Metformin Inhibits the Production of Reactive Oxygen Species from NADH:Ubiquinone Oxidoreductase to Limit Induction of Interleukin-1β (IL-1β) and Boosts Interleukin-10 (IL-10) in Lipopolysaccharide (LPS)-activated Macrophages

J Biol Chem. 2015 Aug 14;290(33):20348-59. doi: 10.1074/jbc.M115.662114. Epub 2015 Jul 7.

Abstract

Metformin, a frontline treatment for type II diabetes mellitus, decreases production of the pro-form of the inflammatory cytokine IL-1β in response to LPS in macrophages. We found that it specifically inhibited pro-IL-1β production, having no effect on TNF-α. Furthermore, metformin boosted induction of the anti-inflammatory cytokine IL-10 in response to LPS. We ruled out a role for AMP-activated protein kinase (AMPK) in the effect of metformin because activation of AMPK with A769662 did not mimic metformin here. Furthermore, metformin was still inhibitory in AMKPα1- or AMPKβ1-deficient cells. The activity of NADH:ubiquinone oxidoreductase (complex I) was inhibited by metformin. Another complex I inhibitor, rotenone, mimicked the effect of metformin on pro-IL-1β and IL-10. LPS induced reactive oxygen species production, an effect inhibited by metformin or rotenone pretreatment. MitoQ, a mitochondrially targeted antioxidant, decreased LPS-induced IL-1β without affecting TNF-α. These results, therefore, implicate complex I in LPS action in macrophages.

Keywords: AMP-activated kinase (AMPK); IL-1; LPS; complex I; metformin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenylate Kinase / genetics
  • Adenylate Kinase / metabolism
  • Animals
  • Electron Transport Complex I / metabolism*
  • Interleukin-10 / biosynthesis*
  • Interleukin-1beta / biosynthesis*
  • Lipopolysaccharides / antagonists & inhibitors
  • Lipopolysaccharides / pharmacology*
  • Macrophage Activation / drug effects
  • Macrophages / drug effects*
  • Macrophages / metabolism
  • Metformin / pharmacology*
  • Mice
  • Mice, Inbred C57BL
  • Reactive Oxygen Species / metabolism*
  • Rotenone / pharmacology

Substances

  • Interleukin-1beta
  • Lipopolysaccharides
  • Reactive Oxygen Species
  • Rotenone
  • Interleukin-10
  • Metformin
  • Adenylate Kinase
  • Electron Transport Complex I