Structural features of cytochrome oxidase | Quarterly Reviews of Biophysics | Cambridge Core (original) (raw)

Extract

This article tries to be a compact summary of some recent research on cytochrome c oxidase (EC 1.9.3.1), an important enzyme in membrane bioenergetics. Cytochrome oxidase is the terminal catalyst of the mitochondrial respiratory chain. It uses the electrons flowing through the chain to reduce oxygen molecules to water. Four electrons and four protons are consumed in the reduction of O2 to two molecules of water (Fig. 1). Cytochrome oxidase contains four redoxactive metal centres. Two of these are copper atoms, two haem A groups. These four centres are employed in the dioxygen-binding site and in the electron-transferring pathways from cytochrome c. The enzyme is also called cytochrome _aa_3, because the protein-bound haems are functionally and spectroscopically different.

References

Anderson, S., Bankier, A. T., Barrell, B. G., De Bruijn, M. H. L., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., Schreier, P. H., Smith, A. J. H., Staden, R. & Young, I. G. (1981). Sequence and organization of the human mitochondrial genome. Nature 290, 457–465.CrossRefGoogle ScholarPubMed

Anderson, S., De Bruijn, M. H. L., Coulson, A. R., Eperon, I. C., Sanger, F. & Young, I. G. (1982). Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J. Mol. Biol. 156, 683–717.CrossRefGoogle ScholarPubMed

AnemüLler, S. & SchäFer, G. (1989). Cytochrome aa 3 from the thermoacidophilic archaebacterium Sulfolobus acidocaldarius. FEBS Lett. 244, 451–455.CrossRefGoogle Scholar

Anraku, Y. & Gennis, R. B. (1987). The aerobic respiratory chain of Escherichia coli. Trends Biochem. Sci. 12, 262–266.CrossRefGoogle Scholar

Au, D. C.-T. & Gennis, R. B. (1987). Cloning of the cyo locus encoding the cytochrome o terminal oxidase complex of Escherichia coli. J. Bacterial. 169, 3237–3242.CrossRefGoogle ScholarPubMed

Babcock, G. T. (1988). Raman scattering by cytochrome oxidase and by heme a model compounds. In Biological Applications of Raman Spectroscopy (ed. Spiro, T. G.), pp. 293–346. New York: Wiley.Google Scholar

Babcock, G. T. & Callahan, P. M. (1983). Redox-linked hydrogen bond Strength changes in cytochrome a: implications for a cytochrome oxidase proton pump. Biochemistry 22, 2314–2319.CrossRefGoogle ScholarPubMed

Babcock, G. T., Callahan, P. M., Ondrias, M. R. & Salmeen, I. (1981). Coordination geometries and vibrational properties of cytochromes a and a 3 in cytochrome oxidase from Soret excitation Raman spectroscopy. Biochemistry 20, 959–966.CrossRefGoogle Scholar

Bisson, R. & Schiavo, G. (1987). Two different forms of cytochrome c oxidase can be purified from the slime mold Dictyostelium discoideum. J. Biol. Chem. 261, 4373–4376.CrossRefGoogle Scholar

Bisson, R. & Schiavo, G. (1989). Slime mold cytochrome c oxidase. An example of environmental influence on subunit composition of a eukaryotic oxidase. Ann. N. Y. Acad. Sci. 550, 325–336.CrossRefGoogle Scholar

Bisson, R., Steffens, G. C. M. & Buse, G. (1982 a). Localization of lipid binding domains on subunit II of beef heart cytochrome c oxidase. J. Biol. Chem. 257, 6716–6720.CrossRefGoogle ScholarPubMed

Bisson, R., Steffens, G. C. M., Capaldi, R. A. & Buse, G. (1982 b). Mapping of the cytochrome c binding site on cytochrome c oxidase. FEBS Lett. 144, 359–363.CrossRefGoogle ScholarPubMed

Boenen, L., Boer, P. H. & Gray, M. W. (1984). The wheat cytochrome oxidase subunit II gene has an intron insert and three radical amino acid changes relative to maize. EMBO J. 3, 2531–2536.CrossRefGoogle Scholar

Bolgiano, B., Smith, L. & Davies, H. C. (1988). Kinetics of the interaction of the cytochrome c oxidase of Paracoccus denitrificans with its own and bovine cytochrome c. Biochim. Biophys. Acta 933, 341–350.CrossRefGoogle ScholarPubMed

Bonitz, S. G., Coruzzi, G., Thalenfeld, B. E., Tzagoloff, A. & Macino, G. (1980). Assembly of the mitochondrial membrane system. Structure and nucleotide sequence of the gene coding for subunit I of yeast cytochrome oxidase. J. Biol. Chem. 255, 11927–11941.CrossRefGoogle Scholar

Brunori, M., Antonini, G., Malatesta, F., Sarti, P. & Wilson, M. T. (1987). Cytochrome c. oxidase: subunit structure and proton pumping. Eur. J. Biochem. 169, 1–8.CrossRefGoogle ScholarPubMed

Buse, G., Steppens, G. C. M. & Meinecke, L. (1983). Cytochrome oxidase: the primary structure of electron and proton translocating subunits and their hints at mechanisms. In Structure and Function of Membrane Proteins (ed. Quaqliariello, E. and Palmieri, F.), pp. 131–138. Amsterdam: Elsevier.Google Scholar

Buse, G., Hensel, S. & Fee, J. D. (1989). Evidence for cytochrome oxidase subunit I and a cytochrome c_-subunit II fused protein in the cytochrome ‘_c 1_aa_ 3’ of Thermus thermophilus. How old is cytochrome oxidase? Eur. J. Biochem. 181, 261–268.CrossRefGoogle Scholar

Callahan, P. M. & Babcock, G. T. (1983). Origin of the cytochrome a absorption red shift: pH-dependent interaction between its heme a formyl and protein in cytochrome oxidase. Biochemistry 22, 452–461.CrossRefGoogle ScholarPubMed

Cantatore, P., Roberti, M., Rainaldi, G., Gadaleta, M. N. & Saccone, C. (1989). The complete nucleotide sequence, gene organization, and genetic code of the mitochondrial genome of Paracentrotus lividus. J. Biol. Chem. 264, 10965–10975.CrossRefGoogle ScholarPubMed

Capaldi, R. A., Darley-Usmar, V., Fuller, S. & Millett, F. (1982). Structural and functional features of the interaction of cytochrome c with complex III and cytochrome c oxidase. FEBS Lett. 138, 1–7.CrossRefGoogle ScholarPubMed

Capaldi, R. A., Takamiya, S., Zhang, Y.-Z.. (1987). Gonzalez-Halphen, D. & Yanamura, W. Structure of cytochrome c oxidase. Curr. Top. Bioenerg. 15, 91–112.CrossRefGoogle Scholar

Casey, R. P., Thelen, M. & Azzi, A. (1980). Dicyclohexyl-carbodiimide binds specifically and covalently to cytochrome c oxidase while inhibiting its H+-translocating activity. J. Biol. Chem. 255, 3994–4000.CrossRefGoogle Scholar

Chepuri, V., Lemieux, L., Au, D. C.-T. & Gennis, R. A. (1990). The sequence of the cyo operon indicates substantial structural similarities between the cytochrome o ubiquinol oxidase of Escherichia coli and the aa 3-type family of cytochrome c oxidases. J. Biol. Chem. (submitted).CrossRefGoogle Scholar

Chothia, C. & Lesk, A. M. (1982). Evolution of proteins formed by beta-sheets. I. Plastocyanin and azurin. J. Mol. Biol. 160, 309–323.CrossRefGoogle ScholarPubMed

Chothia, C. & Lesk, A. M. (1986). The relation between the divergence of sequence and structure in proteins. EMBO J. 5, 823–826.CrossRefGoogle ScholarPubMed

Clary, D. O. & Wolstenholme, D. R. (1983). Nucleotide sequence of a segment of Drosophila mitochondrial DNA that contains the genes for cytochrome c oxidase subunits II and III and ATPase subunit 6. Nucl. Acids Res. ii, 4211–4227.CrossRefGoogle Scholar

Cumsky, M. G. C., Ko, C., Trueblood, C. E. & Poyton, R. O. (1985). Two nonidentical forms of subunit V are functional in yeast cytochrome c oxidase. Proc. Natn Acad. Sci. USA 82, 2235–2239.CrossRefGoogle ScholarPubMed

Deatherage, J. F., Henderson, R. & Capaldi, R. A. (1982). Three-dimensional structure of cytochrome c oxidase vesicle crystals in negative strain. J. Mol. Biol. 158, 487–499.CrossRefGoogle Scholar

De Bruijn, M. H. L. (1983). Drosophila melanogaster mitochondrial DNA, a novel organization and genetic code. Nature 304, 234–241.CrossRefGoogle ScholarPubMed

Deisenhofer, J. & Michel, H. (1989). The photosynthetic reaction from the purple bacterium Rhodopseudomonas viridis. EMBO J. 8, 2149–2170.CrossRefGoogle ScholarPubMed

De Vrij, W., Heyne, R. I. & Konings, W. N. (1989). Characterization and application of a thermostable primary transport system: Cytochrome c oxidase from Bacillus stearothermophilus. Eur. J. Biochem. 178, 763–770.CrossRefGoogle ScholarPubMed

Einarsdottir, O., Choc, M. G., Weldon, S. & Caughey, W. S. (1988). The site and mechanism of dioxygen reduction in bovine heart cytochrome c oxidase. J. Biol. Chem. 263, 13641–13654.CrossRefGoogle ScholarPubMed

Eisenberg, D. (1984). Three-dimensional structure of membrane and surface proteins. Ann. Rev. Biochem. 53, 595–623.CrossRefGoogle ScholarPubMed

Engelman, D. M. & Steitz, T. A. (1981). The spontaneous insertion of proteins into and across the mebranes: the helical hairpin hypothesis. Cell 23, 411–422.CrossRefGoogle Scholar

Feagin, J. E., Abraham, J. M. & Stuart, K. (1988). Extensive editing of the cytochrome c oxidase III transcript in Trypanosoma brucei. Cell 53, 413–422.CrossRefGoogle ScholarPubMed

Fee, J. A., Kuila, D., Mather, M. W. & Yoshida, T. (1986). Respiratory proteins from extremely thermophilic, aerobic bacteria. Biochim. Biophys. Acta 853, 153–185.CrossRefGoogle ScholarPubMed

Fee, J. A., Mather, M. W., Springer, P., Hensel, S. & Buse, G. (1989). Isolation and partial sequence of the A protein gene of Thermits thermophilus cytochrome c 1_aa_ 3. Ann. N. Y. Acad. Sci. 550, 33–38.CrossRefGoogle Scholar

Finel, M. (1988). Proteolysis of Paracoccus denitrificans cytochrome oxidase by trypsin and chymotrypsin. FEBS Lett. 236, 415–419.CrossRefGoogle ScholarPubMed

Finel, M. (1989). Oligomeric structure and subunit requirement of proton-translocating cytochrome oxidase. PhD thesis, University of Helsinki.Google Scholar

Finel, M. & Wikström, M. (1988). Monomerization of cytochrome oxidase may be essential for the removal of subunit III. Eur.J. Biochem. 176, 125–129.CrossRefGoogle ScholarPubMed

Finel, M., Haltia, T., Puustinen, A., Saraste, M. & Wikström, M. (1990). Comparison of structure and function of cytochrome aa 3 and o. In Structure, Function and Biogenesis of Energy Transfer Systems (ed. Quagliariello, E. et al. ). Amsterdam: Eisevier (in the press).Google Scholar

Fox, T. D. (1979). Five TGA “stop” codons occur within the translated sequence of the yeast mitochondrial gene for cytochrome c oxidase subunit II. Proc. Natn. Acad. Sci. USA 76, 6534–6538.CrossRefGoogle ScholarPubMed

Fox, T. D. & Leaver, C. J. (1981). The Zea mays mitochondrial gene coding cytochrome oxidase subunit II has an intervening sequence and does not contain TGA codons. Cell 26, 315–323.CrossRefGoogle Scholar

Frey, T. G., Chan, S. H. P. & Schatz, G. (1978). Structure and orientation of cytochrome c oxidase in crystalline membranes. J. Biol. Chem. 253, 4389–4395.CrossRefGoogle ScholarPubMed

Fuller, S. D., Capaldi, R. A. & Henderson, R. (1979). Structure of cytochrome c oxidase in deoxycholate-derived two-dimensional crystals. J. Mol. Biol. 134, 305–327.CrossRefGoogle ScholarPubMed

Fuller, S. D., Darley-Usmar, V. M. & Capaldi, R. A. (1981). Covalent complex between yeast cytochrome c and beef heart cytochrome c oxidase which is active in electron transfer. Biochemistry 20, 7046–7053.CrossRefGoogle ScholarPubMed

Gelles, J. & Chan, S. I. (1985). Chemical modification of the CuA center in cytochrome c oxidase by sodium p-(hydroxy-mercuri)benzoate. Biochemistry 24, 3963–3972.CrossRefGoogle Scholar

Gennis, R. B. (1989). Biomembranes. Molecular Structure and Function. New York: Springer.CrossRefGoogle Scholar

Georgiou, C. D., Cokic, P., Carter, K., Webster, D. A. & Gennis, R. B. (1988). Relationships between membrane-bound cytochrome o from Vitreoscilla and that of Escherichia coli. Biochim. Biophys. Acta 933, 179–183.CrossRefGoogle ScholarPubMed

Greenwood, C., Thomson, A. J., Barrett, C. P., Peterson, J., George, G. N., Fee, J. A. & Reichardt, J. (1989). Some spectroscopie views of the CuA site in cytochrome c oxidase preparations. Ann. N. Y. Acad. Sci. 550, 47–52.CrossRefGoogle Scholar

Gregory, L. C. & Ferguson-Miller, S. (1988). Effect of subunit III removal on control of cytochrome c oxidase activity by pH. Biochemistry 27, 6307–6314.CrossRefGoogle ScholarPubMed

Gray, H. B. & Malmström, B. G. (1989). Long-range electron transfer in multisite metalloproteins. Biochemistry 28, 7499–7505.CrossRefGoogle ScholarPubMed

Haltia, T., Puustinen, A. & Finel, M. (1988). The Paracoccus denitrificans cytochrome aa 3 has a third subunit. Eur. J. Biochem. 172, 543–546.CrossRefGoogle Scholar

Haltia, T., Finel, M., Harms, N., Nakari, T., Raitio, M., WikströM, M. & Saraste, M. (1989). Deletion of the gene for subunit III leads to defective assembly of bacterial cytochrome oxidase. EMBO J. 8, 3571–3579.CrossRefGoogle ScholarPubMed

Henderson, R., Capaldi, R. A. & Leigh, J. S. (1977). Arrangement of cytochrome oxidase molecules in two-dimensional vesicle crystals. J. Mol. Biol, 122, 631–648.CrossRefGoogle Scholar

Hiesel, R., Schobel, W., Schuster, W. & Brennicke, A. (1987). The cytochrome oxidase subunit I and subunit III genes in Oenothera mitochondria are transcribed from identical promoter sequences. EMBO J. 6, 29–34.CrossRefGoogle ScholarPubMed

Holm, L., Saraste, M. & Wikström, M. (1987). Structural models for redox centres in cytochrome oxidase. EMBO J. 6, 2819–2823.CrossRefGoogle ScholarPubMed

Jacobs, H. T., Elliot, D. J., Math, V. B. & Farquharson, A. (1988). Nucleotide sequence and gene organization of sea urchin mitochondrial DNA. J. Mol. Biol. 202, 185–217.CrossRefGoogle ScholarPubMed

Kadenbach, B., Kuhn-Nentwig, L. & Büge, U. (1987). Evolution of a regulatory enzyme: cytochrome c oxidase (Complex IV). Curr. Top. Bioenerg. 15, 113–161.CrossRefGoogle Scholar

Karlsson, B. G., Aasa, R., MalmströM, B. G. & Lundberg, L. G. (1989). Rack-induced bounding in blue copper proteins: spectroscopie properties and reduction potential of the azurin mutant Met-121 → Leu. FEBS Lett. 253, 99–102.CrossRefGoogle Scholar

Krab, K. & WikströM, M. (1987). Principles of coupling between electron transfer and proton translocation with special reference to proton-translocating mechanisms in cytochrome oxidase. Biochim. Biophys. Acta 895, 25–39.CrossRefGoogle Scholar

Kroneck, P. M. H., Antholine, W. A., Riester, J. & Zumft, W. G. (1988). The cupric site in nitrous oxide reductase contains a mixed-valence <Cu(II), Cu(I)> binuclear center: a multi-frequency electron paramagnetic resonance investigation. FEBS Lett. 242, 70–74.CrossRefGoogle Scholar

Kyte, J. & Doolittle, R. F. (1982). A simple method for displaying the hydrophobic character of a protein. J. Mol. Biol. 157, 105–132.CrossRefGoogle Scholar

Li, P. M., Gelles, J., Chan, S. L., Sullivan, R. J. & Scott, R. A. (1987). Extended X-ray absorption fine structure of copper in CuA-depleted, p-(hydroxymercuri)benzoate-modified, and native cytochrome c oxidase. Biochemistry 26, 2091–2095.CrossRefGoogle ScholarPubMed

Ludwig, B. & Schatz, G. (1980). A two-subunit cytochrome c oxidase (cytochrome aa 3) from Paracoccus denitrificans. Proc. Natn. Acad. Sci. USA 77, 196–200.CrossRefGoogle Scholar

Ludwig, B., Downer, N. W. & Capaldi, R. A. (1979). Labeling of cytochrome c oxidase with 35S diazobenzenesulfonate. Orientation of this electron transfer complex in the inner mitochondrial membrane. Biochemistry 18, 1401–1407.CrossRefGoogle ScholarPubMed

Ludwig, B., Grabo, M., Gregor, I., Lustig, A., Regenass, M. & Rosenbusch, J. P. (1982). Solubilized cytochrome c oxidase from Paracoccus denitrificans is a monomer. J. Biol. Chem. 257, 5576–5578.CrossRefGoogle ScholarPubMed

Malmström, B. G. (1989). The mechanism of proton translocation in respiration and photosynthesis. FEBS Lett. 250, 9–21.CrossRefGoogle ScholarPubMed

Matsushita, K., Patel, L. & Kaback, H. R. (1984). Cytochrome o type oxidase from Escherichia coli. Characterization of the enzyme and mechanism of electrochemical proton gradient generation. Biochemistry 23, 4703–4714.CrossRefGoogle ScholarPubMed

Millett, F., De Jong, C., Paulson, L. & Capaldi, R. A. (1983). Identification of specific carboxylate groups in cytochrome c oxidase that are involved in binding cytochrome c. Biochemistry 22, 546–552.CrossRefGoogle ScholarPubMed

Mogi, T., Stern, L. J., Marti, T., Chao, B. H. & Khorana, H. G. (1988). Aspartic acid substitutions affect proton translocation by bacteriorhodopsin. Proc. Natn. Acad. Sci. 85, 4148–4152.CrossRefGoogle ScholarPubMed

Moody, A. J. & Rich, P. R. (1989). The functional catalytic unit involved in proton pumping by rat liver cytochrome c reductase and by cytochrome c oxidase. Biochim. Biophys. Acta 973, 29–34.CrossRefGoogle ScholarPubMed

Mueller, J. P. & Taber, H. W. (1989). Isolation and sequence ctaA, a gene required for cytochrome aa 3 biosynthesis and sporulation in Bacillus subtilis. J. Bacteriol. 171, 4967–4978.CrossRefGoogle ScholarPubMed

MüLler, M., SchläPfer, B. & Azzi, A. (1988). Preparation of a one-subunit cytochrome oxidase from Paracoccus denitrificans: spectral analysis and enzymatic activity. Biochemistry 27, 7546–7551.CrossRefGoogle ScholarPubMed

Nalecz, K., Bolli, R., Ludwig, B. & Azzi, A. (1985). The role of subunit III in bovine cytochrome c oxidase. Comparison between native, subunit III-depleted and Paracoccus denitrificans enzymes. Biochim. Biophys. Acta 808, 259–272.CrossRefGoogle ScholarPubMed

Ohnishi, T., Lobrutto, R., Salerno, J. C., Bruckner, R. C. & Frey, T. G. (1982). Spatial relationship between cytochrome a and a 3. J. Biol. Chem. 257, 14821–14825.CrossRefGoogle Scholar

Penttilä, T. (1983). Properties and reconstitution ora cytochrome oxidase deficient in subunit III. Eur.J. Biochem. 133, 355–361.CrossRefGoogle Scholar

Poole, R. K. & Ingledew, W. J. (1987). Pathways of electrons to oxygen. In Escherichia coli and Salmonella typhimurium Molecular and Cellular Biology, vol. 1 (ed. Neidhart, F. C. et al. ), pp. 170–200. Washington, D.C.: American Society for Microbiology.Google Scholar

Power, S. D., Lochrie, M. A., Sevarino, K. A., Patterson, T. E. & Poyton, R. O. (1984). The nuclear-coded subunits of yeast cytochrome oxidase. I. Fractionation of the holoenzyme into chemically pure polypeptides and the identification of two new subunits using solvent extraction and reversed phase high performance liquid chromatography. J. Biol. Chem. 259, 6564–6570.CrossRefGoogle ScholarPubMed

Prochaska, L. J., Bisson, R., Capaldi, R. A., Steffens, G. C. M. & Buse, G. (1981). Inhibition of cytochrome c oxidation function by dicyclohexylcarbodiimide. Biochim. Biophys. Acta 637, 360–373.CrossRefGoogle Scholar

Puustinen, A., Finel, M., Virkki, M. & WikströM, M. (1989). Cytochrome o (bo) is a proton pump in Paracoccus dentrificans and Escherichia coli. FEBS Lett. 249, 163–167.CrossRefGoogle Scholar

Püttner, I., Carafoli, E. & Malatesta, F. (1985). Spectroscopie and functional properties of subunit III-depleted cytochrome oxidase. J. Biol. Chem. 260, 3719–3723.CrossRefGoogle Scholar

Raitio, M., Jalli, T. & Saraste, M. (1987). Isolation and analysis of the genes for cytochrome c oxidase in Paracoccus denitrificans. EMBO J. 6, 2825–2833.CrossRefGoogle ScholarPubMed

Raitio, M., Pispa, J., Metso, T. & Saraste, M. (1990). Are there isoenzymes of cytochrome c oxidase in Paracoccus denitrificans? FEBS Lett, (in press).CrossRefGoogle Scholar

Rich, P. R., West, I. C. & Mitchell, P. (1988). The location of CuA in mammalian cytochrome c oxidase. FEBS lett. 233, 25–30.CrossRefGoogle ScholarPubMed

Robinson, N. C. & Capaldi, R. A. (1977). Interaction of detergents with cytochrome oxidase. Biochemistry 16, 375–381.CrossRefGoogle Scholar

Robinson, N. C. & Talbert, L. (1986). Triton X-100 induced dissociation of beef heart cytochrome c oxidase into monomers. Biochemistry 25, 2328–2335.CrossRefGoogle ScholarPubMed

Roe, B. A., Ma, D.-P., Wilson, R. K. & Wong, J. F.-H. (1985). The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J. Biol. Chem. 260, 9759–9774.CrossRefGoogle ScholarPubMed

Salerno, J. C., Bolgiano, B. & Ingledew, W. J. (1989). Potentiometric titration of cytochrome bo type quinol oxidase of Escherichia coli: evidence for heme–heme and copper–heme interaction. FEES Lett. 247, 101–105.CrossRefGoogle ScholarPubMed

Saraste, M., Penttilä, T. & WikströM, M. (1981). Quaternary structure of bovine cytochrome oxidase. Eur. J. Biochem. 115, 261–268.CrossRefGoogle ScholarPubMed

Saraste, M., Raitio, M., Jalli, T., Chepuri, V., Lemieux, L. & Gennis, R. B. (1989). Cytochrome o from Escherichia coli is structurally related to cytochrome aa 3. Ann. N.Y. Acad. Sci. 550, 314–324.CrossRefGoogle Scholar

Saraste, M., Metso, T., Lauraeus, M., Nakari, T. & Jalli, T. (1990). Nucleotide sequence of cta operon coding for the Bacillus subtilis cytochrome oxidase (in preparation).CrossRefGoogle Scholar

Scott, R. A., Schwartz, J. R. & Cramer, S. P. (1986). Structural aspects of the copper sites in cytochrome c oxidase. An X-ray absorption spectroscopic investigation of the resting-state enzyme. Biochemistry 25, 5546–5555.CrossRefGoogle ScholarPubMed

Scott, R. A., Li, P. M. & Chan, S. I. (1989). The binuclear site of cytochrome c oxidase. Structural evidence from iron X-ray absorption spectroscopy. Ann. N. Y. Acad. Sci. 550, 53–58.CrossRefGoogle Scholar

Sone, N. & Yanagita, Y. (1982). A cytochrome aa 3-type terminal oxidase of a thermophilic bacterium. Purification, properties and proton pumping. Biochim. Biophys. Acta 682, 216–226.CrossRefGoogle Scholar

Sone, N., Yokoi, F., Fu, T., Ohta, S., Metso, T., Raitio, M. & Saraste, M. (1988). Nucleotide sequence of the gene coding for cytochrome oxidase subunit I from the thermophilic bacterium. PS3. J. Biochem. 103, 606–610.CrossRefGoogle ScholarPubMed

Sone, N., Shimada, S., Ohmori, T., Souma, Y., Gonda, M. & Ishizuka, M. (1990 a). A fourth subunit is present in cytochrome c oxidase from the thermophilic bacterium PS 3. FEES Lett., in press.CrossRefGoogle Scholar

Steffens, G. J. & Buse, G. (1979). Studies on cytochrome c oxidase, IV. Primary structure and function of subunit II. Hoppe-Seyler's Z. Physiol. Chem. 360, 613–619.Google ScholarPubMed

Steinrücke, P., Steffens, G. C., Panskus, G., Buse, G. & Ludwig, B. (1987). Subunit II of cytochrome oxidase from Paracoccus denitrificans. DNA sequence, gene expression and the protein. Eur. J. Biochem. 167, 431–439.CrossRefGoogle ScholarPubMed

Stevens, T. H. & Chan, S. I. (1981). Histidine is the axial ligand to cytochrome a 3 in cytochrome c oxidase. J. Biol. Chem. 256, 1069–1071.CrossRefGoogle Scholar

Stevens, T. H., Martin, C. T., Wang, H., Brudvig, G. W., Scholes, C. P. & Chan, S. I. (1982). The nature of CuA in cytochrome oxidase. J. Biol. Chem. 257, 12106–12113.CrossRefGoogle Scholar

Thalenfeld, B. E. & Tzagoloff, A. (1980). Assembly of the mitochondrial membrane system. Sequence of the oxiz gene of yeast mitochondrial DNA. J. Biol. Chem. 255, 6173–6180.CrossRefGoogle ScholarPubMed

Valpuesta, J. M., Henderson, R. & Frey, T. G. (1990). A cryo-electron microscope analysis of crystalline cytochrome oxidase. J. Mol. Biol. (in the press).Google Scholar

Viebrock, A. & Zumft, W. G. (1988). Molecular cloning, heterologous expression and primary structure of the structural gene for the copper enzyme nitrous oxide reductase from denitrifying Pseudomonas stutzeri. J. Bacterial. 170, 4658–4668.CrossRefGoogle ScholarPubMed

Weiss, M. S., Wacker, T., Nestel, U., Woitzik, D., Weckesser, J., Kreutz, W., Welte, W. & Schultz, G. E. (1989). The structure of porin from Rhodobacter capsulatus at 0·6 nm resolution. FEBS Lett. 256, 143–146.CrossRefGoogle Scholar

Wikström, M. (1988 a). Mechanism of cell respiration. Properties of individual reaction steps in the catalysis of dioxygen reduction by cytochrome oxidase. Chem. Ser. 28A, 71–74.Google Scholar

Wikström, M. (1988 b). Protonic sidedness of the binuclear iron-copper centre in cytochrome oxidase. FEBS Lett. 231, 247–252.CrossRefGoogle ScholarPubMed

Wikström, M. (1989). Identification of the electron transfers in cytochrome oxidase that are coupled to proton-pumping. Nature 338, 776–778.CrossRefGoogle ScholarPubMed

WikströM, M., Krab, K. & Saraste, M. (1981). Cytochrome Oxidase. A Synthesis. London: Academic Press.Google Scholar

Wikström, M., Saraste, M. & Penttilä, T. (1985). Relationship between structure and function in cytochrome oxidase. In The Enzymes of Biological Membranes, vol. 4 (ed. Martonosi, A. N.), pp. 111–148. New York: Plenum.CrossRefGoogle Scholar

Zimmermann, B. H., Nitsche, C., Fee, J. A., Rusnak, F. & Muenck, E. (1988). Properties of a copper-containing cytochrome ba 3: a second terminal oxidase from the extreme thermophile Thermus thermophilus. Proc. Natn. Acad. Sci. USA 85, 5779–5783.CrossRefGoogle ScholarPubMed