The C9orf72 repeat expansion disrupts nucleocytoplasmic transport

Nature. 2015 Sep 3;525(7567):56-61. doi: 10.1038/nature14973. Epub 2015 Aug 26.

Abstract

The hexanucleotide repeat expansion (HRE) GGGGCC (G4C2) in C9orf72 is the most common cause of amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD). Recent studies support an HRE RNA gain-of-function mechanism of neurotoxicity, and we previously identified protein interactors for the G4C2 RNA including RanGAP1. A candidate-based genetic screen in Drosophila expressing 30 G4C2 repeats identified RanGAP (Drosophila orthologue of human RanGAP1), a key regulator of nucleocytoplasmic transport, as a potent suppressor of neurodegeneration. Enhancing nuclear import or suppressing nuclear export of proteins also suppresses neurodegeneration. RanGAP physically interacts with HRE RNA and is mislocalized in HRE-expressing flies, neurons from C9orf72 ALS patient-derived induced pluripotent stem cells (iPSC-derived neurons), and in C9orf72 ALS patient brain tissue. Nuclear import is impaired as a result of HRE expression in the fly model and in C9orf72 iPSC-derived neurons, and these deficits are rescued by small molecules and antisense oligonucleotides targeting the HRE G-quadruplexes. Nucleocytoplasmic transport defects may be a fundamental pathway for ALS and FTD that is amenable to pharmacotherapeutic intervention.

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

  • Active Transport, Cell Nucleus / genetics*
  • Amyotrophic Lateral Sclerosis / genetics
  • Amyotrophic Lateral Sclerosis / pathology
  • Animals
  • Brain / metabolism
  • Brain / pathology
  • C9orf72 Protein
  • Cell Nucleus / metabolism*
  • DNA Repeat Expansion / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / metabolism
  • Female
  • Frontotemporal Dementia / genetics
  • Frontotemporal Dementia / pathology
  • G-Quadruplexes
  • GTPase-Activating Proteins / metabolism
  • Humans
  • Induced Pluripotent Stem Cells / cytology
  • Induced Pluripotent Stem Cells / metabolism
  • Neurons / metabolism
  • Neurons / pathology
  • Nuclear Pore / chemistry
  • Nuclear Pore / metabolism
  • Nuclear Proteins / metabolism
  • Oligonucleotides, Antisense / genetics
  • Open Reading Frames / genetics*
  • Proteins / genetics*
  • RNA / genetics
  • RNA / metabolism

Substances

  • C9orf72 Protein
  • C9orf72 protein, human
  • Drosophila Proteins
  • GTPase-Activating Proteins
  • Nuclear Proteins
  • Oligonucleotides, Antisense
  • Proteins
  • RANGAP1 protein, human
  • RanGAP protein, Drosophila
  • RNA