Ginsenoside Rg1 protects against ischemic/reperfusion-induced neuronal injury through miR-144/Nrf2/ARE pathway

Acta Pharmacol Sin. 2019 Jan;40(1):13-25. doi: 10.1038/s41401-018-0154-z. Epub 2018 Sep 27.

Abstract

Ginsenoside Rg1 (Rg1), a saponin extracted from Panax ginseng, has been well documented to be effective against ischemic/reperfusion (I/R) neuronal injury. However, the underlying mechanisms remain obscure. In the present study, we investigated the roles of Nrf2 and miR-144 in the protective effects of Rg1 against I/R-induced neuronal injury. In OGD/R-treated PC12 cells, Rg1 (0.01-1 μmol/L) dose-dependently attenuated the cell injury accompanied by prolonging nuclear accumulation of Nrf2, enhancing the transcriptional activity of Nrf2, as well as promoting the expression of ARE-target genes. The activation of the Nrf2/ARE pathway by Rg1 was independent of disassociation with Keap1, but resulted from post-translational regulations. Knockdown of Nrf2 abolished all the protective changes of Rg1 in OGD/R-treated PC12 cells. Furthermore, Rg1 treatment significantly decreased the expression of miR-144, which downregulated Nrf2 production by targeting its 3'-untranlated region after OGD/R. Knockdown of Nrf2 had no effect on the expression of miR-144, suggesting that miR-144 was an upstream regulator of Nrf2. We revealed that there was a direct binding between Nrf2 and miR-144 in PC12 cells. Application of anti-miR-144 occluded the activation of the Nrf2/ARE pathway by Rg1 in OGD/R-treated PC12 cells. In tMCAO rats, administration of Rg1 (20 mg/kg) significantly alleviated ischemic injury, and activated Nrf2/ARE pathway. The protective effects of Rg1 were abolished by injecting of AAV-HIF-miR-144-shRNA into the predicted ischemic penumbra. In conclusion, our results demonstrate that Rg1 alleviates oxidative stress after I/R through inhibiting miR-144 activity and subsequently promoting the Nrf2/ARE pathway at the post-translational level.

Keywords: Nrf2/ARE; PC12 cells; Rg1; ginsenoside; ischemic/reperfusion; miR-144; oxidative stress; stroke; tMCAO rats.

MeSH terms

  • Animals
  • Antioxidant Response Elements / genetics
  • Cell Line, Tumor
  • Down-Regulation / drug effects
  • Ginsenosides / pharmacology*
  • Infarction, Middle Cerebral Artery / drug therapy*
  • Male
  • MicroRNAs / genetics*
  • NF-E2-Related Factor 2 / metabolism
  • Neuroprotective Agents / pharmacology*
  • Rats, Sprague-Dawley
  • Reperfusion Injury / drug therapy*
  • Signal Transduction / drug effects*
  • Up-Regulation / drug effects

Substances

  • Ginsenosides
  • MIRN144 microRNA, rat
  • MicroRNAs
  • NF-E2-Related Factor 2
  • Neuroprotective Agents
  • Nfe2l2 protein, rat
  • ginsenoside Rg1