Von Hippel-Lindau deficiency protects the liver against ischemia/reperfusion injury through the regulation of hypoxia-inducible factor 1α and 2α

Hepatol Commun. 2024 Nov 25;8(12):e0567. doi: 10.1097/HC9.0000000000000567. eCollection 2024 Dec 1.

Abstract

Background: Ischemia and reperfusion (I/R)-induced liver injury contributes to morbidity and mortality during hepatic surgery or liver transplantation. As a pivotal regulator of cancer and inflammation, the role of Von Hippel-Lindau (VHL) in hepatic I/R injury remains undetermined.

Methods: We investigated the role of VHL in hepatic I/R injury by generating VHL conditional knockout (VHL-KO) mice. The downstream mechanisms of VHL were confirmed, and the role of HIF-2α in hepatic I/R injury was further investigated.

Results: In this study, we discovered that VHL upregulation was associated with hepatic I/R injury in a mouse model. VHL gene knockout (VHL-KO) and overexpression (Ad-VHL) mice demonstrated that VHL aggravated liver injury, increased inflammation, and accelerated cell death in hepatic I/R injury. The VHL protein (pVHL) regulates a crucial control mechanism by targeting HIFα subunits for ubiquitin-mediated degradation. In vitro and in vivo studies demonstrated that VHL interacted with and repressed hypoxia-inducible factor 1α (HIF-1α) and hypoxia-inducible factor 2α (HIF-2α) expression during hepatic I/R injury. Notably, the inhibition of HIF-1α or 2α, as well as the concurrent inhibition of HIF-1α and 2α, abrogated the protective effect of VHL-KO. The severe stabilization of HIF-1α or 2α, as well as the simultaneous overexpression of HIF-1α and 2α, compensated for the detrimental effect of VHL.

Conclusions: Thus, we identified the VHL-HIF-1α/HIF-2α axis as an indispensable pathway that may be a novel target for mediating hepatic I/R injury.

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors* / deficiency
  • Basic Helix-Loop-Helix Transcription Factors* / genetics
  • Basic Helix-Loop-Helix Transcription Factors* / metabolism
  • Disease Models, Animal
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit* / metabolism
  • Liver* / metabolism
  • Male
  • Mice
  • Mice, Knockout*
  • Reperfusion Injury* / metabolism
  • Reperfusion Injury* / prevention & control
  • Up-Regulation
  • Von Hippel-Lindau Tumor Suppressor Protein* / genetics
  • Von Hippel-Lindau Tumor Suppressor Protein* / metabolism

Substances

  • Von Hippel-Lindau Tumor Suppressor Protein
  • Basic Helix-Loop-Helix Transcription Factors
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • endothelial PAS domain-containing protein 1
  • VHL protein, mouse
  • Hif1a protein, mouse