Electrostatic interactions between FeS clusters in NADH:Ubiquinone oxidoreductase (complex I) from Escherichia coli

Biochemistry

Volumn 47, Issue 10, 2008, Pages 3185-3193

  Euro, Liliya ^a   Bloch, Dmitry A ^a   Wikström, Mårten ^a   Verkhovsky, Michael I ^a   Verkhovskaya, Marina ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

COULOMB INTERACTIONS; IRON COMPOUNDS; PARAMAGNETIC RESONANCE; PROTEINS; ULTRAVIOLET VISIBLE SPECTROSCOPY;

ELECTROCHEMICAL REDOX TITRATION; UBIQUINONE OXIDOREDUCTASE;

ESCHERICHIA COLI;

FERROUS SULFIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ARTICLE; BACTERIAL GROWTH; ELECTRON SPIN RESONANCE; ENZYME ACTIVATION; ENZYME ANALYSIS; ENZYME PURIFICATION; ESCHERICHIA COLI; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL;

ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRON TRANSPORT COMPLEX I; ELECTROSTATICS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLAVIN MONONUCLEOTIDE; HYDROGEN-ION CONCENTRATION; IRON-SULFUR PROTEINS; OXIDATION-REDUCTION;

ESCHERICHIA COLI;

EID: 40549126917     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi702063t     Document Type: Article

References (33)

1. Sazanov, L. A. (2007) Respiratory complex I: Mechanistic and structural insights provided by the crystal structure of the hydrophilic domain. Biochemistry 46, 2275-2288.
2. Hatefi, Y., Haavik, A. G., and Griffiths, D. E. (1962) Studies on electron transfer system. 40. Preparation and properties of mitochondrial DPNH-coenzyme Q reductase. J. Biol. Chem. 237, 1676-1680.
3. Ingledew, W. J., and Ohnishi, T. (1980) An analysis of some thermodynamic properties of iron-sulphur centres in site I of mitochondria. Biochem. J. 186, 111-117.
4. Zwicker, K., Galkin, A., Drose, S., Grgic, L., Kerscher, S., and Brandt, U. (2006) The Redox-Bohr group associated with iron-sulfur cluster N2 of complex I. J. Biol. Chem. 281, 23013-23017.
5. Meinhardt, S. W., Kula, T., Yagi, T., Lillich, T., and Ohnishi, T. (1987) EPR characterization of the iron-sulfur clusters in the NADH: Ubiquinone oxidoreductase segment of the respiratory chain in Paracoccus denitrificans. J. Biol. Chem. 262, 9147-9153.
6. 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.
7. Yano, T., Sklar, J., Nakamaru-Ogiso, E., Takahashi, Y., Yagi, T., and Ohnishi, T. (2003) Characterization of cluster N5 as a fast-relaxing [4Fe-4S] cluster in the Nqo3 subunit of the proton-translocating NADH-ubiquinone oxidoreductase from Paracoccus denitrificans. J. Biol. Chem. 278, 15514-15522.
8. 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.
9. Ohnishi, T. (1998) Iron-sulfur clusters/semiquinones in complex I. Biochim. Biophys. Acta 1364, 186-206.
10. Hirst, J. (2005) Energy transduction by respiratory complex I - An evaluation of current knowledge. Biochem. Soc. Trans. 33, 525-529.
11. Krishnamoorthy, G., and Hinkle, P. C. (1988) Studies on the electron transfer pathway, topography of iron-sulfur centers, and site of coupling in NADH-Q oxidoreductase. J. Biol. Chem. 263, 17566-17575.
12. Sazanov, L. A., and Hinchliffe, P. (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311, 1430-1436.
13. Calhoun, M. W., and Gennis, R. B. (1993) Demonstration of separate genetic-loci encoding distinct membrane-bound respiratory NADH dehydrogenases in Escherichia coli. J. Bacteriol. 175, 3013-3019.
14. 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.
15. Belevich, G., Euro, L., Wikström, M., and Verkhovskaya, M. (2007) Role of the conserved arginine 274 and histidine 224 and 228 residues in the NuoCD subunit of complex I from Escherichia coli. Biochemistry 46, 526-533.
16. Harder, S. R., Feinberg, B. A., and Ragsdale, S. W. (1989) A spectroelectrochemical cell designed for low temperature electron paramagnetic resonance titration of oxygen-sensitive proteins. Anal. Biochem. 181, 283-287.
17. Harder, S. R., Lu, W. P., Feinberg, B. A., and Ragsdale, S. W. (1989) Spectroelectrochemical studies of the corrinoid/iron-sulfur protein involved in acetyl coenzyme A synthesis by Clostridium thermoaceticum. Biochemistry 28, 9080-9087.
18. Bogachev, A. V., Bertsova, Y. V., Bloch, D. A., and Verkhovsky, M. I. (2006) Thermodynamic properties of the redox centers of Na(+)-translocating NADH:quinone oxidoreductase. Biochemistry 45, 3421-3428.
19. Massey, V., and Palmer, G. (1962) Charge transfer complexes of lipoyl dehydrogenase and free flavins. J. Biol. Chem. 237, 2347-2358.
20. Stankovich, M. T., Schopfer, L. M., and Massey, V. (1978) Determination of glucose oxidase oxidation-reduction potentials and the oxygen reactivity of fully reduced and semiquinoid forms. J. Biol. Chem. 253, 4971-4979.
21. Fu, W., Jack, R. F., Morgan, T. V., Dean, D. R., and Johnson, M. K. (1994) nifU gene product from Azotobacter vinelandii is a homodimer that contains two identical [2Fe-2S] clusters. Biochemistry 33, 13455-13463.
22. Mayhew, S. G., Petering, D., Palmer, G., and Foust, G. P. (1969) Spectrophotometric titration of ferredoxins and chromatium high potential iron protein with sodium dithionite. J. Biol. Chem. 244, 2830-2834.
23. Yano, T., Sled', V. D., Ohnishi, T., and Yagi, T. (1996) Expression and characterization of the flavoprotein subcomplex composed of 50-kDa (NQO1) and 25-kDa (NQO2) subunits of the proton-translocating NADH-quinone oxidoreductase of Paracoccus denitrificans. J. Biol. Chem. 271, 5907-5913.
24. Velazquez, I., Nakamaru-Ogiso, E., Yano, T., Ohnishi, T., and Yagi, T. (2005) Amino acid residues associated with cluster N3 in the NuoF subunit of the proton-translocating NADH-quinone oxidoreductase from Escherichia coli. FEBS Lett. 579, 3164-3168.
25. 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.
26. Barker, C. D., Reda, T., and Hirst, J. (2007) The flavoprotein subcomplex of complex I (NADH:ubiquinone oxidoreductase) from bovine heart mitochondria: Insights into the mechanisms of NADH oxidation and NAD+ reduction from protein film voltammetry. Biochemistry 46, 3454-3464.
27. Nakamaru-Ogiso, E., Yano, T., Yagi, T., and Ohnishi, T. (2005) Characterization of the iron-sulfur cluster N7 (N1c) in the subunit NuoG of the proton-translocating NADH-quinone oxidoreductase from Escherichia coli. J. Biol. Chem. 280, 301-307.
28. Pohl, T., Bauer, T., Dorner, K., Stolpe, S., Sell, P., Zocher, G., and Friedrich, T. (2007) Iron-sulfur cluster N7 of the NADH: ubiquinone oxidoreductase (complex I) is essential for stability but not involved in electron transfer. Biochemistry 46, 6588-6596.
29. Ohnishi, T., Blum, H., Galante, Y. M., and Hatefi, Y. (1981) Iron-sulfur N-1 clusters studied in NADH-ubiquinone oxidoreductase and in soluble NADH dehydrogenase. J. Biol. Chem. 256, 9216-9220.
30. Laurents, D. V., Huyghues-Despointes, B. M., Bruix, M., Thurlkill, R. L., Schell, D., Newsom, S., Grimsley, G. R., Shaw, K. L., Trevino, S., Rico, M., Briggs, J. M., Antosiewicz, J. M., Scholtz, J. M., and Pace, C. N. (2003) Charge-charge interactions are key determinants of the pK values of ionizable groups in ribonuclease Sa (pI = 3.5) and a basic variant (pI = 10.2). J. Mol. Biol. 325, 1077-1092.
31. Schutz, C. N., and Warshel, A. (2001) What are the dielectric "constants" of proteins and how to validate electrostatic models? Proteins 44, 400-417.
32. Albracht, S. P., Dooijewaard, G., Leeuwerik, F. J., and Swol, B. V. (1977) EPR signals of NADH: Q oxidoreductase. Shape and intensity. Biochim. Biophys. Acta 459, 300-317.
33. Grgic, L., Zwicker, K., Kashani-Poor, N., Kerscher, S., and Brandt, U. (2004) Functional significance of conserved histidines and arginines in the 49-kDa subunit of mitochondrial complex I. J. Biol. Chem. 279, 21193-21199.