Functional Redundancy Between Canonical Endocannabinoid Signaling Systems in the Modulation of Anxiety

Biol Psychiatry. 2017 Oct 1;82(7):488-499. doi: 10.1016/j.biopsych.2017.03.002. Epub 2017 Mar 15.

Abstract

Background: Increasing the available repertoire of effective treatments for mood and anxiety disorders represents a critical unmet need. Pharmacological augmentation of endogenous cannabinoid (eCB) signaling has been suggested to represent a novel approach to the treatment of anxiety disorders; however, the functional interactions between two canonical eCB pathways mediated via anandamide (N-arachidonylethanolamine [AEA]) and 2-arachidonoylglycerol (2-AG) in the regulation of anxiety are not well understood.

Methods: We utilized pharmacological augmentation and depletion combined with behavioral and electrophysiological approaches to probe the role of 2-AG signaling in the modulation of stress-induced anxiety and the functional redundancy between AEA and 2-AG signaling in the modulation of anxiety-like behaviors in mice.

Results: Selective 2-AG augmentation reduced anxiety in the light/dark box assay and prevented stress-induced increases in anxiety associated with limbic AEA deficiency. In contrast, acute 2-AG depletion increased anxiety-like behaviors, which was normalized by selective pharmacological augmentation of AEA signaling and via direct cannabinoid receptor 1 stimulation with Δ9-tetrahydrocannabinol. Electrophysiological studies revealed 2-AG modulation of amygdala glutamatergic transmission as a key synaptic correlate of the anxiolytic effects of 2-AG augmentation.

Conclusions: Although AEA and 2-AG likely subserve distinct physiological roles, a pharmacological and functional redundancy between these canonical eCB signaling pathways exists in the modulation of anxiety-like behaviors. These data support development of eCB-based treatment approaches for mood and anxiety disorders and suggest a potentially wider therapeutic overlap between AEA and 2-AG augmentation approaches than was previously appreciated.

Keywords: 2-Arachidonoylglycerol; Amygdala; Anxiety; JZL184; MAGL inhibition; Stress.

MeSH terms

  • Adaptation, Ocular / drug effects
  • Animals
  • Anti-Anxiety Agents / therapeutic use
  • Anxiety / drug therapy*
  • Anxiety / metabolism
  • Anxiety / physiopathology
  • Arachidonic Acids / metabolism*
  • Benzodioxoles / therapeutic use
  • Brain / drug effects
  • Brain / metabolism
  • Brain / physiology
  • Cannabinoid Receptor Agonists / therapeutic use
  • Cyclohexanols / therapeutic use
  • Disease Models, Animal
  • Dronabinol / pharmacology
  • Endocannabinoids / metabolism*
  • Excitatory Postsynaptic Potentials / drug effects
  • Glycerides / metabolism*
  • Heterocyclic Compounds, 1-Ring / therapeutic use
  • Locomotion / drug effects
  • Male
  • Mice
  • Mice, Inbred ICR
  • Piperidines / therapeutic use
  • Polyunsaturated Alkamides
  • Pyridines / therapeutic use
  • Signal Transduction / drug effects*

Substances

  • 1,4,7,10-tetraazacyclododecane-1,4,7-triacetic acid
  • Anti-Anxiety Agents
  • Arachidonic Acids
  • Benzodioxoles
  • Cannabinoid Receptor Agonists
  • Cyclohexanols
  • Endocannabinoids
  • Glycerides
  • Heterocyclic Compounds, 1-Ring
  • JZL 184
  • PF 3845
  • Piperidines
  • Polyunsaturated Alkamides
  • Pyridines
  • Dronabinol
  • 3-(2-hydroxy-4-(1,1-dimethylheptyl)phenyl)-4-(3-hydroxypropyl)cyclohexanol
  • glyceryl 2-arachidonate
  • anandamide