Endophilin-A Deficiency Induces the Foxo3a-Fbxo32 Network in the Brain and Causes Dysregulation of Autophagy and the Ubiquitin-Proteasome System

Cell Rep. 2016 Oct 18;17(4):1071-1086. doi: 10.1016/j.celrep.2016.09.058. Epub 2016 Oct 6.

Abstract

Endophilin-A, a well-characterized endocytic adaptor essential for synaptic vesicle recycling, has recently been linked to neurodegeneration. We report here that endophilin-A deficiency results in impaired movement, age-dependent ataxia, and neurodegeneration in mice. Transcriptional analysis of endophilin-A mutant mice, complemented by proteomics, highlighted ataxia- and protein-homeostasis-related genes and revealed upregulation of the E3-ubiquitin ligase FBXO32/atrogin-1 and its transcription factor FOXO3A. FBXO32 overexpression triggers apoptosis in cultured cells and neurons but, remarkably, coexpression of endophilin-A rescues it. FBXO32 interacts with all three endophilin-A proteins. Similarly to endophilin-A, FBXO32 tubulates membranes and localizes on clathrin-coated structures. Additionally, FBXO32 and endophilin-A are necessary for autophagosome formation, and both colocalize transiently with autophagosomes. Our results point to a role for endophilin-A proteins in autophagy and protein degradation, processes that are impaired in their absence, potentially contributing to neurodegeneration and ataxia.

Keywords: FBXO32; Parkinson’s disease; ataxia; autophagy; endocytosis; endophilin; neurodegeneration; next-generation sequencing; protein homeostasis; ubiquitin-proteasome system.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acyltransferases / deficiency*
  • Acyltransferases / metabolism
  • Aging / pathology
  • Animals
  • Apoptosis
  • Ataxia / genetics
  • Ataxia / pathology
  • Autophagosomes / metabolism
  • Autophagy*
  • Brain / metabolism*
  • Forkhead Box Protein O3 / genetics
  • Forkhead Box Protein O3 / metabolism*
  • HeLa Cells
  • Hippocampus / metabolism
  • Hippocampus / pathology
  • Homeostasis / genetics
  • Humans
  • Male
  • Mice
  • Mice, Knockout
  • Movement Disorders / complications
  • Movement Disorders / pathology
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism*
  • Mutation / genetics
  • Nerve Degeneration / complications
  • Nerve Degeneration / pathology
  • Parkinson Disease / genetics
  • Parkinson Disease / pathology
  • Proteasome Endopeptidase Complex / metabolism*
  • Protein Binding
  • SKP Cullin F-Box Protein Ligases / genetics
  • SKP Cullin F-Box Protein Ligases / metabolism*
  • Transcription, Genetic
  • Ubiquitin / metabolism*
  • Up-Regulation

Substances

  • Forkhead Box Protein O3
  • FoxO3 protein, mouse
  • Muscle Proteins
  • Ubiquitin
  • Acyltransferases
  • 2-acylglycerophosphate acyltransferase
  • FBXO32 protein, human
  • Fbxo32 protein, mouse
  • SKP Cullin F-Box Protein Ligases
  • Proteasome Endopeptidase Complex