A UPR-Induced Soluble ER-Phagy Receptor Acts with VAPs to Confer ER Stress Resistance

Mol Cell. 2020 Sep 17;79(6):963-977.e3. doi: 10.1016/j.molcel.2020.07.019. Epub 2020 Jul 30.

Abstract

Autophagic degradation of the endoplasmic reticulum (ER-phagy) is triggered by ER stress in diverse organisms. However, molecular mechanisms governing ER stress-induced ER-phagy remain insufficiently understood. Here we report that ER stress-induced ER-phagy in the fission yeast Schizosaccharomyces pombe requires Epr1, a soluble Atg8-interacting ER-phagy receptor. Epr1 localizes to the ER through interacting with integral ER membrane proteins VAPs. Bridging an Atg8-VAP association is the main ER-phagy role of Epr1, as it can be bypassed by an artificial Atg8-VAP tether. VAPs contribute to ER-phagy not only by tethering Atg8 to the ER membrane, but also by maintaining the ER-plasma membrane contact. Epr1 is upregulated during ER stress by the unfolded protein response (UPR) regulator Ire1. Loss of Epr1 reduces survival against ER stress. Conversely, increasing Epr1 expression suppresses the ER-phagy defect and ER stress sensitivity of cells lacking Ire1. Our findings expand and deepen the molecular understanding of ER-phagy.

Keywords: ER stress; ER-phagy; ER-plasma membrane contact; UPR; autophagy; autophagy receptor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Autophagosomes / metabolism
  • Autophagy / genetics
  • Autophagy-Related Protein 8 Family / genetics
  • Endoplasmic Reticulum / genetics
  • Endoplasmic Reticulum Stress / genetics*
  • Endoribonucleases / genetics*
  • Gene Expression Regulation, Fungal / genetics
  • Proteolysis
  • R-SNARE Proteins / genetics*
  • Schizosaccharomyces / genetics
  • Schizosaccharomyces pombe Proteins / genetics
  • Unfolded Protein Response / genetics

Substances

  • Autophagy-Related Protein 8 Family
  • R-SNARE Proteins
  • Schizosaccharomyces pombe Proteins
  • autophagy associated protein Atg8, S pombe
  • Endoribonucleases