Skip to main content
Log in

Voltage sensitive, high-conductance chloride channels in the luminal membrane of cultured pulmonary alveolar (type II) cells

  • Transport Processes, Metabolism and Endocrinology; Kidney, Gastrointestinal Tract, and Exocrine Glands
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

The properties of ion channels in patches from the luminal membrane of cultured monolayers of type II alveolar epithelial cells from adult rat lung have been studied. In excised patches, prepared as described to yield the “outside-out” configuration (with cesium ions in the bathing solutions to suppress currents arising from potassium channels), we observed anion-selective channels with a conductance of 350–400 pS, and burst lengths lasting seconds. When patches were bathed in solutions with equal chloride concentrations, channels opened and closed spontaneously at membrane voltages close to zero, but tended to close when the potential was shifted by ±10 mV, particularly in the negative direction. Other anions could pass through these channels with a permeability sequence of I(1.5)>Br(1.02)=>Cl(1.00)>NO3(0.9)>gluconate(0.6) but there was a very low permeability for sodium (P Na/P Cl=0.015±0.006). Calcium ions reduced channel conductance. The channels probably have a role to play in salt absorption by this epithelium, but insufficient information is available about how sodium crosses it for the role of the anion channels in transport to be defined with confidence.

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

  1. Augustus J, Bijman J, Van Os CH (1978) Epithelial resistance of rabbit submaxillary main duct. A tight epithelium with leaky cell membranes. J Membr Biol 43:203–226

    Google Scholar 

  2. Bijman J (1983) Decreased Cl permeability as the basis for increased bioelectrical potentials in cystic fibrosis. Pediat Res 17:701–702

    Google Scholar 

  3. Blatz AC, Magleby KL (1983) Single voltage-dependent chloride-selective channels of large conductance in cultured rat muscle. Biophysics J 43:237–247

    Google Scholar 

  4. Frömter F, Gebler B, Schopow K, Pockrandt-Hemstedt H (1974) Cation and anion permeability of rabbit submaxillary main duct. In: Thorn NA, Petersen OH (eds) Secretory mechanisms of exocrine glands. Munksgaard, Copenhagen, pp 496–513

    Google Scholar 

  5. Goodman BE, Fleischer RS, Crandall EA (1983) Evidence for active Na+ transport by cultured monolayers of pulmonary alveolar epithelial cells. Am J Physiol 245:C78-C83

    Google Scholar 

  6. Gray PT, Bevan S, Ritchie JM (1984) High-conductance anion-selective channels in rat cultured Schwann cells. Proc R Soc London B 221:395–409

    Google Scholar 

  7. Greger R, Schlatter E (1983) Properties of the basolateral membrane of the cortical thick ascending limb of Henle's loop of rabbit kidney. Pflügers Arch 396:325–334

    Google Scholar 

  8. Hamill OP, Bormann J, Sakmann B (1983) Activation of multiple conductance state chloride channels in spinal neurones by glycine and GABA. Nature (Lond) 305:805–808

    Google Scholar 

  9. Hamill OP, Marty A, Neher E, Sakmann B, Sigsworth FS (1981) Improved patch-clamp techniques for high resolution current recording from cells and cell free membrane patches. Pflügers Arch 391:85–100

    Google Scholar 

  10. Hanrahan JW, Alles WP, Lewis SA (1984) A voltage-gated Cl channel in cultural mammalian urinary bladder epithelium: A patch clamp study. Biophysics J 45:300a

    Google Scholar 

  11. Hviid-Larsen E, Rasmussen BE (1982) Chloride channels in toad skin. Philos Trans R Soc London Ser B 299:413–439

    Google Scholar 

  12. Kimura G, Spring KR (1980) Ionic conductance of cell membranes and shunts ofNecturus proximal tubule. In: Boulpaep EL (ed) Cellular mechanisms of renal tubular ion trasport. Current topics in membranes and transport, vol 13. Academic Press, New York, pp 265–281

    Google Scholar 

  13. Maren TH, Rayburn CS, Liddell NE (1976) Inhibition by anions of human red cell carbonic anhydrase B: physiological and biochemical implications. Science 191:469–472

    Google Scholar 

  14. Miller C (1983) Integral membrane channels: Studies in model membranes. Physiol Rev 63:1209–1242

    Google Scholar 

  15. Nelson DJ, Tang JM, Palmer LG (1984) Single-channel recordings of apical membrane chloride conductance in A6 epithelial cells. J Membr Biol 80:81–89

    Google Scholar 

  16. Palade PT, Barchi RL (1977) Characteristics of the chloride conductance in muscle fibres of the rat diaphragm. J Gen Physiol 69:325–342

    Google Scholar 

  17. Quinton PM (1982) Abnormalities in electrolyte secretion in cystic fibrosis sweat glands due to decreased anion permeability. In: Quinton PM, Martinez JR, Hopfer U (eds) Fluid and electrolyte abnormalities in exocrine glands in cystic fibrosis. San Francisco Press, San Francisco, pp 53–76

    Google Scholar 

  18. Quinton PM (1983) Chloride impermeability in cystic fibrosis. Nature (Lond) 301:421–422

    Google Scholar 

  19. Reuss L (1980) Ionic conductance and electrochemical potential differences across membranes of gallbladder epithelium. In: Boulpaep EL (ed) Cellular mechanisms of renal tubular ion transport. Current topics in membranes and transport, vol 13. Academic Press, New York, pp 215–228

    Google Scholar 

  20. Reuss L (1983) Basolateral KCl co-transport in a NaCl-absorbing epithelium. Nature (Lond) 305:723–726

    Google Scholar 

  21. Simonneau M (1984) Ionic channels in mouse multipotential carcinoma cells. Biophysics J 45:308a

    Google Scholar 

  22. Smith GJ, Le Mesurier SM, De Montfort ML, Lykke AWJ (1984) Development and characterization of type 2 pneumocyte-related cell lines from normal adult mouse lung. Pathol 16:401–405

    Google Scholar 

  23. Sonnhof U, Schachner M (1984) Patch clamp investigations of cultured mammalian astrocytes. Pflügers Arch 400:R29

    Google Scholar 

  24. Ussing HH, Leaf A (1978) Transport across multimembrane systems. In: Giebisch G, Tosteson DC, Ussing HH (eds) Membrane transport in biology, vol III. Springer, Berlin Heidelberg New York, pp 1–28

    Google Scholar 

  25. Wright EM, Diamond JM (1977) Anion selectivity in biological systems. Physiol Rev 57:109–156

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schneider, G.T., Cook, D.I., Gage, P.W. et al. Voltage sensitive, high-conductance chloride channels in the luminal membrane of cultured pulmonary alveolar (type II) cells. Pflugers Arch. 404, 354–357 (1985). https://doi.org/10.1007/BF00585348

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00585348

Key words

Navigation