Complex regulation of the TRPM8 cold receptor channel: role of arachidonic acid release following M3 muscarinic receptor stimulation

J Biol Chem. 2011 Mar 18;286(11):9849-55. doi: 10.1074/jbc.M110.162016. Epub 2011 Jan 18.

Abstract

Cold/menthol-activated TRPM8 (transient receptor potential channel melastatin member 8) is primarily expressed in sensory neurons, where it constitutes the principal receptor of environmental innocuous cold. TRPM8 has been shown to be regulated by multiple influences such as phosphorylation, pH, Ca(2+), and lipid messengers. One such messenger is arachidonic acid (AA), which has been shown to inhibit TRPM8 channel activity. However, the physiological pathways mediating the inhibitory effect of AA on TRPM8 still remain unknown. Here, we demonstrate that TRPM8 is regulated via M3 muscarinic acetylcholine receptor-coupled signaling cascade based on the activation of cytosolic phospholipase A2 (cPLA2) and cPLA2-catalyzed derivation of AA. Stimulation of M3 receptors heterologously co-expressed with TRPM8 in HEK-293 cells by nonselective muscarinic agonist, oxotremorine methiodide (Oxo-M), caused inhibition of TRPM8-mediated membrane current, which could be mimicked by AA and antagonized by pharmacological or siRNA-mediated cPLA2 silencing. Our results demonstrate the intracellular functional link between M3 receptor and TRPM8 channel via cPLA2/AA and suggest a novel physiological mechanism of arachidonate-mediated regulation of TRPM8 channel activity through muscarinic receptors. We also summarize the existing TRPM8 regulations and discuss their physiological and pathological significance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arachidonic Acid / metabolism*
  • Arachidonic Acid / pharmacology
  • Gene Silencing
  • Group IV Phospholipases A2 / genetics
  • Group IV Phospholipases A2 / metabolism*
  • HEK293 Cells
  • Humans
  • Phosphorylation / drug effects
  • Receptor, Muscarinic M3 / genetics
  • Receptor, Muscarinic M3 / metabolism*
  • TRPM Cation Channels / genetics
  • TRPM Cation Channels / metabolism*

Substances

  • Receptor, Muscarinic M3
  • TRPM Cation Channels
  • TRPM8 protein, human
  • Arachidonic Acid
  • Group IV Phospholipases A2