Na(+)-activated K+ channels localized in the nodal region of myelinated axons of Xenopus

J Physiol. 1994 Sep 1;479 ( Pt 2)(Pt 2):183-97. doi: 10.1113/jphysiol.1994.sp020287.

Abstract

1. A potassium channel activated by internal Na+ ions (K+Na channel) was identified in peripheral myelinated axons of Xenopus laevis using the cell-attached and excised configurations of the patch clamp technique. 2. The single-channel conductance for the main open state was 88 pS with [K+]o = 105 mM and pS with [K+]o = 2.5 mM ([K+]i = 105 mM). The channel was selectively permeable to K+ over Na+ ions. A characteristic feature of the K+Na channel was the frequent occurrence of subconductance states. 3. The open probability of the channel was strongly dependent on the concentration of Na+ ions at the inner side of the membrane. The half-maximal activating Na+ concentration and the Hill coefficient were 33 mM and 2.9, respectively. The open probability of the channel showed only weak potential dependence. 4. The K+Na channel was relatively insensitive to external tetraethylammonium (TEA+) in comparison with voltage-dependent axonal K+ channels; the half-maximal inhibitory concentration (IC50) was 21.3 mM (at -90 mV). In contrast, the channel was blocked by low concentrations of external Ba2+ and Cs+ ions, with IC50 values of 0.7 and 1.1 mM, respectively (at -90 mV). The block by Ba2+ and Cs+ was more pronounced at negative than at positive membrane potentials. 5. A comparison of the number of K+Na channels in nodal and paranodal patches from the same axon revealed that the channel density was about 10-fold higher at the node of Ranvier than at the paranode. Moreover, a correlation between the number of K+Na channels and voltage-dependent Na+ channels in the same patches was found, suggesting co-localization of both channel types. 6. As weakly potential-dependent ('leakage') channels, axonal K+Na channels may be involved in setting the resting potential of vertebrate axons. Simulations of Na+ ion diffusion suggest two possible mechanisms of activation of K+Na channels: the local increase of Na+ concentration in a cluster of Na+ channels during a single action potential or the accumulation in the intracellular axonal compartment during a train of action potentials.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Axons / drug effects
  • Axons / metabolism*
  • Axons / ultrastructure
  • Barium / pharmacology
  • Cell Membrane Permeability
  • Cesium / pharmacology
  • Demyelinating Diseases / chemically induced
  • Demyelinating Diseases / metabolism
  • Immunohistochemistry
  • Membrane Potentials
  • Microscopy, Electron
  • Myelin Sheath / drug effects
  • Myelin Sheath / metabolism
  • Myelin Sheath / ultrastructure
  • Patch-Clamp Techniques
  • Potassium Channel Blockers
  • Potassium Channels / drug effects
  • Potassium Channels / metabolism*
  • Ranvier's Nodes / drug effects
  • Ranvier's Nodes / metabolism
  • Ranvier's Nodes / ultrastructure*
  • Sodium / metabolism*
  • Sodium Channels / metabolism
  • Tetraethylammonium
  • Tetraethylammonium Compounds / pharmacology
  • Xenopus laevis

Substances

  • Potassium Channel Blockers
  • Potassium Channels
  • Sodium Channels
  • Tetraethylammonium Compounds
  • Cesium
  • Barium
  • Tetraethylammonium
  • Sodium