Pharmacological inhibition of the chemokine CXCL16 diminishes liver macrophage infiltration and steatohepatitis in chronic hepatic injury

PLoS One. 2014 Nov 5;9(11):e112327. doi: 10.1371/journal.pone.0112327. eCollection 2014.

Abstract

Non-alcoholic fatty liver disease (NAFLD) is a major cause of morbidity and mortality in developed countries, resulting in steatohepatitis (NASH), fibrosis and eventually cirrhosis. Modulating inflammatory mediators such as chemokines may represent a novel therapeutic strategy for NAFLD. We recently demonstrated that the chemokine receptor CXCR6 promotes hepatic NKT cell accumulation, thereby controlling inflammation in experimental NAFLD. In this study, we first investigated human biopsies (n = 20), confirming that accumulation of inflammatory cells such as macrophages is a hallmark of progressive NAFLD. Moreover, CXCR6 gene expression correlated with the inflammatory activity (ALT levels) in human NAFLD. We then tested the hypothesis that pharmacological inhibition of CXCL16 might hold therapeutic potential in NAFLD, using mouse models of acute carbon tetrachloride (CCl4)- and chronic methionine-choline-deficient (MCD) diet-induced hepatic injury. Neutralizing CXCL16 by i.p. injection of anti-CXCL16 antibody inhibited the early intrahepatic NKT cell accumulation upon acute toxic injury in vivo. Weekly therapeutic anti-CXCL16 administrations during the last 3 weeks of 6 weeks MCD diet significantly decreased the infiltration of inflammatory macrophages into the liver and intrahepatic levels of inflammatory cytokines like TNF or MCP-1. Importantly, anti-CXCL16 treatment significantly reduced fatty liver degeneration upon MCD diet, as assessed by hepatic triglyceride levels, histological steatosis scoring and quantification of lipid droplets. Moreover, injured hepatocytes up-regulated CXCL16 expression, indicating that scavenging functions of CXCL16 might be additionally involved in the pathogenesis of NAFLD. Targeting CXCL16 might therefore represent a promising novel therapeutic approach for liver inflammation and steatohepatitis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carbon Tetrachloride Poisoning / metabolism
  • Carbon Tetrachloride Poisoning / pathology
  • Chemokine CXCL16
  • Chemokine CXCL6 / biosynthesis*
  • Chemokines, CXC / biosynthesis*
  • Chronic Disease
  • Female
  • Hepatocytes / metabolism
  • Hepatocytes / pathology
  • Humans
  • Liver / metabolism*
  • Liver / pathology
  • Macrophages / metabolism*
  • Macrophages / pathology
  • Male
  • Mice
  • Non-alcoholic Fatty Liver Disease / metabolism*
  • Non-alcoholic Fatty Liver Disease / pathology
  • Receptors, Scavenger / biosynthesis*
  • Up-Regulation*

Substances

  • CXCL16 protein, human
  • Chemokine CXCL16
  • Chemokine CXCL6
  • Chemokines, CXC
  • Cxcl16 protein, mouse
  • Receptors, Scavenger

Grants and funding

This work was supported by the German Research Foundation (DFG Ta434/2-1 to F.T., DFG SFB/TRR 57) and by the Interdisciplinary Center for Clinical Research (IZKF) Aachen. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.