Suppressed basal mitophagy drives cellular aging phenotypes that can be reversed by a p62-targeting small molecule

Dev Cell. 2024 Aug 5;59(15):1924-1939.e7. doi: 10.1016/j.devcel.2024.04.020. Epub 2024 Jun 18.

Abstract

Selective degradation of damaged mitochondria by autophagy (mitophagy) is proposed to play an important role in cellular homeostasis. However, the molecular mechanisms and the requirement of mitochondrial quality control by mitophagy for cellular physiology are poorly understood. Here, we demonstrated that primary human cells maintain highly active basal mitophagy initiated by mitochondrial superoxide signaling. Mitophagy was found to be mediated by PINK1/Parkin-dependent pathway involving p62 as a selective autophagy receptor (SAR). Importantly, this pathway was suppressed upon the induction of cellular senescence and in naturally aged cells, leading to a robust shutdown of mitophagy. Inhibition of mitophagy in proliferating cells was sufficient to trigger the senescence program, while reactivation of mitophagy was necessary for the anti-senescence effects of NAD precursors or rapamycin. Furthermore, reactivation of mitophagy by a p62-targeting small molecule rescued markers of cellular aging, which establishes mitochondrial quality control as a promising target for anti-aging interventions.

Keywords: PINK1; Parkin; aging; autophagy; mitophagy; nicotinamide; nicotinamide riboside; p62; rapamycin; redox; senescence.

MeSH terms

  • Autophagy / drug effects
  • Cellular Senescence* / drug effects
  • Humans
  • Mitochondria* / drug effects
  • Mitochondria* / metabolism
  • Mitophagy* / drug effects
  • Phenotype
  • Protein Kinases / metabolism
  • RNA-Binding Proteins
  • Sequestosome-1 Protein / metabolism
  • Signal Transduction / drug effects
  • Sirolimus / pharmacology
  • Superoxides / metabolism
  • Ubiquitin-Protein Ligases* / genetics
  • Ubiquitin-Protein Ligases* / metabolism

Substances

  • Ubiquitin-Protein Ligases
  • parkin protein
  • PTEN-induced putative kinase
  • Protein Kinases
  • Sequestosome-1 Protein
  • Sirolimus
  • SQSTM1 protein, human
  • P62 protein, human
  • Superoxides
  • RNA-Binding Proteins