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The Structure of Crystalline Bovine Heart Cytochrome c Oxidase

  • Chapter
Frontiers of Cellular Bioenergetics

Abstract

Cytochrome c oxidase, the terminal enzyme in cell respiration, reduces molecular oxygen (O2) to water. The enzyme couples oxygen reduction with the active transport of protons (Ferguson-Miller and Babcock, 1996; Malmström, 1990). Since its discovery (Warburg, 1924), this enzyme has been one of the most extensively investigated systems in bioenergetics, because of its physiological importance. The redox-active centers of the enzyme contain the transition metals, Fe and Cu, and these active-site metals have been the focus of a variety of spectroscopic investigations on the intriguing O2 reduction process (Ferguson-Miller and Babcock, 1996; Malmström, 1990). So far, the enzyme has been isolated from about 80 different organisms, and most of the amino acid sequences from each of these organisms have been determined. Buse and co-workers determined the amino acid sequence of the bovine enzyme, and this pioneering work has been the basis for subsequent structure-function investigations on the enzyme (Hensel and Buse, 1990; Meinecke and Buse, 1986). An ingenious investigation of the subunit composition of the enzyme performed by Kadenback is also a benchmark for the structural characterization of the enzyme (Kadenbach et al., 1983). On the other hand, time-resolved resonance Raman spectroscopy has been a powerful experimental technique for identifying the structure of the intermediate species during the O2 reduction, such as the dioxygen (Fe2+-O2), the ferryl oxide (Fe4+=O), and the hydroxide (Fe3+-OH) intermediates (Ogura et al., 1991; Kitagawa and Ogura, 1997).

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References

  • Anthony, G., Reimann, A., and Kadenbach, B., 1993, Tissue specific regulation of bovine heart cytochrome-c oxidase activity by ADP via interaction with subunit VIa, Proc. Natl. Acad. Sci. USA 90:1652–1656.

    Article  PubMed  CAS  Google Scholar 

  • Antonini, E., Brunori, M., Colosimo, A., Greenwood, C., and Wilson, M. T., 1977, Oxygen “pulsed” cytochrome c oxidase: Functional properties and catalytic relevance, Proc. Natl. Acad. Sci. USA 74:3128–3125.

    Article  PubMed  CAS  Google Scholar 

  • Blair, D. F., Ellis, W. R., Wang, H., Gray, H. B., and Chan, S. I., 1986, Spectroelectrochemical study of cytochrome c oxidase: pH and temperature dependencies of the cytochrome potentials, J. Biol. Chem. 261:11524–11537.

    PubMed  CAS  Google Scholar 

  • Capitanio, N., Capitanio, G., Demarinis, D. A., De Nitto, E., Massari, S., and Papa, S., 1996, Factors affecting the H+/e- stoichiometry in mitochondrial cytochrome c oxidase: Influence of the rate of electron flow and transmembrane ΔpH, Biochemistry 35:10800–10806.

    Article  PubMed  CAS  Google Scholar 

  • Caughey, W. S., 1971, Structur-function relationship in cytochrome c oxidase and other nemo-proteins. Adv. Chem. Ser. 100:248–270.

    Article  Google Scholar 

  • Caughey, W. S., Wallace, W J., Volpe, J. A., and Yoshikawa S., 1976, Cytochrome c oxidase, in: The Enzymes, vol. 13C (R D. Boyer, ed.), pp. 299–344, Academic Press, New York.

    Google Scholar 

  • Chotia, C., Levitt, M., and Richardson, D., 1987, Structure of proteins: Packing of α-helices and pleated sheets, Proc. Natl. Acad. Sci. USA 74:4130–4134.

    Article  Google Scholar 

  • Espe, M. P., Hosler, J. P., Ferguson-Miller, S., Babcock, T., and McCracken, J., 1995, A continuous wave and pulsed EPR characterization of the Mu2+ binding site in Rhodobacter sphaeroides cytochrome c oxidase, Biochemistry 34:7593–7602.

    Article  PubMed  CAS  Google Scholar 

  • Ferguson-Miller, S., and Babcock, G. T., 1996, Heme/copper terminal oxidases, Chem. Rev. 96:2889–2907.

    Article  PubMed  CAS  Google Scholar 

  • Ferguson-Miller, S., Brautigen, D. L., and Margoliash, E., 1976, Correlation of the kinetics of electron transfer activity of various eukaryotic cytochromes with binding to mitochondrial cytochrome c oxidase, J. Biol. Chem. 251:1104–1115.

    PubMed  CAS  Google Scholar 

  • Frank, V., and Kadenbach, B., 1996, Regulation of the H+/e- stoichiometry of cytochrome c oxidase from bovine heart by intermitochondrial ATP/ADP ratios, FEBS Lett. 382:121–124.

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Horsman, J. A., Berry, E., Shapleigh, J. P., Alben, J. O., and Gennis, R. B., 1994, A novel cytochrome c oxidase from Rhodobacter sphaeroides that lacks CuA, Biochemistry 33:3113–3119.

    Article  PubMed  CAS  Google Scholar 

  • Gelles, J., Blair, D. F., and Chan, S. I., 1986, The proton-pumping site of cytochrome c oxidase: A model of its structure and mechanism, Biochim. Biophys. Acta 853:205–236.

    Article  PubMed  CAS  Google Scholar 

  • Gibson, Q. H., and Greenwood, C., 1963, Reactions of cytochrome oxidase with oxygen and carbon monoxide, Biochem. J. 86:54–554.

    Google Scholar 

  • Gibson, Q. H., Greenwood, C., Wharton, D. C., and Palmer, G., 1965, The reaction of cytochrome oxidase with cytochrome c, J. Biol. Chem. 240:888–894.

    PubMed  CAS  Google Scholar 

  • Gray, K. A., Grooms, M., Mylhykallio, H., Moomaw, C., Slaughter, C., and Daldal, F., 1994, Rhodobacter capsulatus contains a novel cb-type cytochrome c oxidase without a CuA center, Biochemistry 33:3120–3127.

    Article  PubMed  CAS  Google Scholar 

  • Han, S., Ching, Y., and Rousseau, D. L., 1990, Primary intermediate in the reaction of oxygen with fully reduced cytochrome c oxidase, Proc. Natl. Acad. Sci. USA 87:2491–2495.

    Article  PubMed  CAS  Google Scholar 

  • Hensel, S., and Buse, G., 1990, Studies on cytochrome-c oxidase, XIV, Biol. Chem. Hoppe-Seyler 371:411–422.

    Article  PubMed  CAS  Google Scholar 

  • Hill, B. C., 1994, Modeling the sequence of electron transfer reaction in the single turnover of reduced, mammalian cytochrome c oxidase, J. Biol. Chem. 269:2419–2425.

    PubMed  CAS  Google Scholar 

  • Hosier, J. P., Espe, M. P., Zhen, Y., Babcock, G. T., and Ferguson-Miller, S., 1995, Analysis of site-directed mutants locates a non-redox-active metal near the active site of cytochrome c oxidase of Rhodobacter sphaeroides, Biochemistry 34:7586–7592.

    Article  Google Scholar 

  • Iwata, S., Ostermeier, C., Ludwig, B., and Michel, H., 1995, Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans, Nature 376:660–669.

    Article  PubMed  CAS  Google Scholar 

  • Jensen, L. H., 1986, The iron-sulfur proteins: An overview, in: Iron-Sulfur Protein Research (H. Matsubara, Y. Katsube, and K. Wada, eds.), pp. 3–21, Springer-Verlag, Berlin.

    Google Scholar 

  • Kadenbach, B., Ungibauer, M., Jarausch, J., Büge, U., and Kuhn-Nentwig, L., 1983, The complexity of respiratory complexes, Trends Biochem. Sci. 8:398–400.

    Article  CAS  Google Scholar 

  • Kitagawa, T., and Mizutani, Y., 1994, Resonance Raman spectra of highly oxidized metallo-porphyrins and heme proteins, Coordination Chem. Rev. 135/136:685–735.

    Article  CAS  Google Scholar 

  • Kitagawa, T., and Ogura, T., 1997, Oxygen activation mechanism at the binuclear site of heme-copper oxidase superfamily as revealed by time-resolved resonance Raman spectroscopy, Prog. Inorg. Chem. 45:431–479.

    Article  CAS  Google Scholar 

  • Kröneck, P. M. H., Antholine, W. A., Riester, J., and Zumft, W. G., 1988, The cupric site in nitrous oxide reductase contains a mixed-valence [Cu(II), Cu(I)] binuclear center: A multifrequency electron paramagnetic resonance investigation, FEBS Lett. 242:70–74.

    Article  PubMed  Google Scholar 

  • Ludwig, B., and Schatz, G., 1980, A two-subunit cytochrome c oxidase (cytochrome a a3) from Paracoccus denitrificans, Proc. Natl. Acad. Sci. USA 77:196–200.

    Article  PubMed  CAS  Google Scholar 

  • Malmström, B. G., 1990, Cytochrome c oxidase as a redox-linked proton pump, Chem. Rev. 90:1247–1260.

    Article  Google Scholar 

  • Meinecke, L., and Buse, G., 1986, Studies on cytochrome-c oxidase, XIII, Biol. Chem. Hoppe-Seyler 367:67–73.

    Article  PubMed  CAS  Google Scholar 

  • Nichols, P., and Wrigglesworth, J. M., 1988, Routes of cytochrome a 3 reduction, Ann. NY Acad. Sci. 550:59–67.

    Article  Google Scholar 

  • Ogura, T., Takahashi, T., Shinzawa-Itoh, K., Yoshikawa, S., and Kitagawa, T., 1990, Observation of the FeII-O2 stretching Raman band for cytochrome oxidase compound A at ambient temperature, J. Am. Chem. Soc. 112:5630–5631.

    Article  CAS  Google Scholar 

  • Ogura, T., Takahashi, T., Shinzawa-Itoh, K., Yoshikawa, S., and Kitagawa, T., 1991, Time-resolved resonance Raman investigation of cytochrome oxidase catalysis: Observation of a new oxygen-isotope sensitive Raman band, Bull. Chem. Soc. Jpn. 64:2901–2907.

    Article  CAS  Google Scholar 

  • Ogura, T., Takahashi, S., Hirota, S., Shinzawa-Itoh, K., Yoshikawa, S., Appelman, E. H., and Kitagawa, T., 1993, Time-resolved resonance Raman elucidation of the pathway for dioxygen reduction by cytochrome c oxidase, J. Am. Chem. Soc. 115:8527–8536.

    Article  CAS  Google Scholar 

  • Puustinen, A., Finel, M., Virkki, M., and Wikström, M., 1989, Cytochrome o(bo) is a proton pump in Paracoccus denitrificans and Escherichia coli, FEBS Lett. 249:163–167.

    Article  PubMed  CAS  Google Scholar 

  • Robinson, N. C., 1982, Specificity and binding affinity of phospholipids to the high-affinity cardiolipin sites of beef heart cytochrome c oxidase, Biochemistry 21:184–188.

    Article  PubMed  CAS  Google Scholar 

  • Scott, R. A., 1989, X-ray absorption spectroscopic investigations of cytochrome c oxidase structure and function, Annu. Rev. Biophys. Biophys. Chem. 18:137–158.

    Article  PubMed  CAS  Google Scholar 

  • Shinzawa-Itoh, K., Ueda, H., Yoshikawa, S., Aoyama, H., Yamashita, E., and Tsukihara, T., 1995, Effects of ethyleneglycol chain length of dodecyl polyethyleneglycol monoether on the crystallization of bovine heart cytochrome c oxidase, J. Mol. Biol. 246:572–575.

    PubMed  CAS  Google Scholar 

  • Steffens, G. C. M., Souliname, T., Wolff, G., and Buse, G., 1993, Stoichiometry and redox behavior of metals in cytochrome-c oxidase, Eur. J. Biochem. 213:1149–1157.

    Article  PubMed  CAS  Google Scholar 

  • Suarez, M. D., Revzin, A., Narlock, R., Kempner, E. S., Thomson, D. A., and Ferguson-Miller, S., 1984, The functional and physical form of mammalian cytochrome c oxidase determined by gel filtration, radiation inactivation, and sedimentation equilibrium analysis, J. Biol. Chem. 259:13791–13799.

    PubMed  CAS  Google Scholar 

  • Thomas, J. W., Puustinen, A., Alben, J. O., Gennis, R. B., and Wikström, M., 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.

    Article  PubMed  CAS  Google Scholar 

  • Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., and Yoshikawa, S., 1995, Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å, Science 269:1069–1074.

    Article  PubMed  CAS  Google Scholar 

  • Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., and Yoshikawa, S., 1996, The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å, Science 272:1136–1144.

    Article  PubMed  CAS  Google Scholar 

  • Van Gelder, B. F., and Beinert, H., 1969, Studies of the heme component of cytochrome c oxidase by EPR spectroscopy, Biochim. Biophys. Acta 189:1–24.

    Article  PubMed  CAS  Google Scholar 

  • Varotsis, C., Woodruff, W H., and Babcock, G. T., 1990, Time resolved Raman detection of v(Fe-O) in an early intermediate in the reaction of O2 by cytochrome oxidase, J. Am. Chem. Soc. 112:1297.

    Article  CAS  Google Scholar 

  • Wang, H., Blair, D. F., Ellis, W. R., Gray, H. B., and Chan, S. I., 1986, Temperature dependence of the reduction potential of CuA in carbon monoxide inhibited cytochrome c oxidase, Biochemistry 25:167–171.

    Article  PubMed  CAS  Google Scholar 

  • Warburg, O., 1924, Üben Eisen, den sauerstoffubentragenden Bestandteil des Atmungsfermentes, Biochem. Z. 152:479–494.

    Google Scholar 

  • Wikström, M. K. F., 1977, Proton pump coupled to cytochrome c oxidase in mitochondria, Nature 266:271–273.

    Article  PubMed  Google Scholar 

  • Wikström, M., and Morgan, J. E., 1992, The dioxygen cycle, J. Biol. Chem. 267:10266–10273.

    PubMed  Google Scholar 

  • Wikström, M., Krab, S., and Saraste, M., 1981, Cytochrome Oxidase-α Synthesis, Academic Press, London.

    Google Scholar 

  • Wikström, M., Bogachev, A., Finel, M., Morgan, J. E., Puustinen, A., Raitio, M., Verkhovskaya, M., and Verkhovsky, M. I., 1994, Mechanism of proton translocation by the respiratory oxidases. The histidine cycle, Biochim. Biophys. Acta 1187:106–111.

    Article  PubMed  Google Scholar 

  • Woodruff, W. H., Einersdóttir, Ó., Dyer, R. B., Bagley, K. A., Palmer, G., Atherton, S. J., Goldbeck, R. A., Dawes, T. D., and Kliger, D. S., 1991, Nature and functional implications of the cytochrome a 3 transients after photodissociation of CO-cytochrome oxidase, Proc. Natl. Acad. Sci. USA 88:2588–2592.

    Article  PubMed  CAS  Google Scholar 

  • Wu, W., Chang, C. K., Varotsis, C., Babcock, G. T., Puustinen, A., and Wikström, M., 1992, Structure of the heme O prosthetic group from the terminal quinol oxidase of Escherichia coli, J. Am. Chem. Soc. 114:1182–1187.

    Article  CAS  Google Scholar 

  • Yoshikawa, S., Choc, M. G., O’Toole, M. C., and Caughey, W. S., 1977, An infrared study of CO binding to heart cytochrome c oxidase and hemoglobin A, J. Biol Chem. 252:5498–5508.

    PubMed  CAS  Google Scholar 

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Author information

Authors and Affiliations

  1. Department of Life Science, Himeji Institute of Technology, Kamigohri, Akoh Hyogo, 678-12, Japan

    Shinya Yoshikawa & Kyoko Shinzawa-Itoh

  2. Institute for Protein Science, Osaka University, Suita, Osaka, 565, Japan

    Tomitake Tsukihara

Authors
  1. Shinya Yoshikawa
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  2. Kyoko Shinzawa-Itoh
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  3. Tomitake Tsukihara
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Editor information

Editors and Affiliations

  1. University of Bari, Bari, Italy

    Sergio Papa  & Ferruccio Guerrieri  & 

  2. University of Amsterdam, Amsterdam, The Netherlands

    Joseph M. Tager

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Yoshikawa, S., Shinzawa-Itoh, K., Tsukihara, T. (1999). The Structure of Crystalline Bovine Heart Cytochrome c Oxidase. In: Papa, S., Guerrieri, F., Tager, J.M. (eds) Frontiers of Cellular Bioenergetics. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-4843-0_6

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  • DOI: https://doi.org/10.1007/978-1-4615-4843-0_6

  • Publisher Name: Springer, Boston, MA

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