Dihydropyrazine induces endoplasmic reticulum stress and inhibits autophagy in HepG2 human hepatoma cells

J Toxicol Sci. 2024;49(7):313-319. doi: 10.2131/jts.49.313.

Abstract

Dihydropyrazines (DHPs) are formed by non-enzymatic glycation reactions in vivo and in food. We recently reported that 3-hydro-2,2,5,6-tetramethylpyrazine (DHP-3), which is a methyl-substituted DHP, caused severe oxidative stress and cytotoxicity. However, the molecular mechanisms underlying the cytotoxic pathways of the DHP response remain elusive. Because oxidative stress induces endoplasmic reticulum (ER) stress and autophagy, we investigated the ability of DHP-3 to modulate the ER stress and autophagy pathways. DHP-3 activated the ER stress pathway by increasing inositol-requiring enzyme 1 (IRE1) and PKR-like ER kinase (PERK) phosphorylation and transcription factor 6 (ATF6) expression. Moreover, DHP-3 increased the expression of activating transcription factor 4 (ATF4) and C/EBP homologous protein (CHOP), which are downstream targets of PERK. In addition, DHP-3 inhibited the autophagy pathway by increasing the accumulation of microtubule-associated protein 1 light chain 3 alpha-phosphatidylethanolamine conjugate (LC3-II) and p62/sequestosome 1 (p62), while decreasing autophagic flux. Taken together, these results indicate that DHP-3 activates the ER stress pathway and inhibits the autophagy pathway, suggesting that the resulting removal of damaged organelles is inadequate.

Keywords: Autophagy; Dihydropyrazine; ER stress; Glycation; HepG2 cells.

MeSH terms

  • Activating Transcription Factor 4* / genetics
  • Activating Transcription Factor 4* / metabolism
  • Activating Transcription Factor 6* / genetics
  • Activating Transcription Factor 6* / metabolism
  • Autophagy* / drug effects
  • Carcinoma, Hepatocellular / metabolism
  • Carcinoma, Hepatocellular / pathology
  • Endoplasmic Reticulum Stress* / drug effects
  • Endoribonucleases / genetics
  • Endoribonucleases / metabolism
  • Hep G2 Cells
  • Humans
  • Liver Neoplasms / metabolism
  • Liver Neoplasms / pathology
  • Microtubule-Associated Proteins / metabolism
  • Oxidative Stress / drug effects
  • Phosphorylation
  • Protein Serine-Threonine Kinases* / genetics
  • Protein Serine-Threonine Kinases* / metabolism
  • Pyrazines* / pharmacology
  • Sequestosome-1 Protein / genetics
  • Sequestosome-1 Protein / metabolism
  • Signal Transduction / drug effects
  • Transcription Factor CHOP / genetics
  • Transcription Factor CHOP / metabolism
  • eIF-2 Kinase* / metabolism

Substances

  • Pyrazines
  • Activating Transcription Factor 4
  • eIF-2 Kinase
  • Activating Transcription Factor 6
  • Protein Serine-Threonine Kinases
  • ATF6 protein, human
  • Transcription Factor CHOP
  • EIF2AK3 protein, human
  • Endoribonucleases
  • ATF4 protein, human
  • ERN1 protein, human
  • DDIT3 protein, human
  • Sequestosome-1 Protein
  • Microtubule-Associated Proteins