Sorafenib attenuates liver fibrosis by triggering hepatic stellate cell ferroptosis via HIF-1α/SLC7A11 pathway

Cell Prolif. 2022 Jan;55(1):e13158. doi: 10.1111/cpr.13158. Epub 2021 Nov 22.

Abstract

Objectives: Evidences demonstrate that sorafenib alleviates liver fibrosis via inhibiting HSC activation and ECM accumulation. The underlying mechanism remains unclear. Ferroptosis, a novel programmed cell death, regulates diverse physiological/pathological processes. In this study, we aim to investigate the functional role of HSC ferroptosis in the anti-fibrotic effect of sorafenib.

Materials and methods: The effects of sorafenib on HSC ferroptosis and ECM expression were assessed in mouse model of liver fibrosis induced by CCl4 . In vitro, Fer-1 and DFO were used to block ferroptosis and then explored the anti-fibrotic effect of sorafenib by detecting α-SMA, COL1α1 and fibronectin proteins. Finally, HIF-1α siRNA, plasmid and stabilizers were applied to assess related signalling pathway.

Results: Sorafenib attenuated liver injury and ECM accumulation in CCl4 -induced fibrotic livers, accompanied by reduction of SLC7A11 and GPX4 proteins. In sorafenib-treated HSC-T6 cells, ferroptotic events (depletion of SLC7A11, GPX4 and GSH; accumulation iron, ROS and MDA) were discovered. Intriguingly, these ferroptotic events were not appeared in hepatocytes or macrophages. Sorafenib-elicited HSC ferroptosis and ECM reduction were abrogated by Fer-1 and DFO. Additionally, both HIF-1α and SLC7A11 proteins were reduced in sorafenib-treated HSC-T6 cells. SLC7A11 was positively regulated by HIF-1α, inactivation of HIF-1α/SLC7A11 pathway was required for sorafenib-induced HSC ferroptosis, and elevation of HIF-1α could inhibit ferroptosis, ultimately limited the anti-fibrotic effect.

Conclusions: Sorafenib triggers HSC ferroptosis via HIF-1α/SLC7A11 signalling, which in turn attenuates liver injury and fibrosis.

Keywords: HIF-1α/SLC7A11; HSCs; ferroptosis; liver fibrosis; sorafenib.

MeSH terms

  • Actins / metabolism
  • Amino Acid Transport System y+ / metabolism*
  • Animals
  • Cell Line
  • Collagen Type I / metabolism
  • Ferroptosis* / drug effects
  • Hepatic Stellate Cells / drug effects
  • Hepatic Stellate Cells / metabolism
  • Hepatic Stellate Cells / pathology*
  • Hepatocytes / drug effects
  • Hepatocytes / metabolism
  • Hepatocytes / pathology
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Liver Cirrhosis / drug therapy*
  • Liver Cirrhosis / pathology
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Macrophages / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Models, Biological
  • Protein Stability / drug effects
  • Signal Transduction* / drug effects
  • Sorafenib / pharmacology
  • Sorafenib / therapeutic use*

Substances

  • Acta2 protein, mouse
  • Actins
  • Amino Acid Transport System y+
  • Collagen Type I
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Slc7a11 protein, mouse
  • Sorafenib