Skip to main content
Log in

Relations between intracellular ion activities and extracellular osmolarity inNecturus gallbladder epithelium

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

Summary

The interactions between ion and water fluxes have an important bearing on osmoregulation and transepithelial water transport in epithelial cells. Some of these interactions were investigated using ion-selective microelectrodes in theNecturus gallbladder. The intracellular activities of K+ and Cl in epithelial cells change when the epithelium is adapted to transport in solutions of a low osmolarity. In order to achieve new steady states at low osmolarities, cells lost K+, Cl and some unidentified anions. Surprisingly, the apparent K+ concentration remained high: at an external osmolartity of 64 mOsm the intracellular K+ concentration averaged 95mm. This imbalance was sensitive to anoxia and ouabain. The effects of abrupt changes in the external osmolarities on the intracellular activities of Na+, K+ and Cl were also investigated. The gradients were effectuated by mannitol. The initial relative rates of change of the intracellular activities of Na+ and Cl were equal. The data were consistent with Na+ and Cl ions initially remaining inside the cell and a cell membraneL p of 10−3 cm sec−1 osm−1, which is close to the values determine by Spring and co-workers (K.R. Spring, A. Hope & B.-E. Persson, 1981.In: Water Transport Across Epithelia. Alfred Benzon Symposium 15. pp. 190–200. Munskgaard, Copenhagen). The initial rate of change of the intracellular activity of K+ was only 0.1–0.2 times the change observed in Na+ and Cl activities, and suggests that K+ ions leave the cell during the osmotically induced H2O efflux and enter with an induced H2O influx. The coupling is between 98 and 102 mmoles liter−1. Various explanations for the anomalous behavior of intracellular K+ ions are considered. A discussion of the apparent coupling between K+ and H2O, observed in nonsteady states, and its effects on the distribution of K+ and H2O across the cell membrane in the steady states, is presented.

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

  • Armstrong, W.McD., Bixenman, W.R., Frey, K.F., Garcia-Diaz, J.F., O'regan, M.G., Owens, J.L. 1979. Energetics of coupled Na+ and Cl entry into epithelial cells of bullfrog small intestine.Biochim. Biophys. Acta 551:207–219

    PubMed  Google Scholar 

  • Bindslev, N., Hansen, A.J. 1981. Mono-/bivalent ion selectivities obtained by the Nicolsky and the electrodiffusional regimes.In: Progress in Enzyme and Ion Selective Electrodes. D.W. Lübbers, H. Acker, R.P. Buck, G. Eisenman, M. Kessler, and W. Simon, editors. pp. 25–31. Springer-Verlag, New York

    Google Scholar 

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

    Google Scholar 

  • Bundgaard, M., Zeuthen, T. 1981. The structure ofNecturus gallbladder epithelium at low osmolarities.J. Physiol. (London) 316:60P

    Google Scholar 

  • Case, R.M., Harper, A.A., Scratcherd, T. 1968. Water and electrolyte secretion by the perfused pancreas of the cat.J. Physiol. (London) 196:133–149

    Google Scholar 

  • Diamond, J.M. 1964. The mechanism of isotonic water transport.J. Gen. Physiol. 48:15–42

    PubMed  Google Scholar 

  • Engbaek, L., Guld, C. 1971. Leakage in glass pipette microelectrodes.In: Proceedings of the 2nd Nordic Meeting on Medical and Biological Engineering, Oslo (Society for Medical and Biological Engineering, Oslo), pp. 116–118

    Google Scholar 

  • Frömter, E. 1972. The route of passive ion movement through the epithelium ofNecturus gallbladder.J. Membrane Biol. 8:259–301

    Google Scholar 

  • Frömter, E., Suzuki, K., Kottra, G., Kampmann, L. 1981. The paracellular shunt conductance ofNecturus gallbladder epithelium: Comparison of measurements obtained by cable analysis with measurements obtained by a new approach based on intracellular impedance analysis.In: Epithelial Ion and Water Transport. A.D.C. Macknight and J.P. Leader, editors. pp. 73–83. Raven Press, New York

    Google Scholar 

  • Garcia-Diaz, J.F., Armstrong, W.McD. 1980. The steady-state relationship between sodium and chloride transmembrane electrochemical potential differences inNecturus gallbladder.J. Membrane Biol. 55:213–222

    Google Scholar 

  • Graf, J., Giebish, G. 1979. Intracellular sodium activity and sodium transport inNecturus gallbladder epithelium.J. Membrane Biol. 47:327–355

    Google Scholar 

  • Hill, B.S., Hill, A.E. 1978. Fluid transfer byNecturus gall bladder epithelium as a function of osmolarity.Proc. R. Soc. London B. 200:151–162

    Google Scholar 

  • Hoffmann, E.K. 1977. Control of cell volume.In: Transport of Ions and Water in Animals. B.L. Gupta, R.B. Moreton, J.L. Oschman, and B.J. Wall, editors. pp. 285–332. Academic Press, New York

    Google Scholar 

  • Huxley, A.F. 1961. A micromanipulator.J. Physiol. (London) 157:5P

    Google Scholar 

  • Kedem, O., Katchalsky, A. 1963a. Permeability of composite membranes. 1. Electric current, volume flow and flow of solute through membranes.Proc. Faraday Soc. 59:1918–1930

    Google Scholar 

  • Kedem, O., Katchalsky, A. 1963b. Permeability of composite membranes. 2. Parallel elements.Proc. Faraday Soc. 59:1931–1940

    Google Scholar 

  • Khuri, R.N., Bogharian, K.K., Agulian, S.K. 1974. Intracellular bicarbonate in single cells ofNecturus kidney proximal tubule.Pfluegers Arch. 249:295–299

    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 

  • Machen, T.E., Zeuthen, T. 1980. Electrophysiology of Cl in the stomach.J. Physiol. (London) 301:48P

    Google Scholar 

  • Macknight, D.C., Leaf, A. 1977. Regulation of cellular volume.Physiol. Rev. 57:511–573

    Google Scholar 

  • Maddrell, S.H.P. 1969. Secretion by the malpighian tubules of rhodnius. The movement of ions and water.J. Exp. Biol. 51:71–97

    Google Scholar 

  • Moody, F.G., Durbin, R.P. 1969. Water flow induced by osmotic and hydrostatic pressure in the stomach.Am. J. Physiol. 217:255–264

    PubMed  Google Scholar 

  • Nelson, D.J., Ehrenfeld, J., Lindemann, B. 1978. Volume changes and potential artifacts of epithelial cells of frog skin following impalement with microelectrodes filled with 3m KCl.J. Membrane Biol. Special Issue:91–119

  • Ramsey, J.A., Brown, R.H.J. 1955. Simplified apparatus and procedure for freezing-point determination upon small volumes of fluid.J. Sci. Instrum. 32:372–375

    Google Scholar 

  • Reuss, L. 1979. Electrical properties of the cellular transepithelial pathway inNecturus gallbladder. III. Ionic permeability of the basolateral cell membrane.J. Membrane Biol. 47:239–259

    Google Scholar 

  • Reuss, L., Finn, A.L. 1975. Electrical properties of the cellular transepithelial pathway inNecturus gallbladder.J. Membrane Biol. 25:115–139

    Google Scholar 

  • Reuss, L., Finn, A.L. 1977. Effects of luminal hyperosmolality on electrical pathways ofNecturus gallbladder.Am. J. Physiol. 232:C99-C108

    PubMed  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

    Google Scholar 

  • Robinson, R.A., Stokes, R.H. 1959. Electrolyte Solutions. Second edition (revised). Butterworths, London

    Google Scholar 

  • Spring, K.R., Hope, A. 1979. Fluid transport and the dimensions of cells and interspaces of livingNecturus gallbladder.J. Gen. Physiol. 73:287–305

    PubMed  Google Scholar 

  • Spring, K.R., Hope, A., Persson, B.-E. 1981.In: Water Transport Across Epithelia. Alfred Benzon Symposium 15. H.H. Ussing, N. Bindslev, N.A. Lassen, and O. Sten-Knudsen, editors. pp. 190–200. Munskgaard, Copenhagen

    Google Scholar 

  • White, J.F. 1976. Intracellular potassium activities inAmphiuma small intestine.Am. J. Physiol. 231:1214–1219

    PubMed  Google Scholar 

  • Zeuthen, T. 1976. The vertebrate gall-bladder. The routes of ion transport.In: Fluid Transport in Epithelia. B.L. Gupta, R.B. Moreton, J.L. Oschman, and B.J. Wall, editors. pp. 511–551. Academic Press, New York

    Google Scholar 

  • Zeuthen, T. 1978. Intracellular gradients of ion activities in the epithelial cells of theNecturus gallbladder recorded with ion-selective microelectrodes.J. Membrane Biol. 39:185–218

    Google Scholar 

  • Zeuthen, T. 1980. How to make and use double-barrelled ion-selective microelectrodes.In: Current Topics in Membranes and Transport. E. Boulpaep, editor. Vol. 13. pp. 31–47. Academic Press, New York

    Google Scholar 

  • Zeuthen, T. 1981a. The intracellular osmolarity during isotonic fluid transport in gallbladder. Alfred Benzon Symposium 15. H.H. Ussing, Bindslev, N.A. Lassen, and O. Sten-Knudsen, editors. pp. 313–324. Munskgaard, Copenhagen

    Google Scholar 

  • Zeuthen, T. 1981b. Ion transport in leaky epithelia studied with ion-selective microelectrodes.In: The Application of Ion-Selective Microelectrodes. T. Zeuthen, editor. pp. 27–46. North Holland/Elsevier

  • Zeuthen, T. 1981c. On the effects of amphotericin B and ouabain on the electrical potentials ofNecturus gallbladder.J. Membrane Biol. 60:167–169

    Google Scholar 

  • Zeuthen, T., Hiam, R.C., Silver, I.A. 1974. Recording of ion activities in the brain.In: Ion Selective Microelectrodes. H. Berman and N. Herbert, editors. pp. 145–156. Plenum Press, London

    Google Scholar 

  • Zeuthen, T., Wright, M. 1981. Epithelial potassium transport: Tracer and electrophysiological studies in choroid plexus.J. Membrane Biol. 60:105–128

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zeuthen, T. Relations between intracellular ion activities and extracellular osmolarity inNecturus gallbladder epithelium. J. Membrain Biol. 66, 109–121 (1982). https://doi.org/10.1007/BF01868487

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01868487

Key words

Navigation