HUWE1 controls MCL1 stability to unleash AMBRA1-induced mitophagy

Cell Death Differ. 2020 Apr;27(4):1155-1168. doi: 10.1038/s41418-019-0404-8. Epub 2019 Aug 21.

Abstract

Receptor-mediated mitophagy is a crucial process involved in mitochondria quality control. AMBRA1 is a mitophagy receptor for the selective removal of damaged mitochondria in mammalian cells. A critical unresolved issue is how AMBRA1-mediated mitophagy is controlled in response to cellular stress. Here, we investigated the role of BCL2-family proteins on AMBRA1-dependent mitophagy and showed that MCL1 delays AMBRA1-dependent mitophagy. Indeed, MCL1 overexpression is sufficient to inhibit recruitment to mitochondria of the E3 Ubiquitin ligase HUWE1, a crucial dynamic partner of AMBRA1, upon AMBRA1-mediated mitophagy induction. In addition, we found that during mitophagy induced by AMBRA1, MCL1 levels decreased but were sustained by inhibition of the GSK-3β kinase, which delayed AMBRA1-mediated mitophagy. Also, we showed that MCL1 was phosphorylated by GSK-3β at a conserved GSK-3 phosphorylation site (S159) during AMBRA1-mediated mitophagy and that this event was accompanied by HUWE1-dependent MCL1 degradation. Altogether, our results demonstrate that MCL1 stability is regulated by the kinase GSK-3β and the E3 ubiquitin ligase HUWE1 in regulating AMBRA1-mediated mitophagy. Our work thus defines MCL1 as an upstream stress-sensitive protein, functional in AMBRA1-mediated mitophagy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism*
  • Antigens, CD34 / metabolism
  • Apoptosis
  • Clone Cells
  • Glycogen Synthase Kinase 3 beta / metabolism
  • HeLa Cells
  • Humans
  • MCF-7 Cells
  • Mitochondria / metabolism
  • Mitophagy*
  • Models, Biological
  • Myeloid Cell Leukemia Sequence 1 Protein / metabolism*
  • Phosphorylation
  • Phosphoserine / metabolism
  • Protein Stability
  • Protein Transport
  • Proteolysis
  • Tumor Suppressor Proteins / metabolism*
  • Ubiquitin-Protein Ligases / metabolism*
  • Ubiquitination

Substances

  • AMBRA1 protein, human
  • Adaptor Proteins, Signal Transducing
  • Antigens, CD34
  • MCL1 protein, human
  • Myeloid Cell Leukemia Sequence 1 Protein
  • Tumor Suppressor Proteins
  • Phosphoserine
  • HUWE1 protein, human
  • Ubiquitin-Protein Ligases
  • Glycogen Synthase Kinase 3 beta