Skip to main content
SpringerLink
Log in

Turnover numbers for ionophore-catalyzed cation transport across the mitochondrial membrane

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

The turnover numbers of the ionophores valinomycin, the macrolide actins, enniatin B and dicyclohexyl 18-crown-6 for translocation of cations through the mitochondrial membrane have been compared quantitatively. The rank order of decreasing maximum turnover number for K+ transport calculated on the basis of the ionophore concentration within the membrane is trinactin>dinactin∼monactin∼ valinomycin>nonactin>18-crown-6>enniatin B. The strength of binding of the ionophores to the mitochondria has the following rank order: valinomycin>macrolide actins>enniatin B>18-crown-6.

A rough proportionality was observed between the transport rate of K+, Rb+, Cs+ or Na+ with a given ionophore and the heterogeneous complexation constant of the corresponding ionophore-cation pair in two-phase extraction experiments. However, the proportionality constants between transport and the heterogeneous complexation constant differ between the ionophores. These comparisons indicate that valinomycin and enniatin B transport cations about 10 times slower than would be expected from their two-phase complexation behavior, using the complexation and transport reactions of the macrolide actins as a basis for comparison. Transport with 18-crown-6 was about 1,000 times slower than predicted. These observations are discussed in terms of partitioning of the ionophores between various regions of the mitochondrial membrane.

The data are discussed in terms of a carrier model involving hydrophilic complexes on the membrane surface in addition to hydrophobic complexes which cross the membrane.

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

  1. Chance, B., Williams, G.R. 1955. Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilisation.J. Biol. Chem. 217:383

    PubMed  Google Scholar 

  2. Ciani, S., Eisenman, G., Szabo, G. 1969. A theory for the effects of neutral carriers such as the macrotetralide actin antibiotics on the electric properties of bilayer membranes.J. Membrane Biol. 1:1

    Google Scholar 

  3. Cockrell, R.S., Harris, E.J., Pressman, B.C. 1966. Energetics of potassium transport in mitochondria induced by valinomycin.Biochemistry 5:2326

    PubMed  Google Scholar 

  4. Eisenman, G., Ciani, S., Szabo, G. 1969. The effects of the macrotetralide actin antibiotics on the equilibrium extraction of alkali metal salts into organic solvents.J. Membrane Biol. 1:294

    Google Scholar 

  5. Estabrook, R.W. 1967. Mitochondrial respiratory control and the polarographic measurement of ADP: O ratios.In: Methods in Enzymology. R. W. Estabrook and M. Pullman, editors. Vol. 10, p. 41. Academic Press, New York-London

    Google Scholar 

  6. Frensdorff, H. K. 1971. Stability constants of cyclic polyether complexes with univalent cations.J. Amer. Chem. Soc. 93:600

    Google Scholar 

  7. Funck, T., Eggers, F., Grell, E. 1972. Kinetik und Mechanismus der selektiven Bindung von Ionen durch Cyclodepsipeptid-Antibiotika.Chimia 26:637

    Google Scholar 

  8. Harris, E.J., Catlin, G., Pressman, B.C. 1967. Effect of transport-inducing antibiotics and other agents on potassium flux in mitochondria.Biochemistry 6:1360

    PubMed  Google Scholar 

  9. Haynes, D.H. 1970. Equilibrium and kinetic properties of ionophores of the valinomycin type in model systems and biological membranes. Ph. D. Thesis. University of Pennsylvania, Philadelphia, Pa., pp. 127–139

    Google Scholar 

  10. Haynes, D.H. 1972. Detection of ionophore cation complexes on phospholipid membranes.Biochim. Biophys. Acta 255:406

    PubMed  Google Scholar 

  11. Haynes, D.H. 1972. The kinetics of potassium ion complexation by ionophores.FEBS Letters 20:221

    PubMed  Google Scholar 

  12. Haynes, D.H. 1972. Studien der Bindung und des Transportes von Ionen und Molekülen an Phospholipid-Membranen.In: Dechema Monographien, Tutzing Symposion der DECHEMA. Vol. 71, pp. 119–133

  13. Haynes, D.H., Kowalsky, A., Pressman, B.C. 1969. Application of nuclear magnetic resonance to the conformational changes in valinomycin during complexation.J. Biol. Chem. 244:502

    PubMed  Google Scholar 

  14. Haynes, D.H., Pressman, B.C. 1974. Two-phase partition studies of alkali cation complexation by ionophores.J. Membrane Biol. 18:1

    Google Scholar 

  15. Haynes, D.H., Pressman, B.C., Kowalsky, A. 1971. A nuclear magnetic resonance study of22Na+ complexing by ionophores.Biochemistry 10:852

    PubMed  Google Scholar 

  16. Ivanov, V.T., Evstratov, A.V., Sumskaya, L.V., Melnik, E.I., Chumburidze, T.S., Portnova, S. L., Balashova, T.A., Ovchinnikov, Yu. A. 1973. Sandwich complexes as a functional form of the enniatin ionophores.FEBS Letters 36:72

    PubMed  Google Scholar 

  17. Junge, W., Schmid, R. 1971. The mechanism of action of valinomycin on the thylakoid membrane: Characterization of the electric current density.J. Membrane Biol. 4:179

    Google Scholar 

  18. Mueller, P., Rudin, D.O. 1967. Development of K+−Na+ discrimination in experimental bimolecular lipid membranes by macrocyclic antibiotics.Biochem. Biophys. Res. Commun. 26:398

    PubMed  Google Scholar 

  19. Pressman, B.C. 1967. Biological applications of ion-specific glass electrodes.In: Methods in Enzymology. R.W. Estabrook and M. Pullman, editors. Vol. 10, p. 714. Academic Press, New York-London

    Google Scholar 

  20. Pressman, B.C. 1968. Ionophorous antibiotics as models for biological transport.Fed. Proc. 27:1283

    PubMed  Google Scholar 

  21. Pressman, B.C., Harris, E.J., Jagger, E.S., Johnson, J.H. 1967. Antibiotic-mediated transport of alkali ions across lipid barriers.Proc. Nat. Acad. Sci. 58:1949

    PubMed  Google Scholar 

  22. Pressman, B.C., Haynes, D.H. 1970. Ionophorous agents as mobile ion carriers.In: The Molecular Basis of Membrane Function. D.C. Tosteson, editor. p. 221. Prentice-Hall, Englewood Cliffs, N.J.

    Google Scholar 

  23. Pressman, B.C., Heeb, M.J. 1971. Permeability studies on erythrocyte ghosts with ionophorous antibiotics.In: Molecular Mechanisms of Antibiotic Action on Protein Biosynthesis and Membranes, Proc. Symp., Granada. E. Muñoz, F. García-Ferrándiz and D. Vázquez, editors. p. 603. Elsevier, New York

    Google Scholar 

  24. Pressman, B.C., Lardy, H.A. 1956. Effect of surface active agents on the latent ATP-ase of mitochondria.Biochim. Biophys. Acta 21:458

    PubMed  Google Scholar 

  25. Schneider, W.C. 1948. Intracellular distribution of enzymes. III. The oxidation of octanoic acid by rat liver fractions.J. Biol. Chem. 176:259

    Google Scholar 

  26. Szabo, G., Eisenman, G., Ciani, S. 1969. The effects of the macrotetralide actin antibiotics on the electrical properties of phospholipid bilayer membranes.J. Membrane Biol. 1:346

    Google Scholar 

  27. Tosteson, D.C., Cook, P.C., Andreoli, T.E., Tieffenberg, M. 1967. The effect of valinomycin on potassium and sodium permeability of HK and LK sheep red cells.J. Gen. Physiol. 50:2513

    PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Duncan H. Haynes & Berton C. Pressman

    Present address: Department of Pharmacology, University of Miami, School of Medicine, Biscayne Annex Box 520875, 33152, Miami, Florida

Authors and Affiliations

  1. Johnson Foundation for Medical Research, University of Pennsylvania, 19104, Philadelphia, Pennsylvania

    Duncan H. Haynes, Theodore Wiens & Berton C. Pressman

Authors
  1. Duncan H. Haynes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Theodore Wiens
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Berton C. Pressman
    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

Haynes, D.H., Wiens, T. & Pressman, B.C. Turnover numbers for ionophore-catalyzed cation transport across the mitochondrial membrane. J. Membrain Biol. 18, 23–38 (1974). https://doi.org/10.1007/BF01870100

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01870100

Keywords

Search

Navigation