Skip to main content

The random collision model and a critical assessment of diffusion and collision in mitochondrial electron transport

Journal of Bioenergetics and Biomembranes volume 18, pages 331–368 (1986)Cite this article

Abstract

This review focuses on our studies over the past ten years which reveal that the mitochondrial inner membrane is a fluid-state rather than a solid-state membrane and that all membrane proteins and redox components which catalyze electron transport and ATP synthesis are in constant and independent diffusional motion. The studies reviewed represent the experimental basis for therandom collision model of electron transport. We present five fundamental postulates upon which the random collision model of mitochondrial electron transport is founded: (1) All redox components areindependent lateral diffusants; (2) Cytochromec diffuses primarily inthree dimensions; (3) Electron transport is adiffusion-coupled kinetic process; (4) Electron transport is amulticollisional, obstructed, long-range diffusional process; (5) The rates of diffusion of the redox components have a direct influence on the overall kinetic process of electron transport and can berate limiting, as indiffusion control. The experimental rationales and the results obtained in testing each of the five postulates of the random collision model are presented. In addition, we offer the basic concepts, criteria and experimental strategies that we believe are essential in considering the significance of the relationship between diffusion and electron transport. Finally, we critically explore and assess other contemporary studies on the diffusion of inner membrane components related to electron transport including studies on: rotational diffusion, immobile fractions, complex formation, dynamic aggregates, and rates of diffusion. Review of all available data confirms the random collision model and no data appear to exist that contravene it. It is concluded that mitochondrial electron transport is a diffusion-based random collision process and that diffusion has an integral and controlling affect on electron transport.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Alecio, M. R., Golan, D. E., Veatch, W. R., and Rando, R. R. (1982).Proc. Natl. Acad. Sci. USA 79, 5171.

    Google Scholar 

  • Aronada, F. J., and Gomez-Fernandez, J. C. (1985).Biochim. Biophys. Acta 820, 16.

    Google Scholar 

  • Barisas, B. G., and Leuther, M. D. (1979).Biophys. Chem. 10, 221.

    Google Scholar 

  • Cadman, A. D., Fleming, R., and Guy, R. H. (1981).Biophys. J. 37, 569.

    Google Scholar 

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

    Google Scholar 

  • Chance, B., and Erecinska, M. (1975).Eur. J. Biochem. 54, 521.

    Google Scholar 

  • Chazotte, B., Wu, E-S., and Hackenbrock, C. R. (1983a).Biochem. Trans. 12, 463.

    Google Scholar 

  • Chazotte, B., Wu, E-S., and Hackenbrock, C. R. (1983b).Fed. Proc. 42, 2170.

    Google Scholar 

  • Chazotte, B., and Hackenbrock, C. R. (1984). InThird European Bioenergetics Conference, Short Reports, p. 697. Congress-Edition, Hanover.

    Google Scholar 

  • Chazotte, B., Wu, E-S., Höchli, M., and Hackenbrock, C. R. (1985).Biochim. Biophys. Acta 818, 87.

    Google Scholar 

  • Davis, D. G. (1972).Biochem. Biophys. Res. Commun. 49, 1492.

    Google Scholar 

  • Davis, D. G., and Inesi, G. (1972).Biochim. Biophys. Acta. 282, 180.

    Google Scholar 

  • Derzko, Z. and Jacobson, K. (1980).Biochemistry 19, 6050.

    Google Scholar 

  • Eisinger, J., Flores, J., and Peterson, W. P. (1986).Biophys. J. 49, 987.

    Google Scholar 

  • Estabrook, R., and Holowinsky, A. (1961).J. Cell Biol. 9, 19.

    Google Scholar 

  • Eyring, H. (1935).J. Chem. Phys. 3, 107.

    Google Scholar 

  • Fato, R., Battino, M., Castelli, G., and Lenaz, G. (1985).FEBS Lett. 179, 238.

    Google Scholar 

  • Feinstein, M. B., Fernandez, S. M., and Shai'afi, R. I. (1975).Biochim. Biophys. Acta 413, 354.

    Google Scholar 

  • Franck, J., and Rabinowitch, E. (1934).Trans. Faraday Soc. 30, 120.

    Google Scholar 

  • Freedman, J. A., and Chan, S. H. P. (1983).J. Biol. Chem. 258, 5885.

    Google Scholar 

  • Gear, A. R. L., and Bednarek, J. M. (1972).J. Cell. Biol. 56, 325.

    Google Scholar 

  • Gupte, S., Wu, E-S., Höchli, L., Höchli, M., Jacobson, K., Sowers, A., and Hackenbrock, C. R. (1984).Proc. Natl. Acad. Sci. USA 81, 2606.

    Google Scholar 

  • Gutman, M. (1980).Biphim. Biophys. Acta 594, 53.

    Google Scholar 

  • Hackenbrock, C. R. (1966).J. Cell Biol. 30, 269.

    Google Scholar 

  • Hackenbrock, C. R. (1968a).J. Cell Biol. 37, 345.

    Google Scholar 

  • Hackenbrock, C. R. (1968b).Proc. Natl. Acad. Sci. USA 61, 598.

    Google Scholar 

  • Hackenbrock, C. R. (1976). InStructure of Biological Membranes: 34th Nobel Foundation Symposium (Abrahamson, S., and Pasher, I., eds), Plenum Press, New York, p. 199.

    Google Scholar 

  • Hackenbrock, C. R. (1981).Trends Biol. Sci. 6, 151.

    Google Scholar 

  • Hackenbrock, C. R., and Hammon, K. M. (1975).J. Biol. Chem. 250, 9185.

    Google Scholar 

  • Hackenbrock, C. R., Höchli, M., and Chau, R. M. (1976).Biochim. Biophys. Acta 455, 466.

    Google Scholar 

  • Hackenbrock, C. R., Gupte, S. S., and Chazotte, B. (1985). InAchievements and Perspectives of Mitochondrial Research, Volume I:Bioenergetics (Quagliariello, E., Slater, E. C., Palmieri, F., Saccone, C., and Kroon, A. M., eds.), Elsevier, Amsterdam, p. 83.

    Google Scholar 

  • Hackenbrock, C. R., Chazotte, B., and Gupte, S. S. (1986). InBiomedical and Clinical Aspects of Coenzyme Q, Volume 5 (Yamamura, U., and Folkers, K., eds.), Elsevier, Amsterdam, in press.

    Google Scholar 

  • Hardt, S. L. (1979).Biophys. Chem. 10, 239.

    Google Scholar 

  • Hatefi, Y., and Galante, Y. M. (1978). InEnergy Conservation in Biological Membranes (Schäfer, G., and Klingenberg, M., eds.), Springer, Berlin, p. 19.

    Google Scholar 

  • Heron, C., Ragan, C. I., and Trumpower, B. L. (1978).Biochem. J. 170, 791.

    Google Scholar 

  • Hille, B. (1984). InIonic Channels of Excitable Membranes, Sinauer Associates, Inc., p. 14.

  • Höchli, M., and Hackenbrock, C. R. (1976).Proc. Natl. Acad. Sci. USA 73, 1636.

    Google Scholar 

  • Höchli, M., and Hackenbrock, C. R. (1977).J. Cell Biol. 72, 278.

    Google Scholar 

  • Höchli, M., and Hackenbrock, C. R. (1979).Proc. Natl. Acad. Sci. USA 76, 1236.

    Google Scholar 

  • Höchli, M., Höchli, L., and Hackenbrock, C. R. (1985).Eur. J. Cell Biol. 38, 1.

    Google Scholar 

  • Hochman, J. H., Schindler, M., Lee, J. G., and Ferguson-Miller, S. (1982).Proc. Natl. Acad. Sci. USA 79, 6866.

    Google Scholar 

  • Hochman, J. H., Schindler, M., Lee, J. G., and Ferguson-Miller, S. (1983). InBiochemistry of Metabolic Processes (Lennon, D., Stratman, F., and Zahlten, R., eds.), Elsevier Biomedical Press, New York, p. 441.

    Google Scholar 

  • Hochman, J., Ferguson-Miller, S., and Schindler, M. (1985).Biochemistry 24, 2507.

    Google Scholar 

  • Horowitz, A. F., Horsely, W. J., and Klein, M. P. (1972).Proc. Natl. Acad. Sci. USA 69, 590.

    Google Scholar 

  • Jacobs, E. E., and Sanadi, D. R. (1960).J. Biol. Chem. 235, 531.

    Google Scholar 

  • Jacobson, K., Derzko, Z., Wu, E-S., Hou, Y., and Poste, G. (1976).J. Supramol. Struct. 5, 565.

    Google Scholar 

  • Jacobson, K., Hou, Y., Derzko, Z., Wojcieszyn, J., and Organisciak, D. (1981).Biochemistry 20, 5268.

    Google Scholar 

  • Johnson, F. H., Eyring, H., and Stover, B. J. (1975). InTheory of Rate Processes in Biology and Medicine, Wiley, New York.

    Google Scholar 

  • Kapitza, H. G., and Sackman, E. (1980).Biochim. Biophys. Acta 595, 56.

    Google Scholar 

  • Kawato, S., Sigel, E., Carafoli, E., and Cherry, R. J. (1981).J. Biol. Chem. 256, 7518.

    Google Scholar 

  • Kawato, S., Lehner, C., Müller, M., and Cherry, R. J. (1982).J. Biol. Chem. 257, 6470.

    Google Scholar 

  • Klingenberg, M., and Kröger, A. (1967). InBiochemistry of Mitochondria (Slater, E. C., Kanigu, Z., and Wojtczak, L., eds.), Academic Press, New York, p. 11.

    Google Scholar 

  • Koppenol, W. H., and Margoliash, E. (1982).J. Biol. Chem. 257, 4426.

    Google Scholar 

  • Kröger, A., and Klingenberg, M. (1973a).Eur. J. Biochem. 34, 313.

    Google Scholar 

  • Kröger, A., and Klingenberg, M. (1973b).Eur. J. Biochem. 39, 598.

    Google Scholar 

  • Lakowicz, J. R., and Hogan, D. (1980).Chem. Phys. Lipids 26, 1.

    Google Scholar 

  • Lee, A. G., Birdsall, N. J., and Metcalfe, J. C. (1973).Biochemistry 12, 1650.

    Google Scholar 

  • Lemasters, J. J. (1978).FEBS Lett. 88, 10.

    Google Scholar 

  • Lenaz, G., Fato, R., Parenti Castilli, G., and Battino, M. (1985). InAchievements and Perspectives in Mitochondrial Research (abstracts) (Quagliariello, E., Slater, E. C., Palmieri, F., Saccone, C., and Kroon, A. M., eds.), Adriatica Editrice, Bari, Italy, p. 62.

    Google Scholar 

  • Lenaz, G., Battino, M., Esposti, M., Fato, R., and Parenti-Castelli, G. (1986). InBiomedical and Clinical Aspects of Coenzyme Q, Volume 5 (Yamamura, Y., and Folkers, K., eds.), Elsevier, Amsterdam, in press.

    Google Scholar 

  • Marcus, R. A., and Sutin, N. (1985).Biochim. Biophys. Acta 811, 265.

    Google Scholar 

  • Peters, R., and Cherry, R. J. (1982).Proc. Natl. Acad. Sci. USA 79, 4317.

    Google Scholar 

  • Rabinowitch, E. (1937).Trans. Faraday. Soc. 33, 1225.

    Google Scholar 

  • Ragan, C. I. (1978).Biochem. J. 172, 539.

    Google Scholar 

  • Ragan, C. I., and Heron, C. (1978).Biochem. J. 174, 783.

    Google Scholar 

  • Ragan, C. I., and Cottingham, I. R. (1985).Biochim. Biophys. Acta 811, 13.

    Google Scholar 

  • Rich, P. (1984).Biochim. Biophys. Acta 768, 53.

    Google Scholar 

  • Rieder, R., and Bosshard, H. R. (1980).J. Biol. Chem. 355, 4732.

    Google Scholar 

  • Rottenberg, H. (1985).Mod. Cell Biol. 4, 47.

    Google Scholar 

  • Saffman, P. G., and Delbrück, M. (1975).Proc. Natl. Acad. Sci. USA 72, 3111.

    Google Scholar 

  • Salemme, F. R. (1977).Annu. Rev. Biochem. 40, 299.

    Google Scholar 

  • Schnaitman, C., and Greenwalt, J. W. (1968).J. Cell. Biol. 38, 158.

    Google Scholar 

  • Schneider, H., Lemasters, J. J., Höchli, M., and Hackenbrock, C. R. (1980a).Proc. Natl. Acad. Sci. USA 77, 442.

    Google Scholar 

  • Schneider, H., Lemasters, J. J., Höchli, M., and Hackenbrock, C. R. (1980b).J. Biol. Chem. 255, 3748.

    Google Scholar 

  • Schneider, H., Lemasters, J. J., and Hackenbrock, C. R. (1982a).J. Biol. Chem. 257, 10789.

    Google Scholar 

  • Schneider, H., Höchli, M., and Hackenbrock, C. R. (1982b).J. Cell Biol. 94, 387.

    Google Scholar 

  • Schwerzmann, K., Cruz-Orive, L. M., Eggman, R., Sänger, A., and Weibel, E. R. (1986).J. Cell Biol. 102, 97.

    Google Scholar 

  • Slater, E. C., Berden, J. A., and Herweijer, M. A. (1985).Biochim. Biophys. Acta 811, 217.

    Google Scholar 

  • Sowers, A. E., and Hackenbrock, C. R. (1981).Proc. Natl. Acad. Sci. USA 78, 6246.

    Google Scholar 

  • Sowers, A. E., and Hackenbrock, C. R. (1985).Biochim. Biophys. Acta 821, 85.

    Google Scholar 

  • Speck, S. H., and Margoliash, E. (1984).J. Biol. Chem. 259, 1064.

    Google Scholar 

  • Stidham, M. A., McIntosh, T. J., and Siedow, J. N. (1984).Biochim. Biophys. Acta 767, 423.

    Google Scholar 

  • Stier, A., and Sackman, E. (1973).Biochim. Biophys. Acta 311, 400.

    Google Scholar 

  • Stonehuerner, J., Williams, S. B., and Miller, F. S. (1979).Biochemistry 18, 5422.

    Google Scholar 

  • Stryer, L. (1978).Annu. Rev. Biochem. 47, 819.

    Google Scholar 

  • Vanderkooi, J., Maniara, G., and Erecinska, M. (1985).J. Cell Biol. 100, 435.

    Google Scholar 

  • Veerman, E. C. I., Wilms, J., Dekker, H. L., Muijsers, A. O., van Buuren, K. J. H., van Gelder, B. F., Osheroff, N., Speck, S. H., and Margoliash, E. (1983).J. Biol. Chem. 258, 5739.

    Google Scholar 

  • Weibel, E. R., Kistler, G. S., and Scherle, W. F. (1966).J. Cell Biol. 30, 23.

    Google Scholar 

Download references

Author information

Affiliations

  1. Laboratories for Cell Biology, Department of Anatomy, School of Medicine, The University of North Carolina at Chapel Hill, 27514, Chapel Hill, North Carolina

    Charles R. Hackenbrock, Brad Chazotte & Sharmila Shaila Gupte

Authors
  1. Charles R. Hackenbrock
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brad Chazotte
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sharmila Shaila Gupte
    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

Hackenbrock, C.R., Chazotte, B. & Gupte, S.S. The random collision model and a critical assessment of diffusion and collision in mitochondrial electron transport. J Bioenerg Biomembr 18, 331–368 (1986). https://doi.org/10.1007/BF00743010

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00743010

Key words

  • Redox components
  • collision efficiency
  • diffusion-coupled reactions
  • diffusion control
  • energy of activation
  • fluorescence recovery after photobleaching
  • resonance energy transfer