Splice-Switching Antisense Oligonucleotides Correct Phenylalanine Hydroxylase Exon 11 Skipping Defects and Rescue Enzyme Activity in Phenylketonuria

Nucleic Acid Ther. 2024;34(3):134-142. doi: 10.1089/nat.2024.0014. Epub 2024 Apr 9.

Abstract

The PAH gene encodes the hepatic enzyme phenylalanine hydroxylase (PAH), and its deficiency, known as phenylketonuria (PKU), leads to neurotoxic high levels of phenylalanine. PAH exon 11 is weakly defined, and several missense and intronic variants identified in patients affect the splicing process. Recently, we identified a novel intron 11 splicing regulatory element where U1snRNP binds, participating in exon 11 definition. In this work, we describe the implementation of an antisense strategy targeting intron 11 sequences to correct the effect of PAH mis-splicing variants. We used an in vitro assay with minigenes and identified splice-switching antisense oligonucleotides (SSOs) that correct the exon skipping defect of PAH variants c.1199+17G>A, c.1199+20G>C, c.1144T>C, and c.1066-3C>T. To examine the functional rescue induced by the SSOs, we generated a hepatoma cell model with variant c.1199+17G>A using CRISPR/Cas9. The edited cell line reproduces the exon 11 skipping pattern observed from minigenes, leading to reduced PAH protein levels and activity. SSO transfection results in an increase in exon 11 inclusion and corrects PAH deficiency. Our results provide proof of concept of the potential therapeutic use of a single SSO for different exonic and intronic splicing variants causing PAH exon 11 skipping in PKU.

Keywords: CRIPSR/Cas; antisense oligonucleotides; knock-in cell model; phenylketonuria; splicing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alternative Splicing / genetics
  • CRISPR-Cas Systems / genetics
  • Exons* / genetics
  • Gene Editing / methods
  • Humans
  • Introns* / genetics
  • Oligonucleotides, Antisense* / genetics
  • Oligonucleotides, Antisense* / pharmacology
  • Oligonucleotides, Antisense* / therapeutic use
  • Phenylalanine Hydroxylase* / genetics
  • Phenylalanine Hydroxylase* / metabolism
  • Phenylketonurias* / genetics
  • Phenylketonurias* / pathology
  • Phenylketonurias* / therapy
  • RNA Splicing* / genetics

Substances

  • Phenylalanine Hydroxylase
  • Oligonucleotides, Antisense