Negative Regulation of Leptin-induced Reactive Oxygen Species (ROS) Formation by Cannabinoid CB1 Receptor Activation in Hypothalamic Neurons

J Biol Chem. 2015 May 29;290(22):13669-77. doi: 10.1074/jbc.M115.646885. Epub 2015 Apr 13.

Abstract

The adipocyte-derived, anorectic hormone leptin was recently shown to owe part of its regulatory effects on appetite-regulating hypothalamic neuropeptides to the elevation of reactive oxygen species (ROS) levels in arcuate nucleus (ARC) neurons. Leptin is also known to exert a negative regulation on hypothalamic endocannabinoid levels and hence on cannabinoid CB1 receptor activity. Here we investigated the possibility of a negative regulation by CB1 receptors of leptin-mediated ROS formation in the ARC. Through pharmacological and molecular biology experiments we report data showing that leptin-induced ROS accumulation is 1) blunted by arachidonyl-2'-chloroethylamide (ACEA) in a CB1-dependent manner in both the mouse hypothalamic cell line mHypoE-N41 and ARC neuron primary cultures, 2) likewise blocked by a peroxisome proliferator-activated receptor-γ (PPAR-γ) agonist, troglitazone, in a manner inhibited by T0070907, a PPAR-γ antagonist that also inhibited the ACEA effect on leptin, 3) blunted under conditions of increased endocannabinoid tone due to either pharmacological or genetic inhibition of endocannabinoid degradation in mHypoE-N41 and primary ARC neuronal cultures from MAGL(-/-) mice, respectively, and 4) associated with reduction of both PPAR-γ and catalase activity, which are reversed by both ACEA and troglitazone. We conclude that CB1 activation reverses leptin-induced ROS formation and hence possibly some of the ROS-mediated effects of the hormone by preventing PPAR-γ inhibition by leptin, with subsequent increase of catalase activity. This mechanism might underlie in part CB1 orexigenic actions under physiopathological conditions accompanied by elevated hypothalamic endocannabinoid levels.

Keywords: Cannabinoid; Cannabinoid Receptor Type 1 (CB1); Hypothalamus; Leptin; Reactive Oxygen Species (ROS).

MeSH terms

  • Adipocytes / cytology
  • Animals
  • Animals, Newborn
  • Arachidonic Acids / chemistry
  • Benzamides / chemistry
  • Body Weight
  • Cannabinoids / metabolism
  • Catalase / metabolism
  • Cells, Cultured
  • Chromans / chemistry
  • Endocannabinoids / metabolism
  • Gene Expression Regulation*
  • Gene Silencing
  • Hydrolysis
  • Hypothalamus / metabolism*
  • Leptin / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Neurons / metabolism*
  • PPAR alpha / metabolism
  • PPAR gamma / metabolism*
  • Pyridines / chemistry
  • RNA, Small Interfering / metabolism
  • Reactive Oxygen Species / metabolism*
  • Receptor, Cannabinoid, CB1 / metabolism*
  • Thiazolidinediones / chemistry
  • Troglitazone

Substances

  • Arachidonic Acids
  • Benzamides
  • Cannabinoids
  • Chromans
  • Endocannabinoids
  • Leptin
  • PPAR alpha
  • PPAR gamma
  • Pyridines
  • RNA, Small Interfering
  • Reactive Oxygen Species
  • Receptor, Cannabinoid, CB1
  • T 0070907
  • Thiazolidinediones
  • arachidonyl-2-chloroethylamide
  • Catalase
  • Troglitazone