Ethanol inhibits activation of NLRP3 and AIM2 inflammasomes in human macrophages--a novel anti-inflammatory action of alcohol

PLoS One. 2013 Nov 11;8(11):e78537. doi: 10.1371/journal.pone.0078537. eCollection 2013.

Abstract

Objective: In the pathogenesis of coronary atherosclerosis, local macrophage-driven inflammation and secretion of proinflammatory cytokines, interleukin-1β (IL-1β) in particular, are recognized as key factors. Moderate alcohol consumption is associated with a reduced risk of coronary artery disease mortality. Here we examined in cultured human macrophages whether ethanol modulates the intracellular processes involved in the secretion of IL-1β.

Results: Ethanol decreased dose-dependently the production of mature IL-1β induced by activators of the NLRP3 inflammasome, i.e. ATP, cholesterol crystals, serum amyloid A and nigericin. Ethanol had no significant effect on the expression of NLRP3 or IL1B mRNA in LPS-primed macrophages. Moreover, secretion of IL-1β was decreased in parallel with reduction of caspase-1 activation, demonstrating that ethanol inhibits inflammasome activation instead of synthesis of pro-IL-1β. Acetaldehyde, a highly reactive metabolite of ethanol, had no effect on the ATP-induced IL-1β secretion. Ethanol also attenuated the secretion of IL-1β triggered by synthetic double-stranded DNA, an activator of the AIM2 inflammasome. Ethanol conferred the inhibitory functions by attenuating the disruption of lysosomal integrity and ensuing leakage of the lysosomal protease cathepsin B and by reducing oligomerization of ASC.

Conclusion: Ethanol-induced inhibition of the NLRP3 inflammasome activation in macrophages may represent a biological pathway underlying the protective effect of moderate alcohol consumption on coronary heart disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alcohol Drinking
  • Anti-Inflammatory Agents, Non-Steroidal / pharmacology*
  • Carrier Proteins / metabolism*
  • Cell Line, Tumor
  • Central Nervous System Depressants / pharmacology
  • Coronary Disease / drug therapy
  • Coronary Disease / metabolism
  • Coronary Disease / pathology
  • DNA-Binding Proteins
  • Ethanol / pharmacology*
  • Humans
  • Inflammasomes / metabolism*
  • Interleukin-1beta / metabolism
  • Lipopolysaccharides / toxicity
  • Macrophages / metabolism*
  • Macrophages / pathology
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nuclear Proteins / metabolism*

Substances

  • AIM2 protein, human
  • Anti-Inflammatory Agents, Non-Steroidal
  • Carrier Proteins
  • Central Nervous System Depressants
  • DNA-Binding Proteins
  • IL1B protein, human
  • Inflammasomes
  • Interleukin-1beta
  • Lipopolysaccharides
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • Nuclear Proteins
  • Ethanol

Grants and funding

The study was supported by Wihuri Research Institute, maintained by the Jenny and Antti Wihuri Foundation. The study was also supported by grants from Ida Montin Foundation and Maire Lisko Foundation (K Nu). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.