The Journal of Membrane Biology

, Volume 66, Issue 1, pp 41–54 | Cite as

The electrophysiology of rabbit descending colon

I. Instantaneous transepithelial current-voltage relations and the current-voltage relations of the Na-entry mechanism
  • Stephen M. Thompson
  • Yuichi Suzuki
  • Stanley G. Schultz


A method is described for determining the “instantaneous” transepithelial current-voltage (I-V) relations across rabbit descending colon and deriving theI-V relations of the amiloride-sensitive Na-entry step across the apical membrane. The latter conforms closely to the predictions of the Goldman-Hodgkin-Katz “constant-field” flux equation over a wide range of values of the transapical electrical potential difference (−120 to +50 mV), suggesting that Na entry is the result of simple electrodiffusion through homogeneous pores or channels. The permeability of the apical membrane to Na averaged 0.012 cm/hr, and the intracellular Na activity averaged 10mm. In the studies, the rate of Na entry across the apical membrane varied, spontaneously, over a fourfold range; this variation is entirely attributable to parallel variations in the partial conductance of the apical membrane to Na with no change in the driving force for this movement.

Bathing the serosal surface of the tissue with a high-K solution abolishes the electrical potential difference across the basolateral membrane and markedly reduces the resistance of that barrier. Under these conditions, theI-V relations of the amiloride-sensitive Na-entry step across the apical membrane also conform closely to the predictions of the “constant-field” flux equation.

Finally, the significance of the point at which the transepithelialI-V relations in the absence and presence of amiloride intersect (“ENa”) and the origin of the “bends” in theseI-V relations at or around this point are discussed. We demonstrate that the point of intersection is simply that value of the transepithelial electrical potential difference at which Na entry is abolished and has no direct bearing on the energetics of the basolateral pump. The “bend” in theI-V relations appears to be due to an increase in the conductance of a pathway in the apical membrane that parallels the Na-entry pathway in the apical membrane that parallels the Na-entry pathway as well as an increase in the conductance of the paracellular pathway; thus, this “bend” does not appear to be directly related to changes in the “active Na transport pathway”.

Key words

colon Na entry electrophysiology current-voltage relations apical membrane amiloride 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bentley, P.J. 1960. The effects of vasopressin on the short-circuit current across the wall of the isolated bladder of the toadBufo marinus.J. Endocrinol. 21:161–170Google Scholar
  2. Bindslev, N., Tormey, J.McD., Pietras, R.J., Wright, E.M. 1974. Electrically and osmotically induced changes in the permeability and structure of toad urinary bladder.Biochim. Biophys. Acta 332:286–297Google Scholar
  3. Chen, J.S., Walser, M. 1975. Sodium fluxes through the active transport pathway in toad bladder.J. Membrane Biol. 21:87–98Google Scholar
  4. Civan, M.M. 1970. Effects of active sodium transport on current-voltage relationship of toad bladder.Am. J. Physiol. 219:234–245PubMedGoogle Scholar
  5. Civan, M.M., Hall, T.E., Gupta, B.L. 1980. Microprobe study of toad urinary bladder in absence of serosal K+ J. Membrane Biol. 55:187–202Google Scholar
  6. Clausen, C., Lewis, S.A., Diamond, J.M. 1979. Impedance analysis of a tight epithelium using a distributed resistance model.Biophys. J. 26:291–318PubMedGoogle Scholar
  7. Finkelstein, A., Mauro, A. 1963. Equivalent circuits as related to ionic systems.Biophys. J. 3:215–233Google Scholar
  8. Finkelstein, A., Mauro, A. 1977. Physical principles and formalisms of electrical excitability.In: Handbook of Physiology, Section I: The Nervous System. E. Kandel, editor, Vol. 1, Part 1, pp. 161–213. American Physiological Society, BethesdaGoogle Scholar
  9. Finn, A.L., Rogenes, P. 1980. The effects of voltage clamping on ion transport pathways in tight epithelial.In: Current Topics in Membranes and Transport. E.L. Boulpaep, editor. Vol. 13, pp. 245–255. Academic Press, New YorkGoogle Scholar
  10. Frizzell, R.A., Koch, M.J., Schultz, S.G. 1976. Ion transport by rabbit colon. I. Active and passive components.J. Membrane Biol. 27:297–316Google Scholar
  11. Frizzell, R.A., Schultz, S.G. 1978. Effect of aldosterone on ion transport by rabbit colonin vitro.J. Membrane Biol. 39:1–26Google Scholar
  12. Frizzell, R.A., Turnheim, K. 1978. Ion transport by rabbit colon. II. Unidirectional sodium influx and the effects of amphotericin B and amiloride.J. Membrane Biol. 40:193–212Google Scholar
  13. Fromm, M., Schultz, S.G. 1981. Some properties of KCl-filled microelectrodes: Correlation of potassium “leakage” with tip resistance.J. Membrane Biol. 62:239–244Google Scholar
  14. Frömter, E., Gebler, B. 1977. Electrical properties of amphibian urinary bladder epithelia. III. The cell membrane resistances and the effect of amiloride.Pfluegers Arch. 371:99–108Google Scholar
  15. 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) 267:137–166Google Scholar
  16. Goldman, D. 1943. Potential, impedance and rectification in membranes.J. Gen. Physiol. 27:37–60Google Scholar
  17. Graf, J., Giebisch, G. 1979. Intracellular sodium activity and sodium transport inNecturus gallbladder epithelium.J. Membrane Biol. 47:327–355Google Scholar
  18. Grinstein, S., Erlij, D. 1978. Intracellular calcium and the regulation of sodium transport in the frog skin.Proc. R. Soc. London B 202:353–360Google Scholar
  19. Helman, S.I., Fisher, R.S., 1977. Microelectrode studies of the active Na transport pathway of frog skin.J. Gen. Physiol. 69:571–604PubMedGoogle Scholar
  20. Helman, S.I., O'Neil, R.G., Fisher, R.S. 1975 Determination of theE Na of frog skin from studies of its current-voltage relationship.Am. J. Physiol. 229:947–951PubMedGoogle Scholar
  21. Higgins, J.T., Jr., Gebler, B., Frömter, E. 1977. Electrical properties of amphibian urinary bladder. II. The cell potential profile inNecturus maculosus.Pfluegers Arch. 371:87–97Google Scholar
  22. 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) 108:37–77Google Scholar
  23. Lee, C.O., Armstrong, W.McD. 1972. Activities of sodium and potassium ions in epithelial cells of small intestine.Science 175:1261–1264Google Scholar
  24. Lewis, S.A., Diamond, J.M. 1946. Na+ transport by rabbit urinary bladder, a tight epithelium.J. Membrane Biol. 28:1–40Google Scholar
  25. Lewis, S.A., Eaton, D.C., Diamond, J.M. 1976. The mechanism of Na+ transport by rabbit urinary bladder.J. Membrane Biol. 28:41–70Google Scholar
  26. Lewis, S.A., Graf, J. 1979. Assessment of impalement damage.Appendix to: Graf, J., Giebisch, G. 1979. Intracellular sodium activity of sodium transport inNecturus gallbladder epithelium.J. Membrane Biol. 47:350–355Google Scholar
  27. Lewis, S.A., Wills, N.K. 1980. Resistive artifacts in liquid-ion exchanger microelectrode estimates of Na+ activity in epithelial cells.Biophys. J. 31:127–138PubMedGoogle Scholar
  28. Li, J.H.-Y., Palmer, L.G., Edelman, I.S., Lindemann, B. 1979. Effect of ADH on Na channel parameters in toad urinary bladder.Pflueger's Arch. 382:R13Google Scholar
  29. Lindemann, B. 1975. Impalement arifacts in microelectrode recording of epithelial membrane potentials.Biophys. J. 15:1161–1164PubMedGoogle Scholar
  30. Lindemann, B., Van Driessche, W. 1977. Sodium-specific membrane channels of frog skin are pores: Current fluctuations reveal high turnover.Science 195:292–294PubMedGoogle Scholar
  31. Macchia, D.D., Helman, S.I. 1979. Transepithelial current-voltage relationships of toad urinary bladder and colon estimates ofE Na and shunt resistance.Biophys. J. 27:371–392PubMedGoogle Scholar
  32. Macknight, A.D.C., DiBona, D.R., Leaf, A. 1980. Sodium transport across toad urinary bladder: A model tight epithelium.Physiol. Rev. 60:615–715PubMedGoogle Scholar
  33. Mandel, L.J., Curran, P.F. 1973. Response of the frog skin to steady-state voltage clamping. II. The active pathway.J. Gen. Physiol. 62:1–24Google Scholar
  34. Morel, F., LeBlanc, G. 1975. Transient current changes and Na compartmentalization in frog skin epithelium.Pfluegers Arch. 358:135–157Google Scholar
  35. Navarte, J., Finn, A.L. 1980. Microelectrode studies in toad urinary bladder epithelium. Effects of Na concentration changes in the mucosal solution on equivalent electromotive forces.J. Gen. Physiol. 75:323–344PubMedGoogle Scholar
  36. 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:91–119Google Scholar
  37. O'Doherty, J., Garcia-Diaz, J.F., Armstrong, W.M. 1979. Sodium-selective liquid ion-exchanger microelectrodes for intracellular measurements.Science 203:1349–1351PubMedGoogle Scholar
  38. O'Neil, R.G., Helman, S.I. 1976. Influence of vasopressin and amiloride on shunt pathways of frog skin.Am. J. Physiol. 231:164–173PubMedGoogle Scholar
  39. 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 metabolismJ. Membrane Biol. 57:59–71Google Scholar
  40. Rawlins, F., Mateu, L., Fragachan, F., Whittembury, G. 1970. Isolated toad skin epithelium: Transport characteristics.Pfluegers Arch. 316:64–80Google Scholar
  41. Rick, R., Dörge, A., Von Arnim, E., Thurau, K. 1978. Electron microprobe analysis of frog skin epithelium: Evidence for a syncytial Na transport compartment.J. Membrane Biol. 39:313–331Google Scholar
  42. Rick, R., Thurau, K. 1978. Electron microprobe analysis of the different epithelial cells of toad urinary bladder.J. Membrane Biol. 39:257–271Google Scholar
  43. Saito, T., Lief, P.D., Essig, A. 1974. Conductance of active and passive pathways in the toad bladder.Am. J. Physiol. 226:1265–1271PubMedGoogle Scholar
  44. Schultz, S.G. 1979. Application of equivalent electrical circuit models to study of sodium transport across epithelial tissues.Fed. Proc. 38:2024–2029PubMedGoogle Scholar
  45. Schultz, S.G. 1981. Homocellular regulatory mechanisms in sodium transporting epithelia.Am. J. Physiol. 241:F579-F590PubMedGoogle Scholar
  46. Schultz, S.G., Frizzell, R.A., Nellans, H.N. 1977. Active sodium transport and the electrophysiology of rabbit colon.J. Membrane Biol. 33:351–384Google Scholar
  47. Schultz, S.G., Thompson, S.M., Suzuki, Y. 1981a. Equivalent electrical circuit models and the study of Na transport across epithelia: II. Nonsteady-state current-voltage relations.Fed. Proc. 40:2443–2449PubMedGoogle Scholar
  48. Schultz, S.G., Thompson, S.M., Suzuki, Y. 1981b. On the mechanism of sodium entry across the apical membrane of rabbit colon.In: Epithelial Ion and Water Transport. A.D.C. Macknight and J.P. Leader, editors. pp. 285–296. Raven Press, New YorkGoogle Scholar
  49. Spooner, P.M., Edelman, I.S. 1975. Further studies on the effect of aldosterone on electrical resistance of toad bladder.Biochim. Biophys. Acta 406:304–314PubMedGoogle Scholar
  50. Suzuki, K., Frömter, E. 1977. The potential and resistance profile ofNecturus gallbladder cells.Pfluegers Arch. 371:109–117Google Scholar
  51. Taylor, A. 1981. Role of cytosolic calcium and Na−Ca exchange in regulation of transepithelial sodium and water absorption.In: Ion Transport by Epithelia. S.G. Schultz, editor. pp. 233–260. Raven Press, New YorkGoogle Scholar
  52. Taylor, A., Windhager, E.E. 1979. Possible role cytosolic calcium and Na−Ca exchange in regulation of transepithelial sodium transport.Am. J. Physiol. 236:F505-F512PubMedGoogle Scholar
  53. 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
  54. Turnheim, K., Frizzell, R.A., Schultz, S.G. 1978. Interaction between cell sodium and the amiloride-sensitive sodium entry step in rabbit colon.J. Membrane Biol. 39:233–256Google Scholar
  55. Ussing, H.H. 1960. The Alkali Metal Ions in Biology. Springer-Verlag, BerlinGoogle Scholar
  56. 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. 23:110–127PubMedGoogle Scholar
  57. Wills, N.K., Eaton, D.C., Lewis, S.A., Ifshin, M.S. 1979a. Currentvoltage relationship of the basolateral membrane of a tight epithelium.Biochim. Biophys. Acta 555:519–523PubMedGoogle Scholar
  58. Wills, N.K., Lewis, S.A. 1980. Intracellular Na+ activity as a function of Na+ transport rate across a tight epithelium.Biophys. J. 30:181–186PubMedGoogle Scholar
  59. Wills, N.K., Lewis, S.A., Eaton, D.C. 1979b. Active and passive properties of rabbit descending colon: A microelectrode and nystatin study.J. Membrane Biol. 45:81–108Google Scholar
  60. Wolff, D., Essig, A. 1977. Kinetics of bidirectional active sodium fluxes in the toad bladder.Biochim. Biophys. Acta 468:271–283PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1982

Authors and Affiliations

  • Stephen M. Thompson
    • 1
  • Yuichi Suzuki
    • 1
  • Stanley G. Schultz
    • 1
  1. 1.Department of Physiology and Cell BiologyUniversity of Texas Medical SchoolHouston

Personalised recommendations