Cholinergic receptor activation on epithelia protects against cytokine-induced barrier dysfunction

Acta Physiol (Oxf). 2015 Apr;213(4):846-59. doi: 10.1111/apha.12469.

Abstract

Aim: Various types of cholinergic receptors are expressed on intestinal epithelia. Their function is not completely understood. We hypothesize that cholinergic receptor activation on epithelium may serve a protective function in cytokine-induced barrier dysfunction.

Methods: The effect of cholinergic receptor activation on cellular barrier function in epithelial cells was assessed by measuring electrical impedance, and by determining para-cellular transport in transwell experiments. Cell lysates treated with cytokine and/or cholinergic agonists were analysed for cyto- and chemokine production, and tight junction (TJ) protein rearrangement was assessed. Primary colonic epithelial cells were isolated from surgically resected colon tissue of patients with inflammatory bowel disease.

Results: IL-1β induced production of chemokines (CXCL-1, CXCL-10, IL-8, CCL-7) and led to a rearrangement of TJ proteins (occludin and ZO-1). This response was inhibited by pre-treatment with muscarinic, rather than nicotinic, acetylcholine receptor agonists. Treatment with IL-1β enhanced paracellular permeability (4kD dextran) and reduced impedance across the monolayer, which was counteracted by pre-incubation with acetylcholine, or muscarinic receptor agonist bethanechol. The protective effect of acetylcholine was antagonized by atropine, underscoring muscarinic receptor involvement. IL-1β induced transcription of myosin light chain kinase and phosphorylation of myosin light chain, and this cytokine-induced phosphorylation of MLC was inhibited by muscarinic receptor agonists. Furthermore, in epithelial cells from resection material of patients with Crohn's disease and ulcerative colitis, high expression of CXCL-8 was associated with a reduced choline acetyl transferase expression, suggesting an aberrant epithelial production of ACh in inflammatory context.

Conclusion: Acetylcholine acts on muscarinic receptors on epithelial cells to maintain epithelial barrier function under inflammatory conditions.

Keywords: cholinergic receptors; epithelial permeability; interleukin-1 beta; myosin light chain; tight junction proteins.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Cell Survival
  • Cytokines / genetics
  • Cytokines / metabolism*
  • Epithelial Cells / cytology*
  • Epithelial Cells / metabolism*
  • Gene Expression Regulation / physiology
  • Humans
  • Interleukin-1beta / pharmacology
  • Mice
  • Occludin / genetics
  • Occludin / metabolism
  • Receptors, Cholinergic / genetics
  • Receptors, Cholinergic / metabolism*
  • Receptors, Muscarinic / genetics
  • Receptors, Muscarinic / metabolism
  • Tight Junctions / metabolism
  • Zonula Occludens-1 Protein / genetics
  • Zonula Occludens-1 Protein / metabolism

Substances

  • Cytokines
  • Interleukin-1beta
  • Occludin
  • Receptors, Cholinergic
  • Receptors, Muscarinic
  • Zonula Occludens-1 Protein