Rivastigmine alleviates experimentally induced colitis in mice and rats by acting at central and peripheral sites to modulate immune responses

PLoS One. 2013;8(2):e57668. doi: 10.1371/journal.pone.0057668. Epub 2013 Feb 28.

Abstract

The cholinergic anti-inflammatory system and α7 nicotinic receptors in macrophages have been proposed to play a role in neuroimmunomodulation and in the etiology of ulcerative colitis. We investigated the ability of a cholinesterase (ChE) inhibitor rivastigmine, to improve the pathology of ulcerative colitis by increasing the concentration of extracellular acetylcholine in the brain and periphery. In combination with carbachol (10 µM), rivastigmine (1 µM) significantly decreased the release of nitric oxide, TNF-α, IL-1β and IL-6 from lipopolysaccharide-activated RAW 264.7 macrophages and this effect was abolished by α7 nicotinic receptor blockade by bungarotoxin. Rivastigmine (1 mg/kg) but not (0.5 mg/kg), injected subcutaneously once daily in BALB/c mice with colitis induced by 4% dextran sodium sulphate (DSS), reduced the disease activity index (DAI) by 60% and damage to colon structure. Rivastigmine (1 mg/kg) also reduced myeloperoxidase activity and IL-6 by >60%, and the infiltration of CD11b expressing cells by 80%. These effects were accompanied by significantly greater ChE inhibition in cortex, brain stem, plasma and colon than that after 0.5 mg/kg. Co-administration of rivastigmine (1 mg/kg) with the muscarinic antagonist scopolamine significantly increased the number of CD11b expressing cells in the colon but did not change DAI compared to those treated with rivastigmine alone. Rivastigmine 1 and 2 mg given rectally to rats with colitis induced by rectal administration of 30 mg dintrobezene sulfonic acid (DNBS) also caused a dose related reduction in ChE activity in blood and colon, the number of ulcers and area of ulceration, levels of TNF-α and in MPO activity. The study revealed that the ChE inhibitor rivastigmine is able to reduce gastro-intestinal inflammation by actions at various sites at which it preserves ACh. These include ACh released from vagal nerve endings that activates alpha7 nicotinic receptors on circulating macrophages and in brainstem neurons.

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / pharmacology*
  • Anti-Inflammatory Agents / therapeutic use
  • Brain / drug effects
  • Brain / enzymology
  • Brain / immunology
  • Brain / metabolism
  • CD11b Antigen / metabolism
  • Cell Line
  • Cholinesterases / blood
  • Cholinesterases / metabolism
  • Colitis, Ulcerative / chemically induced*
  • Colitis, Ulcerative / drug therapy*
  • Colitis, Ulcerative / immunology
  • Colitis, Ulcerative / metabolism
  • Colon / immunology
  • Colon / metabolism
  • Colon / pathology
  • Crohn Disease / chemically induced*
  • Crohn Disease / drug therapy*
  • Crohn Disease / immunology
  • Crohn Disease / metabolism
  • Dextran Sulfate / adverse effects
  • Dinitrofluorobenzene / adverse effects
  • Dinitrofluorobenzene / analogs & derivatives
  • Disease Models, Animal
  • Lipopolysaccharides / pharmacology
  • Macrophages, Peritoneal / drug effects
  • Macrophages, Peritoneal / metabolism
  • Male
  • Mice
  • Nitric Oxide / metabolism
  • Peroxidase / blood
  • Peroxidase / metabolism
  • Phenylcarbamates / pharmacology*
  • Phenylcarbamates / therapeutic use
  • Rats
  • Rivastigmine
  • Thiobarbituric Acid Reactive Substances / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Anti-Inflammatory Agents
  • CD11b Antigen
  • Lipopolysaccharides
  • Phenylcarbamates
  • Thiobarbituric Acid Reactive Substances
  • Tumor Necrosis Factor-alpha
  • 2,4-dinitrofluorobenzene sulfonic acid
  • Nitric Oxide
  • Dextran Sulfate
  • Dinitrofluorobenzene
  • Peroxidase
  • Cholinesterases
  • Rivastigmine

Grants and funding

The authors have no support or funding to report.