Advertisement

The Journal of Membrane Biology

, Volume 64, Issue 1–2, pp 91–102 | Cite as

Aldosterone control of the density of sodium channels in the toad urinary bladder

  • Lawrence G. Palmer
  • Jack H. Y. Li
  • Bernd Lindemann
  • Isidore S. Edelman
Articles

Summary

Near-instantaneous current-voltage relationships and shot-noise analysis of amiloride-induced current fluctuations were used to estimate apical membrane permeability to Na (PNa), intraepithelial Na activity (Na c ), single-channel Na currents (i) and the number of open (conducting) apical Na channels (N0), in the urinary bladder of the toad (Bufo marinus). To facilitate voltageclamping of the apical membrane, the serosal plasma membranes were depolarized by substitution of a high KCl (85mm) sucrose (50mm) medium for the conventional Na-Ringer's solution on the serosal side.

Aldosterone (5×10−7m, serosal side only) elicited proportionate increases in the Na-specific current (INa and inPNa, with no significant change in the dependence ofPNa on mucosal Na (Na o ).PNa and the control ofPNa by aldosterone were substrate-dependent: In substrate-depleted bladders, pretreatment with aldosterone markedly augmented the response to pyruvate (7.5×10−3m) which evoked coordinate and equivalent increases inINa andPNa.

The aldosterone-dependent increase inPNa was a result of an equivalent increase in the area density of conducting apical Na channels. The computed single-channel current did not change. We propose that, following aldosterone-induced protein synthesis, there is a reversible metabolically-dependent recruitment of preexisting Na channels from a reservoir of electrically undetectable channels. The results do not exclude the possibility of a complementary induction of Na-channel synthesis.

Key words

transepithelial Na transport apical Na permeability Na-channel density aldosterone 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aceves, J., Cuthbert, A.W. 1979. Uptake of [3H] bezamil at different sodium concentrations. Inferences regarding the regulation of sodium permeability.J. Physiol. (London) 295:491–504Google Scholar
  2. Armstrong, C.M. 1975. Evidence for ionic pores in excitacle membranes.Biophys. J. 15:932–933PubMedGoogle Scholar
  3. Chu, L.L.H., Edelman, I.S. 1972. Cordycepin and α-amanitin: Inhibitors of transcription as probes of aldosterone action.J. Membrane Biol. 10:291–310Google Scholar
  4. Civan, M.M., Hoffman, R.E. 1971. Effect of aldosterone on electrical resistance of toad bladder.Am. J. Physiol. 220:324–328PubMedGoogle Scholar
  5. Crabbé, J. 1963a. The Sodium-Retaining Action of Aldosterone.Presses Academiques Europeennes S.C. BrusselsGoogle Scholar
  6. Crabbé, J. 1963b. Site of action of aldosterone on the bladder of the toad.Nature (London) 200:787–788Google Scholar
  7. Crabbé, J. 1974. Influence of aldosterone on active sodium transport by the toad bladder: A kinetic approach.Acta Physiol. Scand. 90:417–426PubMedGoogle Scholar
  8. Crabbé, J. 1980. Decreased sensitivity to amiloride of amphibian epithelia treated with aldosterone.Pfluegers Arch. 383:151–158Google Scholar
  9. Cuthbert, A.W., Okpako, D., Shum, W.K. 1974. Aldosterone, moulting and the number of sodium channels in frog skin.Brit. J. Pharmacol. 51:128P Google Scholar
  10. Cuthbert, A.W., Shum, W.K. 1975. Effects of vasopressin and aldosterone on amiloride binding in toad bladder epithelial cells.Proc. R. Soc. London 189:543–575Google Scholar
  11. Edelman, I.S., Bogoroch, R., Porter, G.A. 1963. On the mechanism of action of aldosterone on sodium transport: The role of protein synthesis.Proc. Natl. Acad. Sci. USA 50:1169–1177PubMedGoogle Scholar
  12. Fanestil, D.D., Herman, T.S., Fimognari, G.M., Edelman, I.S. 1968. Oxidative metabolism and aldosterone regulation of sodium transport.In: Regulatory Functions of Biological Membranes. J. Järnefelt, editor, p. 117. Elsevier, AmsterdamGoogle Scholar
  13. Fimognari, G.M., Porter, G.A., Edelman, I.S. 1967. The role of the tricarboxylic acid cycle in the action of aldosterone on sodium transport.Biochim. Biophys. Acta 145:89–99Google Scholar
  14. Frizzell, R.A., Schultz, S.G. 1978. Effect of aldosterone on ion transport by rabbit colonin vitro.J. Membrane Biol. 39:1–26Google Scholar
  15. Fuchs, W., Hviid Larsen, E., Lindemann, B. 1977. Current-voltage curve of sodium channels and concentration dependence of sodium permeability in frog skin.J. Physiol. (London) 267:137–166Google Scholar
  16. Kirsten, E., Kirsten, R., Leaf, A., Sharp, G.W.G. 1968. Increased activity of enzymes of the tricarboxylic acid cycle in response to aldosterone in the toad bladder.Pfluegers Arch. 300:213–225Google Scholar
  17. Law, P.Y., Edelman, I.S. 1978. Induction of citrate synthase by aldosterone in the rat kidney.J. Membrane Biol. 41:41–64Google Scholar
  18. Lewis, S.A., Eaton, D.C., Diamond, J.M. 1976. The mechanism of Na+ transport by rabbit urinary bladder.J. Membrane Biol. 28:41–70Google Scholar
  19. Li, J.H.-Y., Palmer, L.G., Edelman, I.S., Lindemann, B. 1982. The role of sodium-channel density in the natriferic response of the toad urinary bladder to an antidiuretic hormone.J. Membrane Biol. 64:77–89Google Scholar
  20. Lindemann, B., Van Driessche, W. 1977. Sodium-specific membrane channels of frog skin are pores: Current fluctuations reveal high turnover.Science 195:292–294PubMedGoogle Scholar
  21. Lipton, P., Edelman, I.S. 1971. Effects of aldosterone and vasopressin on electrolytes of toad bladder epithelial cells.Am. J. Physiol. 221:733–741Google Scholar
  22. Nagel, W., Crabbé, J. 1980. Mechanism of action of aldosterone on active sodium transport across toad skin.Pfluegers Arch. 385:181–187Google Scholar
  23. Palmer, L.G., Edelman, I.S., Lindemann, B. 1980. Current-voltage analysis of apical sodium transport in toad urinary bladder: Effects of inhibitors of transport and metabolism.J. Membrane Biol. 57:59–71Google Scholar
  24. Porter, G.A., Edelman, I.S. 1964. The action of aldosterone and related corticosteroids on sodium transport across the toad bladder.J. Clin. Invest. 43:611–620PubMedGoogle Scholar
  25. Saito, T., Essig, A. 1973. Effect of aldosterone on active and passive conductance andE Na in the toad bladder.J. Membrane Biol. 13:1–18Google Scholar
  26. Saito, T., Essig, A., Caplan, S.R. 1973. The effect of aldosterone on the energetics of sodium transport in the frog skin.Biochim. Biophys. Acta 318:371–382Google Scholar
  27. Schmidt, U., Schmid, H., Dubach, U.C. 1973. Rapid Na−K-ATPase changes in the nephron of adrenalectomized rats after aldosterone application.Clin. Res. 21:705Google Scholar
  28. Scott, W.N., Reich, I.M., Brown, J.A., Jr., Yang, C.-P.H. 1978. Comparison of toad bladder aldosterone-induced proteins and proteins synthesizedin vitro using aldosterone-induced messenger RNA as template.J. Membrane Biol. Special Issue: 213–220Google Scholar
  29. Scott, W.N., Reich, I.M., Goodman, D.B.P. 1979. Inhibition of fatty acid synthesis prevents incorporation of aldosterone-induced proteins into membranes.J. Biol. Chem. 254:4957–4959PubMedGoogle Scholar
  30. Sharp, G.W.G., Leaf A. 1964. Biological action of aldosteronein vitro.Nature (London) 202:1185–1188Google Scholar
  31. Sharp, G.W.G., Leaf, A. 1966. Mechanism of action of aldosterone.Physiol. Rev. 46:593–633Google Scholar
  32. Spires, D., Weiner, M.W. 1980. Use of an uncoupling agent to distinguish between direct stimulation of metabolism and direct stimulation of transport: Investigation of antidiuretic hormone and aldosterone.J. Pharmacol. Exp. Therap. 214:507–515Google Scholar
  33. Spooner, P.M., Edelman, I.S. 1975. Further studies on the effect of aldosterone on electrical resistance of toad bladder.Biochim. Biophys. Acta 406:304–314PubMedGoogle Scholar
  34. Van Driessche, W., Lindemann, B. 1979. Concentration dependence of currents through single sodium-selective pores in frog skin.Nature (London) 282:519–520Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1982

Authors and Affiliations

  • Lawrence G. Palmer
    • 1
    • 2
  • Jack H. Y. Li
    • 1
    • 2
  • Bernd Lindemann
    • 1
    • 2
  • Isidore S. Edelman
    • 1
    • 2
  1. 1.Department of Biochemistry, College of Physicians and SurgeonsColumbia UniversityNew York
  2. 2.II. Physiologisches Institut der Universität des SaarlandesHomburgWest Germany

Personalised recommendations