The PERK/Nrf2 pathway mediates endoplasmic reticulum stress-induced injury by upregulating endoplasmic reticulophagy in H9c2 cardiomyoblasts

Life Sci. 2019 Nov 15:237:116944. doi: 10.1016/j.lfs.2019.116944. Epub 2019 Oct 8.

Abstract

Aims: Endoplasmic reticulum stress (ERS) is an evolutionarily conserved cell stress response. Recently, it was found that ERS induces not only apoptosis but also endoplasmic reticulophagy (ER-phagy). A previous study demonstrated that inhibition of ER-phagy alleviates cell injury. The purpose of this study was to investigate the involvement of the protein kinase R-like ER kinase (PERK)/nuclear factor erythroid 2-related factor 2 (Nrf2) pathway in ERS-induced ER-phagy in H9c2 cardiomyoblasts. To address this aim, cells were treated with ERS inhibitors and a Nrf2 inhibitor before establishment of thapsigargin (TG)- or tunicamycin (TM)-induced ERS models in H9c2 cardiomyoblasts.

Main methods: Transmission electron microscopy and immunofluorescence staining were used to detect ER-phagy. Western blotting was employed to detect the levels of calreticulin (CRT), total and phosphorylated PERK, nuclear Nrf2, activated transcription factor 4 (ATF4), light chain 3B (LC3B)-II and Beclin 1. Immunofluorescence staining was used to assess subcellular location of Nrf2.

Key finding: TG or TM induced H9c2 cell injury and ER-phagy and upregulated CRT expression, PERK phosphorylation, Nrf2 nuclear translocation, and expression of ATF4, Beclin 1, and LC3B-II compared with control cells. Treatment with ERS inhibitors decreased TG- or TM-induced ER-phagy, downregulated CRT expression, PERK phosphorylation, Nrf2 nuclear translocation and the expression of ATF4, Beclin 1 and LC3B-II. Moreover, a Nrf2 inhibitor downregulated the expression of ATF4, Beclin 1 and LC3B-II and alleviated TG- or TM-induced ER-phagy and H9c2 cell injury.

Significance: These findings suggest that the PERK/Nrf2 pathway mediates upregulation of ER-phagy, thereby inducing cell injury in H9c2 cardiomyoblasts.

Keywords: Endoplasmic reticulophagy; Endoplasmic reticulum stress; H9c2 cell; Nuclear factor erythroid 2-related factor 2; Protein kinase R-like ER kinase.

MeSH terms

  • Activating Transcription Factor 4 / metabolism
  • Animals
  • Apoptosis*
  • Beclin-1 / metabolism
  • Cells, Cultured
  • Endoplasmic Reticulum / metabolism
  • Endoplasmic Reticulum / pathology*
  • Endoplasmic Reticulum Stress*
  • Microtubule-Associated Proteins / metabolism
  • Myocytes, Cardiac / metabolism
  • Myocytes, Cardiac / pathology*
  • NF-E2-Related Factor 2 / metabolism*
  • Oxidative Stress*
  • Phosphorylation
  • Rats
  • Signal Transduction
  • eIF-2 Kinase / metabolism*

Substances

  • Atf4 protein, rat
  • Beclin-1
  • Becn1 protein, rat
  • LC3 protein, rat
  • Microtubule-Associated Proteins
  • NF-E2-Related Factor 2
  • Nfe2l2 protein, rat
  • Activating Transcription Factor 4
  • PERK kinase
  • eIF-2 Kinase