The Hairpin Form of r(G4C2)exp in c9ALS/FTD Is Repeat-Associated Non-ATG Translated and a Target for Bioactive Small Molecules

Cell Chem Biol. 2019 Feb 21;26(2):179-190.e12. doi: 10.1016/j.chembiol.2018.10.018. Epub 2018 Nov 29.

Abstract

The most common genetic cause of amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD) is an expanded G4C2 repeat [(G4C2)exp] in C9ORF72. ALS/FTD-associated toxicity has been traced to the RNA transcribed from the repeat expansion [r(G4C2)exp], which sequesters RNA-binding proteins (RBPs) and undergoes repeat-associated non-ATG (RAN) translation to generate toxic dipeptide repeats. Using in vitro and cell-based assays, we identified a small molecule (4) that selectively bound r(G4C2)exp, prevented sequestration of an RBP, and inhibited RAN translation. Indeed, biophysical characterization showed that 4 selectively bound the hairpin form of r(G4C2)exp, and nuclear magnetic resonance spectroscopy studies and molecular dynamics simulations defined this molecular recognition event. Cellular imaging revealed that 4 localized to r(G4C2)exp cytoplasmic foci, the putative sites of RAN translation. Collectively, these studies highlight that the hairpin structure of r(G4C2)exp is a therapeutically relevant target and small molecules that bind it can ameliorate c9ALS/FTD-associated toxicity.

Keywords: RNA; RNA folding; amyotrophic lateral sclerosis; c9ALS/FTD; chemical biology; drug design; frontotemporal dementia; nucleic acids; small molecules.

Publication types

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

MeSH terms

  • Amyotrophic Lateral Sclerosis / metabolism
  • Amyotrophic Lateral Sclerosis / pathology
  • Binding Sites
  • C9orf72 Protein / genetics*
  • DNA Repeat Expansion / genetics*
  • Frontotemporal Dementia / metabolism
  • Frontotemporal Dementia / pathology
  • Humans
  • Kinetics
  • Molecular Dynamics Simulation
  • Nuclear Magnetic Resonance, Biomolecular
  • Nucleic Acid Conformation
  • Polyribosomes / drug effects
  • Polyribosomes / metabolism
  • Protein Biosynthesis / drug effects
  • RNA-Binding Proteins / chemistry
  • RNA-Binding Proteins / metabolism
  • Small Molecule Libraries / chemistry*
  • Small Molecule Libraries / metabolism
  • Small Molecule Libraries / pharmacology
  • Thermodynamics

Substances

  • C9orf72 Protein
  • RNA-Binding Proteins
  • Small Molecule Libraries

Supplementary concepts

  • Frontotemporal Dementia With Motor Neuron Disease