The Reg3α (HIP/PAP) Lectin Suppresses Extracellular Oxidative Stress in a Murine Model of Acute Liver Failure

PLoS One. 2015 May 4;10(5):e0125584. doi: 10.1371/journal.pone.0125584. eCollection 2015.

Abstract

Background and aims: Acute liver failure (ALF) is a rapidly progressive heterogeneous illness with high mortality rate and no widely accessible cure. A promising drug candidate according to previous preclinical studies is the Reg3α (or HIP/PAP) lectin, which alleviates ALF through its free-radical scavenging activity. Here we study the therapeutic targets of Reg3α in order to gain information on the nature of the oxidative stress associated with ALF.

Methods: Primary hepatocytes stressed with the reactive oxygen species (ROS) inducers TNFα and H2O2 were incubated with a recombinant Reg3α protein. ALF was induced in C57BL/6J mice by an anti-CD95 antibody. Livers and primary hepatocytes were harvested for deoxycholate separation of cellular and extracellular fractions, immunostaining, immunoprecipitation and malondialdehyde assays. Fibrin deposition was studied by immunofluorescence in frozen liver explants from patients with ALF.

Results: Fibrin deposition occurs during experimental and clinical acute liver injuries. Reg3α bound the resulting transient fibrin network, accumulated in the inflammatory extracellular matrix (ECM), greatly reduced extracellular ROS levels, and improved cell viability. Hepatocyte treatment with ligands of death receptors, e.g. TNFα and Fas, resulted in a twofold increase of malondialdehyde (MDA) level in the deoxycholate-insoluble fractions. Reg3α treatment maintained MDA at a level similar to control cells and thereby increased hepatocyte survival by 35%. No antioxidant effect of Reg3α was noted in the deoxycholate-soluble fractions. Preventing fibrin network formation with heparin suppressed the prosurvival effect of Reg3α.

Conclusions: Reg3α is an ECM-targeted ROS scavenger that binds the fibrin scaffold resulting from hepatocyte death during ALF. ECM alteration is an important pathogenic factor of ALF and a relevant target for pharmacotherapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Animals
  • Antigens, Neoplasm / metabolism*
  • Biomarkers, Tumor / metabolism*
  • Cells, Cultured
  • Disease Models, Animal
  • Extracellular Matrix / metabolism
  • Extracellular Space / metabolism*
  • Female
  • Fibrin / metabolism
  • Hepatocytes / metabolism
  • Humans
  • Lectins, C-Type / metabolism*
  • Liver Failure, Acute / metabolism*
  • Liver Failure, Acute / pathology*
  • Male
  • Mice, Inbred C57BL
  • Middle Aged
  • Models, Biological
  • Oxidative Stress*
  • Pancreatitis-Associated Proteins
  • fas Receptor / metabolism

Substances

  • Antigens, Neoplasm
  • Biomarkers, Tumor
  • Lectins, C-Type
  • Pancreatitis-Associated Proteins
  • REG3A protein, human
  • fas Receptor
  • Fibrin

Grants and funding

This work was supported by the French National Research Agency ANR (Programs RIB 00801 and Tecsan 01502 to J. Faivre), the European Commission (project “MODHEP” to J. Faivre), the French National Cancer Institute (INCa Grant 2009-PAIR- INCa to J. Faivre). The authors P. Amouyal and G. Amouyal received salary from Alfact Innovation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.