Deep-intronic ABCA4 variants explain missing heritability in Stargardt disease and allow correction of splice defects by antisense oligonucleotides

Genet Med. 2019 Aug;21(8):1751-1760. doi: 10.1038/s41436-018-0414-9. Epub 2019 Jan 15.

Abstract

Purpose: Using exome sequencing, the underlying variants in many persons with autosomal recessive diseases remain undetected. We explored autosomal recessive Stargardt disease (STGD1) as a model to identify the missing heritability.

Methods: Sequencing of ABCA4 was performed in 8 STGD1 cases with one variant and p.Asn1868Ile in trans, 25 cases with one variant, and 3 cases with no ABCA4 variant. The effect of intronic variants was analyzed using in vitro splice assays in HEK293T cells and patient-derived fibroblasts. Antisense oligonucleotides were used to correct splice defects.

Results: In 24 of the probands (67%), one known and five novel deep-intronic variants were found. The five novel variants resulted in messenger RNA pseudoexon inclusions, due to strengthening of cryptic splice sites or by disrupting a splicing silencer motif. Variant c.769-784C>T showed partial insertion of a pseudoexon and was found in cis with c.5603A>T (p.Asn1868Ile), so its causal role could not be fully established. Variant c.4253+43G>A resulted in partial skipping of exon 28. Remarkably, antisense oligonucleotides targeting the aberrant splice processes resulted in (partial) correction of all splicing defects.

Conclusion: Our data demonstrate the importance of assessing noncoding variants in genetic diseases, and show the great potential of splice modulation therapy for deep-intronic variants.

Keywords: ABCA4; Stargardt disease; antisense oligonucleotide; deep-intronic variant; missing heritability.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP-Binding Cassette Transporters / genetics*
  • Adolescent
  • Adult
  • Aged
  • Child
  • Exons / genetics
  • HEK293 Cells
  • Humans
  • Introns / genetics
  • Middle Aged
  • Mutation / genetics
  • Oligonucleotides, Antisense / genetics*
  • Oligonucleotides, Antisense / pharmacology
  • Pedigree
  • Polymorphism, Single Nucleotide / genetics
  • Protein Isoforms / genetics*
  • RNA Splicing / genetics
  • Stargardt Disease / genetics*
  • Stargardt Disease / pathology
  • Young Adult

Substances

  • ABCA4 protein, human
  • ATP-Binding Cassette Transporters
  • Oligonucleotides, Antisense
  • Protein Isoforms