The steady-state mechanism of cytochrome c oxidase: Redox interactions between metal centres

Biochemical Journal

Volumn 422, Issue 2, 2009, Pages 237-246

  Mason, Maria G ^a   Nicholls, Peter ^a   Cooper, Chris E ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

Author keywords

Cytochrome c oxidase; Haem; Mitochondrion; Near infrared spectroscopy; Redox potential; Steady state enzyme kinetics

Indexed keywords

ABSORBANCE SPECTRUM; AMBIENT OXYGEN; CLASSICAL MODEL; CYTOCHROME C; CYTOCHROME C OXIDASE; ELECTRON TRANSFER; ENZYME COMPLEXES; FERROCYTOCHROME C; HAEM; HIGH POTENTIAL; METAL CENTRES; NEAR-IR; NON-INVASIVE; OVERALL REACTIONS; OXIDIZED ENZYME; RATE DETERMINING STEP; RATE OF REDUCTION; REDOX INTERACTIONS; REDOX POTENTIAL; SPECTRAL FEATURE; STATIC EQUILIBRIUM; STEADY STATE; STEADY-STATE ENZYME KINETICS; STEADY-STATE POTENTIALS;

ENZYME KINETICS; ENZYMES; INFRARED DEVICES; MAMMALS; NEAR INFRARED SPECTROSCOPY; OXYGEN; SECONDARY BATTERIES; SPECTROSCOPIC ANALYSIS;

INFRARED SPECTROSCOPY;

CYTOCHROME C; CYTOCHROME C OXIDASE; HEME; OXYGEN; COPPER; DRUG DERIVATIVE; HEME A;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME MECHANISM; MICHAELIS CONSTANT; MOLECULAR MODEL; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; STEADY STATE; ANIMAL; CATTLE; CHEMISTRY; COMPARATIVE STUDY; HORSE; METABOLISM; PHYSIOLOGY; PROTEIN BINDING;

MAMMALIA;

ANIMALS; CATTLE; COPPER; ELECTRON TRANSPORT COMPLEX IV; HEME; HORSES; OXIDATION-REDUCTION; PROTEIN BINDING;

EID: 70149103333     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20082220     Document Type: Article

References (51)

1. Minnaert, K. (1961) The kinetics of cytochrome c oxidase. 1. The system: cytochrome c-cytochrome oxidase-oxygen. Biochim. Biophys. Acta 50, 23-34
2. Cooper, C. E., Mason, M. G. and Nicholls, P. (2008) A dynamic model of nitric oxide inhibition of mitochondrial cytochrome c oxidase. Biochim. Biophys. Acta 1777, 867-876
3. 3. J. Biol. Chem. 274, 38032-38041
4. Wang, K., Geren, L., Zhen, Y., Ma, L., Ferguson-Miller, S., Durham, B. and Millett, F. (2002) Mutants of the CuA site in cytochrome c oxidase of Rhodobacter sphaeroides: II. Rapid kinetic analysis of electron transfer. Biochemistry 41, 2298-2304
5. Brooks, S. P. and Nicholls, P. (1982) Anion and ionic strength effects upon the oxidation of cytochrome c by cytochrome c oxidase. Biochim. Biophys. Acta 680, 33-43
6. Babcock, G T. and Wikstram, M. (1992) Oxygen activation and the conservation of energy in cell respiration. Nature 356, 301-309
7. Conrad, H. and Smith, L. (1956) A study of the kinetics of the oxidation of cytochrome c by cytochrome c oxidase. Arch. Biochem. Biophys. 63, 403-413
8. Yonetani, T. (1962) Studies on cytochrome oxidase. IV. The cytochrome oxidase activity. J. Biol. Chem. 237, 550-559
9. Gnaiger, E., Steinlechner-Maran, R., Mendez, G., Eberl, T. and Margreiter, R. (1995) Control of mitochondrial and cellular respiration by oxygen. J. Bioenerg. Biomembr 27, 583-596
10. LaManna, J. C. (2003) The redox state of cytochrome oxidase in brain in vivo: an historical perspective. Adv. Exp. Med. Biol. 530, 535-546
11. Chance, B. (1965) Reaction of oxygen with the respiratory chain in cells and tissues. J. Gen. Physiol. 49 (Suppl), 163-195
12. Nicholis, P. (1993) The steady state behaviour of cytochrome c oxidase in proteoliposomes. FEBS Lett. 327, 194-198
13. Beard, D. A. (2005) A biophysical model of the mitochondrial respiratory system and oxidative phosphorylation. PLoS Comput. Biol. 1, e36
14. Korzeniewski, B. and Zoladz, J. A. (2001) A model of oxidative phosphorylation in mammalian skeletal muscle. Biophys. Chem. 92, 17-34
15. Banaji. M., Mallet, A., Elwell, C. E., Nicholls, P. and Cooper, C. E. (2008) A model of brain circulation and metabolism: NIRS signal changes during physiological challenges. PLoS Comput. Biol. 4, e1000212
16. Yonetani, T (1960) Studies on cytochrome oxidase. 1. Absolute and difference absorption spectra. J. Biol. Chem 235, 845-852
17. Fylstra, D., Lasdon, L., Watson, J, and Waren, A. (1998) Design and use of the Microsoft Excel Solver. Interfaces 28, 29-55
18. Moody, A. J. (1996) 'As prepared' forms of fully oxidised haem/Cu teminal oxidases. Biochim. Biophys. Acta 1276, 6-20
19. Wikström, M. and Morgan, J. E. (11992) The dioxygen cycle. Spectral, kinetic, and thermodynamic characteristics of ferryl and peroxy intermediates observed by reversal of the cytochrome oxidase reaction. J. Biol. Chem. 267, 10266-10273
20. Wrigglesworth, J. M. (1984) Formation and reduction of a 'peroxy' intermediate of cytochrome c oxidase by hydrogen peroxide. Biochem. J. 217, 715-719
21. Giuffre, A., Barone, M. C., Mastronicola, D., D'Itri, E., Sarti, P. and Brunori, M. (2000) Reaction of nitric oxide with the turnover intermediates of cytochrome c oxidase: reaction pathway and functional effects. Biochemistry 39, 15446-15453
22. + with heme A in cytochrome oxidase. J. Bioenerg. Biomembr. 12, 325-338
23. Moody, A. J. (1991) Ligation and electronation states of cytochrome-c oxidase in relation to other oxidases and peroxidases. Biochem. Soc. Trans. 19, 617-622
24. Brunori, M., Giuffre, A. and Sarti, P. (2005) Cytochrome c oxidase, ligands and electrons. J. Inorg. Biochern. 99, 324-336
25. Hill, B. C. (1991) The reaction of the electrostatic cytochrome c-cytochrome oxidase complex with oxygen. J. Biol. Chem. 266, 2219-2226
26. Zaslavsky, D., Sadoski, R. C., Wang, K., Durham, B., Gennis, R. B. and Millett, F. (1998) Single electron reduction of cytochrome c oxidase compound F: resolution of partial steps by transient spectroscopy. Biochemistry 37, 14910-14916
27. Belevich, I., Bloch, D. A., Belevich, N., Wilkstrom, M. and Verkhovsky, M. I. (2007) Exploring the proton pump mechanism of cytochrome c oxidase in real time. Proc. Natl. Acad. Sci. U.S.A. 104, 2685-2690
28. Brand, S. E., Rajagukguk, S., Ganesan, K., Goren, L., Fabian, M., Han, D., Gennis, R. B., Durham, B. and Millett, F. (2007) A new ruthenium complex to study single-electron reduction of the pulsed O(H) state of detergent-solubilized cytochrome oxidase. Biochemistry 46, 14610-14618
29. Jancura, D., Antalik, M., Berka, V., Palmer, G. and Fabian, M. (2006) Filling the catalytic site of cytochrome c oxidase with electrons. Reduced CuB facilitates internal electron transfer to heme a3. J. Biol. Chem. 281, 20003-20010
30. Mitchell, R., Mitchell, P. and Rich, P. R. (1991) The assignment of the 655 nm spectral band of cytochrome oxidase. FEBS Lett. 280, 321-324
31. a Erratum (1991) FEBS Lett. 282, 449
32. Wharton, D. C. and Tzagoloff, A. (1964) Studies on the electron transfer system. LVII. The near infrared absorption band of cytochrome oxidase. J. Biol. Chem. 239, 2036-2040
33. Nicholls, P. and Chanady, G. A. (1982) Titration and steady state behaviour of the 830 nm chromophore in cytochrome c oxidase. Biochem. J. 203, 541-549
34. Thömström, P.-E., Brzezinski, P., Frederikson, P.-O. and Malmström, B. G. (1988) Cytochrome c oxidase as an electron-transort-driven proton pump: pH dependence of the reduction levels of the redox centres; during turnover. Biochemistry 27, 5441-5447
35. Ingledew, W. J., Bacon, M. and Rich, P. R. (1992) Characterisation of a near infra-red absorption band of the Escherichia coli quinol oxidase, cytochrome o, which is attributable to the high-spin ferrous haem of the binuclear site. FEBS Lett. 305, 167-170
36. Slutter, C. E., Sanders, D., Wittung, P., Malmstrom, B. G., Aasa, R., Richards, J. H., Gray, H. B. and Fee, J. A. (1996) Water-soluble, recombinant CuA-domain of the cytochrome ba3 subunit II from Thermus thermophilus. Biochemistry 35, 3387-3395
37. Blair, D. F., Ellis, Jr, W. R., Wang, H., Gray, H. B. and Chan, S. I. (1986) Spectroelectrochemical study of cytochrome c oxidase: pH and temperature dependences of the cytochrome potentials. Characterization of site-site interactions. J. Biol. Chem. 261, 11524-11537
38. Moody, A. J. and Rich, P. R. (1990) The effect of pH on redox titrations of haem a in cyanide-liganded cytochrome-c oxidase: experimental and modelling studies. Biochim. Biophys. Acta 1015, 205-215
39. Nicholls, P. and Wrigglesworth, J. M. (1988) Routes of cytochrome a3 reduction. The neoclassical model revisited. Ann. N.Y. Acad. Sci. 550, 59-67
40. Nicholls, P. and Petersen, L. C. (1974) Haem-haem interactions in cytochrome aa3 during the anaerobic-aerobic transition. Biochim. Biophys. Acta 357, 462-467
41. Minnaert, K (1965) Measurement of the equilibrium constant of the reaction between cytochrome c and cytochrome a. Biochim. Biophys. Acta 110, 42-56
42. Wilson, D. F. and Dutton, P. L. (1970) The oxidation-reduction potentials of cytochromes a and a3 in intact rat liver mitochondria. Arch. Biochem. Biophys. 136, 583-585
43. Hinkle, P. and Mitchell, P. (1970) Effect of membrane potential on equilibrium poise between cytochrome a and cytochrome c in rat liver mitochondria. Bioenergetics 1, 45-60
44. Morgan, J. E. and Wikström, M. (1991) Steady-state redox behavior of cytochrome c, cytochrome a, and CuA of cytochrome c oxidase in intact rat liver mitochondria. Biochemistry 30, 948-958
45. Hartzell, C. R. and Beinert, H. (1976) Oxido-reductive titrations of cylochrome c oxidase followed by EPR spectroscopy. Biochim. Biophys. Acta 423, 323-338
46. Wrigglesworth, J. M., Ioannidis, N. and Nicholls, P. (1988) Spectrophotometric characterization of intermediate redox states of cytochrome oxidase. Ann. N.Y. Acad. Sci. 550, 150-160
47. Schroedl, N. A. and Hartzell, C. R. (1977) Oxidative titrations of reduced cytochrome aa3: correlation of midpoint potentials and extinction coefficients observed at three major absorption bands. Biochemistry 16, 4961-4965
48. Farver, O., Einarsdottir, O. and Pecht, I. (2000) Electron transfer rates and equilibrium within cytochrome c oxidase. Eur. J. Biochem. 257, 950-954
49. Pilet, E., Jasaitis, A., Liebl, U. and Vos, M. H. (2004) Electron transfer between hemes in mammalian cytochrome c oxidase. Proc. Natl. Acad. Sci. U.S.A. 101, 16198-16203
50. Liao, G. L. and Palmer, G. (1996) The reduced minus oxidized difference spectra of cytochromes a and a3. BiDchim. Biophys. Acta 1274, 109-111
51. Fabian, M. and Palmer, G. (11995) The interaction of cytochrome oxidase with hydrogen peroxide: the relationship of compounds P and F. Biochemistry 34, 13802-13810