Peripheral contribution of NGF and ASIC1a to colonic hypersensitivity in a rat model of irritable bowel syndrome

Neurogastroenterol Motil. 2013 Nov;25(11):e740-54. doi: 10.1111/nmo.12199. Epub 2013 Jul 31.

Abstract

Background: Irritable bowel syndrome (IBS) is a functional gastrointestinal disorder associated with idiopathic colonic hypersensitivity (CHS). However, recent studies suggest that low-grade inflammation could underlie CHS in IBS. The pro-inflammatory mediator nerve growth factor (NGF) plays a key role in the sensitization of peripheral pain pathways and several studies have reported its contribution to visceral pain development. NGF modulates the expression of Acid-Sensing Ion Channels (ASICs), which are proton sensors involved in sensory neurons sensitization. This study examined the peripheral contribution of NGF and ASICs to IBS-like CHS induced by butyrate enemas in the rat colon.

Methods: Colorectal distension and immunohistochemical staining of sensory neurons were used to evaluate NGF and ASICs contribution to the development of butyrate-induced CHS.

Key results: Systemic injection of anti-NGF antibodies or the ASICs inhibitor amiloride prevented the development of butyrate-induced CHS. A significant increase in NGF and ASIC1a protein expression levels was observed in sensory neurons of rats displaying butyrate-induced CHS. This increase was specific of small- and medium-diameter L1 + S1 sensory neurons, where ASIC1a was co-expressed with NGF or trkA in CGRP-immunoreactive somas. ASIC1a was also overexpressed in retrogradely labeled colon sensory neurons. Interestingly, anti-NGF antibody administration prevented ASIC1a overexpression in sensory neurons of butyrate-treated rats.

Conclusions & inferences: Our data suggest that peripheral NGF and ASIC1a concomitantly contribute to the development of butyrate-induced CHS NGF-ASIC1a interplay may have a pivotal role in the sensitization of colonic sensory neurons and as such, could be considered as a potential new therapeutic target for IBS treatment.

Keywords: acid-sensing ion channel; animal model; colonic hypersensitivity; nerve growth factor; sensory neurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acid Sensing Ion Channel Blockers / pharmacology
  • Acid Sensing Ion Channels / metabolism*
  • Amiloride / pharmacology
  • Animals
  • Disease Models, Animal
  • Ganglia, Spinal / drug effects
  • Ganglia, Spinal / metabolism*
  • Hyperalgesia / etiology*
  • Hyperalgesia / metabolism
  • Hyperalgesia / physiopathology
  • Irritable Bowel Syndrome / metabolism*
  • Irritable Bowel Syndrome / physiopathology
  • Male
  • Nerve Growth Factor / metabolism*
  • Nerve Growth Factor / pharmacology
  • Pain Measurement
  • Rats
  • Rats, Sprague-Dawley

Substances

  • Acid Sensing Ion Channel Blockers
  • Acid Sensing Ion Channels
  • Amiloride
  • Nerve Growth Factor