The RNA-Binding Protein PUM2 Impairs Mitochondrial Dynamics and Mitophagy During Aging

Mol Cell. 2019 Feb 21;73(4):775-787.e10. doi: 10.1016/j.molcel.2018.11.034. Epub 2019 Jan 11.

Abstract

Little information is available about how post-transcriptional mechanisms regulate the aging process. Here, we show that the RNA-binding protein Pumilio2 (PUM2), which is a translation repressor, is induced upon aging and acts as a negative regulator of lifespan and mitochondrial homeostasis. Multi-omics and cross-species analyses of PUM2 function show that it inhibits the translation of the mRNA encoding for the mitochondrial fission factor (Mff), thereby impairing mitochondrial fission and mitophagy. This mechanism is conserved in C. elegans by the PUM2 ortholog PUF-8. puf-8 knock-down in old nematodes and Pum2 CRISPR/Cas9-mediated knockout in the muscles of elderly mice enhances mitochondrial fission and mitophagy in both models, hence improving mitochondrial quality control and tissue homeostasis. Our data reveal how a PUM2-mediated layer of post-transcriptional regulation links altered Mff translation to mitochondrial dynamics and mitophagy, thereby mediating age-related mitochondrial dysfunctions.

Keywords: RNA binding proteins; aging; fission/fusion; mitochondria; mitochondrial dynamics; mitophagy; neurodegeneration; protein aggregation diseases; proteostasis; ribonucleoprotein granules.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Video-Audio Media

MeSH terms

  • Age Factors
  • Aging / genetics
  • Aging / metabolism*
  • Aging / pathology
  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Female
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice, Inbred C57BL
  • Mitochondria / genetics
  • Mitochondria / metabolism*
  • Mitochondria / pathology
  • Mitochondria, Muscle / metabolism
  • Mitochondria, Muscle / pathology
  • Mitochondrial Dynamics*
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism
  • Mitophagy*
  • Muscle, Skeletal / metabolism
  • Muscle, Skeletal / pathology
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism*
  • Signal Transduction
  • Up-Regulation

Substances

  • Caenorhabditis elegans Proteins
  • Membrane Proteins
  • Mff protein, human
  • Mitochondrial Proteins
  • PUF-8 protein, C elegans
  • PUM2 protein, human
  • Pum2 protein, mouse
  • RNA-Binding Proteins
  • mitochondrial fission factor, mouse