Inhibition of COX-2 expression by endocannabinoid 2-arachidonoylglycerol is mediated via PPAR-γ

Br J Pharmacol. 2011 Aug;163(7):1533-49. doi: 10.1111/j.1476-5381.2011.01444.x.

Abstract

Background and purpose: Endocannabinoids have both anti-inflammatory and neuroprotective properties against harmful stimuli. We previously demonstrated that the endocannabinoid 2-arachidonoylglycerol (2-AG) protects hippocampal neurons by limiting the inflammatory response via a CB(1) receptor-dependent MAPK/NF-κB signalling pathway. The purpose of the present study was to determine whether PPARγ, an important nuclear receptor, mediates 2-AG-induced inhibition of NF-κB phosphorylation and COX-2 expression, and COX-2-enhanced miniature spontaneous excitatory postsynaptic currents (mEPSCs).

Experimental approach: By using a whole-cell patch clamp electrophysiological recording technique and immunoblot analysis, we determined mEPSCs, expression of COX-2 and PPARγ, and phosphorylation of NF-kB in mouse hippocampal neurons in culture.

Key results: Exogenous and endogenous 2-AG-produced suppressions of NF-κB-p65 phosphorylation, COX-2 expression and excitatory synaptic transmission in response to pro-inflammatory interleukin-1β (IL-1β) and LPS were inhibited by GW9662, a selective PPARγ antagonist, in hippocampal neurons in culture. PPARγ agonists 15-deoxy-Δ(12,14) -prostaglandin J(2) (15d-PGJ(2)) and rosiglitazone mimicked the effects of 2-AG on NF-κB-p65 phosphorylation, COX-2 expression and mEPSCs, and these effects were eliminated by antagonism of PPARγ. Moreover, exogenous application of 2-AG or elevation of endogenous 2-AG by inhibiting its hydrolysis with URB602 or JZL184, selective inhibitors of monoacylglycerol lipase (MAGL), prevented the IL-1β- and LPS-induced reduction of PPARγ expression. The 2-AG restoration of the reduced PPARγ expression was blocked or attenuated by pharmacological or genetic inhibition of the CB(1) receptor.

Conclusions and implications: Our results suggest that CB(1) receptor-dependent PPARγ expression is an important and novel signalling pathway in endocannabinoid 2-AG-produced resolution of neuroinflammation in response to pro-inflammatory insults.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Anilides / pharmacology
  • Animals
  • Arachidonic Acids / pharmacology*
  • Benzodioxoles / pharmacology
  • Biphenyl Compounds / pharmacology
  • Cannabinoid Receptor Modulators / pharmacology*
  • Cells, Cultured
  • Cyclooxygenase 2 / biosynthesis*
  • Cyclooxygenase 2 / genetics
  • Cyclooxygenase 2 / metabolism
  • Cyclooxygenase 2 Inhibitors / pharmacology
  • Endocannabinoids*
  • Excitatory Postsynaptic Potentials / drug effects
  • Glycerides / pharmacology*
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Inflammation / metabolism
  • Interleukin-1beta / pharmacology
  • Lipopolysaccharides / pharmacology
  • Mice
  • Monoacylglycerol Lipases / antagonists & inhibitors
  • NF-kappa B / antagonists & inhibitors
  • NF-kappa B / metabolism
  • Neurons / drug effects
  • Neurons / metabolism
  • PPAR gamma / agonists
  • PPAR gamma / antagonists & inhibitors
  • PPAR gamma / genetics
  • PPAR gamma / metabolism*
  • Phosphorylation / drug effects
  • Piperidines / pharmacology
  • Prostaglandin D2 / analogs & derivatives
  • Prostaglandin D2 / pharmacology
  • Receptor, Cannabinoid, CB1 / antagonists & inhibitors
  • Receptor, Cannabinoid, CB1 / metabolism
  • Rosiglitazone
  • Signal Transduction / drug effects
  • Synaptic Transmission / drug effects
  • Thiazolidinediones / pharmacology

Substances

  • 15-deoxyprostaglandin J2
  • 2-chloro-5-nitrobenzanilide
  • Anilides
  • Arachidonic Acids
  • Benzodioxoles
  • Biphenyl Compounds
  • Cannabinoid Receptor Modulators
  • Cyclooxygenase 2 Inhibitors
  • Endocannabinoids
  • Glycerides
  • Interleukin-1beta
  • JZL 184
  • Lipopolysaccharides
  • NF-kappa B
  • PPAR gamma
  • Piperidines
  • Receptor, Cannabinoid, CB1
  • Thiazolidinediones
  • URB602
  • Rosiglitazone
  • glyceryl 2-arachidonate
  • Ptgs2 protein, mouse
  • Cyclooxygenase 2
  • Monoacylglycerol Lipases
  • Prostaglandin D2