Summary
A Ca and potential-dependent K channel of large unit conductance was detected in the apical membrane of JTC-12.P3 cells, a continuous epithelial cell line of renal origin. The open probability of the channel is dependent on membrane potential and cytoplasmic-free Ca concentration. At cell-free configuration of the membrane patch, the open probability shows a bell-shaped behavior as function of membrane potential, which decreases at larger depolarization. With increasing Ca concentration, the width of the bell-shaped curve increases and the maximum shifts into the hyperpolarizing direction. For the first time the kinetics of this channel was analyzed under cell-attached conditions. In this case the kinetics could sufficiently be described by a simple open-closed behavior. The channel has an extremely small open probability at resting potential, which increases exponentially with depolarization. The low probability induces an uncertainty about the actual number of channels in the membrane patch. The number of channels is estimated by kinetic analysis. It is discussed that this K channel is essential for the repolarization of the membrane potential during electrogenic sodium-solute cotransport across the apical membrane.
Similar content being viewed by others
References
Barrett, J.N., Magleby, K.L., Pallotta, B.S. 1982. Properties of single calcium-activated potassium channels in cultured rat muscle.J. Physiol. (London) 331:211–230
Bello-Reuss, E. 1982. Electochemical properties of the basolateral membrane of the straight portion of the rabbit proximal renal tubule.J. Physiol. (London) 326:49–63
Biagi, B.A., Kubota, T., Sohtell, M., Giebisch, G.H. 1981. Intracellular potentials in rabbit proximal tubules perfused in vitro.Am. J. Physiol. 240:F200-F210
Burckhardt, G., Murer, H. 1980. A cyanine dye as indicator of membrane potential differences in brush border membrane vesicles. Studies with K+ gradients and Na+/amino acid transport.Adv. Physiol. Sci. 11:409–418
Colquhoun, D., Hawkes, A.G. 1983. The principles of the stochastic interpretation of ion-channel mechanisms.In: Single Channel Recording. B. Sakmann and E. Neher, editors. pp. 135–174. Plenum. New York
Colquhoun, D., Sigworth, F.J. 1983. Fitting and statistical analysis of single channels records.In: Single Channel Recording. B. Sakmann and E. Neher, editors, pp. 191–263. Plenum, New York
Frömter, E. 1979. Solute transport across epithelia: What can we learn from micropuncture studies on kidney tubules?J. Physiol. (London) 288:1–31
Gögelein, H., Greger, R. 1984. Single channel recordings from basolateral and apical membranes of renal proximal tubules.Pfluegers Arch. 401:424–426
Hamill, O.P., Marty, A., Neher, E., Sakman, B., Sigworth, F.J. 1981. Improved patch clamp techniques for high-resolution current recording from cells and cell-free membrane patches.Pfluegers Arch. 391:85–100
Handler, J.S., Perkins, F.M., Johnson, J.P. 1980. Studies of renal cell function using cell culture techniques.Am. J. Physiol. 238:F1-F9
Hunter, M., Lopes, A.G., Boulpaep, E.L., Giebisch, G.H. 1984. Single channel recordings of calcium activated potassium channels in the apical membrane of rabbit cortical collecting duct.Proc. Natl. Acad. Sci. USA 81:4237–4239
Ishizuka, I., Tadano, K., Nagata, N., Niimura, Y., Nagai, Y. 1978. Hormone specific responses and biosynthesis of sulfolipids in cell lines derived from mammalian kidney.Biochim. Biophys. Acta 541:467–482
Katsuta, H., Takaoka, T. 1970. Improved synthetic media suitable for tissue culture of variant mammalian cells.Methods Cell Biol. 14:145–158
Koeppen, B.M., Biagi, B.A., Giebisch, G.H. 1983. Intracellular microelectrode characterization of the rabbit cortical collecting duct.Am. J. Physiol. 244:F35-F47
Kolb, H.A. 1986. Ca-activated maxi-K-channel in chicken myotubes: Slow burst kinetics of multi-channel systems, rectification and serial correlation.Eur. Biophys. J. (submitted)
Kolb, H.A., Brown, C.D.A., Murer, H. 1985. A voltage-sensitive K+ channel in the apical membrane of a cultured renal epithelium (JTC-12).Experientia 41:830
Latorre, R., Miller, C. 1983. Conduction and selectivity in potassium channels.J. Membrane Biol. 71:11–30
Magleby, K.L., Pallotta, B.S., 1983a. Calcium dependence of open and shut interval distributions from calcium-activated potassium channels in cultured rat muscle.J. Physiol. (London) 344:585–604
Magleby, K.L., Pallotta, B.S. 1983b. Burst kinetics of single calcium-activated potassium channels in cultured rat muscle.J. Physiol. (London) 344:605–623
Moczydlowski, E., Latorre, R. 1983. Gating kinetics of Ca2+ activated K+ channels from rat muscle incorporated into planar lipid bilayers.J. Gen. Physiol. 82:511–542
Murer, H., Kinne, R. 1980. The use of isolated membrane vesicles to study epithelial transport processes.J. Membrane Biol. 55:81–95
O'Neil, R.G., Sansom, S.C. 1984. Characterization of apical cell membrane Na+ and K+ conductance of cortical collecting duct using microelectrode techniques.Am. J. Physiol. 247:F14-F24
Petersen, O.H., Maruyama, Y. 1984. Calcium activated potassium channels and their role in secretion.Nature (London) 307:693–696
Portzehl, H., Caldwell, P.C., Rüegg, J.C. 1984. The dependence of contraction and relaxation of muscle fibres from the crabMaia squinado on the internal concentration of free calcium ions.Biochim. Biophys. Acta 79:581–591
Schwarze, W., Kolb, H.A. 1984. Voltage-dependent kinetics of an anionic channel of large unit conductance in macrophages and myotube membranes.Pfluegers Arch. 402:281–291
Takaoka, T., Katsuta, H., Endo, N., Sato, K., Okumura, H. 1962. Establishment of a cell strain, JTC-12, from cynomolgus monkey kidney tissue.Jpn. J. Exp. Med. 32:351–368
Ullrich, K.J. 1979. Sugar, amino acid and Na+ cotransport in the proximal tubule.Annu. Rev. Physiol. 41:181–195
Yellen, G. 1984. Ionic permeation and blockage in Ca2+-activated K+ channels of bovine chromaffin cells.J. Gen. Physiol. 84:157–186
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kolb, H.A., Brown, C.D.A. & Murer, H. Characterization of a Ca-dependent maxi K channel in the apical membrane of a cultured renal epithelium (JTC-12.P3). J. Membrain Biol. 92, 207–215 (1986). https://doi.org/10.1007/BF01869389
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01869389