Antisense Oligonucleotide-Based Downregulation of the G56R Pathogenic Variant Causing NR2E3-Associated Autosomal Dominant Retinitis Pigmentosa

Genes (Basel). 2019 May 10;10(5):363. doi: 10.3390/genes10050363.

Abstract

The recurrent missense variant in Nuclear Receptor Subfamily 2 Group E Member 3 (NR2E3), c.166G>A, p.(Gly56Arg) or G56R, underlies 1%-2% of cases with autosomal dominant retinitis pigmentosa (adRP), a frequent, genetically heterogeneous inherited retinal disease (IRD). The mutant NR2E3 protein has a presumed dominant negative effect (DNE) by competition for dimer formation with Cone-Rod Homeobox (CRX) but with abolishment of DNA binding, acting as a repressor in trans. Both the frequency and DNE of G56R make it an interesting target for allele-specific knock-down of the mutant allele using antisense oligonucleotides (AONs), an emerging therapeutic strategy for IRD. Here, we designed gapmer AONs with or without a locked nucleic acid modification at the site of the mutation, which were analyzed for potential off-target effects. Next, we overexpressed wild type (WT) or mutant NR2E3 in RPE-1 cells, followed by AON treatment. Transcript and protein levels of WT and mutant NR2E3 were detected by reverse transcription quantitative polymerase chain reaction (RT-qPCR) and Western blot respectively. All AONs showed a general knock-down of mutant and WT NR2E3 on RNA and protein level, showing the accessibility of the region for AON-induced knockdown. Further modifications are needed however to increase allele-specificity. In conclusion, we propose the first proof-of-concept for AON-mediated silencing of a single nucleotide variation with a dominant negative effect as a therapeutic approach for NR2E3-associated adRP.

Keywords: G56R; NR2E3; allele-specific knockdown; autosomal dominant; gapmer antisense oligonucleotides; putative dominant negative effect; retinitis pigmentosa.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line
  • Down-Regulation
  • Genes, Dominant
  • Humans
  • Microtubule-Associated Proteins / genetics
  • Microtubule-Associated Proteins / metabolism
  • Mutation
  • Mutation, Missense
  • Oligonucleotides / pharmacology
  • Oligonucleotides, Antisense / genetics
  • Orphan Nuclear Receptors / genetics*
  • Orphan Nuclear Receptors / metabolism
  • Polymorphism, Single Nucleotide / genetics
  • Retina / pathology
  • Retinitis Pigmentosa / genetics*
  • Retinitis Pigmentosa / metabolism

Substances

  • Microtubule-Associated Proteins
  • NR2E3 protein, human
  • Oligonucleotides
  • Oligonucleotides, Antisense
  • Orphan Nuclear Receptors
  • RP1 protein, human
  • locked nucleic acid