Skip to main content
Log in

Quinidine-sensitive K+ channels in the basolateral membrane of embryonic coprodeum epithelium: regulation by aldosterone and thyroxine

  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Basolateral K+ channels and their regulation during aldosterone- and thyroxine-stimulated Na+ transport were studied in the lower intestinal epithelium (coprodeum) of embryonic chicken in vitro. Isolated tissues of the coprodeum were mounted in Ussing chambers and investigated under voltage-clamped conditions. Simultaneous stimulation with aldosterone (1 μmol·l-1) and thyroxine (1 μmol·l-1) raised short-circuit current after a 1- to 2-h latent period. Maximal values were reached after 6–7 h of hormonal treatment, at which time transepithelial Na+ absorption was more than tripled (77±11 μA·cm-2) compared to control (24±8 μA·cm-2). K+ currents across the basolateral membrane with the pore-forming antibiotic amphotericin B and application of a mucosal-to-serosal K+ gradient. This K+ current could be dose dependently depressed by the K+ channel blocker quinidine. Fluctuation analysis of the short-circuit current revealed a spontaneous and a blocker-induced Lorentzian noise component in the power density spectra. The Lorentzian corner frequencies increased linearly with the applied blocker concentration. This enabled the calculation of single K+ channel current and K+ channel density. Single K+ channel current was not affected by stimulation, whereas the number of quinidine-sensitive K+ channels in the basolateral membrane increased from 11 to 26·106·cm-2 in parallel to the hormonal stimulation transepithelial Na+ transport. This suggests that the basolateral membrane is a physiological target during synergistic aldosterone and thyroxine regulation of transepithelial Na+ transport for maintaining intracellular K+ homeostasis.

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

Abbreviations

f :

frequency

f c :

Lorentzian corner frequency

g K :

single K+ channel conductance

HEPES:

N-2-hydroxyethylpiperazin-N'-2-ethansulfonic acid

i K :

single K+ channel current

IAmpho :

amphotericin B induced K+ current

I sc :

short-circuit current

I K :

quinidine blockable K+ current

I max :

maximally blocked current by quinidine

IC 50 :

half-maximal blocker concentration

k on, k off :

on- and off-rate coefficients of reversible single channel block by quinidine

M K :

number of conducting K+ channels

[Q]:

quinidine concentration

R t :

transepithelial resistance

S :

spectral density

S o :

Lorentzian plateau

TBM cells:

toad urinary bladder cell line

References

  • Abramcheck F, Gupta S, Sabatini S, Helman S (1982) Mechanism of action of quinine on Na transport in frog skin. Fed Proc 41:1349

    Google Scholar 

  • Arruda JAL (1983) Characterization of the effect of quinidine on Na transport by the toad and turtle bladders. J Pharmacol Exp Ther 224:297–301

    Google Scholar 

  • Barlet-Bas C, Khadouri C, Marsy S, Doucet A (1988) Sodium-independent in vitro induction of Na+, K+-ATPase by aldosterone in renal target cells: permissive effect of triiodothyronine. Proc Natl Acad Sci USA 85:1707–1711

    Google Scholar 

  • Butt AG, Clapp WL, Frizzell R (1990) Potassium conductance in tracheal epithelium activated by secretion and cell swelling. Am J Physiol 258:C630-C638

    Google Scholar 

  • Clauss W, Dürr JE, Guth D, Skadhauge E (1987) Effects of adrenal steroids on Na transport in the lower intestine (coprodeum) of the hen. J Membr Biol 96:141–152

    Google Scholar 

  • Clauss W, Hoffmann B, Krattenmacher R, Van Driessche W (1993) Current-noise analysis of Na-absorption by the embryonic coprodeum: stimulation by aldosterone and thyroxine. Am J Physiol (in press)

  • Dawson DC, Van Driessche W, Helman SI (1988) Osmotically induced basolateral K+ conductance in turtle colon: lidocaine-induced K+ channel noise. Am J Physiol 254:C165-C174

    Google Scholar 

  • De Wolf I, Van Driessche W (1986) Voltage-dependent Ba2+ block of K+ channels in apical membrane of frog skin. Am J Physiol 251:C696-C706

    Google Scholar 

  • Edmonds CJ, Willis CL (1990) Aldosterone and thyroid hormone interaction on the sodium and potassium transport pathways of rat colonic epithelium. J Endocrinol 124:47–52

    Google Scholar 

  • Fischer H, Clauss W (1990) Regulation of sodium channels in frog lung epithelium: a novel target tissue for aldosterone action. Pflügers Arch 416:62–67

    Google Scholar 

  • Geering K, Girardet M, Bron C, Kraehenbühl JP, Rossier BC (1982) Hormonal regulation of (Na+ K+)-ATPase biosynthesis in the toad bladder. Effect of aldosterone and 3,5,3' triiodo-l-thyronine. J Biol Chem 257:10338–10343

    Google Scholar 

  • Germann WJ, Ernst SA, Dawson DC (1986) Resting and osmotically induced basolateral K conductances in turtle colon. J Gen Physiol 88:253–274

    Google Scholar 

  • Glavinovic MI, Trifaro JM (1988) Quinidine blockade of currents through Ca-activated K channels in bovine chromaffin cells. J Physiol (Lond) 399:139–152

    Google Scholar 

  • Guggino SE, Guggino WB, Green N, Sacktor B (1987) Blocking agents of Ca2+-activated K+ channels in cultured medullary thick ascending limb cells. Am J Physiol 252:C128–137

    Google Scholar 

  • Heinz M, Krattenmacher R, Hoffmann B, Clauss W (1991) Different modes of electrogenic Na+-absorption in the coprodeum of the chicken embryo: role of extracellular Ca2+. J Comp Physiol B 161:363–370

    Google Scholar 

  • Hirakawa T, Kakunaga T (1982) Sodium transport inhibition by amiloride reduces basolateral membrane potassium conductance in tight epithelia. Science 216:525–529

    Google Scholar 

  • Hoffmann B, Krattenmacher R, Heinz M, Habura B, Clauss W (1990). Synergistic stimulation of aldosterone and thyroxine on large intestinal sodium absorption in chicken embryos (abstract). Pflügers Arch 415:R32

  • Horisberger JD (1992) Early effects of aldosterone on apical and basolateral membrane conductances of TBM cells. Am J Physiol 263:C364-C388

    Google Scholar 

  • Illek B, Fischer H, Clauss W (1990) Aldosterone regulation of basolateral potassium channels in alveolar epithelium. Am J Physiol 259:L230-L237

    Google Scholar 

  • Illek B, Fischer H, Kreusel KM, Hegel U, Clauss W (1992) Volume-sensitive basolateral K+ channels in HT-29/B6 cells: block by lidocaine, quinidine, NPPB and Ba2+. Am J Physiol 263:C674-C683

    Google Scholar 

  • Iwatsuki N, Peterson OH (1985) Inhibition of Ca-activated K channels in pig pancreatic acinar cells by Ba, Ca, quinine and quinidine. Biochim Biophys Acta 819:249–257

    Google Scholar 

  • Koefoed-Johnson V, Ussing H (1958) The nature of frog skin potential. Acta Physiol Scand 42:298–308

    Google Scholar 

  • Lang F, Messner F, Rehwald W (1986) Electrophysiology of sodium-couple transport in proximal renal tubules. Am J Physiol 250:F953-F962

    Google Scholar 

  • Lewis SA, Eaton DC, Claussen C, Diamond JM (1977) Nystatin as a probe for investigating the electrical properties of a tight epithelium. J Gen Physiol 70:427–440

    Google Scholar 

  • Lindemann B, Van Driessche W (1977) Sodium-specific membrane channels of frog skin are pores: current fluctuations reveal high turnover. Science 195:292–294

    Google Scholar 

  • Nagel W, Crabbé J (1980) Mechanism of action of aldosterone on active sodium transport across toad skin. Pflügers Arch 385:181–187

    Google Scholar 

  • Palmer LG, Li JHY, Lindemann B, Edelman IS (1982) Aldosterone control of the density of sodium channels in toad urinary bladder. J Membr Biol 64:91–102

    Google Scholar 

  • Richards NW, Dawson DC (1986) Single potassium channels blocked by lidocaine and quinidine in isolated turtle colon epithelial cells. Am J Physiol 251:C85-C89

    Google Scholar 

  • Rick R, Spancken G, Dörge A (1988) Differential effects of aldosterone and ADH on intracellular electrolytes in the toad urinary bladder epithelium. J Membr Biol 101:275–282

    Google Scholar 

  • Schultz SG (1984) A cellular model for active sodium absorption by mammalian colon. Annu Rev Physiol 46:435–451

    Google Scholar 

  • Skadhauge E (1984) Introduction of an epithelium with huge variation in sodium transport and novel aldosterone effects. In: Skadhauge E, Heinze K (eds) Intestinal absorption and secretion. MTB Press, Lancaster, pp 201–208

    Google Scholar 

  • Van Driessche W, Erlij D (1983) Noise analysis of inward and outward Na+ currents across the apical border of ouabain-treated frog skin. Pflügers Arch 398:179–188

    Google Scholar 

  • Van Driessche W, Hillyard SD (1985) Quinidine blockage of K+ channels in the basolateral membrane of larval bullfrog skin. Pflügers Arch 405:S77-S82

    Google Scholar 

  • Van Driessche W, Lindemann B (1978) Low-noise amplification of voltage and current fluctuations arising in epithelia. Rev Sci Instrum 49:52–57

    Google Scholar 

  • Wills NK, Lewis SA, Eaton DC (1979) Active and passive properties of rat descending colon: a microelectrode and nystatin study. J Membr Biol 45:81–108

    Google Scholar 

  • Wong BS (1989) Quinidine blockade of calcium-activated potassium channels in dissociated gastric smooth muscle cells. Pflügers Arch 414:416–422

    Google Scholar 

  • Yeh JZ, Narahashi T (1976) Mechanism of action of quinidine on squid axon membranes. J Pharmacol Exp Ther 196:62–70

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Present address: University of California at Berkeley, Dept. of Molecular and Cell Biology Berkeley, CA 94720, USA

Rights and permissions

Reprints and permissions

About this article

Cite this article

Illek, B., Fischer, H. & Clauss, W. Quinidine-sensitive K+ channels in the basolateral membrane of embryonic coprodeum epithelium: regulation by aldosterone and thyroxine. J Comp Physiol B 163, 556–562 (1993). https://doi.org/10.1007/BF00302114

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00302114

Key words

Navigation