Overriding FUS autoregulation in mice triggers gain-of-toxic dysfunctions in RNA metabolism and autophagy-lysosome axis

Elife. 2019 Feb 12:8:e40811. doi: 10.7554/eLife.40811.

Abstract

Mutations in coding and non-coding regions of FUS cause amyotrophic lateral sclerosis (ALS). The latter mutations may exert toxicity by increasing FUS accumulation. We show here that broad expression within the nervous system of wild-type or either of two ALS-linked mutants of human FUS in mice produces progressive motor phenotypes accompanied by characteristic ALS-like pathology. FUS levels are autoregulated by a mechanism in which human FUS downregulates endogenous FUS at mRNA and protein levels. Increasing wild-type human FUS expression achieved by saturating this autoregulatory mechanism produces a rapidly progressive phenotype and dose-dependent lethality. Transcriptome analysis reveals mis-regulation of genes that are largely not observed upon FUS reduction. Likely mechanisms for FUS neurotoxicity include autophagy inhibition and defective RNA metabolism. Thus, our results reveal that overriding FUS autoregulation will trigger gain-of-function toxicity via altered autophagy-lysosome pathway and RNA metabolism function, highlighting a role for protein and RNA dyshomeostasis in FUS-mediated toxicity.

Keywords: FUS; RNA metabolism; amyotrophic lateral sclerosis (ALS); autophagy-lysosome; frontotemporal degeneration (FTD); homeostasis; mouse; neuroscience.

Publication types

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

MeSH terms

  • Animals
  • Autophagy*
  • Gene Expression Profiling
  • Homeostasis*
  • Humans
  • Lysosomes / metabolism*
  • Mice, Inbred C57BL
  • Mutant Proteins / biosynthesis
  • Mutant Proteins / genetics
  • Mutant Proteins / toxicity
  • RNA / metabolism*
  • RNA-Binding Protein FUS / biosynthesis*
  • RNA-Binding Protein FUS / genetics
  • RNA-Binding Protein FUS / toxicity*

Substances

  • FUS protein, human
  • Mutant Proteins
  • RNA-Binding Protein FUS
  • RNA