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A novel cardiac potassium channel that is active and conductive at depolarized potentials

  • Excitable Tissues and Central Nervous Physiology
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Abstract

We report the existence of a novel potassium channel revealed in single-channel recordings from guinea-pig ventricular heart cells. The channel, observed in ∼10% of patches, demonstrates a 14 pS conductance at physiological potassium concentrations, does not rectify over the voltage range of the action potential, and is quite selective for K ions. The channel activates with depolarization, but does not require intracellular Ca2+ ions to open. Open channel probability increases rapidly (<10 ms) to a plateau in response to depolarizing voltage steps, and demonstrates no detectable inactivation (>600 ms). These features clearly distinguish this channel from other known K channels in cardiac muscle. Because of its high activity at plateau potentials, we propose the namei Kp.

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References

  • Apkon M, Nerbonne JM (1988) Are there multiple types of depolarization-activated K+ channels in adult ventricular myocytes? Biophys J 53:458a (abstr.)

    Google Scholar 

  • Barcenas-Ruiz L, Wier WG (1987) Voltage dependence of intracellular [Ca2+]i transients in guinea pig ventricular myocytes. Circ Res 61:148–154

    Google Scholar 

  • Benndorf K, Markwardt F, Nilius B (1987) Two types of transient outward currents in cardiac ventricular cells of mice. Pflügers Arch 409:641–643

    Google Scholar 

  • Bennett PB, Begenisich TB (1987) Catecholamines modulate the delayed rectifying potassium current (I K ) in guinea pig ventricular myocytes. Pflügers Arch 410:217–219

    Google Scholar 

  • Callewaert G, Vereecke J, Carmeliet E (1986) Existence of a calcium-dependent potassium channel in the membrane of cow cardiac Purkinje cells. Pflügers Arch 406:424–426

    Google Scholar 

  • Carmeliet E, Biermans G, Callewaert G, Vereecke J (1987) Potassium currents in cardiac cells. Experientia 43:1175–1184

    Google Scholar 

  • Clapham D, Logothetis D (1988) Delayed rectifier K+ current in embryonic chick heart ventricle. Am J Physiol 254:H192-H197

    Google Scholar 

  • Colquhoun D, Hawkes AG (1983) The principles of stochastic interpretation of ion-channel mechanisms. In: Sakmann B, Neher E (eds) Single-channel recording. Plenum Press, New York, pp 135–175

    Google Scholar 

  • Colquhoun D, Sigworth FJ (1983) Fitting and statistical analysis of single-channel records. In: Sakmann B, Neher E (eds) Single-channel recording. Plenum Press, New York, pp 191–263

    Google Scholar 

  • Coronado R, Latorre R (1982) Detection of K+ and Cl channels from calf cardiac sarcolemma in planar lipid bilayer membranes. Nature 298:849–852

    Google Scholar 

  • 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

    Google Scholar 

  • Hille B, Schwarz W (1978) Potassium channels as multi-ion single-file pores. J Gen Physiol 72:409–442

    Google Scholar 

  • Horie M, Irisawa H, Noma A (1987) Voltage-independent magnesium block of adenosine-triphosphate-sensitive potassium channel in guinea-pig ventricular cells. J Physiol (Lond) 387: 251–272

    Google Scholar 

  • Iijima T, Taira N (1987) Pinacidil increases the background potassium current in single ventricular cells. Eur J Pharmacol 141:139–141

    Google Scholar 

  • Kakei M, Noma A (1984) Adenosine-5′-triphosphate-sensitive single potassium channel in the atrioventricular node cell of the rabbit heart. J Physiol (Lond) 352:265–284

    Google Scholar 

  • Kakei M, Yoshinaga M, Saito K, Tanaka H (1986) The potassium current activated by 2-nicotinamidoethyl nitrate (nicorandil) in single ventricular cells of guinea pigs. Proc R Soc Lond B 229:331–343

    Google Scholar 

  • Kameyama M, Kakei M, Sato R, Shibasaki T, Matsuda H, Irisawa H (1984) Intracellular Na+ activates a K+ channel in mammalian cardiac cells. Nature 309:354–356

    Google Scholar 

  • Kurachi Y (1985) Voltage-dependent activation of the inward-rectifier potassium channel in the ventricular cell membrane of guinea-pig heart. J Physiol (Lond) 366:365–385

    Google Scholar 

  • Levitan IB (1985) Phosphorylation of ion channels. J Membr Biol 87:177–190

    Google Scholar 

  • Marban E, Tsien RW (1982) Effects of nystatin-mediated intracellular ion substitution on membrane currents in calf Purkinje fibres. J Physiol (Lond) 329:569–587

    Google Scholar 

  • Marty A (1981) Ca-dependent K channels with large unitary conductance in chromaffin cell membranes. Nature 291:497–500

    Google Scholar 

  • Matsuda H, Noma A (1984) Isolation of calcium current and its sensitivity to monovalent cations in dialyzed ventricular cells of guinea-pig. J Physiol 357:553–573

    Google Scholar 

  • Matsuda H, Saigusa A, Irisawa H (1987) Ohmic conductance through the inwardly rectifying K channel and blocking by internal Mg2+. Nature 325:156–159

    Google Scholar 

  • Matsuura H, Ehara T, Imoto Y (1987) An analysis of the delayed outward current in single ventricular cells of the guinea pig. Pflügers Arch 410:596–603

    Google Scholar 

  • Mazzanti M, DeFelice LJ (1988) K channel kinetics during the spontaneous heart beat in embryonic chick ventricle cells. Biophys J (in press)

  • Mitra R, Morad M (1985) A uniform enzymatic method for dissociation of myocytes from hearts and stomachs of vertebrates. Am J Physiol 249:H1056-H1060

    Google Scholar 

  • Noble D (1979) Initiation of the heartbeat. Clarendon Press, Oxford, pp 64–84

    Google Scholar 

  • Noma A (1983) ATP-regulated K+ channels in cardiac muscle. Nature 305:147–148

    Google Scholar 

  • Sakmann B, Trube G (1984) Conductance properties of single inwardly rectifying potassium channels in ventricular cells from guinea-pig heart. J Physiol (Lond) 1984;347:6457

    Google Scholar 

  • Shibasaki T (1987) Conductance and kinetics of delayed rectifier potassium channels in nodal cells of the rabbit heart. J Physiol (Lond) 387:227–250

    Google Scholar 

  • Trautwein W, Kameyama M (1986) Intracellular control of calcium and potassium currents in cardiac cells. Jpn Heart J 27:31–50

    Google Scholar 

  • Trube G, Hescheler J (1984) Inward-rectifying channels in isolated patches of the heart cell membrane: ATP-dependence and comparison with cell-attached patches. Pflügers Arch 401:178–184

    Google Scholar 

  • Tsien RY (1980) New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry 19:2396–2404

    Google Scholar 

  • Yellen G (1982) Single Ca++-activated nonselective cation channels in neuroblastoma. Nature 296:357–359

    Google Scholar 

  • Yue DT, Marban E (1988) A novel cardiac potassium channel that is active and conductive at depolarized potentials. Biophys J 53:641a (abstr.)

    Google Scholar 

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Yue, D.T., Marban, E. A novel cardiac potassium channel that is active and conductive at depolarized potentials. Pflugers Arch. 413, 127–133 (1988). https://doi.org/10.1007/BF00582522

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