Poly(GR) impairs protein translation and stress granule dynamics in C9orf72-associated frontotemporal dementia and amyotrophic lateral sclerosis

Nat Med. 2018 Aug;24(8):1136-1142. doi: 10.1038/s41591-018-0071-1. Epub 2018 Jun 25.

Abstract

The major genetic cause of frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS) is a C9orf72 G4C2 repeat expansion1,2. Proposed mechanisms by which the expansion causes c9FTD/ALS include toxicity from repeat-containing RNA and from dipeptide repeat proteins translated from these transcripts. To investigate the contribution of poly(GR) dipeptide repeat proteins to c9FTD/ALS pathogenesis in a mammalian in vivo model, we generated mice that expressed GFP-(GR)100 in the brain. GFP-(GR)100 mice developed age-dependent neurodegeneration, brain atrophy, and motor and memory deficits through the accumulation of diffuse, cytoplasmic poly(GR). Poly(GR) co-localized with ribosomal subunits and the translation initiation factor eIF3η in GFP-(GR)100 mice and, of importance, in c9FTD/ALS patients. Combined with the differential expression of ribosome-associated genes in GFP-(GR)100 mice, these findings demonstrate poly(GR)-mediated ribosomal distress. Indeed, poly(GR) inhibited canonical and non-canonical protein translation in HEK293T cells, and also induced the formation of stress granules and delayed their disassembly. These data suggest that poly(GR) contributes to c9FTD/ALS by impairing protein translation and stress granule dynamics, consequently causing chronic cellular stress and preventing cells from mounting an effective stress response. Decreasing poly(GR) and/or interrupting interactions between poly(GR) and ribosomal and stress granule-associated proteins may thus represent potential therapeutic strategies to restore homeostasis.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amyotrophic Lateral Sclerosis / metabolism*
  • Animals
  • Behavior, Animal
  • C9orf72 Protein / metabolism*
  • Cluster Analysis
  • Cytoplasmic Granules / drug effects
  • Cytoplasmic Granules / metabolism*
  • Dipeptides / pharmacology*
  • Frontotemporal Dementia / metabolism*
  • Gene Expression Profiling
  • HEK293 Cells
  • Humans
  • Mice, Inbred C57BL
  • Protein Biosynthesis* / drug effects
  • Ribosomal Proteins / metabolism
  • Stress, Physiological* / drug effects

Substances

  • C9orf72 Protein
  • Dipeptides
  • Ribosomal Proteins