Cystathionine γ-lyase deficiency protects mice from galactosamine/lipopolysaccharide-induced acute liver failure

Antioxid Redox Signal. 2014 Jan 10;20(2):204-16. doi: 10.1089/ars.2013.5354. Epub 2013 Aug 22.

Abstract

Aims: Acute liver failure (ALF) is a fatal syndrome attributed to massive hepatocyte death. Hydrogen sulfide (H2S) has been reported to exert cytoprotective or cytotoxic effects. Here, we examined the role of cystathionine γ-lyase (CSE, an enzyme produces H2S) in ALF induced by D-Galactosamine (GalN) and lipopolysaccharide (LPS).

Results: Wild-type (WT) mice exhibited high mortality rate, prominent liver injury, and increased plasma alanine aminotransferase levels after GalN/LPS challenge. Congenital deficiency or chemical inhibition of CSE by DL-propargylglycine attenuated GalN/LPS-induced liver injury. CSE deficiency markedly improved survival rate and attenuated GalN/LPS-induced upregulation of inflammatory cytokines and activation of caspase 3 and poly (ADP-ribose) polymerase (PARP) in the liver. CSE deficiency protected primary hepatocytes from GalN/tumor necrosis factor-α (TNF-α)-induced cell death without affecting LPS-induced TNF-α production from primary peritoneal macrophages. Beneficial effects of CSE deficiency were associated with markedly elevated homocysteine and thiosulfate levels, upregulation of NF-E2 p45-related factor 2 (Nrf2) and antioxidant proteins, activation of Akt-dependent anti-apoptotic signaling, and inhibition of GalN/LPS-induced JNK phosphorylation in the liver. Finally, administration of sodium thiosulfate (STS) attenuated GalN/LPS-induced liver injury via activation of Akt- and Nrf2-dependent signaling and inhibition of GalN/LPS-induced JNK phosphorylation in WT mice.

Innovation: These results suggest that inhibition of CSE or administration of STS prevents acute inflammatory liver failure by augmenting thiosulfate levels and upregulating antioxidant and anti-apoptotic defense in the liver.

Conclusion: Congenital deficiency or chemical inhibition of CSE increases thiosulfate levels in the liver and prevents ALF at least in part by augmentation of antioxidant and anti-apoptotic mechanisms.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Caspase 3 / metabolism
  • Cell Survival / genetics
  • Cystathionine gamma-Lyase / deficiency*
  • Disease Models, Animal
  • Galactosamine / adverse effects*
  • Gene Expression Regulation
  • Hepatocytes / metabolism
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • Lipopolysaccharides / adverse effects*
  • Liver / drug effects
  • Liver / metabolism
  • Liver / pathology
  • Liver Failure, Acute / chemically induced*
  • Liver Failure, Acute / genetics*
  • Liver Failure, Acute / metabolism
  • Liver Failure, Acute / mortality
  • Macrophages, Peritoneal / immunology
  • Macrophages, Peritoneal / metabolism
  • Male
  • Membrane Potential, Mitochondrial / drug effects
  • Mice
  • Models, Biological
  • NF-E2-Related Factor 2 / metabolism
  • Oxidation-Reduction
  • Phosphorylation
  • Poly(ADP-ribose) Polymerases / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Quinone Reductases / metabolism
  • Sulfides / metabolism
  • Thiosulfates / pharmacology
  • Tumor Necrosis Factor-alpha / biosynthesis

Substances

  • Lipopolysaccharides
  • NF-E2-Related Factor 2
  • Proto-Oncogene Proteins c-bcl-2
  • Sulfides
  • Thiosulfates
  • Tumor Necrosis Factor-alpha
  • Galactosamine
  • Quinone Reductases
  • sulfide quinone reductase
  • Poly(ADP-ribose) Polymerases
  • Proto-Oncogene Proteins c-akt
  • JNK Mitogen-Activated Protein Kinases
  • Caspase 3
  • Cystathionine gamma-Lyase
  • sodium thiosulfate