Caulerpenyne, a toxin from the seaweed Caulerpa taxifolia, depresses afterhyperpolarization in invertebrate neurons

Neuroscience. 2001;107(3):519-26. doi: 10.1016/s0306-4522(01)00365-7.

Abstract

The massive invasion of the Mediterranean Sea by the tropical seaweed Caulerpa taxifolia (Vahl) C. Agardh has stimulated several investigations in order to test the environmental risk from an ecotoxicological point of view. The studies carried out on various experimental models have shown that caulerpenyne, the major metabolite synthesized by the seaweed, affects several cellular and molecular targets. In addition, neurological disorders have been reported in patients who accidentally ate C. taxifolia, but no evidence about the potential effects of the seaweed and of its metabolites on nerve cells were up to now available. Herein we describe that caulerpenyne modifies the electrical properties of touch mechanosensory cells of the leech Hirudo medicinalis. The physiological firing of these cells causes an afterhyperpolarization that is mainly due to the activity of the Na+/K+-ATPase and to a lesser extent to a calcium-dependent potassium current. Caulerpenyne depressed this afterhyperpolarization; the effect was dose-dependent and partially reversible. Experiments have been carried out in order to understand the mechanism through which caulerpenyne reduced the afterhyperpolarization. The action of the biotoxin has been tested in the presence of pharmacological blockers of calcium-dependent potassium channels such as cadmium and apamin. In these experimental conditions, caulerpenyne still reduced the residual afterhyperpolarization, suggesting a direct effect of the toxin on the Na+/K+-ATPase. In order to test this hypothesis, we have performed experiments where the Na+/K+-ATPase was activated by the intracellular injection of sodium and where also its basal activity was modified as well. From the data collected we suggest that caulerpenyne inhibits both the basal and the sodium-induced activity of the Na+/K+-ATPase in leech touch neurons.

MeSH terms

  • Animals
  • Apamin / pharmacology
  • Cadmium Chloride / pharmacology
  • Drug Synergism
  • Electrophysiology
  • Leeches / cytology
  • Leeches / drug effects*
  • Leeches / physiology*
  • Marine Toxins / isolation & purification
  • Marine Toxins / pharmacology*
  • Neurons / drug effects*
  • Neurons / physiology*
  • Seaweed / chemistry
  • Sesquiterpenes / isolation & purification
  • Sesquiterpenes / pharmacology*
  • Sodium / pharmacology
  • Sodium-Potassium-Exchanging ATPase / metabolism

Substances

  • Marine Toxins
  • Sesquiterpenes
  • Apamin
  • caulerpenyne
  • Sodium
  • Sodium-Potassium-Exchanging ATPase
  • Cadmium Chloride