Elevated proton leak of the intermediate OH in cytochrome c oxidase

Biophysical Journal

Volumn 96, Issue 11, 2009, Pages 4733-4742

  Bloch, Dmitry A ^a   Jasaitis, Audrius ^a,b   Verkhovsky, Michael I ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; CYTOCHROME C OXIDASE; BACTERIAL PROTEIN; PROTEOLIPID; PROTEOLIPOSOMES; PROTON;

ARTICLE; CONDUCTANCE; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME KINETICS; NONHUMAN; OXIDATION; PARACOCCUS DENITRIFICANS; PROTEOLIPOSOME; PROTON TRANSPORT; SITE DIRECTED MUTAGENESIS; ALGORITHM; ANIMAL; ARTIFICIAL MEMBRANE; CATTLE; CHEMISTRY; ELECTRON; GENETICS; HEART MITOCHONDRION; KINETICS; MITOCHONDRIAL MEMBRANE POTENTIAL; OXIDATION REDUCTION REACTION;

BOVINAE; PARACOCCUS DENITRIFICANS;

ALGORITHMS; ANIMALS; BACTERIAL PROTEINS; CATTLE; ELECTRON TRANSPORT COMPLEX IV; ELECTRONS; KINETICS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MEMBRANES, ARTIFICIAL; MITOCHONDRIA, HEART; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; PARACOCCUS DENITRIFICANS; PROTEOLIPIDS; PROTONS;

EID: 68949103649     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.03.006     Document Type: Article

References (39)

1. Mitchell, P. 1961. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature. 191:144-148.
2. Mitchell, P. 1976. Possible molecular mechanisms of the proton motive function of cytochrome systems. J. Theor. Biol. 62:327-367.
3. Wikström, M. K. 1977. Proton pump coupled to cytochrome c oxidase in mitochondria. Nature. 266:271-273.
4. Babcock, G. T., and M. Wikström. 1992. Oxygen activation and the conservation of energy in cell respiration. Nature. 356:301-309.
5. Belevich, I., and M. I. Verkhovsky. 2008. Molecular mechanism of proton translocation by cytochrome c oxidase. Antioxid. Redox Signal. 10:1-29.
6. Verkhovsky, M. I., A. Jasaitis, M. L. Verkhovskaya, J. E. Morgan, and M. Wikström. 1999. Proton translocation by cytochrome c oxidase. Nature. 400:480-483.
7. Bloch, D., I. Belevich, A. Jasaitis, C. Ribacka, A. Puustinen, et al. 2004. The catalytic cycle of cytochrome c oxidase is not the sum of its two halves. Proc. Natl. Acad. Sci. USA. 101:529-533.
8. Verkhovsky, M. I., I. Belevich, D. A. Bloch, and M. Wikström. 2006. Elementary steps of proton translocation in the catalytic cycle of cytochrome oxidase. Biochim. Biophys. Acta. 1757:401-407.
9. Wikström, M., and M. I. Verkhovsky. 2007. Mechanism and energetics of proton translocation by the respiratory heme-copper oxidases. Biochim. Biophys. Acta. 1767:1200-1214.
10. Drachev, L. A., A. A. Jasaitis, A. D. Kaulen, A. A. Kondrashin, E. A. Liberman, et al. 1974. Direct measurement of electric current generation by cytochrome oxidase, H+-ATPase and bacteriorhodopsin. Nature. 249:321-324.
11. Drachev, L. A., A. D. Kaulen, A. Y. Semenov, I. I. Severina, and V. P. Skulachev. 1979. Lipid-impregnated filters as a tool for studying the electric current-generating proteins. Anal. Biochem. 96:250-262.
12. Verkhovsky,M. I., J. E. Morgan, M. L. Verkhovskaya, and M. Wikström. 1997. Translocation of electrical charge during a single turnover of cytochrome c oxidase. Biochim. Biophys. Acta. 1318:6-10.
13. Jasaitis, A., M. I. Verkhovsky, J. E. Morgan, M. L. Verkhovskaya, and M. Wikström. 1999. Assignment and charge translocation stoichiometries of the major electrogenic phases in the reaction of cytochrome c oxidase with dioxygen. Biochemistry. 38:2697-2706.
14. Chernomordik, L., M. M. Kozlov, and J. Zimmerberg. 1995. Lipids in biological membrane fusion. J. Membr. Biol. 146:1-14.
15. Stegmann, T., J. Teissie, and M. Winterhalter. 2001. Fusion and rupture of lipid model membranes. In Lipid Bilayers: Structure and Interactions. J. Katsaras and T. Gutberlet, editors. Springer-Verlag, Berlin, pp. 265-287.
16. Hendler, R. W., L. A. Drachev, S. Bose, and M. K. Joshi. 2000. On the kinetics of voltage formation in purple membranes of Halobacterium salinarum. Eur. J. Biochem. 267:5879-5890.
17. Schönfeld, M., M. Montal, and G. Feher. 1979. Functional reconstitution of photosynthetic reaction centers in planar lipid bilayers. Proc. Natl. Acad. Sci. USA. 76:6351-6355.
18. Gopher, A., Y. Blatt, M. Schönfeld, M. Y. Okamura, G. Feher, et al. 1985. The effect of an applied electric field on the charge recombination kinetics in reaction centers reconstituted in planar lipid bilayers. Biophys. J. 48:311-320.
19. 2 and its reduction are both retarded by replacement of valine 279 by isoleucine in cytochrome c oxidase from Paracoccus denitrificans. Biochemistry. 39:6365-6372.
20. Hartzell, C. R., and H. Beinert. 1974. Components of cytochrome c oxidase detectable by EPR spectroscopy. Biochim. Biophys. Acta. 368:318-338.
21. 3 from Paracoccus denitrificans. Biochemistry. 38:10670-10677.
22. Ribacka, C., M. I. Verkhovsky, I. Belevich, D. A. Bloch, A. Puustinen, et al. 2005. An elementary reaction step of the proton pump is revealed by mutation of tryptophan-164 to phenylalanine in cytochrome c oxidase from Paracoccus denitrificans. Biochemistry. 44:16502-16512.
23. Rigaud, J. L., B. Pitard, and D. Levy. 1995. Reconstitution of membrane proteins into liposomes: application to energy-transducing membrane proteins. Biochim. Biophys. Acta. 1231:223-246.
24. Belevich, I., A. Tuukkanen, M. Wikström, and M. I. Verkhovsky. 2006. Proton-coupled electron equilibrium in soluble and membrane-bound cytochrome c oxidase from Paracoccus denitrificans. Biochemistry. 45:4000-4006.
25. Orii, Y. 1984. Formation and decay of the primary oxygen compound of cytochrome oxidase at room temperature as observed by stopped flow, laser flash photolysis and rapid scanning. J. Biol. Chem. 259:7187-7190.
26. Orii, Y. 1988. Intermediates in the reaction of reduced cytochrome oxidase with dioxygen. Ann. N.Y. Acad. Sci. 550:105-117.
27. Gibson, Q. H., and C. Greenwood. 1963. Reactions of cytochrome oxidase with oxygen and carbon monoxide. Biochem. J. 86:541-544.
28. Iwata, S., C. Ostermeier, B. Ludwig, and H. Michel. 1995. Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature. 376:660-669.
29. Tsukihara, T., H. Aoyama, E. Yamashita, T. Tomizaki, H. Yamaguchi, et al. 1995. Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å . Science. 269:1069-1074.
30. Konstantinov, A. A., S. Siletsky, D. Mitchell, A. Kaulen, and R. B.Gennis. 1997. The roles of the two proton input channels in cytochrome c oxidase from Rhodobacter sphaeroides probed by the effects of site-directedmutations on time-resolved electrogenic intraprotein proton transfer. Proc. Natl. Acad. Sci. USA. 94:9085-9090.
31. Wikström, M.,A. Jasaitis, C. Backgren, A. Puustinen, and M.I.Verkhovsky. 2000. The role of the D- and K-pathways of proton transfer in the function of the haem-copper oxidases. Biochim. Biophys. Acta. 1459:514-520.
32. Thomas, J. W., A. Puustinen, J. O. Alben, R. B.Gennis, and M.Wikström. 1993. Substitution of asparagine for aspartate-135 in subunit I of the cytochrome bo ubiquinol oxidase of Escherichia coli eliminates proton-pumping activity. Biochemistry. 32:10923-10928.
33. Gorbikova, E. A., N. P. Belevich, M. Wikström, and M. I. Verkhovsky. 2007. Time-resolved ATR-FTIR spectroscopy of the oxygen reaction in the D124N mutant of cytochrome c oxidase from Paracoccus denitrificans. Biochemistry. 46:13141-3148.
34. Cvetkov, T. L., and L. J. Prochaska. 2007. Biophysical and biochemical characterization of reconstituted and purified Rhodobacter sphaeroides cytochrome c oxidase in phospholipid vesicles sheds insight into its functional oligomeric structure. Protein Expr. Purif. 56:189-196.
35. Zaslavsky, D., A. D. Kaulen, I. A. Smirnova, T. Vygodina, and A. A. Konstantinov. 1993. Flash-induced membrane potential generation by cytochrome c oxidase. FEBS Lett. 336:389-393.
36. Ruitenberg, M., A. Kannt, E. Bamberg, B. Ludwig, H. Michel, et al. 2000. Single-electron reduction of the oxidized state is coupled to proton uptake via the K pathway in Paracoccus denitrificans cytochrome c oxidase. Proc. Natl. Acad. Sci. USA. 97:4632-4636.
37. Verkhovsky, M. I., A. Tuukkanen, C. Backgren, A. Puustinen, and M. Wikström. 2001. Charge translocation coupled to electron injection into oxidized cytochrome c oxidase from Paracoccus denitrificans. Biochemistry. 40:7077-7083.
38. Ädelroth, P., R. B. Gennis, and P. Brzezinski. 1998. Role of the pathway through K(I-362) in proton transfer in cytochrome c oxidase from. R. sphaeroides. Biochemistry. 37:2470-2476.
39. Kaila, V. R., M. I. Verkhovsky, G. Hummer, and M. Wikström. 2008. Glutamic acid 242 is a valve in the proton pump of cytochrome c oxidase. Proc. Natl. Acad. Sci. USA. 105:6255-6259.