Mitochondrial E3 ubiquitin ligase MARCH5 controls mitochondrial fission and cell sensitivity to stress-induced apoptosis through regulation of MiD49 protein

Mol Biol Cell. 2016 Jan 15;27(2):349-59. doi: 10.1091/mbc.E15-09-0678. Epub 2015 Nov 12.

Abstract

Ubiquitin- and proteasome-dependent outer mitochondrial membrane (OMM)-associated degradation (OMMAD) is critical for mitochondrial and cellular homeostasis. However, the scope and molecular mechanisms of the OMMAD pathways are still not well understood. We report that the OMM-associated E3 ubiquitin ligase MARCH5 controls dynamin-related protein 1 (Drp1)-dependent mitochondrial fission and cell sensitivity to stress-induced apoptosis. MARCH5 knockout selectively inhibited ubiquitination and proteasomal degradation of MiD49, a mitochondrial receptor of Drp1, and consequently led to mitochondrial fragmentation. Mitochondrial fragmentation in MARCH5(-/-) cells was not associated with inhibition of mitochondrial fusion or bioenergetic defects, supporting the possibility that MARCH5 is a negative regulator of mitochondrial fission. Both MARCH5 re-expression and MiD49 knockout in MARCH5(-/-) cells reversed mitochondrial fragmentation and reduced sensitivity to stress-induced apoptosis. These findings and data showing MARCH5-dependent degradation of MiD49 upon stress support the possibility that MARCH5 regulation of MiD49 is a novel mechanism controlling mitochondrial fission and, consequently, the cellular response to stress.

Publication types

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

MeSH terms

  • Apoptosis / physiology
  • Dynamins
  • GTP Phosphohydrolases / metabolism
  • HCT116 Cells
  • HeLa Cells
  • Homeostasis
  • Humans
  • Membrane Proteins / metabolism*
  • Microtubule-Associated Proteins / metabolism
  • Mitochondria / enzymology
  • Mitochondria / metabolism
  • Mitochondrial Dynamics / physiology*
  • Mitochondrial Membranes / metabolism
  • Mitochondrial Proteins / metabolism*
  • Peptide Elongation Factors / metabolism*
  • Stress, Physiological / physiology
  • Ubiquitin-Protein Ligases / metabolism*
  • Ubiquitination

Substances

  • MIEF2 protein, human
  • Membrane Proteins
  • Microtubule-Associated Proteins
  • Mitochondrial Proteins
  • Peptide Elongation Factors
  • MARCHF5 protein, human
  • Ubiquitin-Protein Ligases
  • GTP Phosphohydrolases
  • DNM1L protein, human
  • Dynamins