Skip to main content
SpringerLink
Log in

Complexity and tissue specificity of the mitochondrial respiratory chain

  • Mini-Review
  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

There is a renewed interest in the structure and functioning of the mitochondrial respiratory chain with the realization that a number of genetic disorders result from defects in mitochondrial electron transfer. These so-called mitochondrial myopathies include diseases of muscle, heart, and brain. The respiratory chain can be fractionated into four large multipeptide complexes, an NADH ubiquinone reductase (complex I), succinate ubiquinone reductase (complex II), ubiquinol oxidoreductase (complex III), and cytochromec oxidase (complex IV). Mitochondrial myopathies involving each of these complexes have been described. This review summarizes compositional and structural data on the respiratory chain proteins and describes the arrangement of these complexes in the mitochondrial inner membrane. This biochemical information is provided as a framework for the diagnosis and molecular characterization of mitochondrial diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Albracht, P. J., Leeuwerik, F. J., and van Swol, B. (1979).FEBS Lett. 104, 197–200.

    Google Scholar 

  • Anderson, S., Bankier, A. T., Barrel, B. G., De Bruyn, M. H. L., Carlson, A. R., Drouin, J., Eperson, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., Schreier, P. H., Smith, A. J. H., Staden, R., and Young, I. G. (1981).Nature (London)290, 457–465.

    Google Scholar 

  • Anderson, W. M., Fowler, W. T., Pennington, R. M., and Fisher, R. R. (1981).J. Biol. Chem. 256, 1888–1895.

    Google Scholar 

  • Anderson, S., de Bruijn, M. H. L., Coulson, A. R., Eperon, I. C., Sanger, F., and Young, I. G. (1982).J. Mol. Biol. 156, 683–717.

    Google Scholar 

  • Azzone, G. F., Colonna, R., and Ziche, B. (1979).Methods Enzymol. 55, 45–50.

    Google Scholar 

  • Beattie, D. S., Clejan, L., Chen, Y-S., Lin, C-I., and Sidhu, A. (1981).J. Bioenerg. Biomembr. 13, 357–373.

    Google Scholar 

  • Bell, R. L., Sweetland, J., Ludwig, B., and Capaldi, R. A. (1979).Proc. Natl. Acad. Sci. USA 76, 741–745.

    Google Scholar 

  • Bertina, R. M., Schrier, P. I., and Slater, E. C. (1973).Biochim. Biophys. Acta 305, 503–518.

    Google Scholar 

  • Bisson, R., Steffens, G. C. M., Capaldi, R. A., and Buse, G. (1982).FEBS Lett. 144, 359–363.

    Google Scholar 

  • Bisson, R., Schiavo, G., and Montecucco, C. (1987).J. Biol. Chem. 262, 5992–5998.

    Google Scholar 

  • Bonitz, S. G., Coruzzi, G., Thalenfeld, B. E., Tzagoloff, A., and Macino, G. (1980).J. Biol. Chem. 255, 11927–11941.

    Google Scholar 

  • Borchart, U., Malchleidt, W., Schagger, H., Link, T. A., and von Jagow, G. (1985).FEBS Lett. 191, 125–130.

    Google Scholar 

  • Borchart, U., Machleidt, W., Schagger, H., Link, T. A., and von Jagow, G. (1986).FEBS Lett. 200, 81–86.

    Google Scholar 

  • Bresolin, N., Zeviani, M., Bonilla, E., Miller, R. H., Leech, R. W., Shanske, S., Nakagawa, M., and DiMauro, S. (1985).Neurology 35, 802–812.

    Google Scholar 

  • Brewald, R., and Buse, G. (1982).Hoppe-Seylers Z. Physiol. Chem. 363, 1141–1153.

    Google Scholar 

  • Briggs, M., and Capaldi, R. A. (1977).Biochemistry 16, 73–78.

    Google Scholar 

  • Brink, J., Hovmoller, S., Ragan, C. I., Cleeter, M. W. J., Boekema, E. J., and van Bruggen, E. F. J. (1987).Eur. J. Biochem. 166, 287–294.

    Google Scholar 

  • Buse, G., and Steffens, G. J. (1978).Hoppe-Seylers Z. Physiol. Chem. 359, 1005–1009.

    Google Scholar 

  • Capaldi, R. A. (1982).Biochim. Biophys. Acta 694, 291–306.

    Google Scholar 

  • Capaldi, R. A., Sweetland, J., and Merli, A. (1977).Biochemistry 16, 5707–5716.

    Google Scholar 

  • Capaldi, R. A., Gonzalez-Halphen, D., and Takamiya, S. (1986).FEBS Lett. 207, 11–17.

    Google Scholar 

  • Chomyn, A., Mariottini, P., Cleeter, M. W. J., Ragan, C. I., Matsuno-Yagi, A., Hatefi, Y., Doolittle, R. F., and Attardi, G. (1985).Nature (London)314, 592–597.

    Google Scholar 

  • Coruzzi, G., and Tzagoloff, A. (1979).J. Biol. Chem. 254, 9324–9330.

    Google Scholar 

  • Darley-Usmar, V. M., Kennaway, N. G., Buist, R. M., and Capaldi, R. A. (1982).Proc. Natl. Acad. Sci. USA 80, 5103–5106.

    Google Scholar 

  • Davis, K. A., and Hatefi, Y. (1971).Biochemistry 10, 2509–2513.

    Google Scholar 

  • Deatherage, J. D., Henderson, R., and Capaldi, R. A. (1982).J. Mol. Biol. 158, 501–514.

    Google Scholar 

  • De Haan, M., Van Loon, A. P. G. M., Kreike, J., Vaessen, R. T. M. J., and Grivell, L. A. (1984).Eur. J. Biochem. 138, 169–177.

    Google Scholar 

  • Dickerson, R. E., and Timkovich, R. (1975). InThe Enzymes (Boyer, P. D., ed.), 3rd edn., Vol. 11, Academic Press, New York, pp. 397–547.

    Google Scholar 

  • DiMauro, S., Mendell, J. R., Sahenk, A., Bachman, D., Scarpa, A., Scofield, R. M., and Reiner, C. (1980).Neurology 30, 795–804.

    Google Scholar 

  • DiMauro, S., Bonilla, E., Zeviani, M., Nakagawa, M., and DeVivo, D. C. (1985).Ann. Neurol. 17, 521–538.

    Google Scholar 

  • DiMauro, S., Servidei, S., Zeviani, M., DiRocco, M., DeVivo, D. C., DiDonato, S., Uziel, G., Berry, K., Hoganson, G., Johnsen, S. D., and Johnson, P. C. (1987).Ann. Neurol. 22, 498–506.

    Google Scholar 

  • Erdwig, M., and Buse, G. (1985).Hoppe-Seylers Z. Physiol. Chem. 366, 257–263.

    Google Scholar 

  • Fleischer, S., Brierley, G., and Klouwen, H. (1961).J. Biol. Chem. 236, 2936–2941.

    Google Scholar 

  • Frey, T. G., Costello, M. J., Karlsson, B., Haselgrove, J. C., and Leigh, J. S. (1982).J. Mol. Biol. 162, 113–130.

    Google Scholar 

  • Fuller, S. D., Capaldi, R. A., and Henderson, R. (1979).J. Mol. Biol. 134, 305–327.

    Google Scholar 

  • Galante, Y., and Hatefi, Y. (1979).Arch. Biochem. Biophys. 192, 559–568.

    Google Scholar 

  • Gellerfors, P., and Nelson, B. D. (1977).Eur. J. Biochem. 80, 275–282.

    Google Scholar 

  • Gregor, I., and Tsugita, A. (1982).J. Biol. Chem. 257, 13081–13087.

    Google Scholar 

  • Gutman, M., Singer, T. P., and Casida, J. E. (1976).J. Biol. Chem. 245, 1992–1997.

    Google Scholar 

  • Gutweniger, H., Bisson, R., and Montecucco, C. (1981).J. Biol. Chem. 256, 11132–11136.

    Google Scholar 

  • Hare, J., Ching, E., and Attardi, G. (1980).Biochemistry 19, 2023–2030.

    Google Scholar 

  • Hatefi, Y., and Stiggel, D. L. (1976). InThe Enzymes (Boyer, P. D., ed.), Vol. 13, Academic Press, New York, pp. 175–297.

    Google Scholar 

  • Hatefi, Y. (1976). InThe Enzymes of Biological Membranes (Martinosi, A., ed.), Plenum, New York, pp. 3–41.

    Google Scholar 

  • Henderson, R., Capaldi, R. A., and Leigh, J. S. (1977).J. Mol. Biol. 112, 631–643.

    Google Scholar 

  • Heron, C., Smith, S., and Ragan, C. I. (1979).Biochem. J. 181, 435–443.

    Google Scholar 

  • Huther, F-J., and Kadenbach, B. (1986).FEBS Lett. 207, 89–94.

    Google Scholar 

  • Ise, W., Hacker, H., and Weiss, H. (1985).EMBO J. 4, 2075–2080.

    Google Scholar 

  • Jarausch, J., and Kadenbach, B. (1985).Eur. J. Biochem. 146, 211–217.

    Google Scholar 

  • John, P., and Whatley, F. R. (1977).Biochem. Biophys. Acta 463, 129–153.

    Google Scholar 

  • Kadenbach, B. (1983).Trends Biochem. Sci. 8, 398–400.

    Google Scholar 

  • Kadenbach, B. (1986).J. Bioenerg. Biomembr. 18, 39–54.

    Google Scholar 

  • Kadenbach, B., and Merle, P. (1981).FEBS Lett. 135, 1–11.

    Google Scholar 

  • Kagawa, Y., Sone, H., Yoshida, M., Hirata, H., and Okamoto, H. (1976).J. Biochem. 80, 141–147.

    Google Scholar 

  • Kawato, S., Sigel, E., Carafoli, E., and Cherry, R. J. (1980).J. Biol. Chem. 255, 5508–5510.

    Google Scholar 

  • Kennaway, N. G., Wagner, M. L., Capaldi, R. A., Takamiya, S., Yanamura, W., Ruitenbeek, W., Sengers, R. C. A., and Trijbels, J. M. F. (1987).J. Inher. Metab. Dis. 10, Suppl. 2, 247–251.

    Google Scholar 

  • Kim, C. H., Radermacher, M., Kessel, M., Frank, J., and King, T. E. (1985).J. Inorg. Biochem. 23, 163–169.

    Google Scholar 

  • Kim, S. J., Lee, K. O., Takamiya, S., and Capaldi, R. A. (1987).Biochim. Biophys. Acta 894, 270–276.

    Google Scholar 

  • Klingenberg, M., Grebe, K., and Scherer, B. (1975).Eur. J. Biochem. 52, 351–363.

    Google Scholar 

  • Koerner, T. J., Hill, J., and Tzagoloff, A. (1985).J. Biol. Chem. 260, 9513–9515.

    Google Scholar 

  • Krebs, J. J. R., Hauser, H., and Carafoli, E. (1979).J. Biol. Chem. 254, 5308–5316.

    Google Scholar 

  • Kuhn-Nentwig, L., and Kadenbach, B. (1985)Eur. J. Biochem. 149, 147–158.

    Google Scholar 

  • Kurowski, B., and Ludwig, B. (1987).J. Biol. Chem. 262, 13805–13811.

    Google Scholar 

  • Lawford, H. G. (1978).Can. J. Biochem. 56, 13–22.

    Google Scholar 

  • Leonard, P., Winfield, P., Arad, T., and Weiss, H. (1981a)J. Mol. Biol. 149, 259–274.

    Google Scholar 

  • Leonard, K., Hovmoller, S., Karlsson, B., Wingfield, P., Li, Y., Perkins, S., and Weiss, H. (1981b). InVectorial Reactions in Electron and Ion Transport in Mitochondria and Bacteria (Palmieri, F., Quagliariello, E., Siliprandi, N., and Slater, E. C., eds.), Elsevier/North-Holland, Amsterdam, pp. 127–138.

    Google Scholar 

  • Leonard, K., Hacker, H., and Weiss, H. (1987).J. Mol. Biol. 194, 277–286.

    Google Scholar 

  • Lorusso, M., Gatti, D., Marzo, M., and Papa, S. (1985).FEBS Lett. 182, 370–374.

    Google Scholar 

  • Ludwig, B. (1986).FEMS Microbiol. Rev. 46, 41–56.

    Google Scholar 

  • Ludwig, B., and Schatz, G. (1980).Proc. Natl. Acad. Sci. USA 77, 196–200.

    Google Scholar 

  • Ludwig, B., Suda, K., and Cerlette, N. (1983).Eur. J. Biochem. 137, 597–602.

    Google Scholar 

  • Maarse, A. C., and Grivell, L. A. (1987).Eur. J. Biochem. 165, 419–425.

    Google Scholar 

  • Maarse, A. C., Van Loon, A. P. G. M., Reizman, H., Gregor, I., Schatz, G., and Grivel L. A. (1984).EMBO J. 3, 2831–2837.

    Google Scholar 

  • Malatesta, F., Darley-Usmar, V. M., de Jong, C., Prochaska, L. G., Bisson, R., Capaldi, R. A., Steffens, G. C. M., and Buse, G. (1983).Biochemistry 22, 4405–4411.

    Google Scholar 

  • Meinecke, L., and Buse, G. (1985).Hoppe-Seylers Z. Physiol. Chem. 366, 687–694.

    Google Scholar 

  • Meinecke, L., and Buse, G. (1986).Hoppe-Seylers Z. Physiol. Chem. 367, 67–73.

    Google Scholar 

  • Meinecke, L., Steffens, G. J., and Buse, G. (1984).Hoppe-Seylers Z. Physiol. Chem. 365, 313–320.

    Google Scholar 

  • Millet, F., Darley-Usmar, V. M., and Capaldi, R. A. (1982).Biochemistry 21, 3857–3862.

    Google Scholar 

  • Montecucco, C., Schiavo, E., and Bisson, R. (1986).Biochem. J. 234, 241–243.

    Google Scholar 

  • Morgan-Hughes, J. A. (1982). InSkeletal Muscle Pathology (Mastaglia, F. L., and Walton, J., eds.), Churchill-Livingstone, New York, pp. 309–399.

    Google Scholar 

  • Morgan-Hughes, J. A., and Landon, D. N. (1983). InMitochondrial Pathology in Muscle Diseases (Scarlato, G., and Cerri, C., eds.), Piccin Medical Books, Padova, Italy, pp. 19–37.

    Google Scholar 

  • Nelson, B. D., and Meldel-Hartvig, I. (1977).Eur. J. Biochem. 80, 267–274.

    Google Scholar 

  • Nobrega, F. G., and Tzagoloff, A. (1980).J. Biol. Chem. 255, 9828–9837.

    Google Scholar 

  • Oudshoorn, P., Van Steeg, H., Swinkels, B. W., Schoppink, P., and Grivell, L. A. (1987).Eur. J. Biochem. 163, 97–103.

    Google Scholar 

  • Phelps, D. C., and Hatefi, Y. (1981).J. Biol. Chem. 256, 8217–8221.

    Google Scholar 

  • Poole, R. K. (1983).Biochim. Biophys. Acta 726, 205–243.

    Google Scholar 

  • Power, S. D., Lochrie, M. A., Patterson, T. E., and Poyton, R. O. (1984a).J. Biol. Chem. 259, 6571–6574.

    Google Scholar 

  • Power, S. D., Lochrie, M. A., and Poyton, R. O. (1984b).J. Biol. Chem. 259, 6575–6578.

    Google Scholar 

  • Power, S. D., Lochrie, M. A., and Poyton, R. O. (1986).J. Biol. Chem. 261, 9206–9209.

    Google Scholar 

  • Pratje, E., Mannhaupt, G., Michaelis, G., and Beyreuther, K. (1983).EMBO J. 2, 1049–1054.

    Google Scholar 

  • Ragan, C. I. (1980). InSubcellular Biochemistry (Roodyn, D. B., ed.), Vol. 7, Plenum Press, New York, pp. 267–307.

    Google Scholar 

  • Ragan, C. I., Galante, Y. M., Hatefi, Y., and Ohnishi, T. (1982)Biochemistry 21, 590–594.

    Google Scholar 

  • Raitio, M., Jalli, T., and Saraste, M. (1987).EMBO J. 6, 2825–2833.

    Google Scholar 

  • Robinson, N. C., and Capaldi, R. A. (1977).Biochemistry 16, 375–381.

    Google Scholar 

  • Sacher, R., Steffens, C. J., and Buse, G. (1979).Hoppe-Seylers Z. Physiol. Chem. 360, 1385–1392.

    Google Scholar 

  • Sadler, I., Suda, K., Schatz, G., Kudewitz, F., and Haid, A. (1984).EMBO J. 3, 2137–2143.

    Google Scholar 

  • Saraste, M., Raitio, M., Jalli, T., and Peramaa, A. (1986).FEBS Lett. 206, 154–156.

    Google Scholar 

  • Schagger, H., von Jagow, G., Borchart, U., and Machleidt, W. (1983).Hoppe-Seylers Z. Physiol. Chem. 364, 307–311.

    Google Scholar 

  • Schagger, H., Borchart, U., Aquila, H., Link, T. A., and von Jagow, G., (1985)FEBS Lett. 190, 89–94.

    Google Scholar 

  • Schagger, H., Link, T. A., Engel, W. D., and von Jagow, G. (1986).Methods Enzymol. 126, 224–237.

    Google Scholar 

  • Schagger, H., Borchart, U., Machleidt, W., Link, T. A., and von Jagow, G. (1987).FEBS Lett. 219, 161–168.

    Google Scholar 

  • Schatz, G., and Butow, R. A. (1983).Cell 32, 316–318.

    Google Scholar 

  • Sengers, R. C. A., Trijbels, J. M. F., Bakkeren, J. A. J. M., Ruitenbeek, W., Janssen, A. J. M., Stadhouders, A. M., and Laak, H. J. (1984).Eur. J. Pediat. 141, 178–180.

    Google Scholar 

  • Sinjorgo, K. M. C., Hakvoort, T. B. M., Durak, I., Draijer, J. W., Post, J. K. P., and Muijers, A. O. (1987a).Biochim. Biophys. Acta 890, 144–150.

    Google Scholar 

  • Sinjorgo, K. M. C., Durak, I., Dekker, H. L., Edel, C. M., Hakvoort, T. B. M., van Gelder, B. F., and Muijsers, A. O. (1987b).Biochim. Biophys. Acta 893, 251–258.

    Google Scholar 

  • Slater, E. C. (1974). InDynamics of Energy Transducing Membranes (Emsler, L., Estabrook, R., and Slater, E. C., eds.), Elsevier/North-Holland, Amsterdam, pp. 1–20.

    Google Scholar 

  • Smith, R. J., and Capaldi, R. A. (1977).Biochemistry 16, 2629–2633.

    Google Scholar 

  • Smith, S., Collingham, I. R., and Ragan, C. I. (1980).FEBS Lett. 110, 279–282.

    Google Scholar 

  • Steffens, G. C. M., Steffens, G. J., and Buse, G. (1979).Hoppe-Seylers Z. Physiol. Chem. 360, 1650–1661.

    Google Scholar 

  • Takamiya, S., Yanamura, W., Capaldi, R. A., Kennaway, N. G., Bart, R., Sengers, R. C. A., Trijbels, J. M. F., and Ruitenbeek, W. (1986).Ann. N.Y. Acad. Sci. 488, 33–43.

    Google Scholar 

  • Takamiya, S., Lindorfer, M. A., and Capaldi, R. A. (1987).FEBS Lett. 218, 277–282.

    Google Scholar 

  • Tanaka, M., Haniu, M., Yasunobu, T., Yu, C-A., Yu, L., Wei, Y-H., and King, T. E. (1979).J. Biol. Chem. 254, 3879–3885.

    Google Scholar 

  • Thalenfield, B. E., and Tzagoloff, A. (1980).J. Biol. Chem. 255, 6173–6180.

    Google Scholar 

  • Tzagoloff, A. (1982).Mitochondria, Plenum Press, New York.

    Google Scholar 

  • Tzagoloff, A., Wu, M., and Crivellone, M. (1986).J. Biol. Chem. 261, 17163–17169.

    Google Scholar 

  • Van Loon, A. P. G. M., De Groot, R. J., De Haan, M., Dekker, A., and Grivell, L. A. (1984).EMBO J. 3, 1039–1043.

    Google Scholar 

  • Vanneste, W. H. (1966).Biochim. Biophys. Acta 113, 175–178.

    Google Scholar 

  • Vignais, P. V., Vignais, P. M., and Defaye, G. (1973).Biochemistry 12, 1508–1519.

    Google Scholar 

  • Vinogradov, A. D., and King, T. E. (1979).Methods Enzymol. 55, 118–127.

    Google Scholar 

  • von Jagow, G., Schagger, H., Riccio, P., Klingenberg, M., and Kolb, H. J. (1977).Biochim. Biophys. Acta 462, 549–556.

    Google Scholar 

  • Wainio, W. W. (1970).The Mammalian Mitochondrial Respiratory Chain, Academic Press, New York.

    Google Scholar 

  • Wakabayashi, S., Matsubara, H., Kim, C. H., and King, T. E. (1982a).J. Biol. Chem. 257, 9335–9344.

    Google Scholar 

  • Wakabayashi, S., Takeda, H., Matsubara, H., Kim, C. H., and King, T. E. (1982b).J. Biochem. 91, 2077–2085.

    Google Scholar 

  • Wakabayashi, S., Takao, T., Shimonishi, Y., Kuramitsu, S., Matsubara, H., Wang, T., Zhang, Z., and King, T. E. (1985).J. Biol. Chem. 260, 337–343.

    Google Scholar 

  • Wright, R. M., Dircks, L. K., and Poyton, R. O. (1986).J. Biol. Chem. 261, 17183–17191.

    Google Scholar 

  • Yagi, T. (1986).Arch. Biochem. Biophys. 250, 302–311.

    Google Scholar 

  • Zeviani, M., Nakagawa, M., Herbert, J., Lomax, M. I., Grossman, L. I., Shebany, A. A., Miranda, A. F., DiMauro, S., and Schon, E. A. (1987a).Gene 55, 205–217.

    Google Scholar 

  • Zeviani, M., Peterson, P. L., Servidel, S., Bonilla, E., and DiMauro, S. (1987b).Neurology 37, 64–70.

    Google Scholar 

  • Zhang, Y-Z., Lindorfer, M., and Capaldi, R. A. (1988).Biochemistry 27, 1389–1394.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Molecular Biology, University of Oregon, 97403, Eugene, Oregon

    Roderick A. Capaldi, Diego Gonzalez Halphen, Yu-Zhong Zhang & Wayne Yanamura

Authors
  1. Roderick A. Capaldi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Diego Gonzalez Halphen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yu-Zhong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wayne Yanamura
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Capaldi, R.A., Halphen, D.G., Zhang, YZ. et al. Complexity and tissue specificity of the mitochondrial respiratory chain. J Bioenerg Biomembr 20, 291–311 (1988). https://doi.org/10.1007/BF00769634

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00769634

Key Words

Search

Navigation