Precise small-molecule cleavage of an r(CUG) repeat expansion in a myotonic dystrophy mouse model

Proc Natl Acad Sci U S A. 2019 Apr 16;116(16):7799-7804. doi: 10.1073/pnas.1901484116. Epub 2019 Mar 29.

Abstract

Myotonic dystrophy type 1 (DM1) is an incurable neuromuscular disorder caused by an expanded CTG repeat that is transcribed into r(CUG)exp The RNA repeat expansion sequesters regulatory proteins such as Muscleblind-like protein 1 (MBNL1), which causes pre-mRNA splicing defects. The disease-causing r(CUG)exp has been targeted by antisense oligonucleotides, CRISPR-based approaches, and RNA-targeting small molecules. Herein, we describe a designer small molecule, Cugamycin, that recognizes the structure of r(CUG)exp and cleaves it in both DM1 patient-derived myotubes and a DM1 mouse model, leaving short repeats of r(CUG) untouched. In contrast, oligonucleotides that recognize r(CUG) sequence rather than structure cleave both long and short r(CUG)-containing transcripts. Transcriptomic, histological, and phenotypic studies demonstrate that Cugamycin broadly and specifically relieves DM1-associated defects in vivo without detectable off-targets. Thus, small molecules that bind and cleave RNA have utility as lead chemical probes and medicines and can selectively target disease-causing RNA structures to broadly improve defects in preclinical animal models.

Keywords: RNA; RNA splicing; chemical biology; genetic disease; nucleic acids.

Publication types

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

MeSH terms

  • Animals
  • Bleomycin / analogs & derivatives*
  • Bleomycin / chemistry
  • Disease Models, Animal
  • Drug Design
  • Humans
  • Mice
  • Myotonic Dystrophy / genetics*
  • Myotonic Dystrophy / metabolism*
  • Oligonucleotides / chemistry*
  • Oligonucleotides / metabolism
  • RNA / genetics*
  • RNA / metabolism*
  • RNA Splicing / genetics*
  • Trinucleotide Repeat Expansion / genetics*

Substances

  • Oligonucleotides
  • cugamycin
  • Bleomycin
  • RNA