Induction of CB1 cannabinoid receptor by inflammation in primary afferent neurons facilitates antihyperalgesic effect of peripheral CB1 agonist

Pain. 2006 Sep;124(1-2):175-83. doi: 10.1016/j.pain.2006.04.001. Epub 2006 May 18.

Abstract

Cannabinoids act on various regions in the nervous system to modulate neuronal activity including nociception. Here, we investigated CB1 receptor expression in primary afferent neurons in the dorsal root ganglion (DRG) and the efficacy of a local (intraplantar) application of the selective CB1 agonist, 2-arachidonyl-2-chloroethylamide (ACEA), on inflammatory thermal hyperalgesia. In situ hybridization showed normal CB1 mRNA expression in 28% of DRG neurons. Peripheral inflammation by CFA (complete Freund's adjuvant) significantly increased the ratio of CB1 mRNA-positive neurons to 43%, primarily with increase in NF200-negative C-fiber nociceptors. Furthermore, CB1 and TRPV1 (transient potential receptor vanilloid subtype-1) co-localization was increased from 41% before inflammation to 67% two days after inflammation. Inflammation also increased CB1 immunoreactivity in DRG neurons and in nerve fibers of the hindpaw dermis, indicating increased CB1 transport from the cell body to the peripheral nerve. The intraplantar application of ACEA attenuated CFA-induced thermal hyperalgesia. The antinociceptive properties of ACEA became more prominent at 2 days after inflammation, compared with those in non-inflamed and inflamed animals at 8 h. These results suggest that CB1 expression in primary afferent neurons is increased by inflammation and that the subsequent increase in CB1 transport to peripheral axons contributes to the increased antihyperalgesic efficacy of locally administered CB1 agonist.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analysis of Variance
  • Animals
  • Arachidonic Acids / pharmacology*
  • Freund's Adjuvant / adverse effects
  • Ganglia, Spinal / pathology
  • Gene Expression / drug effects
  • Hyperalgesia / drug therapy
  • Hyperalgesia / etiology
  • Hyperalgesia / physiopathology
  • Immunohistochemistry / methods
  • In Situ Hybridization / methods
  • Male
  • Neurofilament Proteins / genetics
  • Neurofilament Proteins / metabolism
  • Neurogenic Inflammation / chemically induced
  • Neurogenic Inflammation / drug therapy*
  • Neurogenic Inflammation / metabolism*
  • Neurogenic Inflammation / pathology
  • Neurons, Afferent / drug effects*
  • Neurons, Afferent / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Cannabinoid, CB1 / agonists*
  • Receptor, Cannabinoid, CB1 / genetics
  • Receptor, Cannabinoid, CB1 / metabolism*
  • Skin / innervation
  • Skin / metabolism
  • Time Factors
  • Transient Receptor Potential Channels / genetics
  • Transient Receptor Potential Channels / metabolism

Substances

  • Arachidonic Acids
  • Neurofilament Proteins
  • Receptor, Cannabinoid, CB1
  • Transient Receptor Potential Channels
  • arachidonyl-2-chloroethylamide
  • neurofilament protein H
  • Freund's Adjuvant