Abstract
The presence of Ca2+- and voltage-activated K+ channels was directly demonstrated in the apical cell membrane of gallbladder epithelium by patch-clamp single-channel current recording. In K+-depolarized epithelial cells, negative pipette potentials induced outward current steps when the patch-pipette was filled with Na+-rich solution and these current steps were not affected by the presence or absence of Cl−. When K+-rich solution was in the pipette and K+-depolarized cells were examined, the current-voltage relations were linear with a single-channel conductance of 140 pS and polarity was reversed at 0 mV. In excised inside-out membrane patches, raising the free Ca2+ concentration of the medium facing the inner side of the membrane from 10−7 to 10−6 M evoked a marked increase in open state probability of the channels without affecting the elementary current steps. This suggests that intracellular Ca2+ as a second messenger plays a crucial role in the regulatory mechanism of the membrane potential by modulating the high-conductance apical K+ channels.
Similar content being viewed by others
References
Adams PR, Constanti A, Brown PA, Clark RB (1982) Intracellular Ca2+ activates a fast voltage-sensitive K+ current in vertebrate sympathetic neurons. Nature 296:746–749
Barrett JN, Magleby KL, Pallotta BS (1982) Properties of single calcium-activated potassium channels in cultured rat muscle. J Physiol (Lond) 331:211–230
Findlay I (1984) A patch-clamp study of potassium channels and whole-cell currents in acinar cells of the mouse lacrimal gland. J Physiol (Lond) 350:179–195
Findlay I, Dunne MJ, Petersen OH (1985) High-conductance K+ channel in pancreatic islet cells can be activated and inactivated by internal calcium. J Membr Biol 83:169–175
Frömter E (1972) The route of passive ion movement through the epithelium ofNecturus gallbladder. J Membr Biol 8:259–301
García-Diaz JF, Nagel W, Essig A (1983) Voltage-dependent K conductance at the apical membrane ofNecturus gallbladder. Biophys J 43:269–278
Gögelein H, Van Driessche W (1981a) Noise analysis of the K+ current through the apical membrane ofNecturus gallbladder. J Membr Biol 60:187–198
Gögelein H, Van Driessche W (1981b) The effect of electrical gradients on current fluctuations and impedance recorded fromNecturus gallbladder. J Membr Biol 60:199–209
Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85–100
Henin S, Cremaschi D (1975) Transcellular ion route in rabbit gallbladder. Electrical properties of the epithelial cells. Pflügers Arch 355:125–139
Hunter M, Lopes AG, Boulpaep EL, Giebisch GH (1984) Single channel recordings of calcium-activated potassium channels in the apical membrane of rabbit cortical collecting tubules. Proc Natl Acad Sci USA 81:4237–4239
Marty A (1981) Ca2+-dependent K+ channels with large unitary conductance in chromaffin cell membranes. Nature 291:497–500
Maruyama Y, Petersen OH (1982a) Single-channel currents in isolated patches of plasma membrane from basal surface of pancreatic acini. Nature 299:159–161
Maruyama Y, Petersen OH (1982b) Cholecystokinin activation of single-channel currents is mediated by internal messenger in pancreatic acinar cells. Nature 300:61–63
Maruyama Y, Petersen OH (1984) Control of K+ conductance by cholecystokinin and Ca2+ in single pancreatic acinar cells studied by the patch-clamp technique. J Membr Biol 79:293–300
Maruyama Y, Gallacher DV, Petersen OH (1983a) Voltage and Ca2+-activated K+ channels in basolateral acinar cell membranes of mammalian salivary glands. Nature 302:827–829
Maruyama Y, Petersen OH, Flanagan P, Pearson GT (1983b) Quantification of Ca2+-activated K+ channels under hormonal control in pig pancreatic acinar cells. Nature 305:228–232
Maruyama Y, Nishiyama A, Izumi T, Hoshimiya N, Petersen OH (1986) Ensemble noise and current relaxation analysis of K+ current in single isolated salivary acinar cells from rat. Pflügers Arch 406:69–72
Neher E, Sakmann B, Steinbach JH (1978) The extracellular patchclamp: a method for resolving currents through individual open channels in biological membranes Pflügers Arch 375: 219–228
Petersen OH, Maruyama Y (1984) Calcium-activated potassium channels and their role in secretion. Nature 307: 693–696
Reuss L, Finn AL (1975) Electrical properties of the cellular transepithelial pathway inNecturus gallbladder. II. Ionic permeability of the apical cell membrane. J Membr Biol 25: 141–161
Sakmann B, Neher E (1983) Geometric parameters of pipettes and membrane patches. In: Sakmann B, Neher E (eds) Single-channel recording. Plenum Press, New York, pp 37–51
Spring KR, Hope A (1979) Dimensions of cell and lateral intracellular spaces in livingNecturus gallbladder. Fed Proc 38: 128–133
Stühmer W, Roberts WM, Almers W (1983) The loose patch clamp. In: Sakmann B, Neher E (eds) Single-channel recording. Plenum Press, New York, pp 123–132
Trautmann A, Marty A (1984) Activation of Ca-dependent K channels by carbamoylcholine in rat lacrimal glands. Proc Natl Sci USA 81: 611–615
Van Driessche W, Gögelein H (1978) Potassium channels in the apical membrane of the toad gallbladder. Nature 275: 665–667
Wong BS, Lecar H, Adler N (1982) Single calcium-dependent potassium channels in clonal anterior pituitary cells. Biophys J 39: 313–317
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Maruyama, Y., Matsunaga, H. & Hoshi, T. Ca2+-and voltage activated K+ channel in apical cell membrane of gallbladder epithelium fromTriturus . Pflugers Arch. 406, 563–567 (1986). https://doi.org/10.1007/BF00584021
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00584021