Abstract
Cytochrome c oxidase from bovine heart contains seven high-affinity binding sites for ATP or ADP and three additional only for ADP. One binding site for ATP or ADP, located at the matrix-oriented domain of the heart-type subunit VIaH, increases the H+/e− stoichiometry of the enzyme from heart or skeletal muscle from 0.5 to 1.0 when bound ATP is exchanged by ADP. Two further binding sites for ATP or ADP, located at the cytosolic and the matrix domain of subunit IV, increases the K M for Cytochrome c and inhibit the respiratory activity at high ATP/ADP ratios, respectively. We propose that thermogenesis in mammals is related to subunit VIaL of cytochrome c oxidase with a H+/e− stoichiometry of 0.5 compared to 1.0 in the enzyme from bacteria or ectotherm animals. This hypothesis is supported by the lack of subunit VIa isoforms in cytochrome c oxidase from fish.
Similar content being viewed by others
REFERENCES
Allen, L. A., Zhao, X.-J., Caughey, W., and Poyton, R. O. (1995). “Isoforms of yeast cytochrome c oxidase subunit V affect the binuclear reaction center and alter the kinetic interaction with the isoforms of yeast cytochrome c,” J. Biol. Chem. 270, 110-118.
Anthony, G., Stroh, A., Lottspeich, F., and Kadenbach, B. (1990). “Different isozymes of cytochrome c oxidase are expressed in bovine smooth muscle and skeletal or heart muscle,” FEBS Lett. 277, 97-100.
Anthony, G., Reimann, A., and Kadenbach, B. (1993). “Tissue-specific regulation of bovine heart cytochrome c oxidase by ADP via interaction with subunit VIa,” Proc. Natl. Acad. Sci. USA 90, 1652-1656.
Arnold, S., and Kadenbach, B. (1997). “Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome c oxidase,” Eur. J. Biochem., 249, 350-354.
Arnold, S., Lee, I., Kim, M. J., Song, E., Linder, D., Lottspeich, F., and Kadenbach, B. (1997). “The subunit structure of cytochrome c oxidase from tuna heart and liver,” Eur. J. Biochem., 248, 99-103.
Bisson, R., and Schiavo, G. (1986). “Two different forms of cytochrome c oxidase can be purified from slime mold Dictyostelium discoideum,” J. Biol. Chem., 4373-4376.
Bisson, R., Schiavo, G., and Montecucco, C. (1987). “ATP induces conformational changes in mitochondrial cytochrome c oxidase,” J. Biol. Chem. 262, 5992-5998.
Bisson, R., Vettore, S., Aratri, E., and Sandonà, D. (1997). “Subunit change in cytochrome c oxidase: identification of the oxygen switch in Dictyostelium,” EMBO J. 16, 739-749.
Bolli, R., Nalecz, K. A., and Azzi, A. (1985). “The interconversion between monomeric and dimeric bovine heart cytochrome c oxidase,” Biochimie 67, 119-128.
Bonne, G., Seibel, P., Possekel, S., Marsac, C., and Kadenbach, B. (1993). “Expression of human cytochrome c oxidase subunits during fetal development,” Eur. J. Biochem. 217, 1099-1107.
Capaldi, R. O. (1990). “Structure and function of cytochrome c oxidase,” Annu. Rev. Biochem. 59, 569-596.
Capaldi, R. A., Zhang, Y.-Z., Rizzuto, R., Sandonà, D., Schiavo, G., and Bisson, R. (1990). “The oxygen-regulated subunits of cytochrome c oxidase in Dictyostelium discoideum derive from a common ancestor, “FEBS Lett. 261, 158-160.
Chepuri, V., Lemieux, L., Au, D. C.-T., and Gennis, R. B. (1990). “The sequence of the cyo operon indicates substantial structural similarities between the cytochrome o ubiquinol oxidase of Escherichiacoli and the aa3-type family of cytochrome c oxidases,” J. Biol. Chem. 265, 11185-11192.
Cumsky, M. G., Trueblood, C. E., Ko, C., and Poyton, R. O. (1987). “Structural analysis of two genes encoding divergent forms of yeast cytochrome c oxidase subunit V,” Mol. Cell. Biol. 7, 3511-3519.
Exner, S. (1997). Dissertation, Fachbereich Chemie, Philipps-Universität, Marburg.
Ferguson-Miller, S., Brautigan, D. L., and Margoliash, E. (1976). “Correlation of the kinetics of electron transfer activity of various eukaryotic cytochromes c with binding to mitochondrial cytochrome c oxidase,” J.Biol. Chem. 251, 1104-1115.
Ferguson-Miller, S., Brautigan, D. L., and Margoliash, E. (1978). “Definition of cytochrome c binding domains by chemical modification. III. Kinetics of reaction of carboxydinitrophenyl cytochromes c with cytochrome c oxidase,” J. Biol. Chem. 253, 149-159.
Frank, V. and Kadenbach, B. (1996). Regulation of the H+/e− stoichiometry of cytochrome c oxidase from bovine heart by intraliposomal ATP/ADP ratios,” FEBS Lett. 382, 121-124.
Freund, R., and Kadenbach, B. (1994). “Tissue-specific isoforms for subunit Vb and VIIa were identified in cytochrome c oxidase from rainbow trout,” Eur. J. Biochem. 221, 1111-1116.
From, A. H. L., Zimmer, S. D., Michurski, S. P., Mohanakrishnan, P., Ulstad, V. K., Thoma, W. J., and Ugurbil, K. (1990). “Regulation of the oxidative phosphorylation rate in the intact cell,” Biochemistry 29, 3731-3743.
Geier, B. M., Schägger, H., Ortwein, C., Link, T. A., Hagen, W. R., Brandt, U., and von Jagow, G. (1994). “Kinetic properties and ligand binding of the eleven-subunit cytochrome c oxidase from Saccharomyzes cerevisiae isolated with a novel large-scale purification method,” Eur. J. Biochem. 227, 296-302.
Grossman, L. I., and Lomax, M. I. (1997). “Nuclear genes for cytochrome c oxidase,” Biochim. Biophys. Acta 1352, 174-192.
Hakvoort, T. B. M., Moolenaar, K., Lankvelt, A. H. M., Singorgo, K. M. C., Dekker, H. L., and Muijsers, A. O. (1987). “Separation, stability and kinetics of monomeric and dimeric bovine heart cytochrome c oxidase,” Biochim. Biophys. Acta 894, 347-354.
Hüttemann, M., Exner, S., Arnold, S., Lottspeich, F., and Kadenbach, B. (1997). “The cDNA sequences of cytochrome c oxidase subunit VIa from carp and rainbow trout suggest the absence of isoforms,” Biochim. Biophys. Acta 1319, 14-18.
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.
Kadenbach, B. (1983). “Structure and evolution of the “Atmungsferment” cytochrome c oxidase,” Angew. Chem. Int. Ed. Engl. 22, 275-283.
Kadenbach, B. (1986). “Mini Review. Regulation of respiration and ATP synthesis in higher organisms: Hypothesis,” J. Bioenerg. Biomembr. 18, 39-54.
Kadenbach, B., and Reimann, A. (1992). in: “Molecular Mechanisms in Bioenergetics,” New Comprehensive Biochemistry (Ernster, L. ed.), Elsevier, Amsterdam, pp. 241-263.
Kadenbach, B., Mende, P., Kolbe, H. V. J., Stipani, I., and Palmieri, F. (1982). “The mitochondrial phosphate carrier has an essential requirement for cardiolipin,” FEBS Lett. 139, 109-112.
Kadenbach, B., Stroh, A., Ungibauer, M., Kuhn-Nentwig, L., Büge, U., and Jarausch, J. (1986). “Isozymes of cytochrome c oxidase: characterization and isolation from different tissues,” Methods Enzymol. 126, 32-45.
Kadenbach, B., Kuhn-Nentwig, L., and Büge, U. (1987). “Evolution of a regulatory enzyme: cytochrome c oxidase (complex IV),” Curr. Top. Bioenerg. 15, 113-161.
Kadenbach, B., Stroh, A., Becker, A., Eckerskorn, C., and Lottspeich, F. (1990). “Tissue-and species-specific expression of cytochrome c oxidase isozymes in vertebrates,” Biochim. Biophys. Acta 1015, 368-372.
Kadenbach, B., Barth, J., Akgün, R., Freund, R., Linder, D., and Possekel, S. (1995). “Regulation of mitochondrial energy generation in health and disease,” Biochim. Biophys. Acta 1271, 103-109.
Kadenbach, B., Frank, V., Belyanovitch, L., Linder, D., and Arnold, S. (1997). “Tissue-specific expression of cytochrome c oxidase isoforms and role in nonshivering thermogenesis,” In: Frontiers of Cellular Bioenergetics: Molecular Biology, Biochemistry, and Pathophysiology (Papa, S., Guerrieri, F., and Tager, J.M., eds.), Plenum Press, New York, in press.
Linder, D., Freund, R., and Kadenbach, B. (1995). “Species-specific expression of cytochrome c oxidase isozymes,” Comp. Biochem. Physiol. 112B, 461-469.
Napiwotzki, J., Shinzawa-Itoh, K., Yoshikawa, S., and Kadenbach, B. (1997) “ATP and ADP bind to cytochrome c oxidase and regulate its activity,” Biol. Chem., 378, 1013-1021.
Napiwotzki, J. and Kadenbach, B. (1998). Extramitochrondrial ATP/ADP-ratios regulate cytochrome c oxidase activity via binding to the cytosolic domain of subunit IV. Biol. Chem. 379, 335-339.
Osheroff, N., Brautigan, D. L., and Margoliash, E. (1980). “Mapping of anion binding sites on cytochrome c by differential chemical modifications of lysine residues,” Proc. Natl. Acad. Sci. USA 77, 4439-4443.
Palmieri, F., Indiveri, C., Bisaccia, F., and Krämer, R. (1993). “Functional properties of purified and reconstituted mitochondrial metabolite carriers,” J. Bioenerg. Biomembr. 25, 525-535.
Parsons, W. J., Williams, R. S., Shelton, J. M., Luo, Y., Kessler, D. J., and Richardson, J. A. (1996). “Developmental regulation of cytochrome oxidase subunit VIa isoforms in cardiac and skeletal muscle,” Am. J. Physiol. 270 (Heart Circ. Physiol. 39): H567-H574.
Poyton, R. O., Trueblood, C. E., Wright, R. M., and Farrell, L. E. (1988). “Expression and function of cytochrome c subunit isologues. Modulators of cellular energy production?” Ann. N.Y. Acad. Sci. 550, 289-307.
Reimann, A., Hüther, F.-J., Berden, J. A., and Kadenbach, B. (1988). “Anions induce conformational changes and influence the activity and photoaffinity-labelling by 8-azido-ATP of isolated cytochrome c oxidase,” Biochem. J. 254, 723-730.
Rieger, T., Napiwotzki, J., and Kadenbach, B. (1995). “On the number of nucleotide binding sites in cytochrome c oxidase,” Biochem. Biophys. Res. Commun. 217, 34-40.
Rohdich, F., and Kadenbach, B. (1993). “Tissue-specific regulation of cytochrome c oxidase efficiency by nucleotides,” Biochemistry 32, 8499-8503.
Saccone, C., Pesole, G., and Kadenbach, B. (1991). “Evolutionary analysis of the nucleus-encoded subunits of mammalian cytochrome c oxidase,” Eur. J. Biochem. 195, 151-156.
Saraste, M. (1990). “Structural features of cytochrome oxidase,” Quart. Rev. Biophys. 23, 331-366.
Schneyder, B., Mell, O., Anthony, G., and Kadenbach, B. (1991). “Cross reactivity of monoclonal antibodies and cDNA hybridization suggest evolutionary relationships between subunits VIIa and VIIb,” Eur. J. Biochem. 198, 85-92.
Schwenke, W. B., Soboll, S., Seitz, H. J., and Sies, H. (1981). “Mitochondrial and cytosolic ATP/ADP ratios in rat liver in vivo,” Biochem. J. 200, 405-408.
Segade, F., Hurlé, B., Claudio, E., Ramos, S., and Lazo, P. S. (1996). “Identification of an additional member of the cytochrome c oxidase subunit VIIa family of proteins,” J. Biol. Chem. 271, 12343-12349.
Suarez, M. D., Revzin, A., Natlock, R., Kemper, E. S., Thompson, 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.
Taanman, J.-W., Turina, P., and Capaldi, R.A. (1994). “Regulation of cytochrome c oxidase by interaction of ATP at two binding sites, one on subunit VIa,” Biochemistry 33, 11833-11841.
Trumpower, B.L., and Gennis, R.B. (1994). “Energy transduction by cytochrome complexes in mitochondrial and bacterial respiration: the enzymology of coupling electron transfer reactions to transmembrane proton translocation,” Anna. Rev. Biochem. 63,675-716.
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.
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.
Veech, R. L., Lawson, J. W. R., Cornell, N. W., and Krebs, H. A. (1979) “Cytosolic phosphorylation potential,” J. Biol. Chem. 254, 6538-6547.
Waterland, R. A., Basu, A., Chance, B., and Poyton, R. O. (1991). “The isoforms of yeast cytochrome c oxidase subunit V alter the in vivo kinetic properties of the holoenzyme,” J. Biol. Chem. 266, 4180-4186.
Weishaupt, A., and Kadenbach, B. (1992). “Selective removal of subunit VIb increases the activity of cytochrome c oxidase,” Biochemistry 31, 11477-11481.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kadenbach, B., Napiwotzki, J., Frank, V. et al. Regulation of Energy Transduction and Electron Transfer in Cytochrome c Oxidase by Adenine Nucleotides. J Bioenerg Biomembr 30, 25–33 (1998). https://doi.org/10.1023/A:1020599209468
Issue Date:
DOI: https://doi.org/10.1023/A:1020599209468