Endocannabinoids at the spinal level regulate, but do not mediate, nonopioid stress-induced analgesia

Neuropharmacology. 2006 Mar;50(3):372-9. doi: 10.1016/j.neuropharm.2005.10.007. Epub 2005 Nov 28.

Abstract

Recent work in our laboratories has demonstrated that an opioid-independent form of stress-induced analgesia (SIA) is mediated by endogenous cannabinoids [Hohmann et al., 2005. Nature 435, 1108]. Non-opioid SIA, induced by a 3-min continuous foot shock, is characterized by the mobilization of two endocannabinoid lipids--2-arachidonoylglycerol (2-AG) and anandamide--in the midbrain periaqueductal gray (PAG). The present studies were conducted to examine the contributions of spinal endocannabinoids to nonopioid SIA. Time-dependent increases in levels of 2-AG, but not anandamide, were observed in lumbar spinal cord extracts derived from shocked relative to non-shocked rats. Notably, 2-AG accumulation was of smaller magnitude than that observed previously in the dorsal midbrain following foot shock. 2-AG is preferentially degraded by monoacylglycerol lipase (MGL), whereas anandamide is hydrolyzed primarily by fatty-acid amide hydrolase (FAAH). This metabolic segregation enabled us to manipulate endocannabinoid tone at the spinal level to further evaluate the roles of 2-AG and anandamide in nonopioid SIA. Intrathecal administration of the competitive CB1 antagonist SR141716A (rimonabant) failed to suppress nonopioid SIA, suggesting that supraspinal rather than spinal CB1 receptor activation plays a pivotal role in endocannabinoid-mediated SIA. By contrast, spinal inhibition of MGL using URB602, which selectively inhibits 2-AG hydrolysis in the PAG, enhanced SIA through a CB1-selective mechanism. Spinal inhibition of FAAH, with either URB597 or arachidonoyl serotonin (AA-5-HT), also enhanced SIA through a CB1-mediated mechanism, presumably by increasing accumulation of tonically released anandamide. Our results suggest that endocannabinoids in the spinal cord regulate, but do not mediate, nonopioid SIA.

Publication types

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

MeSH terms

  • Analgesia*
  • Analysis of Variance
  • Animals
  • Arachidonic Acids / metabolism*
  • Arachidonic Acids / pharmacology
  • Behavior, Animal
  • Benzamides / pharmacology
  • Carbamates / pharmacology
  • Dose-Response Relationship, Drug
  • Drug Interactions
  • Endocannabinoids
  • Glycerides / metabolism*
  • Male
  • Mass Spectrometry / methods
  • Pain Measurement / methods
  • Piperidines / pharmacology
  • Polyunsaturated Alkamides
  • Pyrazoles / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Reaction Time / drug effects
  • Rimonabant
  • Serotonin / analogs & derivatives
  • Serotonin / pharmacology
  • Spinal Cord / drug effects
  • Spinal Cord / metabolism*
  • Stress, Psychological / metabolism*
  • Stress, Psychological / psychology
  • Time Factors

Substances

  • Arachidonic Acids
  • Benzamides
  • Carbamates
  • Endocannabinoids
  • Glycerides
  • Piperidines
  • Polyunsaturated Alkamides
  • Pyrazoles
  • arachidonoylserotonin
  • cyclohexyl carbamic acid 3'-carbamoylbiphenyl-3-yl ester
  • Serotonin
  • glyceryl 2-arachidonate
  • Rimonabant
  • anandamide