Deletion of Monoglyceride Lipase in Astrocytes Attenuates Lipopolysaccharide-induced Neuroinflammation

J Biol Chem. 2016 Jan 8;291(2):913-23. doi: 10.1074/jbc.M115.683615. Epub 2015 Nov 12.

Abstract

Monoglyceride lipase (MGL) is required for efficient hydrolysis of the endocannabinoid 2-arachidonoylglyerol (2-AG) in the brain generating arachidonic acid (AA) and glycerol. This metabolic function makes MGL an interesting target for the treatment of neuroinflammation, since 2-AG exhibits anti-inflammatory properties and AA is a precursor for pro-inflammatory prostaglandins. Astrocytes are an important source of AA and 2-AG, and highly express MGL. In the present study, we dissected the distinct contribution of MGL in astrocytes on brain 2-AG and AA metabolism by generating a mouse model with genetic deletion of MGL specifically in astrocytes (MKO(GFAP)). MKO(GFAP) mice exhibit moderately increased 2-AG and reduced AA levels in brain. Minor accumulation of 2-AG in the brain of MKO(GFAP) mice does not cause cannabinoid receptor desensitization as previously observed in mice globally lacking MGL. Importantly, MKO(GFAP) mice exhibit reduced brain prostaglandin E2 and pro-inflammatory cytokine levels upon peripheral lipopolysaccharide (LPS) administration. These observations indicate that MGL-mediated degradation of 2-AG in astrocytes provides AA for prostaglandin synthesis promoting LPS-induced neuroinflammation. The beneficial effect of astrocyte-specific MGL-deficiency is not fully abrogated by the inverse cannabinoid receptor 1 agonist SR141716 (Rimonabant) suggesting that the anti-inflammatory effects are rather caused by reduced prostaglandin synthesis than by activation of cannabinoid receptors. In conclusion, our data demonstrate that MGL in astrocytes is an important regulator of 2-AG levels, AA availability, and neuroinflammation.

Keywords: arachidonic acid (AA) (ARA); astrocyte; endocannabinoid; lipopolysaccharide (LPS); neuroinflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arachidonic Acids / metabolism
  • Astrocytes / enzymology*
  • Astrocytes / pathology
  • Behavior, Animal
  • Brain / enzymology
  • Cytokines / metabolism
  • Endocannabinoids / metabolism
  • Female
  • Gene Deletion*
  • Glial Fibrillary Acidic Protein / metabolism
  • Glycerides / metabolism
  • Inflammation / enzymology*
  • Inflammation / pathology*
  • Lipopolysaccharides
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microglia / metabolism
  • Microglia / pathology
  • Monoacylglycerol Lipases / metabolism*
  • Nervous System / enzymology*
  • Nervous System / pathology*
  • Organ Specificity
  • Receptor, Cannabinoid, CB1 / metabolism

Substances

  • Arachidonic Acids
  • Cytokines
  • Endocannabinoids
  • Glial Fibrillary Acidic Protein
  • Glycerides
  • Lipopolysaccharides
  • Receptor, Cannabinoid, CB1
  • glyceryl 2-arachidonate
  • Monoacylglycerol Lipases