Vagal activities are involved in antigen-specific immune inflammation in the intestine

J Gastroenterol Hepatol. 2011 Jun;26(6):1065-71. doi: 10.1111/j.1440-1746.2011.06710.x.

Abstract

Background and aims: The mechanism of intestinal immune inflammation, such as food allergy, remains to be further understood. The present study aims to investigate the role of the vagal nerve in the pathogenesis of skewed T-helper 2 (Th2) responses in the intestine.

Methods: The expression of the immunoglobulin E (IgE) receptor on the vagus nerve in the mouse intestine was observed by immunohistochemistry. Vagus ganglion neurons (VGN) were isolated from mice and cultured in vitro. The IgE receptor/IgE complex on vagus neurons was examined by immune precipitation assay. A food allergy mouse model was developed; the effect of the partial removal of the vagal nerve (PRVn) via surgery or administration with anticholinergic agents on the suppression of Th2 inflammation was evaluated.

Results: The high-affinity IgE receptor was detected on the intestinal vagus nerve. An increase in the expression of the IgE receptor on the vagus nerve was observed in the intestines of mice with intestinal immune inflammation. Isolated mouse VGN express IgE receptor I, which could form complexes with IgE. Re-exposure to specific antigens activated the sensitized VGN, manifesting the release of transmitter glutamate that could activate dendritic cells by increasing the expression of CD80 and major compatibility complex class II and suppressing interleukin-12. The PRVn suppressed Th2 inflammation in the intestine.

Conclusions: The intestinal vagus nerve in mice expresses a high-affinity IgE receptor. An antigen-specific immune response can activate the vagus nerve in the intestine and induces the release of transmitters to modulate dendritic cell phenotypes that facilitate the development of skewed Th2 polarization in the intestine.

MeSH terms

  • Analysis of Variance
  • Animals
  • B7-1 Antigen / metabolism
  • Cells, Cultured
  • Cholinergic Antagonists / pharmacology
  • Dendritic Cells / immunology
  • Disease Models, Animal
  • Enzyme-Linked Immunosorbent Assay
  • Food Hypersensitivity / immunology*
  • Food Hypersensitivity / physiopathology
  • Food Hypersensitivity / prevention & control
  • Ganglia, Parasympathetic / immunology*
  • Ganglia, Parasympathetic / metabolism
  • Ganglia, Parasympathetic / physiopathology
  • Glutamic Acid / metabolism
  • Histocompatibility Antigens Class II / metabolism
  • Immunoglobulin E / metabolism*
  • Immunohistochemistry
  • Inflammation / immunology*
  • Inflammation / physiopathology
  • Inflammation / prevention & control
  • Interleukin-12 / metabolism
  • Intestines / innervation*
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Ovalbumin
  • Receptors, IgE / metabolism*
  • Th2 Cells / immunology
  • Vagotomy
  • Vagus Nerve / drug effects
  • Vagus Nerve / immunology*
  • Vagus Nerve / metabolism
  • Vagus Nerve / physiopathology
  • Vagus Nerve / surgery

Substances

  • B7-1 Antigen
  • Cholinergic Antagonists
  • Histocompatibility Antigens Class II
  • Receptors, IgE
  • Interleukin-12
  • Immunoglobulin E
  • Glutamic Acid
  • Ovalbumin