Hepatic vagus nerve regulates Kupffer cell activation via α7 nicotinic acetylcholine receptor in nonalcoholic steatohepatitis

J Gastroenterol. 2017 Aug;52(8):965-976. doi: 10.1007/s00535-016-1304-z. Epub 2017 Jan 2.

Abstract

Background: Nonalcoholic fatty liver disease ranges from simple steatosis to nonalcoholic steatohepatitis (NASH). Kupffer cells play a central role in promoting hepatic inflammation, which leads to the development of NASH. We investigated the anti-inflammatory effect of hepatic vagus-mediated stimulation of the α7 nicotinic acetylcholine receptor (α7nAChR) on Kupffer cells in NASH pathogenesis.

Methods: Wild-type (WT) mice undergoing hepatic vagotomy (HV) were fed a methionine- and choline-deficient (MCD) diet for 1 week. α7nAChR knockout (α7KO) chimeric mice were generated by transplanting α7KO bone marrow cells into irradiated and Kupffer cell-deleted WT recipients. Kupffer cells were isolated from WT mice and treated with α7nAChR agonist under stimulation by lipopolysaccharide and/or palmitic acid.

Results: HV aggravated MCD diet-induced NASH in both steatosis and inflammation. The hepatic inflammatory response, including the upregulation of tumor necrosis factor alpha (TNFα), interleukin (IL)-12, and monocyte chemoattractant protein 1 (MCP-1), was accelerated in HV mice, accompanied by the downregulation of PPARα pathway genes. Kupffer cells were highly activated via the phosphorylation and nuclear translocation of nuclear factor-kappa B (NF-κB) in MCD diet-fed HV mice. The α7nAchR agonist suppressed the inflammatory response of primary Kupffer cells induced by lipopolysaccharide and palmitic acid by attenuating the NF-κB cascade. α7KO chimeric mice fed an MCD diet for 1 week developed advanced NASH with highly activated Kupffer cells. The hepatic expression of TNFα, IL-12, and MCP-1 was upregulated in α7KO chimeric mice, accompanied by abnormal lipid metabolism.

Conclusions: Hepatic vagus activity regulates the inflammatory response of Kupffer cells via α7nAChR in NASH development.

Keywords: Fatty liver disease; NAFLD; NASH; Vagotomy; α7nAChR.

MeSH terms

  • Animals
  • Chemokine CCL2 / genetics
  • Chimera
  • Choline / administration & dosage
  • Choline Deficiency / metabolism
  • Down-Regulation
  • Interleukin-12 Subunit p35 / genetics
  • Kupffer Cells / metabolism*
  • Lipopolysaccharides / pharmacology
  • Liver / innervation*
  • Liver / metabolism*
  • Male
  • Methionine / administration & dosage
  • Methionine / deficiency
  • Mice
  • Mice, Knockout
  • NF-kappa B / metabolism
  • Non-alcoholic Fatty Liver Disease / metabolism*
  • PPAR alpha / genetics
  • Palmitic Acid / pharmacology
  • Phosphorylation
  • Tumor Necrosis Factor-alpha / genetics
  • Up-Regulation
  • Vagotomy
  • Vagus Nerve / metabolism*
  • Vagus Nerve Stimulation
  • alpha7 Nicotinic Acetylcholine Receptor / agonists
  • alpha7 Nicotinic Acetylcholine Receptor / deficiency
  • alpha7 Nicotinic Acetylcholine Receptor / genetics
  • alpha7 Nicotinic Acetylcholine Receptor / metabolism*

Substances

  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Il12a protein, mouse
  • Interleukin-12 Subunit p35
  • Lipopolysaccharides
  • NF-kappa B
  • PPAR alpha
  • Tumor Necrosis Factor-alpha
  • alpha7 Nicotinic Acetylcholine Receptor
  • Palmitic Acid
  • Methionine
  • Choline