Skip to main content
Log in

Saturable K+ pathway across the outer border of frog skin (Rana temporaria): Kinetics and inhibition by Cs+ and other cations

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

Summary

The reaction of abdominal skins of the frog speciesRana temporaria on mucosal K+-containing solutions was studied in an Ussing-type chamber by recording transepithelial potential difference (PD), short-circuit current (SCC) and conductance (G). With Na-Ringer's as serosal medium, a linear correlation between PD and the logarithm of the mucosal K+-concentration ([K] o ) was obtained. The K+-dependent SCC saturated with increasing [K] o , and could quickly and reversibly be depressed by addition of Rb+, Cs+, and H+, Li+, Na+, and NH +4 did not influence K+ current. A large scatter was obtained for kinetic parameters like the slope of the PD-log [K] o -line (18–36.5 mV/decade), the apparent Michaelis constant (13–200mm), and the maximal current of the saturable SCC (6–50 μA·cm−2), as well as for the degree of inhibition by Cs+ ions. This seemed to be caused by a time-dependent change during long time exposure to high [K] o (more than 30 sec), thereby inducing a selectivity loss of K+-transporting structures, together with an increase in SCC andG and a decrease in PD. Short time exposure to K+-containing solutions showed a competitive inhibition of K+ current by Cs+ ions, and a Michaelis constant of 6.6mm for the inhibitory action of Cs+. Proton titration resulted in a decrease of K+ current at pH<3. An acidic membrane component (apparent dissociation constant 2.5×10−3 m) is virtually controlling K+ transfer. Reducing the transepithelial K+-concentration gradient by raising the serosal potassium concentration was accompanied by the disappearance of SCC and PD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Biber, T.U.L., Curran, P.F. 1970. Direct measurement of uptake of sodium at the outer surface of the frog skin.J. Gen. Physiol. 56:83

    Google Scholar 

  2. Bindslev, N., Tormey, J.McD., Pietras, R.J., Wright, E.M. 1974. Electrically and osmotically induced changes in permeability and structure of toad urinary bladder.Biochim. Biophys. Acta 332:286

    Google Scholar 

  3. Candia, O.A., Reinach, P.S. 1977. Sodium washout kinetics across inner and outer barriers of the isolated frog skin epithelium.Biochim. Biophys. Acta 468:341

    Google Scholar 

  4. Cereijido, M., Curran, P.F. 1965. Intracellular electrical potentials in frog skin.J. Gen. Physiol. 48:543

    Google Scholar 

  5. Cereijido, M., Rabito, C.A., Rodriguez Boulan, E., Rotunno, C.A. 1974. The sodium-transporting compartment of the epithelium of frog skin.J. Physiol. (London) 237:555

    Google Scholar 

  6. Claude, P. 1978. Morphological factors influencing transepithelial permeability: A model for the resistance of the zonula occludens.J. Membrane Biol. 39:219

    Google Scholar 

  7. DiBona, D.R., Civan, M.M. 1973. Pathways for movement of ions and water across toad urinary bladder. I. Anatomic site of transepithelial shunt pathways.J. Membrane Biol. 12:101

    Google Scholar 

  8. Ehrlich, E.N., Crabbé, J. 1968. The mechanism of action of amipramizide.Pfluegers Arch. 302:79

    Google Scholar 

  9. Erlij, D., Machen, T.E. 1974. Sodium sites and zonulae occludens: Localization at specific regions of epithelial cell membranes.In: Perspectives in Membrane Biology. p. 181. Academic Press, New York

    Google Scholar 

  10. Finn, A.L. 1976. Changing concepts of transepithelial sodium transport.Physiol. Rev. 56(2):453

    Google Scholar 

  11. 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

    Google Scholar 

  12. Gebhardt, U., Fuchs, W., Lindemann, B. 1972. Resistance response of frog skin to brief and long lasting changes of (Na) o and (K) o .In: Role of Membranes in Secretory Process. L. Bolis, R.D. Keynes, and W. Wilbrandt, editors. p. 284. North-Holland, Amsterdam

    Google Scholar 

  13. Helman, S.I., Fisher, R.S. 1977. Microelectrode studies of the active Na transport pathway of frog skin.J. Gen. Physiol. 69:571

    Google Scholar 

  14. Hirschmann, W., Nagel, W. 1978. The outer membrane of frog skin: Impermeable to K+?Pfluegers Arch. 373:R48

    Google Scholar 

  15. Hoshiko, T. 1973. Cation selectivities in frog skin.In: Transport Mechanisms in Epithelia. H.H. Ussing, and N.A. Thorn, editors. p. 99. Munksgaard, Copenhagen; Academic Press, New York

    Google Scholar 

  16. Isenberg, G. 1976. Cardiac Purkinje fibers: Cesium as a tool to block inward rectifying potassium currents.Pfluegers Arch. 365:99

    Google Scholar 

  17. Katz, U. 1978. Changes in ionic conductances and in sensitivity to amiloride during the natural moulting cycle of toad skin (Bufo viridis, L.).J. Membrane Biol. 38:1

    Google Scholar 

  18. Koefoed-Johnson, V., Levi, H., Ussing, H.H. 1952. The mode of passage of chloride ions through the isolated frog skin.Acta Physiol. Scand. 25:150

    Google Scholar 

  19. Lindemann, B. 1970. Electrical excitation of the outer resistive membrane in frog skin epithelium.In: Electrophysiology of Epithelial Cells. G. Giebisch, editor. p. 53. F.K. Schattauer Verlag, Stuttgart-New York

    Google 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

    Google Scholar 

  21. Mandel, L.J., Curran, P.F. 1972. Response of the frog skin of steady-state voltage clamping. I. The shunt pathway.J. Gen. Physiol. 59:503

    Google Scholar 

  22. Mandel, L.J., Curran, P.F. 1972. Response of the frog skin of steady-state voltage clamping. II. The active pathway.J. Gen. Physiol. 62:1

    Google Scholar 

  23. Martinez-Palomo, A., Erlij, D., Bracho, H. 1971. Localization of permeability barriers in the frog skin epithelium.J. Cell Biol. 50:277

    Google Scholar 

  24. Nagel, W. 1976. The intracellular electrical potential profile of the frog skin epithelium.Pfluegers Arch. 365:135

    Google Scholar 

  25. Nagel, W. 1977. The dependence of the electrical potentials across the membranes of the frog skin upon the concentration of sodium in the mucosal solution.J. Physiol. (London) 269:777

    Google Scholar 

  26. Nagel, W., Dörge, A. 1970. Effect of amiloride on sodium transport of frog skin. I. Action on intracellular sodium content.Pfluegers Arch. 317:84

    Google Scholar 

  27. Nielsen, R. 1971. Effect of amphotericin B on the frog skinin vitro. Evidence for outward active potassium transport across the epithelium.Acta Physiol. Scand. 83:106

    Google Scholar 

  28. Nunes, M.A., Lacaz Vieira, F. 1975. Negative potential level in the outer layer of the toad skin.J. Membrane Biol. 24:161

    Google Scholar 

  29. Procopio, J., Lacaz Vieira, F. 1977. Ionic exchanges in isolated and open-circuited toad skin.J. Membrane Biol. 35:219

    Google Scholar 

  30. Reuss, L., Finn, A.L. 1975. Dependence of serosal membrane potential on mucosal membrane potential in toad urinary bladder.Biophys. J. 15:71

    Google Scholar 

  31. Rick, R., Dörge, A., von Arnim, E., Thurau, K. 1978. Electron microprobe analysis of frog skin epithelium: Evidence for a syncytial sodium transport compartment.J. Membrane Biol. 39:313

    Google Scholar 

  32. Schultz, S.G. 1972. Electrical potential differences and eletromotive forces in epithelial tissues.J. Gen. Physiol. 59:794

    Google Scholar 

  33. Shinagawa, Y., Okamoto, J., Kamino, K., Uyeda, M. 1972. Analysis of membrane permeability coefficients of amphibian skin by means of electronic data processing (I).Jpn. J. Physiol. 22:1

    Google Scholar 

  34. Sperelakis, N., Schneider, M.F., Harris, E.J. 1967. Decreased K+ conductance produced by Ba++ in frog sartorius fibers.J. Gen. Physiol. 50:1565

    Google Scholar 

  35. Ussing, H.H. 1960. The frog skin potential.J. Gen. Physiol. 43(Suppl.):135

    Google Scholar 

  36. Ussing, H.H. 1971. Introductory remarks.Phil. Trans. R. Soc. London B. 262:85

    Google Scholar 

  37. Ussing, H.H., Windhager, E.E. 1964. Nature of shunt path and active sodium transport path through frog skin epithelium.Acta Physiol. Scand. 61:484

    Google Scholar 

  38. Ussing, H.H. Zerahn, K. 1951. Active transport of sodium as the source of electric current in the short- circuited isolated frog skin.Acta Physiol. Scand. 23:110

    Google Scholar 

  39. Van Driessche, W., Zeiske, W. 1978. Fluctuations of the K+-current in the frog skin (Rana temporaria).Arch. Int. Physiol. Biochim. 86:684

    Google Scholar 

  40. Zeiske, W. 1978. The stimulation of Na+-uptake in frog skin by uranyl ions.Biochim. Biophys. Acta 509:218

    Google Scholar 

  41. Zeiske, W., Lindemann, B. 1975. Blockage of Na-channels in frog skin by titration with protons and by chemical modification of COO-groups.Pfluegers Arch. 355:R71

    Google Scholar 

  42. Zeiske, W., Van Driessche, W. 1978. K+-uptake across the outer border of frog skin (R. temp.) and its inhibition by Cs-ions.Pfluegers Arch. 373:R48

    Google Scholar 

  43. Zeiske, W., Van Driessche, W. 1978. The origin of K+-dependent current fluctuations in frog skin (R. temp.).Pfluegers Arch. 373:R48

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zeiske, W., Van Driessche, W. Saturable K+ pathway across the outer border of frog skin (Rana temporaria): Kinetics and inhibition by Cs+ and other cations. J. Membrain Biol. 47, 77–96 (1979). https://doi.org/10.1007/BF01869048

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01869048

Keywords

Navigation