ATG4D is the main ATG8 delipidating enzyme in mammalian cells and protects against cerebellar neurodegeneration

Cell Death Differ. 2021 Sep;28(9):2651-2672. doi: 10.1038/s41418-021-00776-1. Epub 2021 Apr 1.

Abstract

Despite the great advances in autophagy research in the last years, the specific functions of the four mammalian Atg4 proteases (ATG4A-D) remain unclear. In yeast, Atg4 mediates both Atg8 proteolytic activation, and its delipidation. However, it is not clear how these two roles are distributed along the members of the ATG4 family of proteases. We show that these two functions are preferentially carried out by distinct ATG4 proteases, being ATG4D the main delipidating enzyme. In mammalian cells, ATG4D loss results in accumulation of membrane-bound forms of mATG8s, increased cellular autophagosome number and reduced autophagosome average size. In mice, ATG4D loss leads to cerebellar neurodegeneration and impaired motor coordination caused by alterations in trafficking/clustering of GABAA receptors. We also show that human gene variants of ATG4D associated with neurodegeneration are not able to fully restore ATG4D deficiency, highlighting the neuroprotective role of ATG4D in mammals.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Autophagy
  • Autophagy-Related Protein 8 Family / metabolism*
  • Autophagy-Related Proteins / metabolism*
  • Cysteine Endopeptidases / metabolism*
  • Disease Models, Animal
  • Humans
  • Mammals
  • Mice
  • Mice, Transgenic
  • Neurodegenerative Diseases / genetics*
  • Neurodegenerative Diseases / pathology

Substances

  • Autophagy-Related Protein 8 Family
  • Autophagy-Related Proteins
  • ATG4D protein, human
  • Cysteine Endopeptidases