Skip to main content
Log in

Single chloride channels in colon mucosa and isolated colonic enterocytes of the rat

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

Summary

Chloride channels from rat colonic enterocytes were studied using the patch-clamp technique. After removal of mucus, inside-out patches were excised from the apical membrane of intact epithelium located at the luminal surface. They contained spontaneously switching Cl channels with a conductance of 35–40 pS. The channels were blocked reversibly by anthracene-9-carboxylic acid (1mm).

In excised patches from single enterocytes, isolated by calcium removal, the Cl channels were studied in more detail. TheI–V relation was linear between ±80 mV. The selectivity was I>Br>Cl=NO 3 >F=HCO 3 .

Thirty pS Cl channels were also found on the basolateral membrane of crypts isolated by brief calcium removal. TheI–V curve of these Cl channels was also linear.

The results provide direct evidence for the existence of Cl channels in the apical membrane of surface cells in colonic mucosa. The properties of these channels are similar to those previously observed when incorporating membrane vesicles into planar lipid bilayers. Both results support the validity of the theoretical models describing intestinal secretion.

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

  • Andres, H., Bock, R., Bridges, R.J., Rummel, W., Schreiner, J. 1985. Submucosal plexus and electrolyte transport across rat colonic mucosa.J. Physiol. (London) 364:301–312

    Google Scholar 

  • Binder, H.J., Sandle, G.I. 1987. Electrolyte absorption and secretion in the mammalian colon.In: Physiology of the Gastro-intestinal Tract. L.R. Johnson, editor. pp. 1389–1418. Raven, New York

    Google Scholar 

  • Bjerknes, M., Cheng, H. 1981. Methods for the isolation of intact epithelium from the mouse intestine.Anat. Rec. 199:565–574

    PubMed  Google Scholar 

  • Bjorkman, D.J., Allan, C.H., Hagen, S.J., Trier, J. 1986. Structural features of absorptive cell and microvillus preparations from rat small intestine.Gastroenterology 91:1401–1414

    PubMed  Google Scholar 

  • Blatz, A.L., Magleby, K.L. 1983. Single voltage-dependent chloride-selective channels of large conductance in cultured rat muscle.Biophys. J. 43:237–241

    Google Scholar 

  • Brasitus, T.A., Dudeja, P.K., Worman, H.J., Foster, E.S. 1986. The lipid fluidity of rat colonic brush-border membrane vesicles modulates Na+−H+ exchange and osmotic water permeability.Biochim. Biophys. Acta 855:16–24

    PubMed  Google Scholar 

  • Brasitus, T.A., Keresztes, R.S. 1984. Protein-lipid interactions in antipodal plasma membranes of rat colonocytes.Biochim. Biophys. Acta 773:290–300

    PubMed  Google Scholar 

  • Bridges, R.J., Rack, M., Rummel, W., Schreiner, J. 1986. Mucosal plexus and electrolyte transport across the rat colonic mucosa.J. Physiol. (London) 376:531–542

    Google Scholar 

  • Fernandez, Y.J., Boigegrain, R.M., Cambon-Gros, C.D., Mitjavala, S.E. 1984. Sensitivity of Na+-coupledd-glucose uptake, Mg2+-ATPase and sucrase to perturbations of the fluidity of brush-border membrane vesicles induced byn-aliphatic alcohols.Biochim. Biophys. Acta 770:171–177

    PubMed  Google Scholar 

  • Frizzell, R.A., Heintze, K. 1979. Electrogenic chloride secretion by mammalian colon.In: Mechanisms of Intestinal Secretion. H.J. Binder, editor. pp. 101–110. Alan R. Liss, New York

    Google Scholar 

  • Frizzell, R.A., Rechkemmer, G., Shoemaker, R.L. 1986. Altered regulation of airway epithelial cell chloride channels in cystic fibrosis.Science 233:558–560

    PubMed  Google Scholar 

  • Giraldez, F., Sepulveda, F.V., Sheppard, D.N. 1988. A chloride conductance activated by adenosine 3′, 5′-cyclic monophosphate in the apical membrane ofNecturus enterocytes.J. Physiol. (London) 395:597–623

    Google Scholar 

  • Greger, R., Schlatter, E., Gögelein, H. 1985. Cl-channels in the apical membrane of the rectal gland “induced” by cAMP.Pfluegers Arch. 403:446–448

    Google Scholar 

  • Greger, R., Schlatter, E., Gögelein, H. 1987. Chloride channels in the luminal membrane of the rectal gland of the dogfish (Squalus acanthias).Pfluegers Arch. 409:114–121

    Google Scholar 

  • Halm, D.R., Rechkemmer, G.R., Schoumacher, R.A., Frizzell, R.A. 1988. Apical membrane chloride channels in a colonic cell line activated by secretory agonists.Am. J. Physiol. 254:C505-C511

    PubMed  Google Scholar 

  • Hamill, O.P., Marty, A., Neher, E., Sakmann, B., Sigworth, F.J. 1981. Improved patch-clamp technique for high-resolution current recordings from cells and cell-free membrane patches.Pfluegers Arch. 391:85–100

    Article  Google Scholar 

  • Hayslett, J.P., Gögelein, H., Kunzelmann, K., Greger, R. 1987. Characteristics of apical chloride channels in human colon cells (HT 29).Pfluegers Arch. 410:487–494

    Google Scholar 

  • Horvath, P.J., Ferriola, P.C., Weiser, M.M., Duffey, M.E. 1986. Localization of chloride secretion in rabbit colon: Inhibition by anthracene-9-carboxylic acid.Am. J. Physiol. 250:G185-G190

    PubMed  Google Scholar 

  • Lipkin, M. 1981. Proliferation and differentiation of gastrointestinal cells in normal and disease states.In: Physiology of the Gastrointestinal Tract. L.R. Johnson, editor. pp. 145–168. Raven, New York

    Google Scholar 

  • Lübcke, R., Haag, K., Berger, E., Knauf, H., Gerok, W. 1986. Ion transport in rat proximal colon in vivo.Am. J. Physiol. 251:G132-G139

    PubMed  Google Scholar 

  • Nelson, D.J., Tang, J.M., Palmer, L.G. 1984. Single-channel recordings of apical membrane chloride conductance in A6 epithelial cells.J. Membrane Biol. 80:81–89

    Google Scholar 

  • Perris, A.D. 1965. Isolation of the epithelial cells of the rat small intestine.Can. J. Biochem. 44:687–693

    Google Scholar 

  • Reinhardt, R., Bridges, R.J., Rummel, W., Lindemann, B. 1987. Properties of an anion-selective channel from rat colonic enterocyte plasma membranes reconstituted into planar phospholipid bilayers.J. Membrane Biol. 95:47–54

    Google Scholar 

  • Shoemaker, R.L., Frizzell, R.A., Dwyer, T.M., Farley J.M. 1986. Single chloride channel currents from canine tracheal epithelial cells.Biochim. Biophys. Acta 858:235–242

    PubMed  Google Scholar 

  • Welsh, M.J. 1986. An apical-membrane chloride channel in human tracheal epithelium.Science 232:1648–1650

    PubMed  Google Scholar 

  • Welsh, M.J., Liedtke, C.M. 1986. Chloride and potassium channels in cystic fibrosis airway epithelia.Nature (London) 322:467–470

    Google Scholar 

  • Welsh, M.J., Smith, P.L., Fromm, M., Frizzell, R.A. 1982. Crypts are the site of intestinal fluid and electrolyte secretion.Science 218:1219–1221

    PubMed  Google Scholar 

  • Ziomek, C.A., Schulman, S., Edidin, M. 1980. Redistribution of membrane protein in isolated mouse intestinal epithelial cells.J. Cell Biol. 86:849–857

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Diener, M., Rummel, W., Mestres, P. et al. Single chloride channels in colon mucosa and isolated colonic enterocytes of the rat. J. Membrain Biol. 108, 21–30 (1989). https://doi.org/10.1007/BF01870422

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01870422

Key Words

Navigation