ross, M. F., Hagen, T. M., Murphy, M. P., and Beckman, J. S. (2006) Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc. Natl. Acad. Sci. U.S.A. 103, 15038-15043.
37. Pryor, W. A., and Squadrito, G. L. (1995) The chemistry of peroxynitrite: A product from the reaction of nitric oxide and superoxide. Am. J. Physiol. 268, L699-L722.
38. Kooy, N. W., Royall, J. A., Ischiropoulos, H., and Beckman, J. S. (1994) Peroxynitrite-mediated oxidation of dihydrorhodamine 123. Free Radical Biol. Med. 16, 149-156.
39. 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. Biophys. Acta 1604, 135-150.
40. Halliwell, B., and Gutteridge, J. M. C. (1998) Free Radicals in Biology and Medicine, 3rd ed., Oxford University Press, New York.
41. Imlay, J. A., and Fridovich, I. (1991) Assay of metabolic superoxide production in Escherichia coli. J. Biol. Chem. 266, 6957-6965.
42. 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.
43. Sinegina, L., Wikström, M., Verkhovsky, M. I., and Verkhovskaya, M. L. (2005) Activation of isolated NADH:ubiquinone reductase I (complex I) from Escherichia coli by detergent and phospholipids. Recovery of ubiquinone reductase activity and changes in EPR signals of iron-sulfur clusters. Biochemistry 44, 8500-8506.
44. Tarpey, M. M., and Fridovich, I. (2001) Methods of detection of vascular reactive species: Nitric oxide, superoxide, hydrogen peroxide, and peroxynitrite. Circ. Res. 89, 224-236.
45. Münzel, T., Afanas'ev, I. B., Kleschyov, A. L., and Harrison, D. G. (2002) Detection of superoxide in vascular tissue. Arterioscler., Thromb., Vasc. Biol. 1761-1768.
46. Halliwell, B., and Whiteman, M. (2004) Measuring reactive species and oxidative damage in vivo and in cell culture: How should you do it and what do the results mean? Br. J. Pharmacol. 142, 231-255.
47. Hille, R., and Massey, V. (1981) Studies on the oxidative half-reaction of xanthine oxidase. J. Biol. Chem. 256, 9090-9095.
48. 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.
49. 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.