Ceramide, an apoptotic rheostat, inhibits CCAAT/enhancer binding protein-beta and NF-E2-related factor-2 activation: the role in glutathione S-transferase A2 gene repression

Drug Metab Dispos. 2004 Sep;32(9):893-7.

Abstract

Ceramide is a sphingolipid that acts as a second messenger in signaling systems. Sphingomyelinase generates ceramide in response to cytotoxic stimuli. CCAAT/enhancer binding protein-beta (C/EBPbeta) and NF-E2-related factor-2 (Nrf2) are both involved in the regulation of the genes encoding phase II detoxification enzymes including glutathione S-transferase (GST). In the present study, we examined the effects of ceramide on C/EBPbeta or Nrf2 activation and on the inducible GSTA2 gene transactivation. C2-ceramide (C2), a cell-permeable analog, inhibited GSTA2 induction by oltipraz or tert-butylhydroquinone (t-BHQ) in H4IIE cells, whereas dihydro-C2-ceramide (dihydro-C2), an inactive analog, had no effect. Immunoblot analysis revealed that C2 prevented increase in the level of nuclear C/EBPbeta by oltipraz, whereas the level of C/EBPbeta in total cell lysates was not changed. Increase in nuclear Nrf2 by t-BHQ was also prevented by C2 treatment. Decreases in nuclear C/EBPbeta and Nrf2 by C2 were reversed by treatment of cells with N-benzoyloxycarbonyl (Z)-Leu-Leu-leucinal (MG132), a proteasome inhibitor, verifying the previous observations that the transcription factors were degraded by the proteasome system. In another study, we found that ceramide decreased nuclear hepatic nuclear factor-1 (HNF1), whose binding to the HNF1-response element in the GSTA2 gene was responsible for the constitutive and inducible gene expression. To define the role of C/EBPbeta or Nrf2 repression in GST expression under the condition excluding the negative regulation by C2-mediated HNF1 suppression, luciferase activity was determined in the cells transfected with DeltaHNF-pGL-1651 plasmid lacking the HNF1-response element. In the cells transfected with DeltaHNF-pGL-1651, C2 decreased the luciferase induction by oltipraz or t-BHQ. Thus, ceramide inhibits C/EBPbeta or Nrf2 activation, which contributes to repression of GSTA2 gene transactivation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Apoptosis / physiology
  • CCAAT-Enhancer-Binding Protein-beta / antagonists & inhibitors*
  • CCAAT-Enhancer-Binding Protein-beta / drug effects
  • CCAAT-Enhancer-Binding Protein-beta / metabolism
  • Cell Line
  • Ceramides / chemistry
  • Ceramides / metabolism
  • Ceramides / pharmacology*
  • DNA-Binding Proteins / antagonists & inhibitors*
  • DNA-Binding Proteins / drug effects
  • DNA-Binding Proteins / metabolism
  • Gene Silencing / drug effects*
  • Gene Silencing / physiology
  • Glutathione Transferase / drug effects
  • Glutathione Transferase / genetics*
  • Glutathione Transferase / metabolism*
  • Hepatocytes / cytology
  • Hydroquinones / antagonists & inhibitors
  • Hydroquinones / pharmacology
  • Isoenzymes / genetics*
  • NF-E2-Related Factor 2
  • Pyrazines / antagonists & inhibitors
  • Pyrazines / pharmacology
  • Rats
  • Sphingolipids / chemistry
  • Sphingolipids / metabolism
  • Sphingolipids / pharmacology
  • Thiones
  • Thiophenes
  • Trans-Activators / antagonists & inhibitors*
  • Trans-Activators / drug effects
  • Trans-Activators / metabolism

Substances

  • CCAAT-Enhancer-Binding Protein-beta
  • Ceramides
  • DNA-Binding Proteins
  • Hydroquinones
  • Isoenzymes
  • NF-E2-Related Factor 2
  • Nfe2l2 protein, rat
  • Pyrazines
  • Sphingolipids
  • Thiones
  • Thiophenes
  • Trans-Activators
  • oltipraz
  • 2-tert-butylhydroquinone
  • Glutathione Transferase
  • glutathione S-transferase alpha