Maturation and Clearance of Autophagosomes in Neurons Depends on a Specific Cysteine Protease Isoform, ATG-4.2

Dev Cell. 2019 Apr 22;49(2):251-266.e8. doi: 10.1016/j.devcel.2019.02.013. Epub 2019 Mar 14.

Abstract

In neurons, defects in autophagosome clearance have been associated with neurodegenerative disease. Yet, the mechanisms that coordinate trafficking and clearance of synaptic autophagosomes are poorly understood. Here, we use genetic screens and in vivo imaging in single neurons of C. elegans to identify mechanisms necessary for clearance of synaptic autophagosomes. We observed that autophagy at the synapse can be modulated in vivo by the state of neuronal activity, that autophagosomes undergo UNC-16/JIP3-mediated retrograde transport, and that autophagosomes containing synaptic material mature in the cell body. Through forward genetic screens, we then determined that autophagosome maturation in the cell body depends on the protease ATG-4.2, but not the related ATG-4.1, and that ATG-4.2 can cleave LGG-1/Atg8/GABARAP from membranes. Our studies revealed that ATG-4.2 is specifically necessary for the maturation and clearance of autophagosomes and that defects in transport and ATG-4.2-mediated maturation genetically interact to enhance abnormal accumulation of autophagosomes in neurons.

Keywords: ATG-4.2; ATG4; UNC-16/JIP3; activity; autophagy; clearance; degradation; maturation; synapse; transport.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Autophagosomes / metabolism*
  • Autophagy / physiology*
  • Autophagy-Related Proteins / metabolism*
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / metabolism
  • Cysteine Proteases / metabolism
  • Microtubule-Associated Proteins / metabolism
  • Neurodegenerative Diseases / metabolism
  • Neurons / metabolism
  • Phagosomes / metabolism
  • Protein Isoforms
  • Signal Transduction / physiology
  • Synapses / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Autophagy-Related Proteins
  • Caenorhabditis elegans Proteins
  • Microtubule-Associated Proteins
  • Protein Isoforms
  • unc-16 protein, C elegans
  • Cysteine Proteases