The Journal of Membrane Biology

, Volume 49, Issue 4, pp 345–362 | Cite as

Intracellular ionic activities and transmembrane electrochemical potential differences in gallbladder epithelium

  • Luis Reuss
  • Steven A. Weinman
Article

Summary

Intracellular ion activities inNecturus gallbladder epithelium were measured with liquid ion-exchanger microelectrodes. Mean values for K, Cl and Na activities were 87, 35 and 22mm, respectively. The intracellular activities of both K and Cl are above their respective equilibrium values, whereas the Na activity is far below. This indicates that K and Cl are transported uphill toward the cell interior, whereas Na is extruded against its electrochemical gradient. The epithelium transports NaCl from mucosa to serosa. From the data presented and the known Na and Cl conductances of the cell membranes, we conclude that neutral transport driven by the Na electrochemical potential difference can account for NaCl entry at the apical membrane. At the basolateral membrane, Na is actively transported. Because of the low Cl conductance of the membrane, only a small fraction of Cl transport can be explained by diffusion. These data suggest that Cl transport across the basolateral membrane is a coupled process which involves a neutral NaCl pump, downhill KCl transport, or a Cl-anion exchange system.

Keywords

Apical Membrane Basolateral Membrane Cell Interior Couple Process Electrochemical Gradient 

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References

  1. Armstrong, W. McD., O'Doherty, J., García-Díaz, J.F., O'Regan, M.G. 1979. The Na+ electrochemical gradient and solute accumulation in epithelial cells of the small intestine.Fed. Proc. (in press) Google Scholar
  2. Cremaschi, D., Hénin, S. 1975. Na+ and Cl transepithelial routes in rabbit gallbladder. Tracer analysis of the transports.Pfluegers Arch. 361:33Google Scholar
  3. Cremaschi, D., Hénin, S., Meyer, G., Bacciola, T. 1977. Does amphotericin B unmask an electrogenic Na+ pump in rabbit gallbladder? Shift of gallbladders with negative to gallbladders with positive transepithelial p.d.'s.J. Membrane Biol. 34:55Google Scholar
  4. DeLong, J., Civan, M.M. 1978. Dissociation of cellular K+ accumulation from net Na+ transport by toad urinary bladder.J. Membrane Biol. 42:19Google Scholar
  5. Diamond, J.M. 1968. Transport mechanisms in the gallbladder.In: Handbook of Physiology, Section 6. C.F. Code, editor. Vol. V, p. 2451. Williams & Wilkins, BaltimoreGoogle Scholar
  6. Dietschy, J.M., Moore, E.W. 1964. Diffusion potentials and potassium distribution across the gallbladder wall.J. Clin. Invest. 43:1551PubMedGoogle Scholar
  7. Duffey, M.E., Turnheim, K., Frizzell, R.A., Schultz, S.G. 1978. Intracellular chloride activities in rabbit gallbladder: Direct evidence for the role of the sodium-gradient in energizing “uphill” chloride transport.J. Membrane Biol. 42:229Google Scholar
  8. Frizzell, R.A., Dugas, M.C., Schultz, S.G. 1975. Sodium chloride transport by rabbit gallbladder. Direct evidence for a coupled NaCl influx process.J. Gen. Physiol. 65:769PubMedGoogle Scholar
  9. Frömter, E. 1972. The route of passive ion movement through, the epithelium ofNecturus gallbladder.J. Membrane Biol. 8:259Google Scholar
  10. Fujimoto, M., Kubota, T. 1976. Physicochemical properties of a liquid ion exchanger microelectrode and its application to biological fluids.Jpn. J. Physiol. 26:631PubMedGoogle Scholar
  11. Higgins, J.T., Jr., Gebler, B., Frömter, E. 1977. Electrical properties of amphibian urinary bladder epithelia. II. The cell potential profile inNecturus maculosus.Pfluegers Arch. 371:87Google Scholar
  12. Khuri, R.N., Hajjar, J.J., Agulian, S., Bogharian, K., Kalloghlian, A., Bizri, H. 1972. Intracellular potassium in cells of the proximal tubule ofNecturus maculosus.Pfluegers Arch. 338:73Google Scholar
  13. Lindemann, B. 1975. Impalement artifacts in microelectrode recordings of epithelial membrane potentials.Biophys. J. 15:1161PubMedGoogle Scholar
  14. Loewenstein, W.R., Nakas, M., Socolar, S.J. 1967. Junctional membrane uncoupling. Permeability transformation of a cell membrane junction.J. Gen. Physiol. 50:1865PubMedGoogle Scholar
  15. Mills, J.W., DiBona, D.R. 1978. Distribution of Na+ pump sites in the frog gallbladder.Nature (London) 271:273Google Scholar
  16. Nellans, H.N., Frizzell, R.A., Schultz, S.G. 1973. Coupled sodium-chloride influx across the brush border of rabbit ileum.Am. J. Physiol. 225:467PubMedGoogle Scholar
  17. Nelson, D.J., Ehrenfeld, J., Lindemann, B. 1978. Volume changes and potential artifacts of epithelial cells of frog skin following impalements with microelectrodes filled with 3m KCl.J. Membrane Biol. Special Issue:91Google Scholar
  18. Ogden, T.E., Citron, M.C., Pierantoni, R. 1978. The jet stream microbeveler: An inexpensive way to bevel ultrafine glass micropipettes.Science 201:469PubMedGoogle Scholar
  19. Orme, F.W. 1969. Liquid ion-exchanger microelectrodes.In: Glass Microelectrodes. M. Lavallee, O.F. Schanne, and N.C. Hebert, editors. p. 376. Wiley, New YorkGoogle Scholar
  20. Palmer, L.G., Century, T.J., Civan, M.M. 1978. Activity coefficients of intracellular Na+ and K+ during development of frog oocytes.J. Membrane Biol. 40:25Google Scholar
  21. Palmer, L.G., Civan, M.M. 1975. Intracellular distribution of free potasium inChironomus salivary glands.Science 188:1321PubMedGoogle Scholar
  22. Reuss, L. 1978. Effects of amphotericin B on the electrical properties ofNecturus gallbladder: Intracellular microelectrode studies.J. Membrane Biol. 41:65Google Scholar
  23. Reuss, L. 1979a. Electrical properties of the cellular transepithelial pathway inNecturus gallbladder. III. Ionic permeability of the basolateral cell membrane.J. Membrane Biol. 47:239Google Scholar
  24. Reuss, L. 1979b. Ion conductances and electrochemical gradient across membranes of gallbladder epithelium.In: Membrane Transport Processes. Vol. 13. Current Topics in Membrane and Transport. E. Boulpaep, editor. Academic Press, New York(in press) Google Scholar
  25. Reuss, L., Bello-Reuss, E., Grady, T.P. 1979. Effects of ouabain on fluid transport and electrical properties ofNecturus gallbladder. Evidence in favor of a neutral basolateral sodium transport mechanism.J. Gen. Physiol. 73:385PubMedGoogle Scholar
  26. Reuss, L., Finn, A.L. 1975a Electrical properties of the cellular transepithelial pathway inNecturus gallbladder. I. Circuit analysis and steady-state effects of mucosal solution ionic substitutions.J. Membrane Biol. 25:115Google Scholar
  27. Reuss, L., Finn, A.L. 1975b. Electrical properties of the cellular transepithelial pathway inNecturus gallbladder. II. Ionic permeability of the apical cell membrane.J. Membrane Biol. 25:141Google Scholar
  28. Reuss, L., Finn, A.L. 1977. Effects of luminal hyperosmolality on electrical pathways ofNecturus gallbladder.Am. J. Physiol. 232:C99PubMedGoogle Scholar
  29. Rose, R.C. 1978. Electrolyte absorption by gallbladders: Models of transport.Life Sci. 23:1517PubMedGoogle Scholar
  30. Saunders, J.H., Brown, H.M. 1977. Liquid and solid-state Cl-sensitive microelectrodes. Characteristics and application to intracellular Cl activity in Balanus photoreceptor.J. Gen. Physiol. 70:507PubMedGoogle Scholar
  31. Spring, K.R., Kimura, G. 1978. Chloride reabsorption by renal proximal tubules ofNecturus.J. Membrane Biol. 38:233Google Scholar
  32. Spring, K.R., Kimura, G. 1979. Ion activities inNecturus proximal tubule.Fed. Proc. (in press) Google Scholar
  33. Suzuki, K., Frömter, E. 1977. The potential and resistance profile ofNecturus gallbladder cells.Pfluegers Arch. 371:109Google Scholar
  34. Van Os, C.H., Slegers, J.F.G. 1971. Correlation between (Na−K)-activated ATPase activities and the rate of isotonic fluid transport of gallbladder epithelium.Biochim. Biophys. Acta 241:89PubMedGoogle Scholar
  35. Van Os, C.H., Slegers, J.F.G. 1975. The electrical potential profile of gallbladder epithelium.J. Membrane Biol. 24:341Google Scholar
  36. Walker, J.L., Jr. 1971. Ion specific liquid exchanger microelectrodes.Anal. Chem. 43:89A Google Scholar
  37. Zeuthen, T. 1977. Intracellular gradients of electrical potential in the epithelial cells of theNecturus gallbladder.J. Membrane Biol. 33:281Google Scholar
  38. Zeuthen, T. 1978. Intracellular gradients of ion activities in the epithelial cells of theNecturus gallbladder recorded with ion-selective microelectrodes.J. Membrane Biol. 39:185Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1979

Authors and Affiliations

  • Luis Reuss
    • 1
  • Steven A. Weinman
    • 1
  1. 1.Department of Physiology & BiophysicsWashington University School of MedicineSt. Louis

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