Non-parenchymal TREM-2 protects the liver from immune-mediated hepatocellular damage

Gut. 2019 Mar;68(3):533-546. doi: 10.1136/gutjnl-2017-314107. Epub 2018 Jan 27.

Abstract

Objective: Liver injury impacts hepatic inflammation in part via Toll-like receptor (TLR) signalling. Triggering receptor expressed on myeloid cells 2 (TREM-2) modulates TLR4-mediated inflammation in bone marrow (BM)-derived macrophages but its function in liver injury is unknown. Here we hypothesised that the anti-inflammatory effects of TREM-2 on TLR signalling may limit hepatic injury.

Design: TREM-2 expression was analysed in livers of humans with various forms of liver injury compared with control individuals. Acute and chronic liver injury models were performed in wild type and Trem-2-/- mice. Primary liver cells from both genotypes of mice were isolated for in vitro experiments.

Results: TREM-2 was expressed on non-parenchymal hepatic cells and induced during liver injury in mice and man. Mice lacking TREM-2 exhibited heightened liver damage and inflammation during acute and repetitive carbon tetrachloride and acetaminophen (APAP) intoxication, the latter of which TREM-2 deficiency was remarkably associated with worsened survival. Liver damage in Trem-2-/- mice following chronic injury and APAP challenge was associated with elevated hepatic lipid peroxidation and macrophage content. BM transplantation experiments and cellular reactive oxygen species assays revealed effects of TREM-2 in the context of chronic injury depended on both immune and resident TREM-2 expression. Consistent with effects of TREM-2 on inflammation-associated injury, primary hepatic macrophages and hepatic stellate cells lacking TREM-2 exhibited augmented TLR4-driven proinflammatory responses.

Conclusion: Our data indicate that by acting as a natural brake on inflammation during hepatocellular injury, TREM-2 is a critical regulator of diverse types of hepatotoxic injury.

Keywords: acute liver failure; chronic liver disease; hepatic stellate cell; immune-mediated liver damage; inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetaminophen
  • Aged
  • Animals
  • Carbon Tetrachloride
  • Case-Control Studies
  • Female
  • Hematopoietic Stem Cells / metabolism
  • Hepatocytes / metabolism
  • Humans
  • Inflammation Mediators / metabolism
  • Kupffer Cells / metabolism
  • Lipid Peroxidation / physiology
  • Liver / metabolism*
  • Liver Cirrhosis / etiology
  • Liver Cirrhosis / immunology
  • Liver Cirrhosis / metabolism*
  • Liver Cirrhosis, Experimental / immunology
  • Liver Cirrhosis, Experimental / metabolism
  • Male
  • Membrane Glycoproteins / deficiency
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism
  • Membrane Glycoproteins / physiology*
  • Mice, Knockout
  • Middle Aged
  • Reactive Oxygen Species / metabolism
  • Receptors, Immunologic / deficiency
  • Receptors, Immunologic / genetics
  • Receptors, Immunologic / metabolism
  • Receptors, Immunologic / physiology*
  • Toll-Like Receptor 4 / physiology
  • Up-Regulation / physiology

Substances

  • Inflammation Mediators
  • Membrane Glycoproteins
  • Reactive Oxygen Species
  • Receptors, Immunologic
  • TREM2 protein, human
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • Trem2 protein, mouse
  • Acetaminophen
  • Carbon Tetrachloride