IL-17a exacerbates hepatic ischemia-reperfusion injury in fatty liver by promoting neutrophil infiltration and mitochondria-driven apoptosis

J Leukoc Biol. 2020 Nov;108(5):1603-1613. doi: 10.1002/JLB.3MA0520-716R. Epub 2020 Jun 12.

Abstract

Hepatic ischemia-reperfusion (IR) injury is a critical issue during liver transplantation (LT). Recent studies have demonstrated that IL-17a contributes to IR injury and steatohepatitis. However, the underlying mechanism is not understood. This study aimed to examine the role of IL-17a on hepatic IR injury in fatty liver and to investigate the underlying mechanisms. The correlation between serum IL-17a levels and liver function was analyzed in LT patients receiving fatty (n = 42) and normal grafts (n = 44). Rat LT model was applied to validate the clinical findings. IL-17a knockout (KO) and wild-type mice were fed with high-fat diets to induce fatty liver and subjected to hepatic IR injury with major hepatectomy. Frequency of circulating neutrophils and IL-17a expression on PBMCs were analyzed by flow cytometry. Mitochondrial outer membrane permeabilization (MOMP) was examined by a living intravital image system. Serum IL-17a was elevated after human LT, especially with fatty grafts. The aspartate aminotransferase and alanine transaminase levels were increased in recipients with fatty grafts compared with normal grafts. In rat LT model, the intragraft IL-17a expression was significantly higher in fatty grafts than normal ones post-LT. KO of IL-17a in mice notably attenuated liver damage after IR injury in fatty liver, characterized by better-preserved liver architecture, improved liver function, and reduced neutrophil infiltration. MOMP triggered cell death after hepatic IR injury in a caspase-independent way via IL-17a/NF-κB signaling pathway. KO of IL-17a protected the fatty liver against IR injury through the suppression of neutrophil infiltration and mitochondria-driven apoptosis.

Keywords: MOMP; NF-κB signaling; apoptosis; inflammation; liver transplantation; neutrophils.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / immunology*
  • Fatty Liver / immunology*
  • Fatty Liver / pathology
  • Female
  • Humans
  • Interleukin-17 / immunology*
  • Male
  • Mitochondria, Liver / immunology*
  • Mitochondria, Liver / pathology
  • Neutrophil Infiltration*
  • Neutrophils / immunology*
  • Neutrophils / pathology
  • Rats
  • Rats, Sprague-Dawley
  • Reperfusion Injury / immunology*
  • Reperfusion Injury / pathology

Substances

  • IL17A protein, human
  • Il17a protein, rat
  • Interleukin-17