Impeding Transcription of Expanded Microsatellite Repeats by Deactivated Cas9

Mol Cell. 2017 Nov 2;68(3):479-490.e5. doi: 10.1016/j.molcel.2017.09.033. Epub 2017 Oct 19.

Abstract

Transcription of expanded microsatellite repeats is associated with multiple human diseases, including myotonic dystrophy, Fuchs endothelial corneal dystrophy, and C9orf72-ALS/FTD. Reducing production of RNA and proteins arising from these expanded loci holds therapeutic benefit. Here, we tested the hypothesis that deactivated Cas9 enzyme impedes transcription across expanded microsatellites. We observed a repeat length-, PAM-, and strand-dependent reduction of repeat-containing RNAs upon targeting dCas9 directly to repeat sequences; targeting the non-template strand was more effective. Aberrant splicing patterns were rescued in DM1 cells, and production of RAN peptides characteristic of DM1, DM2, and C9orf72-ALS/FTD cells was drastically decreased. Systemic delivery of dCas9/gRNA by adeno-associated virus led to reductions in pathological RNA foci, rescue of chloride channel 1 protein expression, and decreased myotonia. These observations suggest that transcription of microsatellite repeat-containing RNAs is more sensitive to perturbation than transcription of other RNAs, indicating potentially viable strategies for therapeutic intervention.

Keywords: C9ORF72/ALS/FTD; CRISPR; Cas9; RNA polymerase II; RNA toxicity; amyotrophic lateral sclerosis; microsatellite repeat disease; myotonic dystrophy; transcription.

MeSH terms

  • Alternative Splicing
  • Animals
  • C9orf72 Protein / genetics
  • C9orf72 Protein / metabolism
  • CD24 Antigen / genetics
  • CD24 Antigen / metabolism
  • CRISPR-Associated Proteins / metabolism*
  • CRISPR-Cas Systems*
  • Chloride Channels / genetics
  • Chloride Channels / metabolism
  • Dependovirus / genetics
  • Disease Models, Animal
  • Down-Regulation
  • Endonucleases / metabolism*
  • Enzyme Activation
  • Female
  • Genetic Therapy / methods*
  • Genetic Vectors
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Male
  • Mice, Transgenic
  • Microsatellite Repeats*
  • Myoblasts / metabolism
  • Myoblasts / pathology
  • Myotonic Dystrophy / genetics
  • Myotonic Dystrophy / metabolism
  • Myotonic Dystrophy / pathology
  • Myotonic Dystrophy / therapy*
  • RNA, Guide, CRISPR-Cas Systems / biosynthesis
  • RNA, Guide, CRISPR-Cas Systems / genetics
  • Transcription, Genetic*
  • Transduction, Genetic
  • ran GTP-Binding Protein / genetics
  • ran GTP-Binding Protein / metabolism

Substances

  • C9orf72 Protein
  • C9orf72 protein, human
  • CD24 Antigen
  • CD24 protein, human
  • CLC-1 channel
  • CRISPR-Associated Proteins
  • Chloride Channels
  • RNA, Guide, CRISPR-Cas Systems
  • Endonucleases
  • ran GTP-Binding Protein