Abstract
The presence of additional subunits in cytochrome oxidase distinguish the multicellular eukaryotic enzyme from that of a simple unicellular bacterial enzyme. The number of these additional subunits increases with increasing evolutionary stage of the organism. Subunits I–III of the eukaryotic enzyme are related to the three bacterial subunits, and they are encoded on mito-chondrial DNA. The additional subunits are nuclear encoded. Experimental evidences are presented here to indicate that the lower enzymatic activity of the mammalian enzyme is due to the presence of nuclear-coded subunits. Dissociation of some of the nuclear-coded subunits (e.g., VIa) by laurylmaltoside and anions increased the activity of the rat liver enzyme to a value similar to that of the bacterial enzyme. Further, it is shown that the intraliposomal nucleotides influence the kinetics of ferrocytochromec oxidation by the reconstituted enzyme from bovine heart but not fromP. denitrificans. The regulatory function attributed to the nuclear-coded subunits of mammalian cytochromec oxidase is also demonstrated by the tissue-specific response of the reconstituted enzyme from bovine heart but not from bovine liver to intraliposomal ADP. These enzymes from bovine heart and liver differ in the amino acid sequences of subunits VIa, VIIa, and VIII. The results presented here are taken to indicate a regulation of cytochromec oxidase activity by nuclear-coded subunits which act like receptors for allosteric effectors and influence the catalytic activity of the core enzyme via conformational changes.
Similar content being viewed by others
References
Albracht, S. P. J., Van Verseveld, H. W., and Kalkman, M. L. (1980).Biochim. Biophys. Acta 593, 173–186.
Antonini, G., Malatesta, F., Sarti, P., Vallone, B., and Brunori, M. (1988).Biochem. J. 256, 835–840.
Bisson, R., and Schiavo, G. (1986).J. Biol. Chem. 261, 4373–4376.
Bisson, R., and Schiavo, G. (1988).Ann. N.Y. Acad. Sci. 550, 325–336.
Bisson, R., Steffens, G. C. M., Capaldi, R. A., and Buse, G. (1982).FEBS Lett. 144, 359–363.
Bisson, R., Schiavo, G., and Montecucco, C. (1987).J. Biol. Chem. 262, 5992–5998.
Bolgiano, B., Smith, L., and Davies, H. C. (1989).Biochim. Biophys. Acta 973, 227–234.
Bombelka, E., Richter, F.-W., Stroh, A., and Kadenbach, B. (1986).Biochem. Biophys. Res. Commun. 140, 1007–1014.
Büge, U., and Kadenbach, B. (1986).Eur. J. Biochem. 161, 383–390.
Buse, G., Hensel, S., and Fee, J. A. (1989).Eur. J. Biochem. 181, 261–268.
Capaldi, R. A., Malatesta, F., and Darley-Usmar, V. M. (1983).Biochim. Biophys. Acta 726, 135–148.
Cumsky, M. G., Trueblood, C. E., Ko, C., and Poyton, R. O. (1987).Mol. Cell. Biol. 7, 3511–3519.
Darnell, J. E., and Doolittle, W. F. (1986).Proc. Natl. Acad. Sci. USA 83, 1271–1274.
Fee, J. A., Kuila, D., Mather, M. W., and Yoshida, T. (1986).Biochim. Biophys. Acta 853, 153–185.
Fee, J. A., Mather, M. W., Springer, P., Hensel, S., and Buse, G. (1988).Ann. N.Y. Acad. Sci. 550, 33–38.
Gregory, L. C., and Ferguson-Miller, S. (1988).Biochemistry 27, 6307–6314.
Haltia, T., Finel, M., Harms, N., Nakari, T., Raitio, M., Wikström, M., and Saraste, M. (1989).EMBO J. 8, 3571–3579.
Hill, B. C., and Robinson, N. C. (1986).J. Biol. Chem. 261, 15356–15359.
Hüther, F.-J., and Kadenbach, B. (1986).FEBS Lett. 207, 89–94.
Hüther, F.-J., and Kadenbach, B. (1987).Biochem. Biophys. Res. Commun. 147, 1268–1275.
Hüther, F.-J., and Kadenbach, B. (1988).Biochem. Biophys. Res. Commun. 153, 525–534.
Hüther, F.-J., Berden, J., and Kadenbach, B. (1988).J. Bioenerg. Biomembr. 20, 503–516.
Kadenbach, B. (1986).J. Bioenerg. Biomembr. 18, 39–54.
Kadenbach, B., and Merle, P. (1981).FEBS Lett. 135, 1–11.
Kadenbach, B., Büge, U., Jarausch, J., and Merle, P. (1981). InVectorial Reactions in Electron and Ion Transport in Mitochondria and Bacteria (Palmieri, F.,et al., eds.), Elsevier North-Holland Biomedical Press, pp. 11–23.
Kadenbach, B., Hartmann, R., Glanville, R., and Buse, G. (1982).FEBS Lett. 138, 236–238 (1982).
Kadenbach, B., Jarausch, J., Hartmann, R., and Merle, P. (1983).Anal. Biochem. 129, 517–521.
Kadenbach, B., Kuhn-Nentwig, L., and Büge, U. (1987a).Curr. Top. Bioenerg. 15, 113–161.
Kadenbach, B., Stroh, A., Hüther, F.-J., and Berden, J. (1987b). InCytochrome Systems: Molecular Biology and Bioenergetics (Papa, S., Chance, B., and Ernster, L., eds.), Plenum Press, New York, pp. 399–406.
Kadenbach, B., Reimann, A., Stroh, A., and Hüther, F.-J. (1988). InOxidases and Related Redox Systems (King, T. E., Mason, H. S., and Morrison, M., eds.), A. R. Liss Inc., New York, pp. 653–668.
Kadenbach, B., Stroh, A., Becker, A., Eckerskorn, C., and Lottspeich, F. (1990).Biochim. Biophys. Acta 1015, 368–372.
Koppenol, W. H., and Margoliash, E. (1982).J. Biol. Chem. 257, 4426–4437.
Kossekova, G., Atanasov, B., Bolli, R., and Azzi, A. (1989).Biochem. J. 262, 591–596.
Labonia, N., Müller, M., and Azzi, A. (1988).Biochem. J. 254, 139–145.
Lightowlers, R., Takamiya, S., Wessling, R., Lindorfer, M., and Capaldi, R. A. (1989).J. Biol. Chem. 264, 16858–16860.
Lightowlers, R., Ewart, G., Aggeler, R., Zhang, Y.-Z., Calavetta, L., and Capaldi, R. A. (1990).J. Biol. Chem. 265, 2677–2681.
Ludwig, B. (1980).Biochim. Biophys. Acta 594, 177–189.
Ludwig, B. (1987).FEMS Microbiol. Rev. 46, 41–56.
Ludwig, B., and Schatz, G. (1980).Proc. Natl. Acad. Sci. USA 77, 196–200.
Malatesta, F., Antonini, G., Sarti, P., and Brunori, M. (1987).Biochem. J. 248, 161–165.
McEwen, J. E., Ko, C., Kloeckner-Gruissem, B., and Poyton, R. O. (1986).J. Biol. Chem. 261, 11872–11879.
Merle, P., and Kadenbach, B. (1982).Eur. J. Biochem. 125, 239–244.
Montecucco, C., Schiavo, G., and Bisson, R. (1986).Biochem. J. 234, 241–243.
Montecucco, C., Schiavo, G., Bacci, B., and Bisson, R. (1987).Comp. Biochem. Physiol. 87B, 851–856.
Müller, M., Schläpfer, B., and Azzi, A. (1988).Proc. Natl. Acad. Sci. USA 85, 6647–6651.
Penttilä, T., Saraste, M., and Wikström, M. (1979).FEBS Lett.,101, 295–300.
Poole, R. K. (1983).Biochim. Biophys. Acta 726, 205–243.
Power, S. D., Lochrie, M. A., Sevarino, K. A., Patterson, T. E., and Poyton, R. O. (1984).J. Biol. Chem. 259, 6564–6570.
Poyton, R. O., Trueblood, C. E., Wright, R. M., and Farrell, L. E. (1988).Ann. N.Y. Acad. Sci. 550, 289–307.
Prochaska, L. J., and Fink, P. S. (1987).J. Bioenerg. Biomembr. 19, 143–166.
Püttner, J., Carafoli, E., and Malatesta, F. (1985).J. Biol. Chem. 260, 3719–3723.
Raitio, M., Jalli, T., and Saraste, M. (1987).EMBO J. 6, 2825–2833.
Reimann, A., Hüther, F.-J., Berden, J. A., and Kadenbach, B. (1988).Biochem. J. 254, 723–730.
Rigoulet, M., Guerin, B., and Denis, M. (1987).Eur. J. Biochem. 168, 275–279.
Rosevear, P., Van Aken, T., Baxter, J., and Ferguson-Miller, S. (1980).Biochemistry 19, 4108–4115.
Saraste, M., Raitio, M., Jalli, T., Chepuri, V., Lemieux, L., and Gennis, R. (1988).Ann. N.Y. Acad. Sci. 550, 314–324.
Schägger, H., and von Jagow, G. (1987).Anal. Biochem. 166, 368–379.
Schlerf, A., Droste, M., Winter, M., and Kadenbach, B. (1988).EMBO. J. 7, 2387–2391.
Steffens, G. C. M., Buse, G., Oppliger, W., and Ludwig, B. (1983).Biochem. Biophys. Res. Commun. 116, 335–340.
Steffens, G. C. M., Biewald, R., and Buse, G. (1987).Eur. J. Biochem. 164, 295–300.
Steverding, D., and Kadenbach, B. (1989).Biochem. Biophys. Res. Commun. 160, 1132–1139.
Steverding, D., and Kadenbach, B. (1990).J. Bioenerg. Biomembr. 22, 197–205.
Stroh, A., and Kadenbach, B. (1986).Eur. J. Biochem. 156, 199–204.
Thiel, C., and Kadenbach, B. (1989).FEBS Lett. 251, 270–274.
Thompson, D. A., and Ferguson-Miller, S. (1983).Biochemistry 22, 3178–3187.
Thompson, D. A., Gregory, L., and Ferguson-Miller, S. (1985).J. Inorg. Biochem. 23, 357–364.
Trueblood, C. E., and Poyton, R. O. (1987).Mol. Cell. Biol. 7, 3520–3526.
Van Beeumen, J. J., Van Kuilenberg, A. B. P., Van Bun, S., Van den Boert, C., Tager, J. M., and Muijsers, A. O. (1990).FEBS Lett. 263, 213–216.
Van Kuilenberg, A. B. P., Muijsers, A. O., Demol, H., Dekker, H. L., and Van Beeumen, J. J. (1988).FEBS Lett. 240, 127–132.
Werner, S. (1977).Eur. J. Biochem. 79, 103–110.
Wikström, M., Krab, K., and Saraste, M., eds. (1981).Cytochrome Oxidase. A Synthesis, Academic Press, New York.
Yamanaka, T., Fukumori, Y., Yamazaki, T., Kato, H., and Nakayama, K. (1985).J. Inorg. Biochem. 23, 273–277.
Yamazaki, R. K. (1975).J. Biol. Chem. 250, 7924–7930.
Yanamura, W., Zhang, Y.-Z., Takamiya, S., and Capaldi, R. A. (1988).Biochemistry 27, 4909–4914.
Yang, D. Y., Oyaizu, Y., Oyaizu, H., Olsen, G. J., and Woese, C. R. (1985).Proc. Natl. Acad. Sci. USA 82, 4443–4447.
Zimmermann, B. H., Nitsche, C. I., Fee, J. A., Rusnak, F., and Münck, E. (1988).Proc. Natl. Acad. Sci. USA 85, 5779–5783.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kadenbach, B., Stroh, A., Hüther, F.J. et al. Evolutionary aspects of cytochromec oxidase. J Bioenerg Biomembr 23, 321–334 (1991). https://doi.org/10.1007/BF00762225
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00762225