P2X7 receptor-dependent intestinal afferent hypersensitivity in a mouse model of postinfectious irritable bowel syndrome

J Immunol. 2011 Aug 1;187(3):1467-74. doi: 10.4049/jimmunol.1100423. Epub 2011 Jun 22.

Abstract

The ATP-gated P2X(7) receptor (P2X(7)R) was shown to be an important mediator of inflammation and inflammatory pain through its regulation of IL-1β processing and release. Trichinella spiralis-infected mice develop a postinflammatory visceral hypersensitivity that is reminiscent of the clinical features associated with postinfectious irritable bowel syndrome. In this study, we used P2X(7)R knockout mice (P2X(7)R(-/-)) to investigate the role of P2X(7)R activation in the in vivo production of IL-1β and the development of postinflammatory visceral hypersensitivity in the T. spiralis-infected mouse. During acute nematode infection, IL-1β-containing cells and P2X(7)R expression were increased in the jejunum of wild-type (WT) mice. Peritoneal and serum IL-1β levels were also increased, which was indicative of elevated IL-1β release. However, in the P2X(7)R(-/-) animals, we found that infection had no effect upon intracellular, plasma, or peritoneal IL-1β levels. Conversely, infection augmented peritoneal TNF-α levels in both WT and P2X(7)R(-/-) animals. Infection was also associated with a P2X(7)R-dependent increase in extracellular peritoneal lactate dehydrogenase, and it triggered immunological changes in both strains. Jejunal afferent fiber mechanosensitivity was assessed in uninfected and postinfected WT and P2X(7)R(-/-) animals. Postinfected WT animals developed an augmented afferent fiber response to mechanical stimuli; however, this did not develop in postinfected P2X(7)R(-/-) animals. Therefore, our results demonstrated that P2X(7)Rs play a pivotal role in intestinal inflammation and are a trigger for the development of visceral hypersensitivity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Disease Models, Animal
  • Hypersensitivity / genetics
  • Hypersensitivity / immunology*
  • Hypersensitivity / parasitology
  • Inflammation Mediators / metabolism
  • Inflammation Mediators / physiology
  • Interleukin-1beta / metabolism
  • Intestinal Mucosa / immunology*
  • Intestinal Mucosa / parasitology*
  • Intestinal Mucosa / pathology
  • Irritable Bowel Syndrome / genetics
  • Irritable Bowel Syndrome / immunology*
  • Irritable Bowel Syndrome / parasitology
  • Macrophages, Peritoneal / immunology
  • Macrophages, Peritoneal / parasitology
  • Macrophages, Peritoneal / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Receptors, Purinergic P2X7 / deficiency
  • Receptors, Purinergic P2X7 / genetics
  • Receptors, Purinergic P2X7 / physiology*
  • Signal Transduction / genetics
  • Signal Transduction / immunology
  • Trichinella spiralis / immunology*
  • Trichinellosis / genetics
  • Trichinellosis / immunology
  • Trichinellosis / pathology
  • Visceral Afferents / immunology*
  • Visceral Afferents / parasitology
  • Visceral Afferents / pathology

Substances

  • Inflammation Mediators
  • Interleukin-1beta
  • P2rx7 protein, mouse
  • Receptors, Purinergic P2X7