Antisense suppression of the nonsense mediated decay factor Upf3b as a potential treatment for diseases caused by nonsense mutations

Genome Biol. 2018 Jan 15;19(1):4. doi: 10.1186/s13059-017-1386-9.

Abstract

Background: About 11% of all human genetic diseases are caused by nonsense mutations that generate premature translation termination codons (PTCs) in messenger RNAs (mRNA). PTCs not only lead to the production of truncated proteins, but also often result in decreased mRNA abundance due to nonsense-mediated mRNA decay (NMD). Although pharmacological inhibition of NMD could be an attractive therapeutic approach for the treatment of diseases caused by nonsense mutations, NMD also regulates the expression of 10-20% of the normal transcriptome.

Results: Here, we investigate whether NMD can be inhibited to stabilize mutant mRNAs, which may subsequently produce functional proteins, without having a major impact on the normal transcriptome. We develop antisense oligonucleotides (ASOs) to systematically deplete each component in the NMD pathway. We find that ASO-mediated depletion of each NMD factor elicits different magnitudes of NMD inhibition in vitro and are differentially tolerated in normal mice. Among all of the NMD factors, Upf3b depletion is well tolerated, consistent with previous reports that UPF3B is not essential for development and regulates only a subset of the endogenous NMD substrates. While minimally impacting the normal transcriptome, Upf3b-ASO treatment significantly stabilizes the PTC-containing dystrophin mRNA in mdx mice and coagulation factor IX mRNA in a hemophilia mouse model. Furthermore, when combined with reagents promoting translational read-through, Upf3b-ASO treatment leads to the production of functional factor IX protein in hemophilia mice.

Conclusions: These data demonstrate that ASO-mediated reduction of the NMD factor Upf3b could be an effective and safe approach for the treatment of diseases caused by nonsense mutations.

Keywords: ASO; Hemophilia; NMD; PTC; RNA; Upf3b.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cells, Cultured
  • Codon, Nonsense*
  • Dystrophin / genetics
  • Factor IX / metabolism
  • Hemophilia B / genetics
  • Hemophilia B / metabolism
  • Hemophilia B / therapy
  • Liver / metabolism
  • Mice
  • Nonsense Mediated mRNA Decay*
  • Oligonucleotides, Antisense*
  • RNA Stability
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins / antagonists & inhibitors*
  • RNA-Binding Proteins / genetics
  • Transcriptome

Substances

  • Codon, Nonsense
  • Dystrophin
  • Oligonucleotides, Antisense
  • RNA, Messenger
  • RNA-Binding Proteins
  • UPF3B protein, mouse
  • Factor IX