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Reconstitution of a calcium-activated potassium channel in basolateral membranes of rabbit colonocytes into planar lipid bilayers

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Summary

A highly enriched preparation of basolateral membrane vesicles was isolated from rabbit distal colon surface epithelial cells employing the method described by Wiener, Turnheim and van Os (Weiner, H., Turnheim, K., van Os, C.H. (1989)J. Membrane Biol.110:147–162) and incorporated into planar lipid bilayers. With very few exceptions, the channel activity observed was that of a high conductance, Ca2+-activated K+ channel. This channel is highly selective for K+ over Na+ and Cl−, displays voltage-gating similar to “maxi” K(Ca) channels found in other cell membranes, and kinetic analyses are consistent with the notion that K+ diffusion through the channel involves either the binding of a single K+ ion to a site within the channel or “single-filling” (“multi-ion occupancy”). Channel activity is inhibited by the venom from the scorpionLeiurus quinquestriatus, Ba2+, quinine, and trifluoperazine. The possible role of this channel in the function of these cells is discussed.

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References

  • Alvarez, O. 1986. How to set up a bilayer system.In: Ion Channl Reconstitution. C. Miller, editor. pp. 115–130. Plenum, New York

    Google Scholar 

  • Anderson, C.S., MacKinnon, R., Smith, C., Miller, C. 1988. Charybdotoxin block of single Ca2+-activated K+ channels. Effects of channel gating, voltage, and ionic strength.J. Gen. Physiol. 91:317–333

    Google Scholar 

  • Bear, C.E., Petersen, O.H. 1987.l-alanine evokes opening of single Ca2+-activated K+ channels in rat liver cells.Pflueger's Arch. 410:342–344

    Google Scholar 

  • Brown, P.D., Loo, D.D.F., Wright, E.M. 1988. Ca2+-activated K+ channels in the apical membrane ofNecturus choroid plexus.J. Membrane Biol. 105:207–219

    Google Scholar 

  • Chang, D., Dawson, D.C. 1988. Digitonin-permeabilized colonic cell layers. Demonstration of calcium-activated basolateral K+ and Cl− conductances.J. Gen. Physiol. 92:281–306

    Google Scholar 

  • Christensen, O. 1987. Mediation of cell volume regulation by Ca influx through stretch activated channels.Nature (London) 330:66–68

    Google Scholar 

  • Christensen, O., Zeuthen, T. 1987. Maxi K+ channels in leaky epithelia are regulated by intracellular Ca2+, pH and membrane potential.Pfluegers Arch. 408:249–259

    Google Scholar 

  • Cohen, F., 1986. Fusion of liposomes to planar bilayers.In: Ion Channel Reconstitution. C. Miller, editor. pp. 131–139. Plenum, New York

    Google Scholar 

  • Costantin, J., Alcalen, S., Otero, A., Dubinsky, W.P., Schultz, S.G. 1989. Reconstitution of an inwardly rectifying potassium channel from the basolateral membranes ofNecturus enterocytes into planar lipid bilayers.Proc. Natl. Acad. Sci. USA 86:5212–5216

    Google Scholar 

  • Dawson, D.C. 1987. Properties of epithelial potassium channels.Curr. Topics Membr. Transp. 28:41–71

    Google Scholar 

  • Dawson, D.C., van Driessche, W., Helman, S.I. 1988. Osmotically induced basolateral K conductance in turtle colon: Lidocaine induced K channel noise.Am. J. Physiol. 254:C165-C174

    Google Scholar 

  • Dedman, J.R. 1986. Mediation of intracellular calcium: Variances on a common theme.Cell Calcium 7:297–307

    Google Scholar 

  • Eisenman, G., Latorre, R., Miller, C. 1986. Multi-ion conduction and selectivity in the high-conductance Ca-activated K+ channel from skeletal muscle.Biophys. J. 50:1025–1034

    Google Scholar 

  • Fabiato, A., Fabiato, F. 1979. Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells.J. Physiol. (Paris) 75:463–505

    Google Scholar 

  • Findlay, I., Dunne, M.J., Petersen, O.H. 1985a. High-conductance K channel in pancreatic acinar cells can be activated and inactivated by internal calcium.J. Membrane Biol. 83:169–175

    Google Scholar 

  • Findlay, I., Dunne, M.J., Ullrich, S., Wollheim, C.B., Petersen, O.H. 1985b. Quinine inhibits Ca2+-independent K+ channels whereas tetraethylammonium inhibits Ca2+-activated K+ channels in insulin secreting cells.FEBS Lett. 185:4–8

    Google Scholar 

  • Germann, W.J., Ernst, S.A., Dawson, D.C. 1986. Resting and osmotically induced basolateral K conductances in turtle colon.J. Gen. Physiol. 88:253–274

    Google Scholar 

  • Grasset, E., Gunter-Smith, P., Schultz, S.G. 1983. Effects of Na-coupled alanine transport on intracellular K activities and the K conductance of the basolateral membranes ofNecturus small intestine.J. Membrane Biol. 71:89–94

    Google Scholar 

  • Gunter-Smith, P.J., Grasset, E., Schultz, S.G. 1982. Sodium-coupled amino acid and sugar transport byNecturus small intestine: An equivalent electrical circuit analysis of a rheogenic co-transport system.J. Membrane Biol. 66:25–39

    Google Scholar 

  • Hille, B. 1984. Ionic Channels of Excitable Membranes. Sinauer, Sunderland, MA

    Google Scholar 

  • Hinrichsen, R.D., Burgess-Cassler, A., Soltvedt, B.C., Hennesey, T., Kung, C. 1986. Restoration by calmodulin of a Cadependent K current missing in a mutant ofParamecium.Science 232:503–506

    Google Scholar 

  • Kristensen, L.O. 1986. Associations between transports of alanine and cations across cell membranes in rat hepatocytes.Am. J. Physiol. 251:G575-G584

    Google Scholar 

  • Latorre, R. 1986. The large calcium-activated potassium channel.In: Ion Channel Reconstitution. C. Miller, editor. pp. 431–467. Plenum, New York

    Google Scholar 

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

    Google Scholar 

  • Lau, K.R., Hudson, R.L., Schultz S.G. 1984. Cell swelling induces a barium-inhibitable potassium conductance in the basolateral membrane ofNecturus small intestine.Proc. Natl. Acad. Sci. USA 81:3591–3594

    Google Scholar 

  • Lau, K.R., Hudson, R.L., Schultz, S.G. 1986. Effect of hypertonicity on the increase in basolateral conductance ofNecturus small intestine in response to Na-sugar cotransport.Biochim. Biophys. Acta 855:193–196

    Google Scholar 

  • Laver, D.R., Fairley, K.A., Walker, N.A. 1989. Ion permeation in a K+ channel inChara australis: Direct evidence for diffusion limitation of ion flow in a maxi-K channel.J. Membrane Biol. 108:153–164

    Google Scholar 

  • Miller, C., Latorre, R., Reisin, I. 1987. Coupling of voltagedependent gating and Ba2+ block in the high-conductance Ca2+-activated K+ channel.J. Gen. Physiol. 90:427–449

    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 

  • Moczydlowski, E., Lucchesi, K., Ravindran, A. 1988. An emerging pharmacology of peptide toxins targeted against potassium channels.J. Membrane Biol. 105:95–111

    Google Scholar 

  • Moore, P.B., Dedman, J.R. 1982. Calcium-dependent protein binding to phenothiazine columns.J. Biol. Chem. 257:9663–9667

    Google Scholar 

  • Morris, A.P., Gallacher, D.V., Lee, J.A.C. 1986. A large conductance, voltage- and calcium-activated K+ channel in the basolateral membranes of rat enterocytes.FEBS Lett. 206:87–92

    Google Scholar 

  • Okada, Y., Yada, T., Ohno-Shosaka, T., Oiki, S. 1987. Evidence for the involvement of calmodulin in the operation of Ca-activated K channels in mouse fibroblasts.J. Membrane Biol. 96:121–128

    Google Scholar 

  • Pape, L., Kristensen, G.I. 1984. A calmodulin activated Ca2+-dependent K+ channel in human erythrocyte membrane inside-out vesicles.Biochem. Biophys. Acta 770:1–6

    Google Scholar 

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

    Google Scholar 

  • Potter, G.D., Tran, T., Sellin, J.H. 1989. Colonic epithelial cell calcium response to bile acidin vitro.Gastroenterology 96:A398

    Google Scholar 

  • Richards, N.W., Dawson, D.C. 1986. Single potassium channels blocked by lidocaine and quinidine in isolated turtle colon epithelial cells.Am. J. Physiol. 251:C85-C89

    Google Scholar 

  • Robinson, R.A., Stokes, R.H. 1959. Electrolyte solutions. (2nd Ed.) Academic, New York

    Google Scholar 

  • Schultz, S.G. 1980. Basic Principles of Membrane Transport. Cambridge University Press, New York

    Google Scholar 

  • Schultz, S.G. 1981. Homocellular regulatory mechanisms in sodium-transporting epithelia. Avoidance of extinction by “flush-through.”Am. J. Physiol. 241:F579-F590

    Google Scholar 

  • Schultz, S.G. 1986. Cellular models of epithelial ion transport.In: Physiology of Membrane Disorders (2nd Ed.) T.E. Andreoli, J.F. Hoffman, D.F. Fanestil, and S.G. Schultz, editors. pp. 519–534, Plenum, New York

    Google Scholar 

  • Schultz, S.G. 1989. Intracellular sodium activities and basolateral membrane potassium conductances of sodium-absorbing epithelial cells.Curr. Topics Membr. Transp. 34:21–44

    Google Scholar 

  • Schultz, S.G., Frizzell, R.A., Nellans, H.N. 1977. Active sodium transport and the electrophysiology of rabbit colon.J. Membrane Biol. 33:351–384

    Google Scholar 

  • Sepúlveda, F.V., Mason, W.T. 1985. Single channel recordings obtained from basolateral membranes of isolated rabbit enterocytes.FEBS Lett. 191:87–91

    Google Scholar 

  • Sheppard, D.N., Giraldez, F., Sepúlveda, F.V. 1988a. Kinetics of voltage- and Ca2+-activation and Ba2+ blockade of a largeconductance K+ channel fromNecturus enterocytes.J. Membrane Biol. 105:65–75

    Google Scholar 

  • Sheppard, D.N., Giraldez, F., Sepúlveda, F.V. 1988b. K+ channels activated byl-alanine transport in isolatedNecturus enterocytes.FEBS Lett. 234:446–448

    Google Scholar 

  • Vergara, C., Latorre, R. 1983. Kinetics of Ca2+-activated K+ channels from rabbit muscle incorporated into planar bilayers. Evidence for a Ca2+ and Ba2+ blockade.J. Gen Physiol. 82:543–568

    Google Scholar 

  • Vestergaard-Bogind, B., Stampe, P., Christophersen, P. 1985. Single-file diffusion through the Ca-activated K channel of human red cells.J. Membrane Biol. 88:67–75

    Google Scholar 

  • Weiss, B., Levin, R.M. 1978. Mechanism for selectively inhibiting the activation of cyclic nucleotide phosphodiesterase and adenylate cyclase by antipsychotic agents.Adv. Cyclic Nucleotide Res. 9:285–303

    Google Scholar 

  • Welsh, M.J., McCann, J.D. 1985. Intracellular calcium regulates potassium channels in a chloride-secreting epithelium.Proc. Nat'l. Acad. Sci. USA 82:8823–8826

    Google Scholar 

  • Wen, Y., Famulski, K.S., Carofoli, E. 1984. Ca2+-dependent K+ permeability of heart sarcolemmal vesicles. Modulation by cAMP-dependent protein kinase activity and by calmodulin.Biochem. Biophys. Res. Commun. 122:237–243

    Google Scholar 

  • Wiener, H., Turnheim, K., van, Os, C.H. 1989. Rabbit distal colon epithelium: I. Isolation and characterization of basolateral plasma membrane vesicles from surface and crypt cells.J. Membrane Biol. 110:147–162

    Google Scholar 

  • Wong, S.M., Chase, H.S. 1986. Role of intracellular calcium in cellular volume regulation.Am. J. Physiol. 250:C841-C852

    Google Scholar 

  • Yingst, D.R., Hoffman, J.F. 1984. Ca-induced K transport in human red blood cell ghosts containing Arsenazo III.J. Gen. Physiol. 83:19–45

    Google Scholar 

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  1. K. Turnheim

    Present address: Pharmakologisches Institut der Universitat Wien, Wahringer Strasse 13a, A-1090, Wien, Austria

Authors and Affiliations

  1. Department of Physiology and Cell Biology, University of Texas Medical School, 77225, Houston, Texas

    K. Turnheim, J. Costantin, S. Chan & S. G. Schultz

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  1. K. Turnheim
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  4. S. G. Schultz
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Turnheim, K., Costantin, J., Chan, S. et al. Reconstitution of a calcium-activated potassium channel in basolateral membranes of rabbit colonocytes into planar lipid bilayers. J. Membrain Biol. 112, 247–254 (1989). https://doi.org/10.1007/BF01870955

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  • DOI: https://doi.org/10.1007/BF01870955

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