Upregulation of neuronal ER-phagy improves organismal fitness and alleviates APP toxicity

Cell Rep. 2024 May 28;43(5):114255. doi: 10.1016/j.celrep.2024.114255. Epub 2024 May 17.

Abstract

ER-phagy, a selective autophagy targeting the endoplasmic reticulum (ER) for lysosomal degradation through cargo receptors, plays a critical role in ER quality control and is linked to various diseases. However, its physiological and pathological roles remain largely unclear due to a lack of animal model studies. This study establishes Drosophila as an in vivo ER-phagy model. Starvation triggers ER-phagy across multiple fly tissues. Disturbing ER-phagy by either globally upregulating or downregulating ER-phagy receptors, Atl or Rtnl1, harms the fly. Notably, moderate upregulation of ER-phagy in fly brains by overexpressing Atl or Rtnl1 significantly attenuates age-associated neurodegenerations. Furthermore, in a Drosophila model of Alzheimer's disease expressing human amyloid precursor protein (APP), impaired ER-phagy is observed. Enhancing ER-phagy in the APP-expressing fly brain facilitates APP degradation, significantly alleviating disease symptoms. Therefore, our findings suggest that modulating ER-phagy may offer a therapeutic strategy to treat aging and diseases associated with ER protein aggregation.

Keywords: APP; Atg8a; Atl; CP: Cell biology; CP: Molecular biology; ER-phagy; Rtnl1; aging; cargo receptor; macro-autophagy; neurodegeneration.

MeSH terms

  • Alzheimer Disease / genetics
  • Alzheimer Disease / metabolism
  • Alzheimer Disease / pathology
  • Amyloid beta-Protein Precursor* / genetics
  • Amyloid beta-Protein Precursor* / metabolism
  • Animals
  • Autophagy*
  • Brain / metabolism
  • Brain / pathology
  • Disease Models, Animal
  • Drosophila Proteins* / genetics
  • Drosophila Proteins* / metabolism
  • Drosophila melanogaster* / metabolism
  • Endoplasmic Reticulum* / metabolism
  • Humans
  • Neurons* / metabolism
  • Up-Regulation*

Substances

  • Amyloid beta-Protein Precursor
  • Drosophila Proteins