The Journal of Membrane Biology

, Volume 71, Issue 3, pp 209–218 | Cite as

Chloride secretion by canine tracheal epithelium: III. Membrane resistances and electromotive forces

  • Michael J. Welsh
  • Phillip L. Smith
  • Raymond A. Frizzell


We used intracellular microelectrode techniques and equivalent electrical circuit analysis to examine the changes in individual membrane resistances and electromotive forces that accompany stimulation of Cl secretion across canine tracheal epithelium. Tissues were pretreated with indomethacin (10−6m, mucosal solution) to reduce basel Cl secretion rate. Subsequent addition of epinephrine (10−6m, submucosal solution) increased the rate of electrogenic Cl secretion as indicated by an increase in the short-circuit current (Isc) and decrease in the transepithelial resistance (R t ). The reduction inR t was due to decreases in bothR a andR b (the resistances of the apical and basolateral cell membranes, respectively).

At the apical membrane, a nearly 10-fold decrease inR a was accompanied by reversal of the electromotive force (E a ) from +11±9 mV to −31±3 mV. Variations in Cl secretion rate induced by indomethacin and epinephrine disclosed a direct relation betweenR a andE a . In the presence of indomethacinR a was high andE a was consistent with the chemical potential difference for Na across the apical membrane (ca. +60 mV), reflecting the predominance of Na absorption across indomethacin-treated tissues. In the presence of epinephrine,R a was low andE a was consistent with the chemical potential difference for Cl across this barrier (−31 mV), reflecting the dominance of Cl secretion across epinephrine-treated tissues. These findings suggest that the conversion from absorption to secretion primarily involves a secretogogue-induced decrease in apical membrane resistance to Cl.

At the basolateral membrane, epinephrine decreasedR b threefold without markedly altering the electromotive force across this barrier (E b ). To the extent thatR b andE b represent the resistance and chemical potential difference for K diffusion across the basolateral membrane, the inverse relation betweenR b andIsc suggests that stimulation is associated with increased basolateral membrane K permeability without marked changes in intracellular K activity.

Key words

tracheal epithelium Cl secretion electrophysiology equivalent electrical circuit epinephrine 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Al-Bazzaz, F.J., Al-Awqati, Q. 1979. Interaction between sodium and chloride transport in canine tracheal mucosa.J. Appl. Physiol. 46:111–119Google Scholar
  2. Al-Bazzaz, F.J., Cheng, E. 1979. Effect of catecholamines on ion transport in dog tracheal epithelium.J. Appl. Physiol. 47:397–403Google Scholar
  3. Al-Bazzaz, F., Yadava, V.P., Westenfelder, C. 1981. Modification of Na and Cl transport in canine tracheal mucosa by prostaglandins.Am. J. Physiol. 240:F101-F105Google Scholar
  4. Boulpaep, E.L. 1976. Electrical phenomena in the nephron.Kidney Int. 9:88–102Google Scholar
  5. Cuthbert, A.W., Fanelli, G.M., Sciabine, A. 1979. Amiloride and Epithelial Sodium Transport. Urban and Schwarzenberg, Inc., Baltimore, Md.Google Scholar
  6. Davis, C.W., Finn, A.L. 1982. Sodium transport inhibition by amiloride reduces basolateral membrane potassium conductance in tight epithelia.Science 216:525–527Google Scholar
  7. Finkelstein, A., Mauro, A. 1963. Equivalent circuits as related to ionic systems.Biophys. J. 3:215–237Google Scholar
  8. Frizzell, R.A., Field, M., Schultz, S.G. 1979. Sodium-coupled chloride transport by epithelial tissues.Am. J. Physiol. 236:F1-F8Google Scholar
  9. Frömter, E. 1972. The route of passive ion movement through the epithelium ofNecturus gallbladder.J. Membrane Biol. 8:259–301Google Scholar
  10. 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
  11. Gunter-Smith, P., Grasset, E., Schultz, S.G. 1982. Sodiumcoupled amino acid and sugar transport by necturus small intestine. An equivalent electrical circuit analysis of a rheogenic co-transport system.J. Membrani Biol (in press) Google Scholar
  12. Klyce, S.D., Wong, R.K.S. 1977. Site and mode of adrenalin action on chloride transport across the rabbit corneal epithelium.J. Physiol. 266:777–799Google Scholar
  13. 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
  14. Nagel, W., Reinach, P. 1980. Mechanism of stimulation by epinephrine of active transepithelial Cl transport in isolated frog cornea.J. Membrane Biol. 56:73–79Google Scholar
  15. Olver, R.E., Davis, B., Marin, M.G., Nadel, J.A. 1975. Active transport of Na+ and Cl across the canine tracheal epithelium in vitro.Am. Rev. Respir. Dis. 112:811–815Google Scholar
  16. Reuss, L., Finn, A.L. 1974. Passive electrical properties of toad urinary bladder epithelium: Intracellular electrical coupling and transepithelial, cellular and shunt conductances.J. Gen. Physiol. 64:1–25Google Scholar
  17. Reuss, L., Finn, A.L. 1975. Electrical properties of the cellular transepithelial pathway inNecturus gallbladder. I. Circuit analysis and steady-state effects of mucosal solution ionic substitutions.J. Membrane Biol. 25:115–139Google Scholar
  18. Schultz, S.G. 1979. Application of equivalent electrical circuit models to study of sodium transport across epithelial tissues.Fed. Proc. 38:2024–2029Google Scholar
  19. Schultz, S.G. 1981. Homocellular regulatory mechanisms in sodium-transporting epithelia: Avoidance of extinction by “flush through”.Am. J. Physiol. 241:F579-F590Google Scholar
  20. 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
  21. Shorofsky, S., Field, M., Fozzard, H. 1980. Electrophysiologic studies of canine tracheal epithelium.J. Gen. Physiol. 76:27aGoogle Scholar
  22. Smith, P.L., Frizzell, R.A. 1982. Changes in intracellular K activity after stimulation of chloride secretion in canine tracheal epithelium.Chest 81:5sGoogle Scholar
  23. Smith, P.L., Welsh, M.J., Stoff, J.S., Frizzell, R.A. 1982. Chloride secretion by canine tracheal epithelium: I. Role of intracellular cAMP levels.J. Membrane Biol. 70:217–226Google Scholar
  24. Welsh, M.J. 1982. The effect of barium and potassium on chloride secretion by canine tracheal epithelium.Fed. Proc. 41:1260Google Scholar
  25. Welsh, M.J. 1983. Inhibition of chloride secretion by furosemide in canine tracheal epithelium.J. Membrane Biol. 71:219–226Google Scholar
  26. Welsh, M.J., Smith, P.L., Frizzell, R.A. 1981. Intracellular chloride activities in the isolated perfused shark rectal gland.Clin. Res. 29:480AGoogle Scholar
  27. Welsh, M.J., Smith, P.L., Frizzell, R.A. 1982. Chloride secretion by canine tracheal epithelium: II. The cellular electrical potential profile.J. Membrane Biol. 70:227–238Google Scholar
  28. Welsh, M.J., Widdicombe, J.H. 1980. Pathways of ion movement in the canine tracheal epithelium.Am. J. Physiol. 239:F215-F221Google Scholar
  29. Widdicombe, J.H., Basbaum, C.B., Highland, E. 1981. Ion contents and other properties of isolated cells from dog tracheal epithelium.Am. J. Physiol. 241:C184-C192Google Scholar
  30. Widdicombe, J.H., Basbaum, C.B., Yee, J.Y. 1979a. Localization of Na pumps in the tracheal epithelium of the dog.J. Cell Biol. 82:380–390Google Scholar
  31. Widdicombe, J.H., Ueki, I.F., Bruderman, I., Nadel, J.A. 1979b. The effects of sodium substitution and ouabain on ion transport by dog tracheal epithelium.Am. Rev. Respir. Dis. 120:385–392Google Scholar
  32. Widdicombe, J.H., Welsh, M.J. 1980. Ion transport by dog tracheal epithelium.Fed. Proc. 39:3062–3066Google Scholar
  33. Yonath, J., Civan, M.M. 1971. Determination of the driving force of the Na+ pump in toad bladder by means of vasopressin.J. Membrane Biol. 5:366–385Google Scholar
  34. Zadunaisky, J.A., Spring, K.R., Shindo, T. 1979. Intracellular chloride activity in the corneal epithelium.Fed. Proc. 38:1059Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1983

Authors and Affiliations

  • Michael J. Welsh
    • 1
    • 2
  • Phillip L. Smith
    • 1
    • 2
  • Raymond A. Frizzell
    • 1
    • 2
  1. 1.Department of Physiology and Cell BiologyUniversity of Texas Medical School at HoustonHouston
  2. 2.Pulmonary Division, Department of Internal MedicineUniversity of Iowa College of MedicineIowa City

Personalised recommendations