Acid Sphingomyelinase Activation and ROS Generation Potentiate Antiproliferative Effects of Mitomycin in HCC

Int J Mol Sci. 2024 Nov 13;25(22):12175. doi: 10.3390/ijms252212175.

Abstract

Sphingolipids play a major role in the regulation of hepatocellular apoptosis and proliferation. We have previously identified sphingolipid metabolites as biomarkers of chronic liver disease and hepatocellular carcinoma. Human hepatocellular carcinoma cell lines were transfected with a plasmid vector encoding for acid sphingomyelinase. Overexpressing cells were subsequently treated with mitomycin and cell proliferation, acid sphingomyelinase activity, sphingolipid concentrations, and generation of reactive oxygen species were assessed. The stimulation of acid sphingomyelinase-overexpressing cell lines with mitomycin showed a significant activation of the enzyme (p < 0.001) followed by an accumulation of various ceramide species (p < 0.001) and reactive oxygen radicals (p < 0.001) as compared to control transfected cells. Consequently, a significant reduction in cell proliferation was observed in acid sphingomyelinase-overexpressing cells (p < 0.05) which could be diminished by the simultaneous application of antioxidant agents. Moreover, the application of mitomycin induced significant alterations in mRNA expression levels of ceramidases and sphingosine kinases (p < 0.05). Our data suggest that the overexpression of the acid sphingomyelinase in human hepatoma cell lines enhances the in vitro antiproliferative potential of mitomycin via accumulation of ceramide and reactive oxygen species. The selective activation of acid sphingomyelinase might offer a novel therapeutic approach in the treatment of hepatocellular carcinoma.

Keywords: ASM; ceramide; hepatocellular carcinoma; reactive oxygen species; sphingolipids.

MeSH terms

  • Apoptosis / drug effects
  • Carcinoma, Hepatocellular* / drug therapy
  • Carcinoma, Hepatocellular* / genetics
  • Carcinoma, Hepatocellular* / metabolism
  • Carcinoma, Hepatocellular* / pathology
  • Cell Line, Tumor
  • Cell Proliferation* / drug effects
  • Ceramides* / metabolism
  • Enzyme Activation / drug effects
  • Humans
  • Liver Neoplasms* / drug therapy
  • Liver Neoplasms* / genetics
  • Liver Neoplasms* / metabolism
  • Liver Neoplasms* / pathology
  • Mitomycin* / pharmacology
  • Reactive Oxygen Species* / metabolism
  • Sphingomyelin Phosphodiesterase* / genetics
  • Sphingomyelin Phosphodiesterase* / metabolism

Substances

  • Sphingomyelin Phosphodiesterase
  • Mitomycin
  • Reactive Oxygen Species
  • Ceramides