Arachidonic acid potentiates acid-sensing ion channels in rat sensory neurons by a direct action

Neuroscience. 2007 Mar 16;145(2):686-98. doi: 10.1016/j.neuroscience.2006.12.024. Epub 2007 Jan 29.

Abstract

Acid-sensing ion channels (ASICs) are activated by a decrease in extracellular pH. ASICs are expressed in nociceptive sensory neurons, and several lines of evidence suggest that they are responsible for signaling the pain caused by extracellular acidification, but little is understood of the modulation of ASICs by pro-inflammatory factors. Using whole-cell patch clamp we demonstrate that low pH evokes three distinct inward currents in rat dorsal root ganglion neurons: a slowly inactivating transient current, a rapidly inactivating transient current, and a sustained current. All three currents were potentiated by arachidonic acid (AA), to 123%, 171%, and 264% of peak current, respectively. Membrane stretch had no effect on proton-gated currents, implying that AA is unlikely to act via local membrane deformation. The current carried by heterologously expressed ASIC1a and ASIC3 was also potentiated by AA. AA potentiates ASIC activation by a direct mechanism, because inhibition of AA metabolism had no effect on potentiation, and potentiation of single ASIC2a channels could be observed in cell-free patches. Potentiation by lipids with the same chain length as AA increased as the number of double bonds was increased. AA is known to be released in inflammation and the results suggest that AA may be an important pro-inflammatory agent responsible for enhancing acid-mediated pain.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acid Sensing Ion Channels
  • Animals
  • Animals, Newborn
  • Arachidonic Acid / metabolism*
  • Arachidonic Acid / pharmacology
  • Cells, Cultured
  • Degenerin Sodium Channels
  • Epithelial Sodium Channels / drug effects
  • Epithelial Sodium Channels / metabolism
  • Ganglia, Spinal / drug effects
  • Ganglia, Spinal / metabolism*
  • Inflammation / chemically induced
  • Inflammation / metabolism
  • Inflammation / physiopathology
  • Inflammation Mediators / metabolism
  • Inflammation Mediators / pharmacology
  • Ion Channel Gating / drug effects
  • Ion Channel Gating / physiology
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Membrane Proteins / drug effects
  • Membrane Proteins / metabolism*
  • Nerve Tissue Proteins / drug effects
  • Nerve Tissue Proteins / metabolism*
  • Neurons, Afferent / drug effects
  • Neurons, Afferent / metabolism*
  • Nociceptors / drug effects
  • Nociceptors / metabolism*
  • Pain / chemically induced
  • Pain / metabolism*
  • Pain / physiopathology
  • Patch-Clamp Techniques
  • Rats
  • Rats, Wistar
  • Sodium Channels / drug effects
  • Sodium Channels / metabolism*

Substances

  • ASIC3 protein, rat
  • Acid Sensing Ion Channels
  • Asic2 protein, rat
  • Degenerin Sodium Channels
  • Epithelial Sodium Channels
  • Inflammation Mediators
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Sodium Channels
  • Arachidonic Acid