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Oxygen activation and the conservation of energy in cell respiration

Nature volume 356, pages 301–309 (1992)Cite this article

Abstract

Many of the membrane-associated oxidases that catalyse respiratory reduction of 02 to water simultaneously couple this exergonic reaction to the translocation of protons across the inner mitochondrial membrane, or the cell membrane in prokaryotes, a process by which metabolic energy is conserved for subsequent synthesis of ATP. The molecular mechanism of 02 reduction and its linkage to H+ translocation are now emerging. The bimetallic haem iron–copper reaction centre in this family of enzymes is the critical structure for catalysis of both these processes.

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References

  1. Mitchell, P. Eur. J. Biochem. 95, 1–20 (1979).

    CAS  PubMed  Google Scholar 

  2. Wikström, M. Nature 266, 271–273 (1977).

    ADS  PubMed  Google Scholar 

  3. Solioz, M., Carafoli, E. & Ludwig, B. J. biol. Chem. 257, 1579–1582 (1982).

    CAS  PubMed  Google Scholar 

  4. Sone, N. & Hinkle, P. J. biol. Chem. 257, 12600–12604 (1982).

    CAS  PubMed  Google Scholar 

  5. Puustinen, A., Finel, M., Virkki, M. & Wikström, M. FEBS Lett. 249, 163–167 (1989).

    CAS  PubMed  Google Scholar 

  6. Babcock, G. T. et al. Biochemistry 28, 9557–9565 (1989).

    CAS  PubMed  Google Scholar 

  7. George, P. in Oxidases and Related Redox Systems Vol. 1 (eds King, T. E., Mason, H. S. & Morrison, M.) 3–33 (Wiley, New York, 1965).

    Google Scholar 

  8. Rodgers, M. A. J. & Powers, E. L. (eds) Oxygen and Oxy-Radicals in Chemistry and Biology (Academic, New York, 1981).

  9. Naqui, A., Chance, B. & Cadenas, E. A. Rev. Biochem. 55, 137–166 (1986).

    CAS  Google Scholar 

  10. Beinert, H. Chemica Scripta 28A, 35–40 (1988).

    Google Scholar 

  11. Malmström, B. G. Chem. Rev. 90, 1247–1260 (1990).

    Google Scholar 

  12. Wikström, M., Krab, K. & Saraste, M. Cytochrome Oxidase—A Synthesis (Academic, New York and London, 1981).

    Google Scholar 

  13. Ludwig, B. FEMS Microbiol. Rev. 46, 41–56 (1987).

    CAS  Google Scholar 

  14. Anraku, Y. A. Rev. Biochem. 57, 101–132 (1988).

    CAS  Google Scholar 

  15. Saraste, M. Q. Rev. Biophys. 23, 331–336 (1990).

    CAS  PubMed  Google Scholar 

  16. Zimmerman, B. H., Nitsche, C. I., Fee, J. A., Rusnak, F. & Munck, E. Proc. natn. Acad. Sci. U.S.A. 85, 5779–5783 (1988).

    ADS  Google Scholar 

  17. Chepuri, V., Lemieux, L., Au, D. C.-T. & Gennis, R. B. J. biol. Chem. 265, 11185–11192 (1990).

    CAS  PubMed  Google Scholar 

  18. Lauraeus, M., Haltia, T., Saraste, M. & Wikström, M. Eur. J. Biochem. 197, 699–705 (1991).

    CAS  PubMed  Google Scholar 

  19. Lübben, M., Kolmer, B. & Saraste, M. EMBO J. 11, 805–812 (1992).

    PubMed  PubMed Central  Google Scholar 

  20. Santana, M. et al. J. biol. Chem. (in the press).

  21. Puustinen, A. & Wikström, M. Proc. natn. Acad. Sci. U.S.A. 88, 6122–6126 (1991).

    ADS  CAS  Google Scholar 

  22. Wu, W. et al. J. Am. Chem. Soc. 114, 1182–1187 (1992).

    CAS  Google Scholar 

  23. Salerno, J. C., Bolgiano, B., Poole, R. B. & Ingledew, W. J. J. biol. Chem. 265, 4364–4368 (1990).

    CAS  PubMed  Google Scholar 

  24. Lemieux, L. J., Calhoun, M. W., Thomas, Ingledew, W. J. & Gennis, R. B. J. biol. Chem. (in the press).

  25. Minagawa, J., Mogi, T., Gennis, R. B. & Anraku, Y. J. biol. Chem. (in the press).

  26. Shapleigh, J. et al. Proc. natn. Acad. Sci. U.S.A. (in the press).

  27. Holm, L., Saraste, M. & Wikström, M. EMBO J. 6, 2819–2823 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Haltia, T. & Wikström, M. in (ed. Ernster, L.) Molecular Mechanisms in Bioenergetics (Elsevier, Amsterdam, in the press).

  29. Steffens, G. J. & Buse, G. Hoppe-Seyler's Z. physiol. Chem. 360, 613–619 (1979).

    CAS  Google Scholar 

  30. Martin, C. T., Scholes, C. P. & Chan, S. I. J. biol. Chem. 263, 8420–8429 (1988).

    CAS  PubMed  Google Scholar 

  31. Kroneck, P. M. H., Antholine, W. A., Riester, J. & Zumft, W. G. FEBS Lett. 242, 70–74 (1988).

    CAS  PubMed  Google Scholar 

  32. Puustinen, A., Finel, M., Haltia, T., Gennis, R. B. & Wikström, M. Biochemistry 30, 3936–3942 (1991).

    CAS  PubMed  Google Scholar 

  33. Capaldi, R. A. Archs Biochem. Biophys. 280, 252–262 (1990).

    CAS  Google Scholar 

  34. Haltia, T. et al. EMBO J. 8, 3571–3579 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Haltia, T., Saraste, M. & Wikström, M. EMBO J. 10, 2015–2021 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Wikström, M. Chemica Scripta 28A, 71–74 (1988).

    Google Scholar 

  37. Wikström, M. Nature 338, 776–778 (1989).

    ADS  PubMed  Google Scholar 

  38. Chance, B., Saronio, C. & Leigh, J. S. Jr J. biol. Chem. 250, 9226–9237 (1975).

    CAS  PubMed  Google Scholar 

  39. Bouges-Bocquet, B. Biochim. biophys. Acta 594, 85–103 (1980).

    CAS  PubMed  Google Scholar 

  40. Gibson, Q. & Greenwood, C. Biochem. J. 86, 541–554 (1963).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Mims, M. P., Porras, A. G., Olson, J. S., Noble, R. W. & Peterson, J. A. J. biol. Chem. 258, 14219–14232 (1983).

    CAS  PubMed  Google Scholar 

  42. Chang, C. K. & Dolphin, D. Proc. natn. Acad. Sci. U.S.A. 73, 3338–3342 (1976).

    ADS  CAS  Google Scholar 

  43. Alben, J. O., Moh, P. P., Fiamingo, F. G. & Altschuld, R. A. Proc. natn. Acad. Sci. U.S.A. 78, 234–237 (1981).

    ADS  CAS  Google Scholar 

  44. Findsen, E. W., Centeno, J., Babcock, G. T. & Ondrias, M. R. J. Am. chem. Soc. 109, 5367–5372 (1987).

    CAS  Google Scholar 

  45. Woodruff, W. H. et al. Proc. natn. Acad. Sci. U.S.A. 88, 2588–2592 (1991).

    ADS  CAS  Google Scholar 

  46. Blackmore, R. S., Greenwood, C. & Gibson, Q. H. J. biol. Chem. 266, 19245–19249 (1991).

    CAS  PubMed  Google Scholar 

  47. Wikström, M. Proc. natn. Acad. Sci. U.S.A. 78, 4051–4054 (1981).

    ADS  Google Scholar 

  48. Wikström, M. Chemica Scripta 27B, 53–58 (1987).

    Google Scholar 

  49. Wikström, M. FEBS Lett. 231, 247–252 (1988).

    PubMed  Google Scholar 

  50. Babcock, G. T., Jean, J. M., Johnston, L. N., Palmer, G. & Woodruff, W. H. J. Am. chem. Soc. 106, 8305–8306 (1984).

    CAS  Google Scholar 

  51. Orii, Y. J. biol. Chem. 259, 7187–7190 (1984).

    CAS  PubMed  Google Scholar 

  52. Orii, Y. Ann. N.Y. Acad. Sci. 550, 105–117 (1988).

    ADS  CAS  PubMed  Google Scholar 

  53. Varotsis, C., Woodruff, W. H. & Babcock, G. T. J. Am. Chem. Soc. 111, 6439–6440 (1989); 112, 1297 (1990).

    CAS  Google Scholar 

  54. Ogura, T., Takahashi, S., Shinzawa-Itoh, K., Yoshikawa, S. & Kitagawa, T. J. Am. chem. Soc. 112, 5630–5631 (1990).

    CAS  Google Scholar 

  55. Han, S., Ching, Y.-C. & Rousseau, D. L. Proc. natn. Acad. Sci. U.S.A. 87, 2491–2495 (1990).

    ADS  CAS  Google Scholar 

  56. Oertling, W. A., Kean, R. T., Wever, R. & Babcock, G. T. Inorg. Chem. 29, 2633–2645 (1990).

    CAS  Google Scholar 

  57. Lindsay, J. G., Owen, C. S. & Wilson, D. F. Archs. Biochem. Biophys. 169, 492–505 (1975).

    CAS  Google Scholar 

  58. Malatesta, F., Sarti, P., Antonini, G., Vallone, B. & Brunori, M. Proc. natn. Acad. Sci. U.S.A. 87, 7410–7413 (1990).

    ADS  CAS  Google Scholar 

  59. Clore, G. M., Andréasson, L.-E., Karlsson, B. & Malmström, B. G. Biochem. J. 185, 139–154 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Hill, B. C., Greenwood, C. & Nicholls, P. Biochim. biophys. Acta 853, 91–113 (1986).

    CAS  PubMed  Google Scholar 

  61. Varotsis, C. & Babcock, G. T. Biochemistry 29, 7357–7362 (1990).

    CAS  PubMed  Google Scholar 

  62. Han, S., Ching, Y.-C. & Rousseau, D. L. Proc. natn. Acad. Sci. U.S.A. 87, 8408–8412 (1990).

    ADS  CAS  Google Scholar 

  63. Wilson, M. T., Jensen, P., Aasa, R., Malmström, B. G. & Vänngård, T. Biochem. J. 203, 483–492 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Malmström, B. G. A. Rev. Biochem. 51, 21–59 (1982).

    Google Scholar 

  65. Varotsis, C., Woodruff, W. H. & Babcock, G. T. J. biol. Chem. 265, 11131–11136 (1990).

    CAS  PubMed  Google Scholar 

  66. Han, S., Ching, Y.-C. & Rousseau, D. L. Biochemistry 29, 1380–1384 (1990).

    CAS  PubMed  Google Scholar 

  67. Morgan, J. E. & Wikström, M. Biochemistry 30, 948–958 (1991).

    CAS  PubMed  Google Scholar 

  68. Oliveberg, M., Hallén, S. & Nilsson, T. Biochemistry 30, 436–440 (1991).

    CAS  PubMed  Google Scholar 

  69. Poulos, T. L. Adv. Inorg. Biochem. 7, 1–52 (1987).

    Google Scholar 

  70. Tabushi, I. Coord. Chem. Revs. 86, 1–42 (1988).

    CAS  Google Scholar 

  71. Traylor, T. G. Pure appl. Chem. 63, 265–274 (1991).

    CAS  Google Scholar 

  72. Babcock, G. T. in Biological Applications of Resonance Raman Spectroscopy Vol. 3 (ed. Sprio, T. G.) 294–346 (Wiley, New York, 1988).

    Google Scholar 

  73. Ogura, T., Takahashi, S., Shinzawa-Itoh, K., Yoshikawa, S. & Kitagawa, T. Bull. Chem. Soc. Jpn. (in the press).

  74. Varotsis, C., Zhang, Y. & Babcock, G. T. Proc. natn. Acad. Sci. U.S.A. (submitted).

  75. Ahmad, S. et al. Inorg. Chem. 27, 2230–2233 (1988).

    CAS  Google Scholar 

  76. Proniewicz, L. M., Paeng, I. R. & Nakamoto, K. J. Am. Chem. Soc. 113, 3294–3303 (1991).

    CAS  Google Scholar 

  77. Yoshikawa, S. & Caughey, W. S. J. biol. Chem. 265, 7945–7958 (1990).

    CAS  PubMed  Google Scholar 

  78. Blair, D. F., Witt, S. N. & Chan, S. I. J. Am. chem Soc. 107, 7389–7399 (1985).

    CAS  Google Scholar 

  79. Hansson, O., Karlsson, B., Aasa, R., Vänngård, T. & Malmström, B. G. EMBO J. 1, 1295–1297 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Ogura, T., Takahashi, S., Shinzawa-Itoh, K., Yoshikawa, S. & Kitagawa, T. J. biol. Chem. 265, 14721–14723 (1990).

    CAS  PubMed  Google Scholar 

  81. Han, S., Ching, Y.-C. & Rousseau, D. L. Nature 348, 89–90 (1990).

    ADS  CAS  PubMed  Google Scholar 

  82. Wrigglesworth, J. M. Biochem. J. 217, 715–719 (1984).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Vygodina, T., & Konstantinov, A. A. Biochem. biophys. Acta 973, 390–398 (1989).

    CAS  PubMed  Google Scholar 

  84. Vygodina, T. V., Schmidmeyer, K. & Konstantinov, A. A. Biol. Membr. (in Russian) (in the press)

  85. Williams, R. J. P. J. theor. Biol. 1, 1–17 (1961).

    CAS  PubMed  Google Scholar 

  86. Mitchell, P. in Of Oxygen, Fuels and Living Matter (ed. Semenza, G.) 1–160 (Wiley, New York, 1981).

    Google Scholar 

  87. Chan, S. I. & Li, P. M. Biochemistry 29, 1–12 (1990).

    CAS  PubMed  Google Scholar 

  88. Nicholls, P. & Wrigglesworth, J. M. Ann. N. Y. Acad. Sci. 550, 59–67 (1988).

    ADS  CAS  PubMed  Google Scholar 

  89. Kobayashi, K., Une, H. & Hayashi, K. J. biol. Chem. 264, 7976–7980 (1989).

    CAS  PubMed  Google Scholar 

  90. Hill, B. C. J. biol. Chem. 266, 2219–2226 (1991).

    CAS  PubMed  Google Scholar 

  91. Antalis, T. M. & Palmer, G. J. biol. Chem. 257, 6194–6206 (1982).

    CAS  PubMed  Google Scholar 

  92. Wikström, M. & Krab, K. Biochim. biophys Acta 549, 177–222 (1979).

    PubMed  Google Scholar 

  93. Blair, D. F., Gelles, J. & Chan, S. I. Biophys. J. 50, 713–733 (1986).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  94. Krab, K. & Wikström, M. Biochim. biophys. Acta 895, 25–39 (1987).

    CAS  PubMed  Google Scholar 

  95. Malmström, B. G. FEBS Lett. 250, 9–21 (1989).

    PubMed  Google Scholar 

  96. Scott, R. A. A. Rev. Biophys. biophys. Chem. 18, 137–158 (1989).

    CAS  Google Scholar 

  97. Henderson, R. et al. J. molec. Biol. 213, 899–929 (1990).

    CAS  PubMed  Google Scholar 

  98. Wikström, M. & Krab, K. in Energy Conservation in Biological Membranes (eds Schäfer, G. & Klingenberg, M.) 128–139 (Springer, Berlin and Heidelberg, 1978).

    Google Scholar 

  99. Mitchell, P. Ann. N. Y. Acad. Sci. 550, 185–198 (1988).

    ADS  CAS  PubMed  Google Scholar 

  100. Williams, R. J. P. FEBS Lett. 226, 1–7 (1987).

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Chemistry, Michigan State University, East Lansing, Michigan, 48824, USA

    Gerald T. Babcock

  2. Department of Medical Chemistry, University of Helsinki, Helsinki, 00170, Finland

    Mårten Wikström

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Babcock, G., Wikström, M. Oxygen activation and the conservation of energy in cell respiration. Nature 356, 301–309 (1992). https://doi.org/10.1038/356301a0

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