Skip to main content
Log in

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

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

Summary

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 (10−6 m, mucosal solution) to reduce basel Cl secretion rate. Subsequent addition of epinephrine (10−6 m, submucosal solution) increased the rate of electrogenic Cl secretion as indicated by an increase in the short-circuit current (I sc) 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 andI sc suggests that stimulation is associated with increased basolateral membrane K permeability without marked changes in intracellular K activity.

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

  • Al-Bazzaz, F.J., Al-Awqati, Q. 1979. Interaction between sodium and chloride transport in canine tracheal mucosa.J. Appl. Physiol. 46:111–119

    Google Scholar 

  • Al-Bazzaz, F.J., Cheng, E. 1979. Effect of catecholamines on ion transport in dog tracheal epithelium.J. Appl. Physiol. 47:397–403

    Google Scholar 

  • 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-F105

    Google Scholar 

  • Boulpaep, E.L. 1976. Electrical phenomena in the nephron.Kidney Int. 9:88–102

    Google Scholar 

  • Cuthbert, A.W., Fanelli, G.M., Sciabine, A. 1979. Amiloride and Epithelial Sodium Transport. Urban and Schwarzenberg, Inc., Baltimore, Md.

    Google Scholar 

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

    Google Scholar 

  • Finkelstein, A., Mauro, A. 1963. Equivalent circuits as related to ionic systems.Biophys. J. 3:215–237

    Google Scholar 

  • Frizzell, R.A., Field, M., Schultz, S.G. 1979. Sodium-coupled chloride transport by epithelial tissues.Am. J. Physiol. 236:F1-F8

    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., Gebler, B. 1977. Electrical properties of amphibian urinary bladder epithelia. III. The cell membrane resistances and the effect of amiloride.Pfluegers Arch. 371:99–108

    Google Scholar 

  • 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)

  • Klyce, S.D., Wong, R.K.S. 1977. Site and mode of adrenalin action on chloride transport across the rabbit corneal epithelium.J. Physiol. 266:777–799

    Google Scholar 

  • Lewis, S.A., Eaton, D.C., Diamond, J.M. 1976. The mechanism of Na+ transport by rabbit urinary bladder.J. Membrane Biol. 28:41–70

    Google Scholar 

  • Nagel, W., Reinach, P. 1980. Mechanism of stimulation by epinephrine of active transepithelial Cl transport in isolated frog cornea.J. Membrane Biol. 56:73–79

    Google Scholar 

  • 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. 112:811–815

    Google Scholar 

  • 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. 64:1–25

    Google Scholar 

  • 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. 25:115–139

    Google Scholar 

  • Schultz, S.G. 1979. Application of equivalent electrical circuit models to study of sodium transport across epithelial tissues.Fed. Proc. 38:2024–2029

    Google Scholar 

  • Schultz, S.G. 1981. Homocellular regulatory mechanisms in sodium-transporting epithelia: Avoidance of extinction by “flush through”.Am. J. Physiol. 241:F579-F590

    Google Scholar 

  • Schultz, S.G., Frizzell, R.A., Nellans, H.N. 1977. Active sodium transport and the electrophysiology of rabbit colon.J. Membrane Biol. 33:351–384

    Google Scholar 

  • Shorofsky, S., Field, M., Fozzard, H. 1980. Electrophysiologic studies of canine tracheal epithelium.J. Gen. Physiol. 76:27a

    Google Scholar 

  • Smith, P.L., Frizzell, R.A. 1982. Changes in intracellular K activity after stimulation of chloride secretion in canine tracheal epithelium.Chest 81:5s

    Google Scholar 

  • 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. 70:217–226

    Google Scholar 

  • Welsh, M.J. 1982. The effect of barium and potassium on chloride secretion by canine tracheal epithelium.Fed. Proc. 41:1260

    Google Scholar 

  • Welsh, M.J. 1983. Inhibition of chloride secretion by furosemide in canine tracheal epithelium.J. Membrane Biol. 71:219–226

    Google Scholar 

  • Welsh, M.J., Smith, P.L., Frizzell, R.A. 1981. Intracellular chloride activities in the isolated perfused shark rectal gland.Clin. Res. 29:480A

    Google Scholar 

  • 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. 70:227–238

    Google Scholar 

  • Welsh, M.J., Widdicombe, J.H. 1980. Pathways of ion movement in the canine tracheal epithelium.Am. J. Physiol. 239:F215-F221

    Google Scholar 

  • 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-C192

    Google Scholar 

  • Widdicombe, J.H., Basbaum, C.B., Yee, J.Y. 1979a. Localization of Na pumps in the tracheal epithelium of the dog.J. Cell Biol. 82:380–390

    Google Scholar 

  • 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. 120:385–392

    Google Scholar 

  • Widdicombe, J.H., Welsh, M.J. 1980. Ion transport by dog tracheal epithelium.Fed. Proc. 39:3062–3066

    Google Scholar 

  • 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. 5:366–385

    Google Scholar 

  • Zadunaisky, J.A., Spring, K.R., Shindo, T. 1979. Intracellular chloride activity in the corneal epithelium.Fed. Proc. 38:1059

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Welsh, M.J., Smith, P.L. & Frizzell, R.A. Chloride secretion by canine tracheal epithelium: III. Membrane resistances and electromotive forces. J. Membrain Biol. 71, 209–218 (1983). https://doi.org/10.1007/BF01875462

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01875462

Key words

Navigation