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The mechanism of cation permeation in rabbit gallbladder

Dilution potentials and biionic potentials

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Summary

The experimental measurements of passive ion permeation in rabbit gallbladder presented in this paper include: single-salt dilution potentials as a function of concentration gradient; comparison of dilution potentials for different alkali chlorides; comparison of biionic potentials for different alkali chlorides; and biionic mixture potentials as a function of cation concentration gradient. Both dilution potentials and biionic potentials yield the permeability sequence K+>Rb+>Na+>Li+>Cs+, a sequence consistent with simple considerations of ion-site interactions and ion hydration energies. Construction of empirical selectivity isotherms for alkali cation permeation in epithelia shows that permeability ratios are nearer one in the gallbladder and other epithelia than in most other biological membranes, indicating a relatively hydrated permeation route. Evaluation of the results of this and the preceding paper suggests the following: that cations permeate gallbladder epithelium via channels with fixed neutral sites; that the rate-controlling membrane is thick enough that microscopic electroneutrality must be obeyed; that virtually all anion conductance is in a shunt which develops with time after dissection; that apparent permeability changes with solution composition are due to the non-ideal activity factorn being less than 1.0; that effects of pH, Ca++, and ionic strength may involve changes in the anion/cation mobility ratio owing to changes in wall charges or dipoles; and that the permeation route may reside in the tight junctions. A similar mechanism may be applicable to cation permeation in other epithelia.

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References

  • Barry, P. H., Diamond, J. M. 1970. Junction potentials, electrode standard potentials, and other problems in interpreting electrical properties of membranes.J. Membrane Biol. 3:93.

    Article  CAS  Google Scholar 

  • —— 1971. A theory of ion permeation through membranes with fixed neutral sites.J. Membrane Biol. 4:295.

    Article  CAS  Google Scholar 

  • Bungenberg de Jong, H. G. 1949. Reversal of charge phenomena, equivalent weight and specific properties of the ionised groups.In: Colloid Science, vol. 2. H. R. Kruyt, editor. p. 259. Elsevier, New York.

    Google Scholar 

  • Cass, A., Finkelstein, A., Krespi, V. 1970. The ion permeability induced in thin lipid membranes by the polyene antibiotics nystatin and amphotericin B.J. Gen. Physiol. 56:100.

    Article  PubMed  CAS  Google Scholar 

  • Conti, F., Eisenman, G. 1965. The steady-state properties of an ion exchange membrane with fixed sites.Biophys. J. 5:511.

    PubMed  CAS  Google Scholar 

  • —— 1966. The steady-state properties of an ion exchange membrane with mobile sites.Biophys. J. 6:227.

    PubMed  CAS  Google Scholar 

  • Diamond, J. M. 1962. The mechanism of solute transport by the gall-bladder.J. Physiol. 161:474.

    PubMed  CAS  Google Scholar 

  • — 1964. The mechanism of isotonic water transport.J. Gen. Physiol. 48:15.

    Article  PubMed  CAS  Google Scholar 

  • — 1968. Transport mechanisms in the gall-bladder.In: Handbook of Physiology: Alimentary Canal, vol. 5, p. 2451. American Physiological Society, Washington.

    Google Scholar 

  • —, Wright, E. M. 1969. Biological membranes: The physical basis of ion and nonelectrolyte selectivity.Ann. Rev. Physiol. 31:581.

    Article  CAS  Google Scholar 

  • Doremus, R. H. Ion exchange in glasses.In: Ion Exchange, vol. 2. J. A. Marinsky, editor. p. 1. Dekker, New York.

  • Eisenman, G. 1961. On the elementary atomic origin of equilibrium ionic specificity.In: Symposium on Membrane Transport and Metabolism. A. Kleinzeller and A. Kotyk, editors. p. 163. Academic Press, New York.

    Google Scholar 

  • — 1962. Cation selective glass electrodes and their mode of operation.Biophys. J. 2; Part 2:259.

    PubMed  CAS  Google Scholar 

  • — 1963. The influence of Na, K, Li, Rb, and Cs on cellular potentials and related phenomena.Bol. Inst. Estud. Méd. Biol. 21:155.

    CAS  Google Scholar 

  • — 1965. Some elementary factors involved in specific ion permeation.In: Proc. 23rd Intern. Congr. Physiol. Sci., Tokyo. p. 489. Excerpta Med. Found., Amsterdam.

    Google Scholar 

  • — 1967. The origin of the glass-electrode potential.In: Glass Electrodes for Hydrogen and other Cations. G. Eisenman, editor. p. 133. Dekker, New York.

    Google Scholar 

  • — 1969. The ion exchange characteristics of the hydrated surface of Na+ selective glass electrodes.In: Glass Microelectrodes. M. Lavallée, O. Schanne, and N. C. Hébert, editors. p. 32. Wiley, New York.

    Google Scholar 

  • —, 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. 1:94.

    Article  Google Scholar 

  • Garrels, R. M., Christ, C. L. 1965. Solutions, Minerals, and Equilibria. Harper and Row, New York.

    Google Scholar 

  • Goldman, D. E. 1943. Potential, impedance, and rectification in membranes.J. Gen. Physiol. 27:37.

    Article  CAS  Google Scholar 

  • Goodenough, D. A., Revel, J. P. 1970. A fine structural analysis of intercellular junctions in the mouse liver.J. Cell Biol. 45:272.

    Article  PubMed  CAS  Google Scholar 

  • Hagiwara, S., Toyama, K., Hayashi, H. 1971. Mechanisms of anion and cation permeation in the resting membrane of a barnacle muscle fiber.J. Gen. Physiol. (in press).

  • Hodgkin, A. L., Katz, B. 1949. The effect of sodium ions on the electrical activity of the giant axon of the squid.J. Physiol. 108:37.

    Google Scholar 

  • Leb, D. E., Hoshiko, T., Lindley, B. D. 1965. Effects of alkali metal cations on the potential across toad and bullfrog urinary bladder.J. Gen. Physiol. 48:527.

    Article  PubMed  CAS  Google Scholar 

  • Lindley, B. D., Hoshiko, T. 1964. The effects of alkali metal cations and common anions on the frog skin potential.J. Gen. Physiol. 47:749.

    Article  PubMed  CAS  Google Scholar 

  • Machen, T. E. 1970. Anion Selectivity and Permeation Mechanism in Rabbit Gallbladder Epithelium. Ph. D. Dissertation, University of California at Los Angeles.

  • —, Diamond, J. M. 1969. An estimate of the salt concentration in the lateral intercellular spaces of rabbit gall-bladder during maximal fluid transport.J. Membrane Biol. 1:194.

    Article  Google Scholar 

  • McLaughlin, S. G. A., Szabo, G., Eisenman, G., Ciani, S. 1970. The effects of surface charge on the conductance of phospholipid membranes.Proc. Nat. Acad. Sci. 67:1268.

    Article  PubMed  CAS  Google Scholar 

  • Neumcke, B., Läuger, P. 1969. Nonlinear electrical effects in lipid bilayer membranes. II. Integration of the generalized Nernst-Planck equations.Biophys. J. 9:1160.

    PubMed  CAS  Google Scholar 

  • Robinson, R. A., Stokes, R. H. 1965. Electrolyte Solutions. Butterworths, London.

    Google Scholar 

  • Rothstein, A., Demis, C. 1953. The relationship of the cell surface to metabolism. The stimulation of fermentation by extracellular potassium.Arch. Biochem. Biophys. 44:18.

    Article  PubMed  CAS  Google Scholar 

  • Sandblom, J. P., Eisenman, G. 1967. Membrane potentials at zero current: the significance of a constant ionic permeability ratio.Biophys. J. 7:217.

    Article  PubMed  CAS  Google Scholar 

  • Schultz, S. G., Curran, P. F., Wright, E. M. 1967. Interpretation of the hexose-dependent electrical potential differences in small intestine.Nature 214:509.

    Article  PubMed  CAS  Google Scholar 

  • Smulders, A. P. 1970. The Permeability of the Gall-Bladder to Non-Electrolytes. Ph. D. Dissertation, University of California at Los Angeles.

  • Smulders, A. P., Wright, E. M. 1971. The magnitude of non-electrolyte selectivity in the gallbladder epithelium.J. Membrane Biol. (in press).

  • Smyth, D. H., Wright, E. M. 1966. Streaming potentials in the rat small intestine.J. Physiol. 182:591.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Teorell, T. 1953. Transport processes and electrical phenomena in ionic membranes.Prog. Biophys. Biophys. Chem. 3:305.

    CAS  Google Scholar 

  • Tormey, J. M., Diamond, J. M. 1967. The ultrastructural route of fluid transport in rabbit gall bladder.J. Gen. Physiol. 50:2031.

    Article  PubMed  CAS  Google Scholar 

  • Wheeler, H. O. 1963. Transport of electrolytes and water across wall of rabbit gall bladder.Amer. J. Physiol. 205:427.

    PubMed  CAS  Google Scholar 

  • Wright, E. M., Barry, P. H., Diamond, J. M. 1971. The mechanism of cation permeation in rabbit gallbladder: Conductances, the current-voltage relation, the concentration dependence of anion-cation discrimination, and the calcium competition effect.J. Membrane Biol. 4:331.

    Article  CAS  Google Scholar 

  • —, Diamond, J. M. 1968. Effects of pH and polyvalent cations on the selective permeability of gall-bladder epithelium to monovalent ions.Biochim. Biophys. Acta 163:57.

    Article  PubMed  CAS  Google Scholar 

  • —, Prather, J. W. 1970. The permeability of the frog choroid plexus to nonelectrolytes.J. Membrane Biol. 2:127.

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Physiology, University of California Medical Center, 90024, Los Angeles, California

    Peter H. Barry, Jared M. Diamond & Ernest M. Wright

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  1. Peter H. Barry
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  2. Jared M. Diamond
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  3. Ernest M. Wright
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Barry, P.H., Diamond, J.M. & Wright, E.M. The mechanism of cation permeation in rabbit gallbladder. J. Membrain Biol. 4, 358–394 (1971). https://doi.org/10.1007/BF02431979

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  • DOI: https://doi.org/10.1007/BF02431979

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