Skip to main content
Log in

Characterization of a Ca-dependent maxi K channel in the apical membrane of a cultured renal epithelium (JTC-12.P3)

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

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.

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

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Frömter, E. 1979. Solute transport across epithelia: What can we learn from micropuncture studies on kidney tubules?J. Physiol. (London) 288:1–31

    Google Scholar 

  • Gögelein, H., Greger, R. 1984. Single channel recordings from basolateral and apical membranes of renal proximal tubules.Pfluegers Arch. 401:424–426

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Katsuta, H., Takaoka, T. 1970. Improved synthetic media suitable for tissue culture of variant mammalian cells.Methods Cell Biol. 14:145–158

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Latorre, R., Miller, C. 1983. Conduction and selectivity in potassium channels.J. Membrane Biol. 71:11–30

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Murer, H., Kinne, R. 1980. The use of isolated membrane vesicles to study epithelial transport processes.J. Membrane Biol. 55:81–95

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Petersen, O.H., Maruyama, Y. 1984. Calcium activated potassium channels and their role in secretion.Nature (London) 307:693–696

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Ullrich, K.J. 1979. Sugar, amino acid and Na+ cotransport in the proximal tubule.Annu. Rev. Physiol. 41:181–195

    PubMed  Google Scholar 

  • Yellen, G. 1984. Ionic permeation and blockage in Ca2+-activated K+ channels of bovine chromaffin cells.J. Gen. Physiol. 84:157–186

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01869389

Key Words

Navigation