Sulforaphane Inhibits Lipopolysaccharide-Induced Inflammation, Cytotoxicity, Oxidative Stress, and miR-155 Expression and Switches to Mox Phenotype through Activating Extracellular Signal-Regulated Kinase 1/2-Nuclear Factor Erythroid 2-Related Factor 2/Antioxidant Response Element Pathway in Murine Microglial Cells

Front Immunol. 2018 Jan 23:9:36. doi: 10.3389/fimmu.2018.00036. eCollection 2018.

Abstract

Sulforaphane (SFN) is a natural product with cytoprotective, anti-inflammatory, and antioxidant effects. In this study, we evaluated the mechanisms of its effects on lipopolysaccharide (LPS)-induced cell death, inflammation, oxidative stress, and polarization in murine microglia. We found that SFN protects N9 microglial cells upon LPS-induced cell death and suppresses LPS-induced levels of secreted pro-inflammatory cytokines, tumor necrosis factor-alpha, interleukin-1 beta, and interleukin-6. SFN is also a potent inducer of redox sensitive transcription factor, nuclear factor erythroid 2-related factor 2 (Nrf2), which is responsible for the transcription of antioxidant, cytoprotective, and anti-inflammatory genes. SFN induced translocation of Nrf2 to the nucleus via extracellular signal-regulated kinase 1/2 (ERK1/2) pathway activation. siRNA-mediated knockdown study showed that the effects of SFN on LPS-induced reactive oxygen species, reactive nitrogen species, and pro-inflammatory cytokine production and cell death are partly Nrf2 dependent. Mox phenotype is a novel microglial phenotype that has roles in oxidative stress responses. Our results suggested that SFN induced the Mox phenotype in murine microglia through Nrf2 pathway. SFN also alleviated LPS-induced expression of inflammatory microRNA, miR-155. Finally, SFN inhibits microglia-mediated neurotoxicity as demonstrated by conditioned medium and co-culture experiments. In conclusion, SFN exerts protective effects on microglia and modulates the microglial activation state.

Keywords: Mox phenotype; lipopolysaccharide; miR-155; microglia; nuclear factor erythroid 2-related factor 2; sulforaphane.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / pharmacology*
  • Antioxidant Response Elements / physiology
  • Antioxidants / pharmacology*
  • Apoptosis / drug effects
  • Cell Line
  • Coculture Techniques
  • Culture Media, Conditioned / pharmacology
  • Cytokines / metabolism
  • Enzyme Activation / drug effects
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Humans
  • Inflammation / drug therapy
  • Isothiocyanates / pharmacology*
  • Lipopolysaccharides
  • MafK Transcription Factor / metabolism
  • Mice
  • MicroRNAs / biosynthesis*
  • Microglia / metabolism*
  • NF-E2-Related Factor 2 / genetics
  • NF-E2-Related Factor 2 / metabolism*
  • Oxidative Stress / drug effects
  • RNA Interference
  • RNA, Small Interfering / genetics
  • Sulfoxides

Substances

  • Anti-Inflammatory Agents
  • Antioxidants
  • Culture Media, Conditioned
  • Cytokines
  • Isothiocyanates
  • Lipopolysaccharides
  • MafK Transcription Factor
  • Mafk protein, mouse
  • MicroRNAs
  • Mirn155 microRNA, mouse
  • NF-E2-Related Factor 2
  • Nfe2l2 protein, mouse
  • RNA, Small Interfering
  • Sulfoxides
  • Extracellular Signal-Regulated MAP Kinases
  • sulforaphane