Noise analysis reveals K+ channel conductance fluctuations in the apical membrane of rabbit colon

Abstract

In this paper we describe current fluctuations in the mammalian epithelium, rabbit descending colon. Pieces of isolated colon epithelium bathed in Na+ or K+ Ringer's solutions were studied under short-circuit conditions with the current noise spectra recorded over the range of 1-200 Hz. When the epithelium was bathed on both sides with Na+ Ringer's solution (the mucosal solution contained 50 microM amiloride), no Lorentzian components were found in the power spectrum. After imposition of a potassium gradient across the epithelium by replacement of the mucosal solution by K+ Ringer's (containing 50 microM amiloride), a Lorentzian component appeared with an average corner frequency, fc = 15.6 +/- 0.91 Hz and a mean plateau value So = (7.04 +/- 2.94) x 10(-20) A2 sec/cm2. The Lorentzian component was enhanced by voltage clamping the colon in a direction favorable for K+ entry across the apical membrane. Elimination of the K+ gradient by bathing the colon on both sides with K+ Ringer's solutions abolished the noise signal. The Lorentzian component was also depressed by mucosal addition of Cs+ or tetraethylammonium (TEA) and by serosal addition of Ba2+. The one-sided action of these K+ channel blockers suggests a cellular location for the fluctuating channels. Addition of nystatin to the mucosal solution abolished the Lorentzian component. Serosal nystatin did not affect the Lorentzian noise. This finding indicates an apical membrane location for the fluctuating channels. The data were similar in some respects to K+ channel fluctuations recorded from the apical membranes of amphibian epithelia such as the frog skin and toad gallbladder. The results are relevant to recent reports concerning transcellular potassium secretion in the colon and indicate that the colon possesses spontaneously fluctuating potassium channels in its apical membranes in parallel to the Na+ transport pathway.