The Journal of Membrane Biology

, Volume 105, Issue 3, pp 257–263 | Cite as

Voltage dependence of the basolateral membrane conductance in theAmphiuma collecting tubule

  • Jean-Daniel Horisberger
  • Gerhard Giebisch


The basolateral potassium conductance of cells of most epithelial cells plays an important role in the transcellular sodium transport inasmuch as the large negative equilibrium potential of potassium across this membrane contributes to the electrical driving force for Na+ across the apical membrane. In the present study, we have attempted to establish, theI-V curve of the basolateral membrane of theAmphiuma collecting tubule, a membrane shown to be K+ selective. TransepithelialI-V curves were obtained in short, isolated perfused collecting tubule segments. The “shunt” conductance was determined using amiloride to block the apical membrane Na+ conductance. In symmetrical solutions, the “shunt”I-V curve was linear (conductance: 2.2±0.3 mS·cm−2). Transcellular current was calculated by subtracting the “shunt” current from the transepithelial current in the absence of amiloride. Using intracellular microelectrodes, it was then possible to measure the basolateral membrane potential simultaneously with the transcellular current. The basolateral conductance was found to be voltage dependent, being activated by hyperpolarization: conductance values at −30 and −80 mV were 3.6±1.0 and 6.6±1.0 mS·cm−2, respectively. BasolateralI-V curves were thus clearly different from that predicted by the “constant field” model. These results indicate that the K+-selective basolateral conductance of an amphibian collecting tubule shows inward (“anomalous”) rectification. Considering the electrogenic nature basolateral Na−K-pump, this may account for coupling between pump-generated potential and basolateral K+ conductance.

Key Words

Amphiuma collecting tubule basolateral membrane potassium conductance I-V curve 


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  1. 1.
    Boulpaep, E.L. 1966. Potassium and chloride conductances of the peritubular membrane of proximal tubular cells ofNecturus kidney.Biophys. J. 6:133(abstr.) Google Scholar
  2. 2.
    Chase, H.S., Jr 1984. Does calcium couple the apical and basolateral membrane permeabilities in epithelia.Am. J. Physiol. 247:F869-F876Google Scholar
  3. 3.
    Davis, C.W., Finn, A.L. 1982. Sodium transport inhibition by amiloride reduces basolateral membrane potassium conductance in tight epithelia.Science 216:525–527PubMedGoogle Scholar
  4. 4.
    De Weer, P. 1986. The electrogenic sodium pump: Thermodynamics and kinetics.In: Progress in Zoology. H.C. Luttgau, editor. Vol. 33, pp. 387–399. Gustav Fischer Verlag, New YorkGoogle Scholar
  5. 5.
    Germann, W.J., Ernst, S.A., Dawson, D.C. 1986. Resting and osmotically induced basolateral K conductances in turtle colon.J. Gen. Physiol. 88:253–274PubMedGoogle Scholar
  6. 6.
    Germann, W.J., Lowy, M.E., Ernst, S.A., Dawson, D.C. 1986. Differentiation of two distinct K conductances in the basolateral membrane of turtle colon.J. Gen. Physiol. 88:237–251PubMedGoogle Scholar
  7. 7.
    Gogelein, H., Greger, R. 1987. Properties of single K+ channels in the basolateral membrane of rabbit proximal straight tubules.Pfluegers Arch. 410:288–295Google Scholar
  8. 8.
    Grasset, E., Gunter-Smith, P., Schultz, S.G. 1983. Effects of Na-coupled alanine transport on intra-cellular K activities and the K conductance of the basolateral membrane ofNecturus small intestine.J. Membrane Biol. 71:89–94Google Scholar
  9. 9.
    Hagiwara, S. 1983. Membrane Potential-Dependent Ion Channels in Cell Membrane. pp. 65–79. Raven, New YorkGoogle Scholar
  10. 10.
    Helman, S.I., Fischer, R.S. 1977. Microelectrode studies of the active Na+ transport pathway of frog skin.J. Gen. Physiol. 69:571–604PubMedGoogle Scholar
  11. 11.
    Helman, S.I., Nagel, W., Fischer, R.S. 1979. Ouabain on active transepithelial sodium transport in frog skin.J. Gen. Physiol. 74:105–127Google Scholar
  12. 12.
    Hille, B. 1984. Potassium channels and chloride channels.In: Ionic Channels of Excitable Membranes. B. Hille, editor. pp. 99–116. Sinauer, Sunderland, MAGoogle Scholar
  13. 13.
    Horisberger, J.-D., Giebisch, G. 1987. Na−K-pump current inAmphiuma collecting tubule: Dependence on voltage and external K concentration.J. Gen. Physiol. 90:22a(abstr.) Google Scholar
  14. 14.
    Horisberger, J.-D., Giebisch, G. 1988. Intracellular Na+ and K+ activities and membrane conductances in the collecting tubule ofAmphiuma. J. Gen. Physio. (in press) Google Scholar
  15. 15.
    Horisberger, J.-D., Hunter, M., Stanton, B.A., Giebisch, G. 1987. The collecting tubule ofAmphiuma: II. Effects of potassium adaptation.Am. J. Physiol. 253:F1273-F1282PubMedGoogle Scholar
  16. 16.
    Hunter, M., Horisberger, J.-D., Stanton, B.A., Giebisch, G. 1987. The collecting tubule of Amphiuma: I. Electrophysiological characterization.Am. J. Physiol. 253:F1263-F1272PubMedGoogle Scholar
  17. 17.
    Kawahara, K., Hunter, M., Giebisch, G. 1987. Potassium channels inNecturus proximal tubule.Am. J. Physiol. 253:F488-F494PubMedGoogle Scholar
  18. 18.
    Kirk, K.L., Dawson, D.C. 1983. Basolateral potassium channels in turtle colon.J. Gen. Physiol. 82:297–313PubMedGoogle Scholar
  19. 19.
    Kirk, K.L., Halm, D.R., Dawson, D.C. 1980. Active sodium transport by turtle colon via an electrogenic Na−K exchange pump.Nature (London) 287:237–239Google Scholar
  20. 20.
    Lang, F., Messner, G., Rehwald, W. 1986. Electrophysiology of sodium-coupled transport in proximal renal tubules.Am. J. Physiol. 250:F953-F962PubMedGoogle Scholar
  21. 21.
    Lewis, S.A., Hanrahan, J.W. 1985. Apical and basolateral membrane ionic channels in rabbit urinary bladder epithelium.Pfluegers Arch. 405(Suppl. 1)S83-S88Google Scholar
  22. 22.
    Lewis, S.A., Wills, N.K. 1983. Apical membrane permeability and kinetic properties of the sodium pump in rabbit urinary bladder.J. Physiol. (London) 341:169–184Google Scholar
  23. 23.
    Lindau, M., Fernandez, J.M. 1986. A patch-clamp study of histamine secreting cells.J. Gen. Physiol. 88:349–368PubMedGoogle Scholar
  24. 24.
    Matsuda, H., Saigusa, A., Irisawa, H. 1987. Ohmic conductance through the inwardly rectifying K channel and blocking by internal Mg++.Nature (London) 325:156–159Google Scholar
  25. 25.
    Messner, G., Oberleithner, H., Lang, F. (1985). The effect of phenylalanine on the electrical properties of proximal tubule cells in the frog kidney.Pfluegers Arch.404:138–144Google Scholar
  26. 26.
    Nagel, W. 1985. Basolateral membrane ionic conductance in frog skin.Pfluegers Arch. 405:S39-S43Google Scholar
  27. 27.
    Palmer, L.G. 1984. Voltage-dependent block by amiloride and other monovalent cations of apical Na channels in the toad urinary bladder.J. Membrane Biol. 80:153–165Google Scholar
  28. 28.
    Parent, L., Cardinal, J., Sauvé, R. 1988. Single-channel analysis of a K channel at basolateral membrane of rabbit proximal convoluted tubule.Am. J. Physiol. 254:F105-F113PubMedGoogle Scholar
  29. 29.
    Sackin, H., Boulpaep, E.L., 1983. Rheogenic transport in the renal proximal tubule.J. Gen. Physiol. 82:819–851PubMedGoogle Scholar
  30. 30.
    Sackin, H., Palmer, L.G. 1987. Basolateral potassium channels in renal proximal tubule.Am. J. Physiol. 253:F476-F487PubMedGoogle Scholar
  31. 31.
    Schoen, H.F., Erlij, D. 1985. Current-voltage relations of the apical and basolateral membranes of the frog skin.J. Gen. Physiol. 86:257–287PubMedGoogle Scholar
  32. 32.
    Schultz, S.G. 1985. Regulatory mechanisms in sodium-absorbing epithelia.In: The Kidney: Physiology and Pathology. D.W. Seldin and G. Giebisch, editors pp. 189–198. Raven, New YorkGoogle Scholar
  33. 33.
    Schultz, S.G., Thompson, S.M., Hudson, R.L., Thomas, S.R., Suzuki Y. 1984. Electrophysiology ofNecturus urinary bladder: II. Time-dependent current-voltage relations of the basolateral membranes.J. Membrane Biol. 79:257–269Google Scholar
  34. 34.
    Takeda, K., Schini, V., Stoeckel, H. 1987. Voltage-activated potassium, but not calcium currents in cultured bovine aortic endothelial cells.Pfluegers Arch. 410:385–393Google Scholar
  35. 35.
    Thomas, S.R., Suzuki, Y., Thompson, S.M., Schultz, S.G. 1983. Electrophysiology ofNecturus urinary bladder: I. “Instantaneous” current-voltage relations in the presence of varying mucosal sodium concentrations.J. Membrane Biol. 73:157–175Google Scholar
  36. 36.
    Thompson, S.M., Suzuki, Y., Schultz, S.G. 1982. The electrophysiology of rabbit descending colon: II. Current-voltage relations of the apical membrane, the basolateral membrane and the parallel pathways.J. Membrane Biol. 66:55–61Google Scholar
  37. 37.
    Thompson, S.M., Suzuki, Y., Schultz, S.G. 1982. The electrophysiology of the rabbit descending colon: I. Instantaneous transepithelial current-voltage relations and the current-voltage relations of the Na-entry mechanism.J. Membrane Biol. 66:41–54Google Scholar
  38. 38.
    Warncke, J., Lindemann, B. 1985. Voltage dependence of Na channel blockage by amiloride: Relaxation effects in admittance spectra.J. Membrane Biol. 86:255–265Google Scholar
  39. 39.
    Welling, P.A., O'Neil, R.G. 1987. Cell swelling increases basolateral membrane Cl and K conductances of the rabbit proximal straight tubule.Kidney Int. 31:452(abstr.) Google Scholar
  40. 40.
    Wills, N.K., Eaton, D.C., Lewis, S.A., Ifshin, M.S. 1979. Current-voltage relationship of the basolateral membrane of a tight epithelium.Biochim. Biophys. Acta 555:519–523PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1988

Authors and Affiliations

  • Jean-Daniel Horisberger
    • 1
  • Gerhard Giebisch
    • 1
  1. 1.Department of PhysiologyYale University School of MedicineNew Haven

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