Disrupted stress-induced analgesia in a neuropathic pain state is rescued by the endocannabinoid degradation inhibitor JZL195

J Neurochem. 2024 Nov;168(11):3801-3812. doi: 10.1111/jnc.16146. Epub 2024 Jun 22.

Abstract

Acute stress normally engages descending brain pathways to produce an antinociceptive response, known as stress-induced analgesia. Paradoxically, these descending pain modulatory pathways are also involved in the maintenance of the abnormal pain associated with chronic neuropathic pain. It remains unclear how stress-induced analgesia is affected by neuropathic pain states. We therefore examined the impact of a chronic constriction nerve-injury (CCI) model of neuropathic pain on restraint stress-induced analgesia in C57BL/6 mice. Thirty minutes of restraint stress produced analgesia in the hotplate thermal nociceptive assay that was less in CCI compared to control mice who underwent a sham-surgery. In sham but not CCI mice, stress-induced analgesia was reduced by the opioid receptor antagonist naltrexone. The cannabinoid CB1 receptor antagonist AM281 did not affect stress-induced analgesia in either sham or CCI mice. Low-dose pre-treatment with the dual fatty acid amide hydrolase and monoacylglycerol lipase inhibitor JZL195 increased stress-induced analgesia in CCI but not sham mice. The JZL195 enhancement of stress-induced analgesia in CCI mice was abolished by AM281 but was unaffected by naltrexone. These findings indicate that the acute opioid-mediated analgesic response to a psychological stressor is disrupted in a nerve-injury model of neuropathic pain. Importantly, this impairment of stress-induced analgesia was rescued by blockade of endocannabinoid breakdown via a cannabinoid CB1 receptor dependent mechanism. These findings suggest that subthreshold treatment with endocannabinoid degradation blockers could be used to alleviate the disruption of endogenous pain control systems in a neuropathic pain state.

Keywords: analgesia; cannabinoid; endogenous; neuropathic pain; stress.

MeSH terms

  • Amidohydrolases / antagonists & inhibitors
  • Analgesia / methods
  • Animals
  • Carbamates
  • Endocannabinoids* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • Monoacylglycerol Lipases / antagonists & inhibitors
  • Monoacylglycerol Lipases / metabolism
  • Morpholines
  • Naltrexone / analogs & derivatives
  • Naltrexone / pharmacology
  • Narcotic Antagonists / pharmacology
  • Neuralgia* / drug therapy
  • Neuralgia* / metabolism
  • Pain Measurement / drug effects
  • Pain Measurement / methods
  • Piperazines
  • Piperidines / pharmacology
  • Piperidines / therapeutic use
  • Pyrazoles / pharmacology
  • Receptor, Cannabinoid, CB1 / antagonists & inhibitors
  • Receptor, Cannabinoid, CB1 / metabolism
  • Restraint, Physical
  • Stress, Psychological* / complications

Substances

  • Endocannabinoids
  • JZL195
  • Naltrexone
  • Narcotic Antagonists
  • Monoacylglycerol Lipases
  • AM 281
  • Receptor, Cannabinoid, CB1
  • Amidohydrolases
  • Pyrazoles
  • Piperidines
  • fatty-acid amide hydrolase
  • Carbamates
  • Morpholines
  • Piperazines