Skip to main content
SpringerLink
Log in

Electrophysiology ofNecturus urinary bladder: II. Time-dependent current-voltage relations of the basolateral membranes

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

Summary

As reported previously (S.R. Thomas et al.,J. Membrane Biol. 73:157–175, 1983) the current-voltage (I–V) relations of the Na-entry step across the apical membrane of short-circuitedNecturus urinary bladder in the presence of varying mucosal Na concentrations are (i) time-independent between 20–90 msec and (ii) conform to the Goldman-Hodgkin-Katz constant field flux equation for a single cation over a wide range of voltages.

In contrast, theI–V relations of the basolateral membrane under these conditions are (i) essentially linear between the steady-state, short-circuited condition and the reversal potential (E s); and (ii) are decidedly time-dependent withE s increasing and the slope conductance,E s, decreasing between 20 and 90 msec after displacing the transepithelial electrical potential difference. Evidence is presented that this time-dependence cannot be attributed entirely to the electrical capacitance of the tissue.

The values ofg s determined at 20 msec are linear functions of the short-circuit current,I sc, confirming the relations reported previously, which were obtained using a more indirect approach.

The values ofE s determined at 20 msec are significantly lower than any reasonable estimate of the electromotive force for K across the basolateral membrane, indicating that this barrier possesses a significant conductance to other ions which may exceed that to K. In addition, these values increase linearly with decreasingI sc and approach the value of the electrical potential difference across the basolateral membrane observed when Na entry across the apical membrane is blocked with amiloride or when Na is removed from the mucosal solution.

A possible explanation for the time-dependence ofE s andg s is offered and the implications of these findings regarding the interpretation of previous microelectrophysiologic studies of epithelia are discussed.

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

  • Attwell, D. 1979. Problems in the interpretation of membrane current-voltage relations.In: Membrane Transport Processes. Vol. 3, pp. 29–41. C.F. Stevens and R.W. Tsien, editors, Raven, New York

    Google Scholar 

  • Benos, D.J., Hyde, B.A., Latorre, R. 1983. Sodium flux ratio through the amiloride-sensitive entry pathway in frog skin.J. Gen. Physiol. 81:667–685

    PubMed  Google Scholar 

  • Bindsley, 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 332:286–297

    Google Scholar 

  • Bobrycki, V.A., Mills, J.W., Macknight, A.D.C., DiBona, D.R. 1981. Structural responses to voltage-clamping in the toad urinary bladder. I. The principle role of granular cells in the active transport of sodium.J. Membrane Biol. 60:21–33

    Google Scholar 

  • Boulpaep, E.L., Sackin, H. 1980. Electrical analysis of intraepithelial barriers.In: Current Topics in Membranes and Transport. Vol. 13, pp. 169–197. E.L. Boulpaep, editor. Academic, New York

    Google Scholar 

  • Brown, A.C., Kastella, K.G. 1965. The AC impedance of frog skin and its relation to active transport.Biophys. J. 5:591–606

    PubMed  Google Scholar 

  • Clausen, C., Wills, N.K. 1981. Impedance analysis in epithelia.In: Ion Transport by Epithelia. S.G. Schultz, editor. pp. 79–92. Raven, New York

    Google Scholar 

  • Cuthbert, A.W., Painter, E. 1969. Capacitance changes in frog skin caused by theophylline and antidiuretic hormone.Br. J. Pharmacol. Chemother. 37:314–324

    Google Scholar 

  • Davis, C.W., Finn, A.L. 1982. Sodium transport inhibition reduces basolateral membrane conductance in tight epithelia.Science 216:525–527

    PubMed  Google Scholar 

  • DeLong, J., Civian, M.M. 1983. Microelectrode study of K+ accumulation by tight epithelia: I. Baseline values of split frog skin and toad urinary bladder.J. Membrane Biol. 72:183–193

    Google Scholar 

  • Els, W.J., Helman, S.I. 1981. Vasopressin, theophylline, PGE2 and indomethacin on active Na transport in frog skin: Studies with microelectrodes.Am. J. Physiol. 241:F279-F288

    Google Scholar 

  • Finkelstein, A. 1964. Electrical excitability of isolated frog skin and toad urinary bladder.J. Gen. Physiol. 47:545–565

    PubMed  Google Scholar 

  • Fishman, H.M., Macey, R.I. 1969. TheN-shaped current-potential characteristic in frog skin: I. Time development during step voltage clamp.Biophys. J. 9:127–139

    PubMed  Google Scholar 

  • Frömter, E., Higgins, J.T., Gebler, B. 1981. Electrical properties of amphibian urinary bladder epithelia: IV. The current-voltage relationship of the sodium channels in the apical cell membrane.In: Ion Transport by Epithelia. S.G. Schultz, editor. pp. 31–45. Raven, New York

    Google Scholar 

  • Fuchs, W., Larsen, E.H., Lindemann, B. 1977. Current-voltage curve of sodium channels and concentration dependence of sodium permeability in frog skin.J. Physiol. (London) 267:137–166

    Google Scholar 

  • Garcia-Diaz, J.F., O'Doherty, J., Armstrong, W.McD. 1978. Potential profile, K and Na activities inNecturus small intestine.Physiologist 21:41 (Abstr.)

    PubMed  Google Scholar 

  • Garty, H., Edelman, I.S., Lindemann, B. 1983. Metabolic regulation of apical sodium permeability in toad urinary bladder in the presence and absence of aldosterone.J. Membrane Biol. 74:15–24

    Google Scholar 

  • Goldman, D.E. 1943. Potential, impedance and rectification in membranes.J. Gen. Physiol. 27:37–60

    Article  Google Scholar 

  • Goudeau, H., Weitzerbin, J., Mintz, E.,Gingold, M.P., Nagel, W. 1982. Microelectrode studies of the effect of lanthanum on the electrical potential and resistance of outer and inner membranes of isolated frog skin.J. Membrane Biol. 66:123–132

    Google Scholar 

  • Grasset, E., Gunter-Smith, P., Schultz, S.G. 1983. Effects of Na-coupled alanine transport on intracellular K activities and the K conductance of the basolateral membranes ofNecturus small intestine.J. Membrane Biol. 71:89–94

    Google Scholar 

  • Helman, S.I., Fisher, R.S. 1977. Microelectrode studies of the active Na transport pathway of frog skin.J. Gen. Physiol. 69:571–604

    PubMed  Google Scholar 

  • Helman, S.I., Nagel, W., Fisher, R.S. 1979. Ouabain on active transepithelial Na transport in frog skin: Studies with microelectrodes.J. Gen. Physiol. 74:105–127

    PubMed  Google Scholar 

  • Hodgkin, A.L., Katz, B. 1949. The effect of sodium ions on the electrical activity of the giant axon of the squid.J. Physiol. (London) 108:37–77

    Google Scholar 

  • Koefoed-Johnsen, V., Ussing, H.H. 1958. The nature of the frog skin potential.Acta Physiol. Scand. 42:298–308

    PubMed  Google Scholar 

  • Kubota, T., Biagi, B.A., Giebisch, G. 1983. Intracellular potassium activity measurements in single proximal tubules ofNecturus kidney.J. Membrane Biol. 73:51–60

    Google Scholar 

  • Larsen, E-H., Kristensen, P. 1978. Properties of a conductive cellular chloride pathway in the skin of the toad (Bufo bufo).Acta Physiol. Scand. 102:1–21

    PubMed  Google Scholar 

  • Läuger, P., Neumcke, B. 1973. Ion conductances in lipid bilayers.In: Membranes: A Series of Advances Volume 2, pp. 1–59. G. Eisenman, editor. Marcell Dekker, New York

    Google Scholar 

  • Lewis, S.A., Wills, N.K., Eaton, D.C. 1978. Basolateral membrane potential of a tight epithelium: Ionic diffusion and electrogenic pumps.J. Membrane Biol. 41:117–148

    Google Scholar 

  • 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. 64:77–89

    Google Scholar 

  • Lindemann, B. 1982. Dependence of ion flow through channels on the density of fixed charges at the channel opening.Biophys. J. 39:15–22

    PubMed  Google Scholar 

  • Lindemann, B., Driesche, W. van 1977. Sodium-specific membrane channels of frog skin are pores: Current fluctuations reveal high turnover.Science 195:292–294

    PubMed  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. 47:749–771

    PubMed  Google Scholar 

  • Macknight, A.D.C. 1977. Contribution of mucosal chloride to chloride in toad bladder epithelial cells.J. Membrane Biol. 36:55–63

    Google Scholar 

  • MacRobbie, E.A.C., Ussing, H.H. 1961. Osmotic behavior of the epithelial cells of frog skin.Acta Physiol. Scand. 53:348–365

    PubMed  Google Scholar 

  • Mandel, L.J., Curran, P.F. 1972. Response of the frog skin to steady-state voltage clamping. I. The shunt pathway.J. Gen. Physiol. 59:503–518

    PubMed  Google Scholar 

  • Maruyama, Y., Gallacher, D.V., Peterson, O.H. 1983. Voltage and Ca-activated K-channel in baso-lateral acinar cell membranes of mammalian salivary glands.Nature (London) 302:827–829

    Article  Google Scholar 

  • Nagel, W. 1978. Effects of antidiuretic hormone upon electrical potential and resistance of apical and basolateral membranes of frog skin.J. Membrane Biol. 42:99–122

    Google Scholar 

  • Nagel, W., Crabbé, J. 1980. Mechanism of action of aldosterone on active sodium transport across toad skin.Pflueger's Arch. 385:181–187

    Google Scholar 

  • Nagel, W., Essig, A. 1982. Relationship of transepithelial electrical potential to membrane potentials and conductance ratios in frog skin.J. Membrane Biol. 69:125–136

    Google Scholar 

  • Nagel, W., Garcia-Diaz, J.F., Essig, A. 1983. Contribution of junctional conductance to the cellular voltage-divider ratio in frog skin.Pflueger's Arch. 399:336–341

    Google Scholar 

  • Palmer, L.G. 1982. Na transport and flux ratio through apical channels in toad urinary bladder.Nature (London) 297:688–690

    Google Scholar 

  • 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. 57:59–71

    Google Scholar 

  • Palmer, L.G., Li, J.H.-Y., Lindemann, B., Edelman, I.S. 1982. Aldosterone control of the density of sodium channels in the toad urinary bladder.J. Membrane Biol. 64:91–102

    Google Scholar 

  • Reuss, L., Weinman, S.A. 1979. Intracellular ionic activities and transmembrane electrochemical potential differences in gallbladder epithelium.J. Membrane Biol. 49:345–362

    Article  Google Scholar 

  • Schanne, O.F., P.-Ceretti, E.R. 1978. Impedance Measurements in Biological Cells. John Wiley & Sons, New York

    Google Scholar 

  • Schifferdecker, E., Frömter, E. 1978. The AC impedance ofNecturus gallbladder epithelium.Pfluegers Arch. 377:125–133

    Google Scholar 

  • Schultz, S.G. 1980. Basic Principles of Membrane Transport. Cambridge University Press, New York

    Google Scholar 

  • Schultz, S.G., Thompson, S.M., Suzuki, Y. 1981. Equivalent electrical circuit models and the study of Na transport across epithelia: Nonsteady-state current-voltage relations.Fed. Proc. 40:2443–2449

    Google Scholar 

  • Smith, P.G. 1971. The low frequency electrical impedance of the isolated frog skin.Acta Physiol. Scand. 81:355–366

    Google Scholar 

  • Smith, P.G. 1975. Aldosterone-induced moulting in amphibian skin and its effect on electrical capacitance.J. Membrane Biol. 22:165–181

    Google Scholar 

  • Suzuki, Y., Kottra, G., Kampmann, L., Frömter, E. 1982. Square wave pulse analysis of cellular and paracellular conductance pathways inNecturus gallbladder epitheliumPfluegers Arch. 394:302–312

    Google Scholar 

  • Thompson, S.M., Suzuki, Y., Schultz, S.G. 1982. The electrophysiology of rabbit descending colon. I. Instantaneous transepithelial current-voltage relations and the current-voltage relation of the Na-entry mechanism.J. Membrane Biol. 66:41–54

    Article  Google Scholar 

  • 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 73:157–175

    Article  Google Scholar 

  • Turnheim, K., Thompson, S.M., Schultz, S.G. 1983. Relation between intracellular sodium and active sodium transport in rabbit colon: Current-voltage relations of the apical sodium entry mechanism in the presence of varying luminal sodium concentrations.J. Membrane Biol. 76:299–309

    Article  Google Scholar 

  • Ussing, H.H. 1949. The distinction by means of tracers between active transport and diffusion.Acta Physiol. Scand. 19:43–56

    Google Scholar 

  • Ussing, H.H., Biber, T.U.L., Bricker, N.S. 1965. Exposure of the isolated frog skin to high potassium concentrations at the internal surface: II. Changes in epithelial cell volume, resistance and response to antidiuretic hormone.J. Gen. Physiol. 48:425–433

    PubMed  Google Scholar 

  • Van Driessche, W., Lindemann, B. 1979. Concentration dependence of currents through single sodium-selective pores in frog skin.Nature (London) 282:519–520

    Google Scholar 

  • Warncke, J., Lindemann, B. 1981. Effect of ADH on the capacitance of apical epithelial membranes.In: Advances in Physiological Sciences. Vol. 3: Physiology of Non-Excitable Cells. J. Salanki, editor. pp. 129–133. Pergamon, New York

    Google Scholar 

  • 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 555:519–523

    PubMed  Google Scholar 

  • Zeiske, W., Driessche, W. van 1981. Apical K-channels in frog skin (Rana temporaria): Cation adsorption and voltage influence gating kinetics.Pfluegers Arch. 390:22–29

    Google Scholar 

Download references

Author information

Author notes

  1. S. Randall Thomas

    Present address: Laboratoire de Physiologie Renale, Hospital des Enfants Malades, I.N.S.E.R.M., U. 192, Paris, France

  2. Yuichi Suzuki

    Present address: Department of Physiology, Yamagata University School of Medicine, 990-23, Yamagata, Japan

Authors and Affiliations

  1. Department of Physiology and Cell Biology, University of Texas School of Medicine, 77025, Houston, Texas

    Stanley G. Schultz, Stephen M. Thompson, Randall Hudson, S. Randall Thomas & Yuichi Suzuki

Authors
  1. Stanley G. Schultz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen M. Thompson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Randall Hudson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Randall Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuichi Suzuki
    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

Schultz, S.G., Thompson, S.M., Hudson, R. et al. Electrophysiology ofNecturus urinary bladder: II. Time-dependent current-voltage relations of the basolateral membranes. J. Membrain Biol. 79, 257–269 (1984). https://doi.org/10.1007/BF01871064

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01871064

Key Words

Search

Navigation