TLR2 and TLR9 modulate enteric nervous system inflammatory responses to lipopolysaccharide

J Neuroinflammation. 2016 Aug 18;13(1):187. doi: 10.1186/s12974-016-0653-0.

Abstract

Background: Accumulating evidence suggest that the enteric nervous system (ENS) plays important roles in gastrointestinal inflammatory responses, which could be in part mediated by Toll-like receptor (TLR) activation. The aim of this study was to characterise the expression and functionality of TLR2/4/9 in the ENS.

Methods: TLR2/4/9 expression was assessed in the plexuses of adult rats and embryonic ENS cultures by immunofluorescence and quantitative PCR. Following stimulation with TLR2/4/9 ligands or their combinations, activation of NF-kB, production of TNF-α, IL-6 and MCP-1 and chemoattraction of RAW264.7 macrophages were evaluated by means of Western blot, ELISA, immunofluorescence and migration assays in transwell inserts.

Results: TLR2/4/9 staining colocalised with enteric neuronal markers, whereas their presence in enteroglial processes was low to inexistent. Stimulation of ENS cultures with selective ligands induced NF-kB activation and release of cytokines and chemokines by neurons and resident immunocytes. TLR2 neutralisation before lipopolysaccharide (LPS) challenge reduced production of inflammatory mediators, whereas combination of TLR2/4 ligands promoted macrophage migration. Combined stimulation of cultures with LPS and the CpG oligonucleotide 1826 (TLR4/9 ligands) caused a synergic increase in chemoattraction and cytokine production.

Conclusions: Our results suggest that the ENS, and particularly enteric neurons, can integrate a variety of microbial signals and respond in a relatively selective fashion, depending on the particular TLRs stimulated. These findings additionally suggest that the ENS is capable of initiating a defensive response against pathogens and expanding inflammation.

Keywords: Chemoattraction; Enteric nervous system; Enteric neuron; Inflammation; TLR2; TLR4; TLR9.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies / pharmacology
  • Cells, Cultured
  • Chemokine CCL2 / metabolism
  • Disease Models, Animal
  • Embryo, Mammalian
  • Enteric Nervous System / drug effects
  • Enteric Nervous System / metabolism*
  • Enteric Nervous System / pathology
  • Female
  • Gene Expression Regulation / drug effects
  • Inflammation / chemically induced*
  • Inflammation / pathology*
  • Lipopolysaccharides / toxicity*
  • Male
  • Mice
  • NF-kappa B / metabolism
  • Neurons / drug effects
  • Neurons / metabolism
  • Pregnancy
  • Rats
  • Rats, Sprague-Dawley
  • Signal Transduction / drug effects
  • Toll-Like Receptor 2 / immunology
  • Toll-Like Receptor 2 / metabolism*
  • Toll-Like Receptor 9 / immunology
  • Toll-Like Receptor 9 / metabolism*

Substances

  • Antibodies
  • Ccl2 protein, rat
  • Chemokine CCL2
  • Lipopolysaccharides
  • NF-kappa B
  • Tlr2 protein, rat
  • Toll-Like Receptor 2
  • Toll-Like Receptor 9