Ionic basis of the resting membrane potential and action potential in the pharyngeal muscle of Caenorhabditis elegans

J Neurophysiol. 2002 Feb;87(2):954-61. doi: 10.1152/jn.00233.2001.

Abstract

The pharynx of C. elegans is a rhythmically active muscle that pumps bacteria into the gut of the nematode. This activity is maintained by action potentials, which qualitatively bear a resemblance to vertebrate cardiac action potentials. Here, the ionic basis of the resting membrane potential and pharyngeal action potential has been characterized using intracellular recording techniques. The resting membrane potential is largely determined by a K(+) permeability, and a ouabain-sensitive, electrogenic pump. As previously suggested, the action potential is at least partly dependent on voltage-gated Ca(2+) channels, as the amplitude was increased as extracellular Ca(2+) was increased, and decreased by L-type Ca(2+) channel blockers verapamil and nifedipine. Barium caused a marked prolongation of action potential duration, suggesting that a calcium-activated K(+) current may contribute to repolarization. Most notably, however, we found that action potentials were abolished in the absence of external Na(+). This may be due, at least in part, to a Na(+)-dependent pacemaker potential. In addition, the persistence of action potentials in nominally free Ca(2+), the inhibition by Na(+) channel blockers procaine and quinidine, and the increase in action potential frequency caused by veratridine, a toxin that alters activation of voltage-gated Na(+) channels, point to the involvement of a voltage-gated Na(+) current. Voltage-clamp analysis is required for detailed characterization of this current, and this is in progress. Nonetheless, these observations are quite surprising in view of the lack of any obvious candidate genes for voltage-gated Na(+) channels in the C. elegans genome. It would therefore be informative to re-evaluate the data from these homology searches, with the aim of identifying the gene(s) conferring this Na(+), quinidine, and veratridine sensitivity to the pharynx.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 4-Aminopyridine / pharmacology
  • Action Potentials / drug effects
  • Action Potentials / physiology*
  • Animals
  • Barium / pharmacology
  • Caenorhabditis elegans / physiology*
  • Calcium / metabolism
  • Calcium Channel Blockers / pharmacology
  • Calcium Channels / physiology
  • Chloride Channels / pharmacology
  • Chlorides / metabolism
  • Electrophysiology
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Muscarinic Antagonists / pharmacology
  • Nifedipine / pharmacology
  • Pharyngeal Muscles / physiology*
  • Potassium / metabolism
  • Potassium Channel Blockers / pharmacology
  • Potassium Channels / physiology
  • Quinidine / pharmacology
  • Sodium / metabolism
  • Sodium Channels / physiology
  • Verapamil / pharmacology
  • Veratridine / pharmacology

Substances

  • Calcium Channel Blockers
  • Calcium Channels
  • Chloride Channels
  • Chlorides
  • Muscarinic Antagonists
  • Potassium Channel Blockers
  • Potassium Channels
  • Sodium Channels
  • Barium
  • Veratridine
  • Sodium
  • 4-Aminopyridine
  • Verapamil
  • Nifedipine
  • Quinidine
  • Potassium
  • Calcium