Quercetin improves cerebral ischemia/reperfusion injury by promoting microglia/macrophages M2 polarization via regulating PI3K/Akt/NF-κB signaling pathway

Biomed Pharmacother. 2023 Dec:168:115653. doi: 10.1016/j.biopha.2023.115653. Epub 2023 Oct 7.

Abstract

The modulation of microglial polarization from the pro-inflammatory M1 to the anti-inflammatory M2 phenotype shows promise as a therapeutic strategy for ischemic stroke. Quercetin, a natural flavonoid abundant in various plants, possesses anti-inflammatory, anti-apoptotic, and antioxidant properties. Nevertheless, its effect and underlying mechanism on microglia/macrophages M1/M2 polarization in the treatment of cerebral ischemia/reperfusion injury (CI/RI) remain poorly explored. In the current study, we observed that quercetin ameliorated neurological deficits, reduced infarct volume, decreased the number of M1 microglia/macrophages (CD16/32+/Iba1+), and enhanced the number of M2 microglia/macrophages (CD206+/Iba1+) after establishing the CI/RI model in rats. Subsequent in vivo and in vitro experiments indicated that quercetin downregulated M1 markers (CD86, iNOS, TNF-α, IL-1β, and IL-6) and upregulated M2 markers (CD206, Arg-1, IL-10, and TGF-β). Network pharmacology analysis and molecular docking revealed that the PI3K/Akt/NF-κB signaling pathway emerged as the core pathway. Western blot confirmed that quercetin upregulated the phosphorylation of PI3K and Akt, while alleviating the phosphorylation of IκBα and NF-κB both in vivo and in vitro. However, the PI3K inhibitor LY294002 reversed the effects of quercetin on M2 polarization and the expression of key proteins in the PI3K/Akt/NF-κB pathway in primary microglia after oxygen-glucose deprivation/reoxygenation (OGD/R) in vitro. Collectively, our findings demonstrate that quercetin facilitates microglia/macrophages M2 polarization by modulating the PI3K/Akt/NF-κB signaling pathway in the treatment of CI/RI. These findings provide novel insights into the therapeutic mechanisms of quercetin in ischemic stroke.

Keywords: Cerebral Ischemia/Reperfusion Injury; Microglia/macrophages; Neuroinflammation; PI3K/Akt/NF-κB; Polarization; Quercetin.

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / metabolism
  • Anti-Inflammatory Agents / pharmacology
  • Anti-Inflammatory Agents / therapeutic use
  • Brain Ischemia* / drug therapy
  • Brain Ischemia* / metabolism
  • Ischemic Stroke* / drug therapy
  • Macrophages / metabolism
  • Microglia
  • Molecular Docking Simulation
  • NF-kappa B / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • Quercetin / metabolism
  • Quercetin / pharmacology
  • Quercetin / therapeutic use
  • Rats
  • Reperfusion Injury* / drug therapy
  • Reperfusion Injury* / metabolism
  • Signal Transduction

Substances

  • NF-kappa B
  • Proto-Oncogene Proteins c-akt
  • Quercetin
  • Phosphatidylinositol 3-Kinases
  • Anti-Inflammatory Agents