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Cl and K+ channel currents during the action potential in Chara. simultaneous recording of membrane voltage and patch currents

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Abstract

Patch currents in the cell attached-mode and action potentials (AP) have been recorded simultaneously in internodal cells of Chara corallina. The action potentials are closely correlated with transient patch currents. With pipettes containing either 50 mm CaCl2 or 100 nm KCl plus 1 or 5 mm CaCl2, these transients measured up to 100 to 200 pA per patch at zero mV. Transients had a mean duration (time during which the current was ≥ half maximum peak amplitude) of about 1 sec, a maximum slope for current rising of about 400 pA sec−1 and a maximum rate of about 100 pA sec−1 for current decay, with no obvious effect of external Ca2+ on either of these parameters. In well-resolved recordings of current transients triggered by an action potential (AP), activities of two types of Cl-conducting channels (15 and 38 pS) have been identified. Since activity of these channels was only observed during action potentials but not upon positive voltage steps, these channels are not directly voltage gated but point to a cytoplasmic gating factor which accumulates during excitation and propagates from excited areas to the patch. A K+-conducting channel (40 pS) could be identified as well during an AP, when 100 mm KCl was in the pipette solution. The activity of this channel relaxed at the end of the APs with a time constant of about 3 sec. Stimulated activity of this channel is understood to cause the repolarization overshoot during the final phase of the action potential, whereas the transient activation of the Cl channels determines the fast voltage changes of the action potential.

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References

  • Armstrong, C.M., Binstock, L. 1965. Anomalous rectification in the squid giant axon injected with tetraethylammonium chloride. J. Gen. Physiol. 48:859–872

    Google Scholar 

  • Azimov, R.R., Geletyuk, V.l., Berestovskii, G.N. 1984. Single potential-dependent K+ channel of the cells of the alga Nitellopsis obtusa. Biofizika 32:79–84

    Google Scholar 

  • Beilby, M.J., Blatt, M.R. 1986. Simultaneous measurements of cytoplasmic K+ concentration and plasma membrane electrical parameters in single samples of Chara corallina. Plant Physiol. 82:417–422

    Google Scholar 

  • Beilby, M.J., Coster, H.G.L. 1979a. The action potential in Chara corallina II. Two activation-inactivation transients in voltage clamps of the plasmalemma. Aust. J. Plant Physiol. 6:323–325

    Google Scholar 

  • Beilby, M.J., Coster, H.G.L. 1979b. The action potential in Chara corallina III. The Hodgkin-Huxley parameters for the plasmalemma. Aust. J. Plant Physiol. 6:337–353

    Google Scholar 

  • Beilby, M.J., Mimura, T., Shimmen, T. 1993. The proton pump, high pH channels, and excitation: voltage clamp studies of intact and perfused cells of Nitellopsis obtusa. Protoplasma 175:144–152

    Google Scholar 

  • Berestovskii, G.N., Zherelova, O.M., Kataev, A.A. 1987. Ionic channels in characean algal cells. Biofizika 32:1011–1027

    Google Scholar 

  • Coleman, H.A. 1986. Chloride currents in Chara—A patch-clamp study. J. Membrane Biol. 93:55–61

    Google Scholar 

  • Findlay, G.P., Hope, A.B. 1964. Ionic relations of cells of Chara australis. VII. The separate electrical characteristics of the plasmalemma and tonoplast. Austr. J. Biol. Sci. 17:62–77

    Google Scholar 

  • Fischmeister, R., DeFelice, L.J., Ayer, R.K., Levi, R., DeHaan, R.L. 1984. Channel currents during spontaneous action potentials in embryonic chick heart cells. Biophys. J. 46:267–272

    Google Scholar 

  • Gaffey, C.T., Mullins, L.J. 1958. Ion fluxes during the action potential in Chara. J. Physiol. 144:505–524

    Google Scholar 

  • Hille, B. 1967. The selective inhibition of delayed potassium currents in nerve by tetraethylammonium ion. J. Gen. Physiol. 50:1287–1302

    Google Scholar 

  • Hope, A.B., Findlay, G.P. 1964. The action potential in Chara. Plant Cell Physiol. 5:377–379

    Google Scholar 

  • Kataev, A.A., Zherelova, O.M., Berestovskii, G.N. 1988. Effect of charged local anaesthetics on inactivation of Ca2+-activated Cl channels of Characean algae. Biofizika 33:1076–1084

    Google Scholar 

  • Katsuhara, M., Mimura, T., Tazawa, M. 1990. ATP-regulated ion channels in the plasma membrane of a Characeae alga Nitellopsis obtusa. Plant Physiol. 93:343–346

    Google Scholar 

  • Kikuyama, M. 1986. Ion effluxes during excitation of Characeae. Plant Cell Physiol. 27:1213–1216

    Google Scholar 

  • Kikuyama, M., Oda, K., Shimmen, T., Hayama, T., Tazawa, M. 1984. Potassium and chloride efflux during excitation of Characean cells. Plant Cell Physiol 25:965–974

    Google Scholar 

  • Kikuyama, M., Simada, K., Hiramoto, Y. 1993. Cessation of cytoplasmic streaming follows an increase of cytoplasmic Ca2+ during action potential in Nitella. Protoplasma 174:142–146

    Google Scholar 

  • Kishimoto, U. 1966. Repetitive action potentials in Nitella internodes. Plant Cell Physiol. 7:547–558

    Google Scholar 

  • Koppenhöfer, E. 1972. Die Wirkung von Kupfer, TTX, Cocain und TEA auf das Ruhe- und Aktionspotential von Nitella. Pfluegers Arch. 336:299–309

    Google Scholar 

  • Laver, D.R. 1991. A surgical method for accessing the plasma membrane of Chara australis. Protoplasma 161:79–84

    Google Scholar 

  • Lunevsky, V.Z., Zherelova, O.M., Vostrikov, I.Y., Berestovskii, G.N. 1983. Excitation of Characeae cell membranes as a result of activation of calcium and chloride channels. J. Membrane Biol. 72:43–58

    Google Scholar 

  • Mazzanti, M., DeFelice, L.J. 1988. K channel kinetics during the spontaneous heart beat in embryonic chick ventricle cells. Biophys. J. 54:1139–1148

    Google Scholar 

  • Mazzanti, M., DeFelice, L.J. 1990. Ca channel gating during cardiac action potentials. Biophys. J. 58:1059–1065

    Google Scholar 

  • Miller, A.J., Sanders, D. 1987. Depletion of cytosolic free calcium induced by photosynthesis. Nature 326:397–400

    Google Scholar 

  • Milton, R.L., Cadwell, J.H. 1990. How do patch clamp seals form? Pfluegers Arch. 416:758–765

    CAS  Google Scholar 

  • Oda, K. 1976. Simultaneous recording of potassium and chloride efflux during an action potential in Chara corallina. Plant Cell Physiol. 17:1085–1088

    Google Scholar 

  • Okihara, K., Ohkawa, T.A., Kasai, M. 1993. Effect of calmodulin on Ca2+-dependent Cl-sensitive anion channels in the Chara plasmalemma: a patch clamp study. Plant Cell Physiol. 34:75–82

    Google Scholar 

  • Okihara, K., Kiyosawa, K. 1988. Ion composition of the Chara internode. Plant Cell Physiol. 29:21–25

    Google Scholar 

  • Okihara, K., Ohkawa, T., Tsutsui, I., Kasai, M. 1991. A calcium-dependent and voltage-dependent chloride-sensitive anion channel in the Chara plasmalemma: a patch-clamp study. Plant Cell Physiol. 32:593–602

    Google Scholar 

  • Robinson, R.A., Stokes, R.H. 1968. Electrolyte Solutions. Butter worth Scientific Publications, London

    Google Scholar 

  • Reid, R.J., Tester, M. 1992. Measurements of Ca2+ fluxes in intact plant cells. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 338:73–82

    Article  CAS  PubMed  Google Scholar 

  • Shiina, T., Tazawa, M. 1987. Demonstration and characterization of Ca2+ channel in tonoplast free cells of Nitellopsis obtusa. J. Membrane Biol. 96:263–276

    Google Scholar 

  • Shiina, T., Wayne, R., Tung, H.Y.L., Tazawa, M. 1988. Possible involvement of protein phosphorylation/dephosphorylation in the modulation of Ca2+ channel in tonoplast-free cells of Nitellopsis. J. Membrane Biol. 102:255–264

    Google Scholar 

  • Shimmen, T., Kikuyama, M., Tazawa, M. 1976. Demonstration of two stable potential states of plasmalemma of Chara without tonoplast. J. Membrane Biol. 30:249–270

    Google Scholar 

  • Shimmen, T., Tazawa, M. 1983, Activation of K+-channel in membrane excitation of Nitella axilliformis. Plant Cell Physiol. 24: 1511–1524

    Google Scholar 

  • Tester, M. 1990. Plant ion channels: whole-cell and single-channel studies. New Phytol. 114:305–340

    Google Scholar 

  • Thiel, G., Homann, U., Gradmann, D. 1993. Microscopic elements of electrical excitation in Chara: Transient activity of Cl channels in the plasma membrane. J. Membrane Biol. 134:53–66

    Google Scholar 

  • Thiel, G., MacRobbie, E.A.C., Hanke, D.E. 1990. Raising the intra cellular level of inositol 1,4,5-trisphosphate changes plasma membrane ion transport in Characean algae. EMBO J. 9:1737–1741

    Google Scholar 

  • Tsutsui, I., Ohkawa, T., Nagai, R., Kishimoto, U. 1987. Role of calcium ion in the excitability and electrogenic pump activity of the Chara corallina membrane: I. Effects of La3+, verapamil, EGTA, W-7 and TFP on the action potential. J. Membrane Biol. 96:65–74

    Google Scholar 

  • Williamson, R.E., Ashley, C.C. 1982. Free Ca2+ and cytoplasmic streaming in the alga Chara. Nature 296:647–651

    Google Scholar 

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The financial support by the Deutsche Forschungsgemeinschaft is gratefully acknowledged. The authors thank Prof. D. Gradmann for constructive and stimulating criticism and J. Blatt for help in preparing the manuscript.

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Homann, U., Thiel, G. Cl and K+ channel currents during the action potential in Chara. simultaneous recording of membrane voltage and patch currents. J. Membarin Biol. 141, 297–309 (1994). https://doi.org/10.1007/BF00235139

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  • DOI: https://doi.org/10.1007/BF00235139

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