Stimulation of alpha7 nicotinic acetylcholine receptor by nicotine attenuates inflammatory response in macrophages and improves survival in experimental model of sepsis through heme oxygenase-1 induction

Antioxid Redox Signal. 2011 Jun;14(11):2057-70. doi: 10.1089/ars.2010.3555. Epub 2011 Mar 17.

Abstract

Activation of nicotinic acetylcholine receptor alpha7 subunit (α7nAChR) by nicotine leads to the improved survival rate in experimental model of sepsis. Previously, we demonstrated that heme oxygenase (HO)-1 inducers or carbon monoxide significantly increased survival of lipopolysaccharide (LPS)-induced and cecal ligation and puncture-induced septic mice by reduction of high mobility group box 1 release, a late mediator of sepsis. However, that activation of α7nAChR by nicotine provides anti-inflammatory action through HO-1 upregulation has not been elucidated. Here we show that HO-1-inducible effect by nicotine was mediated through sequential event-Ca(2+) influx, classical protein kinase C activation, and reactive oxygen species production-which activates phosphoinositol-3-kinase/Akt/Nrf-2 pathway. In addition, HO-1 is required for nicotine-mediated suppression of tumor necrosis factor-α, inducible nitric oxide synthase, and high mobility group box 1 expression induced by LPS in macrophages, as evidenced by the fact that nicotine failed to inhibit production of these mediators when HO-1 was suppressed. Importantly, nicotine-induced survival rate was reduced by inhibition of HO-1 in LPS- and cecal ligation and puncture-treated septic mice. Collectively, these data suggest that activation of α7nAChR by nicotine is critical in the regulation of anti-inflammatory process, which could be mediated through HO-1 expression. Thus, we conclude that activation of α7nAChR by nicotine provides anti-inflammatory action through HO-1 upregulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / pharmacology*
  • Calcium Signaling / drug effects
  • Cell Line
  • Endotoxemia / genetics
  • Endotoxemia / metabolism
  • Gene Expression Regulation / drug effects
  • HMGB1 Protein / metabolism
  • Heme Oxygenase-1 / antagonists & inhibitors
  • Heme Oxygenase-1 / genetics
  • Heme Oxygenase-1 / metabolism*
  • Humans
  • Inflammation / chemically induced
  • Inflammation / prevention & control*
  • Kaplan-Meier Estimate
  • Lipopolysaccharides / toxicity
  • Macrophages / drug effects*
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Inbred BALB C
  • NADPH Oxidases / metabolism
  • NF-E2-Related Factor 2 / metabolism
  • Nicotine / pharmacology*
  • Nicotinic Agonists / pharmacology*
  • Nitric Oxide Synthase Type II / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Protein Kinase C / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • Reactive Oxygen Species / metabolism
  • Receptors, Nicotinic / metabolism*
  • Sepsis / genetics
  • Sepsis / metabolism*
  • Signal Transduction / drug effects
  • Tumor Necrosis Factor-alpha / metabolism
  • alpha7 Nicotinic Acetylcholine Receptor

Substances

  • Anti-Inflammatory Agents
  • Chrna7 protein, human
  • Chrna7 protein, mouse
  • HMGB1 Protein
  • Lipopolysaccharides
  • NF-E2-Related Factor 2
  • Nfe2l2 protein, mouse
  • Nicotinic Agonists
  • Reactive Oxygen Species
  • Receptors, Nicotinic
  • Tumor Necrosis Factor-alpha
  • alpha7 Nicotinic Acetylcholine Receptor
  • Nicotine
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse
  • Heme Oxygenase-1
  • NADPH Oxidases
  • Phosphatidylinositol 3-Kinases
  • Proto-Oncogene Proteins c-akt
  • Protein Kinase C