High-throughput screening yields several small-molecule inhibitors of repeat-associated non-AUG translation

J Biol Chem. 2019 Dec 6;294(49):18624-18638. doi: 10.1074/jbc.RA119.009951. Epub 2019 Oct 23.

Abstract

Repeat-associated non-AUG (RAN) translation is a noncanonical translation initiation event that occurs at nucleotide-repeat expansion mutations that are associated with several neurodegenerative diseases, including fragile X-associated tremor ataxia syndrome (FXTAS), ALS, and frontotemporal dementia (FTD). Translation of expanded repeats produces toxic proteins that accumulate in human brains and contribute to disease pathogenesis. Consequently, RAN translation constitutes a potentially important therapeutic target for managing multiple neurodegenerative disorders. Here, we adapted a previously developed RAN translation assay to a high-throughput format to screen 3,253 bioactive compounds for inhibition of RAN translation of expanded CGG repeats associated with FXTAS. We identified five diverse small molecules that dose-dependently inhibited CGG RAN translation, while relatively sparing canonical translation. All five compounds also inhibited RAN translation of expanded GGGGCC repeats associated with ALS and FTD. Using CD and native gel analyses, we found evidence that three of these compounds, BIX01294, CP-31398, and propidium iodide, bind directly to the repeat RNAs. These findings provide proof-of-principle supporting the development of selective small-molecule RAN translation inhibitors that act across multiple disease-causing repeats.

Keywords: C9orf72; FXTAS; Lou Gehrig's disease; RAN translation; RNA; amyotrophic lateral sclerosis (ALS) (Lou Gehrig disease); drug screening; neurodegeneration; small molecule; translation.

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

  • Amyotrophic Lateral Sclerosis / drug therapy
  • Amyotrophic Lateral Sclerosis / genetics*
  • Animals
  • Ataxia / drug therapy
  • Ataxia / genetics*
  • Azepines / pharmacology
  • Azepines / therapeutic use
  • Cells, Cultured
  • Circular Dichroism
  • DNA Repeat Expansion / drug effects
  • DNA Repeat Expansion / genetics
  • Drug Evaluation, Preclinical
  • Fragile X Syndrome / drug therapy
  • Fragile X Syndrome / genetics*
  • HEK293 Cells
  • Humans
  • Neurodegenerative Diseases / genetics
  • Propidium / pharmacology
  • Propidium / therapeutic use
  • Pyrimidines / pharmacology
  • Pyrimidines / therapeutic use
  • Quinazolines / pharmacology
  • Quinazolines / therapeutic use
  • Rats
  • Tremor / drug therapy
  • Tremor / genetics*
  • Trinucleotide Repeat Expansion / drug effects
  • Trinucleotide Repeat Expansion / genetics*

Substances

  • Azepines
  • BIX 01294
  • Pyrimidines
  • Quinazolines
  • Propidium
  • CP 31398

Supplementary concepts

  • Fragile X Tremor Ataxia Syndrome