PORIMIN: The key to (+)-Usnic acid-induced liver toxicity and oncotic cell death in normal human L02 liver cells

J Ethnopharmacol. 2021 Apr 24:270:113873. doi: 10.1016/j.jep.2021.113873. Epub 2021 Jan 21.

Abstract

Ethnopharmacological relevance: Usnic acid (UA) is one of the well-known lichen metabolites that induces liver injury. It is mainly extracted from Usnea longissima and U. diffracta in China or from other lichens in other countries. U. longissima has been used as traditional Chinese medicine for treatment of cough, pain, indigestion, wound healing and infection. More than 20 incidences with hepatitis and liver failure have been reported by the US Food and Drug Administration since 2000. UA is an uncoupler of oxidative phosphorylation causing glutathione and ATP depletion. Previous histological studies observed extensive cell and organelle swellings accompanied with hydrotropic vacuolization of hepatocytes.

Aim of the study: This study was to investigate the mechanism of UA-induced liver toxicity in normal human L02 liver cells and ICR mice using various techniques, such as immunoblotting and siRNA transfection.

Materials and methods: Assays were performed to evaluate the oxidative stress and levels of GSH, MDA and SOD. Double flouresencence staining was used for the detection of apoptotic cell death. The protein expressions, such as glutathione S transferase, glutathione reductase, glutathione peroxidase 4, catalase, c-Jun N-terminal protein kinase, caspases, gastamin-D and porimin were detected by Western blotting. Comparisons between transfected and non-transfected cells were applied for the elucidation of the role of porimin in UA-induced hepatotoxicity. Histopathological examination of mice liver tissue, serum total bilirubin and hepatic enzymes of alanine aminotransferase and aspatate aminotransferase were also studied.

Results: The protein expressions of glutathione reductase, glutathione S transferase and glutathione peroxidase-4 were increased significantly in normal human L02 liver cells. Catalase expression was diminished in dose-dependent manner. Moreover, (+)-UA did not induce the activation of caspase-3, caspase-1 or gasdermin-D. No evidence showed the occurrence of pyroptosis. However, the porimin expressions were increased significantly. In addition, (+)-UA caused no cytotoxicity in the porimin silencing L02 cells.

Conclusions: In conclusion, (+)-UA induces oncotic L02 cell death via increasing protein porimin and the formation of irreversible membrane pores. This may be the potential research area for future investigation in different aspects especially bioactivity and toxicology.

Keywords: Gasdermin-D; Hepatotoxicity; Oncotic cell death; Porimin; Usnea.

MeSH terms

  • Animals
  • Anti-Infective Agents / toxicity*
  • Benzofurans / toxicity*
  • Caspase Inhibitors / pharmacology
  • Caspases / metabolism
  • Cell Death / drug effects
  • Cell Line
  • Cell Survival / drug effects
  • Chemical and Drug Induced Liver Injury / metabolism*
  • Chemical and Drug Induced Liver Injury / pathology
  • Gene Knockdown Techniques
  • Glutathione / metabolism
  • Glutathione / pharmacology
  • Hepatocytes / drug effects*
  • Hepatocytes / metabolism*
  • Humans
  • Intracellular Signaling Peptides and Proteins / drug effects
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Ischemia / chemically induced
  • Ischemia / metabolism*
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • Liver / drug effects
  • Liver / pathology
  • Mice
  • Mice, Inbred ICR
  • Necrosis / chemically induced
  • Oxidative Stress / drug effects
  • Phosphate-Binding Proteins / metabolism
  • Receptors, Cell Surface / drug effects
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*

Substances

  • Anti-Infective Agents
  • Benzofurans
  • Caspase Inhibitors
  • GSDMD protein, human
  • Intracellular Signaling Peptides and Proteins
  • Phosphate-Binding Proteins
  • Receptors, Cell Surface
  • TMEM123 protein, human
  • usnic acid
  • JNK Mitogen-Activated Protein Kinases
  • Caspases
  • Glutathione