Ubiquitination and proteasomal degradation of ATG12 regulates its proapoptotic activity

Autophagy. 2014;10(12):2269-78. doi: 10.4161/15548627.2014.981914.

Abstract

During macroautophagy, conjugation of ATG12 to ATG5 is essential for LC3 lipidation and autophagosome formation. Additionally, ATG12 has ATG5-independent functions in diverse processes including mitochondrial fusion and mitochondrial-dependent apoptosis. In this study, we investigated the regulation of free ATG12. In stark contrast to the stable ATG12-ATG5 conjugate, we find that free ATG12 is highly unstable and rapidly degraded in a proteasome-dependent manner. Surprisingly, ATG12, itself a ubiquitin-like protein, is directly ubiquitinated and this promotes its proteasomal degradation. As a functional consequence of its turnover, accumulation of free ATG12 contributes to proteasome inhibitor-mediated apoptosis, a finding that may be clinically important given the use of proteasome inhibitors as anticancer agents. Collectively, our results reveal a novel interconnection between autophagy, proteasome activity, and cell death mediated by the ubiquitin-like properties of ATG12.

Keywords: ATG, autophagy-related; ATG12; Act D, actinomycin D; BCL2L1, BCL2-like 1; BH3, BCL2 homology domain 3; CHX, cycloheximide; HBSS, Hank's balanced salt solution; LC3/MAP1LC3, microtubule-associated protein 1 light chain 3; MEF, mouse embryonic fibroblast; RNAi, RNA interference; UB, ubiquitin; UBL, ubiquitin-like protein; apoptosis; proteasomal degradation; ubiquitin-like protein; ubiquitination.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / physiology*
  • Autophagy / physiology*
  • Autophagy-Related Protein 12
  • Cell Death / physiology
  • Humans
  • Mice
  • Microtubule-Associated Proteins / metabolism
  • Mitochondria / metabolism*
  • Proteasome Endopeptidase Complex / metabolism*
  • Protein Processing, Post-Translational / physiology
  • Small Ubiquitin-Related Modifier Proteins / metabolism*
  • Ubiquitin-Conjugating Enzymes / metabolism
  • Ubiquitination / physiology*

Substances

  • ATG12 protein, human
  • Autophagy-Related Protein 12
  • Microtubule-Associated Proteins
  • Small Ubiquitin-Related Modifier Proteins
  • Ubiquitin-Conjugating Enzymes
  • Proteasome Endopeptidase Complex