Sortilin Deficiency Reduces Ductular Reaction, Hepatocyte Apoptosis, and Liver Fibrosis in Cholestatic-Induced Liver Injury

Am J Pathol. 2017 Jan;187(1):122-133. doi: 10.1016/j.ajpath.2016.09.005. Epub 2016 Nov 11.

Abstract

Sortilin, a member of the vacuolar protein sorting 10 domain receptor family, traffics newly synthesized proteins from the trans-Golgi network to secretory pathways, endosomes, and cell surface. Sortilin-trafficked molecules, including IL-6 and acid sphingomyelinase (aSMase), mediate cholangiocyte proliferation and liver inflammation, hepatic stellate cell activation, hepatocyte apoptosis, and fibrosis. Based on these sortilin-regulated functions, we investigated its role in biliary damage leading to hepatocellular injury and fibrosis. Sortilin-/- mice displayed impaired inflammation and ductular reaction 3 days after bile duct ligation (BDL), as demonstrated by reduced cholangiocyte proliferation and activation and reduced serum IL-6. Interestingly, liver fibrosis was reduced in Sortilin-/- mice after both BDL and carbon tetrachloride treatment, in line with attenuated in vitro activation of Sortilin-/- hepatic stellate cells. Sortilin-/- hepatic aSMase activity was reduced in the BDL and carbon tetrachloride models and accompanied by reduced in vivo hepatocyte apoptosis. In addition, wild type (WT), but not Sortilin-/- hepatocytes, had increased aSMase-dependent susceptibility to bile acid-induced apoptosis in vitro. Mechanistically, short-term IL-6 neutralization in bile duct-ligated WT mice decreased hepatic inflammation and reactive cholangiocyte-derived cytokines and chemokines, without affecting fibrosis, whereas pharmacological inhibition of aSMase activity was not sufficient to attenuate hepatic fibrosis. Only combined IL-6 and aSMase inhibition significantly reduced fibrosis in bile duct-ligated WT mice. We conclude that sortilin regulates cholestatic liver damage and fibrosis via effects on both aSMase activity and serum IL-6.

MeSH terms

  • Adaptor Proteins, Vesicular Transport / deficiency*
  • Adaptor Proteins, Vesicular Transport / metabolism
  • Animals
  • Apoptosis*
  • Bile Ducts / pathology*
  • Cell Proliferation
  • Chemokines / metabolism
  • Cholestasis / complications*
  • Cholestasis / pathology
  • Hepatic Stellate Cells / metabolism
  • Hepatic Stellate Cells / pathology
  • Hepatocytes / metabolism
  • Hepatocytes / pathology*
  • Inflammation / pathology
  • Interleukin-6 / metabolism
  • Ligation
  • Liver / injuries*
  • Liver / metabolism
  • Liver / pathology
  • Liver Cirrhosis / complications
  • Liver Cirrhosis / metabolism
  • Liver Cirrhosis / pathology*
  • Mice, Inbred C57BL
  • Neutralization Tests
  • Phenotype
  • Sphingomyelin Phosphodiesterase / metabolism

Substances

  • Adaptor Proteins, Vesicular Transport
  • Chemokines
  • Interleukin-6
  • ASMase, mouse
  • Sphingomyelin Phosphodiesterase
  • sortilin