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A TEA-insensitive flickering potassium channel active around the resting potential in myelinated nerve

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Summary

A novel potassium-selective channel which is active at membrane potentials between — 100 mV and +40 mV has been identified in peripheral myelinated axons of Xenopus laevis using the patch-clamp technique. At negative potentials with 105 mm-K on both sides of the membrane, the channel at 1 kHz resolution showed a series of brief openings and closings interrupted by longer closings, resulting in a flickery bursting activity. Measurements with resolution up to 10 kHz revealed a single-channel conductance of 49 pS with 105 mm-K and 17 pS with 2.5 mm-K on the outer side of the membrane. The channel was selective for K ions over Na ions (P Na/P K = 0.033). The probability of being within a burst in outside-out patches varied from patch to patch (>0.2, but often >0.9), and was independent of membrane potential. Open-time histograms were satisfactorily described with a single exponential (τ o= 0.09 msec), closed times with the sum of three exponentials (τ c= 0.13, 5.9, and 36.6 msec). Sensitivity to external tetraethylammonium was comparatively low (IC50 = 19.0 mm). External Cs ions reduced the apparent unitary conductance for inward currents at E m= −90 mV (IC50 = 1.1 mm). Ba and, more potently, Zn ions lowered not only the apparent singlechannel conductance but also open probability. The local anesthetic bupivacaine with high potency reduced probability of being within a burst (IC50 = 165 nm). The flickering K channel is clearly different from the other five types of K channels identified so far in the same preparation. We suggest that this channel may form the molecular basis of the resting potential in vertebrate myelinated axons.

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References

  1. Adrian, R.H., Chandler, W.K., Hodgkin, A.L. 1970. Slow changes in potassium permeability in skeletal muscle. J. Physiol. 208:645–668

  2. Ashcroft, F.M., Ashcroft, S.J.H., Harrison, D.E. 1988. Properties of single potassium channels modulated by glucose in rat pancreatic β-cells. J. Physiol. 400:501–527

  3. Baker, M., Bostock, H., Grafe, P., Martius, P. 1987. Function and distribution of three types of rectifying channel in rat spinal root myelinated axons. J. Physiol. 383:45–67

  4. Barrett, E.F., Barrett, J.N. 1982. Intracellular recording from vertebrate myelinated axons: Mechanism of the depolarizing afterpotential. J. Physiol. 323:117–144

  5. Chang, D.C. 1986. Is the K permeability of the resting membrane controlled by the excitable K channel? Biophys. J. 50:1095–1100

  6. Chiu, S.Y., Ritchie, J.M. 1982. Evidence for the presence of potassium channels in the internode of frog myelinated nerve fibres. J. Physiol. 322:485–501

  7. Chiu, S.Y., Ritchie, J.M. 1984. On the physiological role of internodal potassium channels and the security of conduction in myelinated nerve fibres. Proc. R. Soc. Lond. B220:415–422

  8. Colquhoun, D., Hawkes, A.G. 1982. On the stochastic properties of bursts of single ion channel openings and of clusters of bursts. Philos. Trans. R. Soc. London B300:1–59

  9. Colquhoun, D., Sigworth, F.J. 1983. Fitting and statistical analysis of single-channel records. In: Single-Channel Recording. B. Sakmann and E. Neher, editors. pp. 191–263. Plenum, New York and London

  10. Constanti, A., Galvan, M. 1983. Fast inward-rectifying current accounts for anomalous rectification in olfactory cortex neurones. J. Physiol 385:153–178

  11. DeFelice, L.J. 1981. Introduction to Membrane Noise. Plenum, New York

  12. Grygorezyk, R., Schwarz, W. 1985. Ca2+-activated K+ permeability in human erythrocytes: Modulation of single-channel events. Eur. Biophys. J. 12:57–65

  13. Hagiwara, S., Miyazaki, S., Rosenthal, N.P. 1976. Potassium current and the effect of cesium on this current during anomalous rectification of the egg cell membrane of a starfish. J. Gen. Physiol. 67:621–638

  14. Halliwell, J.V., Adams, P.R. 1982. Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res. 250:71–92

  15. Hamill, O.P., Marty, A., Neher, E., Sakmann, 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

  16. Hamill, O.P. 1983. Potassium and chloride channels in red blood cells. In: Single-Channel Recording. B. Sakmann and E. Neher, editors. pp. 451–471. Plenum, London

  17. Haydon, D.A., Requena, J., Simon, A.J.B. 1988. The potassium conductance of the resting squid axon and its blockage by clinical concentrations of general anaesthetics. J. Physiol. 402:363–374

  18. Hille, B. 1973. Potassium channels in myelinated nerve: Selective permeability to small cations. J. Gen. Physiol. 61:669–686

  19. Hille, B. 1992. Ionic Channels of Excitable Membranes. Sinauer, Sunderland

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

  21. Huxley, A.F., Stämpfli, R. 1951. Direct determination of membrane resting potential and action potential in single myelinated nerve fibres. J. Physiol. 112:476–495

  22. Hwa, G.G.C., Avoli, M. 1991. Hyperpolarizing inward rectification in rat neocortical neurons located in the superficial layers. Neurosci. Lett. 124:65–68

  23. Jack, J.J.B. 1976. Electrophysiological properties of peripheral nerve. In: The Peripheral Nerve. D.N. Landon, editor. pp. 740–818. Chapman and Hall, London

  24. Jonas, P., Bräu, M.E., Hermsteiner, M., Vogel, W. 1989. Singlechannel recording in myelinated nerve fibers reveals one type of Na channel but different K channels. Proc. Natl. Acad. Sci. USA 86:7238–7242

  25. Jonas, P., Koh, D.-S., Kampe, K., Hermsteiner, M., Vogel, W. 1991. ATP-sensitive and Ca-activated K channels in vertebrate axons: novel links between metabolism and excitability. Pfluegers Arch. 418:68–73

  26. Jones, S.W. 1989. On the resting potential of isolated frog sympathetic neurons. Neuron 3:153–161

  27. Klein, M., Camardo, J., Kandel, E.R. 1982. Serotonin modulates a specific potassium current in the sensory neurons that show presynaptic facilitation in Aplysia. Proc. Natl. Acad. Sci. USA 79:5713–5717

  28. Koh, D.-S., Jonas, P., Bräu, M., Hermsteiner, M., Vogel, W. 1991. A TEA-insensitive potassium channel with complex gating recorded from amphibian myelinated nerve fibres. Pfluegers Arch. 418:R30

  29. Mayer, M.L., Westbrook, G.L. 1983. A voltage-clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurones. J. Physiol. 340:19–45

  30. McManus, O.B., Magleby, K.L. 1988. Kinetic states and modes of single large-conductance calcium-activated potassium channels in cultured rat skeletal muscle. J. Physiol. 402:79–120

  31. Nonner, W. 1969. A new voltage clamp method for Ranvier nodes. Pfluegers Arch. 309:176–192

  32. Quayle, J.M., Standen, N.B., Stanfield, P.R. 1988. The voltagedependent block of ATP-sensitive potassium channels of frog skeletal muscle by caesium and barium ions. J. Physiol. 405:677–697

  33. Rae, J.L., Dewey, J., Cooper, K. 1989. Properties of single potassium-selective ionic channels from the apical membrane of rabbit corneal endothelium. Exp. Eye Res. 49:591–609

  34. Sakmann, B., Neher, E. 1983. Geometric parameters of pipettes and membrane patches. In: Single-Channel Recording. B. Sakmann, and E. Neher, editors. pp. 37–51. Plenum, New York and London

  35. Sakmann, B., Trube, G. 1984. Voltage-dependent inactivation of inward-rectifying single-channel currents in the guinea-pig heart cell membrane. J. Physiol. 347:659–683

  36. Schmidt, H., Stämpfli, R. 1966. Die Wirkung von Tetraäthylammoniumchlorid auf den einzelnen Ranvierschen Schnürring. Pfluegers Arch. 287:311–325

  37. Spalding, B.C., Swift, J.G., Horowicz, P. 1986. Zinc inhibition of potassium efflux in depolarized frog muscle and its modification by external hydrogen ions and diethylpyrocarbonate treatment. J. Membrane Biol. 93:157–164

  38. Takahashi, T. 1990. Inward rectification in neonatal rat spinal motoneurones. J. Physiol. 423:47–62

  39. Yamamoto, D., Suzuki, N. 1987. Blockage of chloride channels by HEPES buffer. Proc. R. Soc. London B230:93–100

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

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Additional information

A grant from the Konrad-Adenauer-Stiftung to D.-S.K. is gratefully acknowledged, and this paper constitutes a part of his dissertation. We thank Drs. H. Bostock, B. Neumcke, D. Siemen and Mr. G. Reid for reading the manuscript and Mrs. Elke Schmidt for technical assistance. Financial support was received from the Deutsche Forschungsgemeinschaft (Vol88/13-2).

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Koh, D., Jonas, P., Bräu, M.E. et al. A TEA-insensitive flickering potassium channel active around the resting potential in myelinated nerve. J. Membarin Biol. 130, 149–162 (1992). https://doi.org/10.1007/BF00231893

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Key Words

  • patch clamp
  • myelinated nerve fiber
  • potassium channel
  • flicker kinetics
  • resting potential