Regulation of transient receptor potential channels of melastatin type 8 (TRPM8): effect of cAMP, cannabinoid CB(1) receptors and endovanilloids

Exp Cell Res. 2007 May 15;313(9):1911-20. doi: 10.1016/j.yexcr.2007.01.008. Epub 2007 Jan 18.

Abstract

The transient receptor potential channel of melastatin type 8 (TRPM8), which is gated by low (<25 degrees C) temperature and chemical compounds, is regulated by protein kinase C-mediated phosphorylation in a way opposite to that observed with the transient receptor potential channel of vanilloid type 1 (TRPV1), i.e. by being desensitized and not sensitized. As TRPV1 is sensitized also by protein kinase A (PKA)-mediated phosphorylation, we investigated the effect of two activators of the PKA pathway, 8-Br-cAMP and forskolin, on the activity of menthol and icilin at TRPM8 in HEK-293 cells stably overexpressing the channel (TRPM8-HEK-293 cells). We also studied the effect on TRPM8 of: (1) a series of compounds previously shown to activate or antagonize TRPV1, and (2) co-stimulation of transiently co-expressed cannabinoid CB(1) receptors. Both 8-Br-cAMP (100 microM) and forskolin (10 microM) right-shifted the dose-response curves for the TRPM8-mediated effect of icilin and menthol on intracellular Ca(2+). The inhibitory effects of 8-Br-cAMP and forskolin were attenuated by the selective PKA inhibitor Rp-cAMP-S. Stimulation of human CB(1) receptors transiently co-expressed in TRPM8-HEK-293 cells also inhibited TRPM8 response to icilin. Finally, some TRPV1 agonists and antagonists, but not iodinated antagonists, antagonized icilin- and much less so menthol-, induced TRPM8 activation. Importantly, the endovanilloids/endocannabinoids, anandamide and NADA, also antagonized TRPM8 at submicromolar concentrations. Although these findings need to be confirmed by experiments directly measuring TRPM8 activity in natively TRPM8-expressing cells, they support the notion that the same regulatory events have opposing actions on TRPM8 and TRPV1 receptors and identify anandamide and NADA as the first potential endogenous functional antagonists of TRPM8 channels.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 8-Bromo Cyclic Adenosine Monophosphate / pharmacology
  • Arachidonic Acids / metabolism
  • Arachidonic Acids / pharmacology
  • Benzaldehydes / chemistry
  • Cannabinoid Receptor Modulators / metabolism*
  • Cannabinoid Receptor Modulators / pharmacology
  • Cell Line
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism*
  • Colforsin / pharmacology
  • Cyclic AMP / metabolism*
  • Cyclic AMP-Dependent Protein Kinases / drug effects
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Dopamine / analogs & derivatives
  • Dopamine / metabolism
  • Dopamine / pharmacology
  • Dose-Response Relationship, Drug
  • Drug Interactions / physiology
  • Endocannabinoids
  • Enzyme Inhibitors / pharmacology
  • Humans
  • Ion Channel Gating / drug effects
  • Ion Channel Gating / physiology
  • Menthol / pharmacology
  • Polyunsaturated Alkamides / metabolism
  • Polyunsaturated Alkamides / pharmacology
  • Pyrimidinones / pharmacology
  • Receptor, Cannabinoid, CB1 / drug effects
  • Receptor, Cannabinoid, CB1 / genetics
  • Receptor, Cannabinoid, CB1 / metabolism*
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • TRPM Cation Channels / drug effects
  • TRPM Cation Channels / genetics
  • TRPM Cation Channels / metabolism*
  • Transfection

Substances

  • Arachidonic Acids
  • Benzaldehydes
  • Cannabinoid Receptor Modulators
  • Endocannabinoids
  • Enzyme Inhibitors
  • Polyunsaturated Alkamides
  • Pyrimidinones
  • Receptor, Cannabinoid, CB1
  • TRPM Cation Channels
  • TRPM8 protein, human
  • arachidonyl dopamine
  • Menthol
  • Colforsin
  • 8-Bromo Cyclic Adenosine Monophosphate
  • vanillin
  • icilin
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases
  • anandamide
  • Dopamine