Corticosterone mediates reciprocal changes in CB 1 and TRPV1 receptors in primary sensory neurons in the chronically stressed rat

Gastroenterology. 2011 Feb;140(2):627-637.e4. doi: 10.1053/j.gastro.2010.11.003. Epub 2010 Nov 9.

Abstract

Background & aims: Chronic stress is associated with visceral hyperalgesia in functional gastrointestinal disorders. We investigated whether corticosterone plays a role in chronic psychological stress-induced visceral hyperalgesia.

Methods: Male rats were subjected to 1-hour water avoidance (WA) stress or subcutaneous corticosterone injection daily for 10 consecutive days in the presence or absence of corticoid-receptor antagonist RU-486 and cannabinoid-receptor agonist WIN55,212-2. The visceromotor response to colorectal distension was measured. Receptor protein levels were measured and whole-cell patch-clamp recordings were used to assess transient receptor potential vanilloid type 1 (TRPV1) currents in L6-S2 dorsal root ganglion (DRG) neurons. Mass spectrometry was used to measure endocannabinoid anandamide content.

Results: Chronic WA stress was associated with visceral hyperalgesia in response to colorectal distension, increased stool output and reciprocal changes in cannabinoid receptor 1 (CB1) (decreased) and TRPV1 (increased) receptor expression and function. Treatment of WA stressed rats with RU-486 prevented these changes. Control rats treated with serial injections of corticosterone in situ showed a significant increase in serum corticosterone associated with visceral hyperalgesia, enhanced anandamide content, increased TRPV1, and decreased CB1 receptor protein levels, which were prevented by co-treatment with RU-486. Exposure of isolated control L6-S2 DRGs in vitro to corticosterone reproduced the changes in CB1 and TRPV1 receptors observed in situ, which was prevented by co-treatment with RU-486 or WIN55,212-2.

Conclusions: These results support a novel role for corticosterone to modulate CB1 and TRPV1-receptor pathways in L6-S2 DRGs in the chronic WA stressed rat, which contributes to visceral hyperalgesia observed in this model.

Publication types

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

MeSH terms

  • Animals
  • Benzoxazines / pharmacology
  • Chronic Disease
  • Colon / drug effects
  • Colon / metabolism
  • Corticosterone / pharmacology
  • Corticosterone / physiology*
  • Disease Models, Animal
  • Feces
  • Ganglia, Spinal / drug effects
  • Hyperalgesia / etiology
  • Hyperalgesia / metabolism*
  • Male
  • Mifepristone / pharmacology
  • Morpholines / pharmacology
  • Naphthalenes / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Cannabinoid, CB1 / analysis
  • Receptor, Cannabinoid, CB1 / metabolism*
  • Receptors, Glucocorticoid / antagonists & inhibitors
  • Sensory Receptor Cells / chemistry
  • Sensory Receptor Cells / drug effects*
  • Sensory Receptor Cells / metabolism
  • Stress, Psychological / complications*
  • Stress, Psychological / metabolism
  • TRPV Cation Channels / analysis
  • TRPV Cation Channels / metabolism*

Substances

  • Benzoxazines
  • Morpholines
  • Naphthalenes
  • Receptor, Cannabinoid, CB1
  • Receptors, Glucocorticoid
  • TRPV Cation Channels
  • Trpv1 protein, rat
  • Mifepristone
  • (3R)-((2,3-dihydro-5-methyl-3-((4-morpholinyl)methyl)pyrrolo-(1,2,3-de)-1,4-benzoxazin-6-yl)(1-naphthalenyl))methanone
  • Corticosterone