Polyunsaturated fatty acids are potent openers of human M-channels expressed in Xenopus laevis oocytes

Acta Physiol (Oxf). 2016 Sep;218(1):28-37. doi: 10.1111/apha.12663. Epub 2016 Mar 23.

Abstract

Aim: Polyunsaturated fatty acids have been reported to reduce neuronal excitability, in part by promoting inactivation of voltage-gated sodium and calcium channels. Effects on neuronal potassium channels are less explored and experimental data ambiguous. The aim of this study was to investigate anti-excitable effects of polyunsaturated fatty acids on the neuronal M-channel, important for setting the resting membrane potential in hippocampal and dorsal root ganglion neurones.

Methods: Effects of fatty acids and fatty acid analogues on mouse dorsal root ganglion neurones and on the human KV 7.2/3 channel expressed in Xenopus laevis oocytes were studied using electrophysiology.

Results: Extracellular application of physiologically relevant concentrations of the polyunsaturated fatty acid docosahexaenoic acid hyperpolarized the resting membrane potential (-2.4 mV by 30 μm) and increased the threshold current to evoke action potentials in dorsal root ganglion neurones. The polyunsaturated fatty acids docosahexaenoic acid, α-linolenic acid and eicosapentaenoic acid facilitated opening of the human M-channel, comprised of the heteromeric human KV 7.2/3 channel expressed in Xenopus oocytes, by shifting the conductance-vs.-voltage curve towards more negative voltages (by -7.4 to -11.3 mV by 70 μm). Uncharged docosahexaenoic acid methyl ester and monounsaturated oleic acid did not facilitate opening of the human KV 7.2/3 channel.

Conclusions: These findings suggest that circulating polyunsaturated fatty acids, with a minimum requirement of multiple double bonds and a charged carboxyl group, dampen excitability by opening neuronal M-channels. Collectively, our data bring light to the molecular targets of polyunsaturated fatty acids and thus a possible mechanism by which polyunsaturated fatty acids reduce neuronal excitability.

Keywords: KCNQ potassium channel family; M-channel; electrophysiology; epilepsy; excitability; polyunsaturated fatty acids.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Fatty Acids, Omega-3 / pharmacology
  • Fatty Acids, Unsaturated / pharmacology*
  • Ganglia, Spinal / cytology
  • Ganglia, Spinal / drug effects
  • Hippocampus / drug effects
  • Humans
  • Ion Channel Gating / drug effects
  • KCNQ2 Potassium Channel / agonists*
  • KCNQ3 Potassium Channel / agonists*
  • Membrane Potentials / drug effects
  • Mice, Inbred C57BL
  • Neurons / drug effects
  • Oocytes / drug effects
  • Oocytes / metabolism
  • Patch-Clamp Techniques
  • Xenopus laevis

Substances

  • Fatty Acids, Omega-3
  • Fatty Acids, Unsaturated
  • KCNQ2 Potassium Channel
  • KCNQ2 protein, human
  • KCNQ3 Potassium Channel
  • KCNQ3 protein, human

Associated data

  • GENBANK/NM_000219
  • GENBANK/NM_004518
  • GENBANK/NM_004519
  • GENBANK/NM_172201