Cyclopentenone Prostaglandins and Structurally Related Oxidized Lipid Species Instigate and Share Distinct Pro- and Anti-inflammatory Pathways

Cell Rep. 2020 Mar 31;30(13):4399-4417.e7. doi: 10.1016/j.celrep.2020.03.019.

Abstract

Oxidized lipids play a critical role in a variety of diseases with two faces: pro- and anti-inflammatory. The molecular mechanisms of this Janus-faced activity remain largely unknown. Here, we have identified that cyclopentenone-containing prostaglandins such as 15d-PGJ2 and structurally related oxidized phospholipid species possess a dual and opposing bioactivity in inflammation, depending on their concentration. Exposure of dendritic cells (DCs)/macrophages to low concentrations of such lipids before Toll-like receptor (TLR) stimulation instigates an anti-inflammatory response mediated by nuclear factor erythroid 2-related factor 2 (Nrf2)-dependent inhibition of nuclear factor κB (NF-κB) activation and downstream targets. By contrast, high concentrations of such lipids upon TLR activation of DCs/macrophages result in inflammatory apoptosis characterized by mitochondrial depolarization and caspase-8-mediated interleukin (IL)-1β maturation independently of Nrf2 and the classical inflammasome pathway. These results uncover unexpected pro- and anti-inflammatory activities of physiologically relevant lipid species generated by enzymatic and non-enzymatic oxidation dependent on their concentration, a phenomenon known as hormesis.

Keywords: 15d-PGJ2; IL-1β; Nrf2; OXPHOS; caspase-8; cyclopentenone prostaglandins; dendritic cells; inflammatory apoptosis; macrophages; oxidized phospholipids.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / pharmacology*
  • Apoptosis / drug effects
  • CD40 Antigens / metabolism
  • Caspase 8 / metabolism
  • Cell Death / drug effects
  • Cell Differentiation / drug effects
  • Cyclopentanes / pharmacology*
  • Dendritic Cells / drug effects
  • Dendritic Cells / metabolism
  • Inflammasomes / metabolism
  • Inflammation / genetics
  • Inflammation / pathology*
  • Interleukins / genetics
  • Kelch-Like ECH-Associated Protein 1 / metabolism
  • Lipopolysaccharides / pharmacology
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Mitogen-Activated Protein Kinases / metabolism
  • NF-E2-Related Factor 2 / metabolism
  • NF-kappa B / metabolism
  • Oxidation-Reduction
  • Phenotype
  • Prostaglandin D2 / analogs & derivatives
  • Prostaglandin D2 / chemistry
  • Prostaglandin D2 / pharmacology
  • Prostaglandins / pharmacology*
  • Signal Transduction
  • Th1 Cells / drug effects
  • Toll-Like Receptors / metabolism
  • Transcription, Genetic / drug effects
  • Up-Regulation / drug effects

Substances

  • 15-deoxyprostaglandin J2
  • Anti-Inflammatory Agents
  • CD40 Antigens
  • Cyclopentanes
  • Inflammasomes
  • Interleukins
  • Kelch-Like ECH-Associated Protein 1
  • Lipopolysaccharides
  • NF-E2-Related Factor 2
  • NF-kappa B
  • Prostaglandins
  • Toll-Like Receptors
  • Mitogen-Activated Protein Kinases
  • Caspase 8
  • cyclopentenone
  • Prostaglandin D2