Omega-3 polyunsaturated fatty acids suppress the inflammatory responses of lipopolysaccharide-stimulated mouse microglia by activating SIRT1 pathways

Biochim Biophys Acta Mol Cell Biol Lipids. 2017 May;1862(5):552-560. doi: 10.1016/j.bbalip.2017.02.010. Epub 2017 Feb 22.

Abstract

Obesity and diabetes are known risk factors for dementia, and it is speculated that chronic neuroinflammation contributes to this increased risk. Microglia are brain-resident immune cells modulating the neuroinflammatory state. Eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), the major ω-3 polyunsaturated fatty acids (PUFAs) of fish oil, exhibit various effects, which include shifting microglia to the anti-inflammatory phenotype. To identify the molecular mechanisms involved, we examined the impact of EPA, DHA, and EPA+DHA on the lipopolysaccharide (LPS)-induced cytokine profiles and the associated signaling pathways in the mouse microglial line MG6. Both EPA and DHA suppressed the production of the pro-inflammatory cytokines TNF-α and IL-6 by LPS-stimulated MG6 cells, and this was also observed in LPS-stimulated BV-2 cells, the other microglial line. Moreover, the EPA+DHA mixture activated SIRT1 signaling by enhancing mRNA level of nicotinamide phosphoribosyltransferase (NAMPT), cellular NAD+ level, SIRT1 protein deacetylase activity, and SIRT1 mRNA levels in LPS-stimulated MG6. EPA+DHA also inhibited phosphorylation of the stress-associated transcription factor NF-κB subunit p65 at Ser536, which is known to enhance NF-κB nuclear translocation and transcriptional activity, including cytokine gene activation. Further, EPA+DHA increased the LC3-II/LC3-I ratio, an indicator of autophagy. Suppression of TNF-α and IL-6 production, inhibition of p65 phosphorylation, and autophagy induction were abrogated by a SIRT1 inhibitor. On the other hand, NAMPT inhibition reversed TNF-α suppression but not IL-6 suppression. Accordingly, these ω-3 PUFAs may suppress neuroinflammation through SIRT1-mediated inhibition of the microglial NF-κB stress response and ensue pro-inflammatory cytokine release, which is implicated in NAMPT-related and -unrelated pathways.

Keywords: Autophagy; Inflammation; Microglia; NF-κB; SIRT1; ω-3 PUFAs.

MeSH terms

  • Animals
  • Cytokines / biosynthesis
  • Docosahexaenoic Acids / metabolism
  • Eicosapentaenoic Acid / metabolism
  • Fatty Acids, Omega-3 / metabolism*
  • Fish Oils / metabolism
  • Inflammation / chemically induced
  • Inflammation / genetics
  • Inflammation / metabolism*
  • Inflammation / pathology
  • Lipopolysaccharides / toxicity
  • Mice
  • Microglia / drug effects
  • Microglia / metabolism*
  • Microglia / pathology
  • Nicotinamide Phosphoribosyltransferase / biosynthesis
  • Risk Factors
  • Signal Transduction
  • Sirtuin 1 / biosynthesis*
  • Sirtuin 1 / genetics
  • Tumor Necrosis Factor-alpha / biosynthesis

Substances

  • Cytokines
  • Fatty Acids, Omega-3
  • Fish Oils
  • Lipopolysaccharides
  • Tumor Necrosis Factor-alpha
  • Docosahexaenoic Acids
  • Eicosapentaenoic Acid
  • Nicotinamide Phosphoribosyltransferase
  • nicotinamide phosphoribosyltransferase, mouse
  • Sirt1 protein, mouse
  • Sirtuin 1