Intronic PAH gene mutations cause a splicing defect by a novel mechanism involving U1snRNP binding downstream of the 5' splice site

PLoS Genet. 2018 Apr 23;14(4):e1007360. doi: 10.1371/journal.pgen.1007360. eCollection 2018 Apr.

Abstract

Phenylketonuria (PKU), one of the most common inherited diseases of amino acid metabolism, is caused by mutations in the phenylalanine hydroxylase (PAH) gene. Recently, PAH exon 11 was identified as a vulnerable exon due to a weak 3' splice site, with different exonic mutations affecting exon 11 splicing through disruption of exonic splicing regulatory elements. In this study, we report a novel intron 11 regulatory element, which is involved in exon 11 splicing, as revealed by the investigated pathogenic effect of variants c.1199+17G>A and c.1199+20G>C, identified in PKU patients. Both mutations cause exon 11 skipping in a minigene system. RNA binding assays indicate that binding of U1snRNP70 to this intronic region is disrupted, concomitant with a slightly increased binding of inhibitors hnRNPA1/2. We have investigated the effect of deletions and point mutations, as well as overexpression of adapted U1snRNA to show that this splicing regulatory motif is important for regulation of correct splicing at the natural 5' splice site. The results indicate that U1snRNP binding downstream of the natural 5' splice site determines efficient exon 11 splicing, thus providing a basis for development of therapeutic strategies to correct PAH exon 11 splicing mutations. In this work, we expand the functional effects of non-canonical intronic U1 snRNP binding by showing that it may enhance exon definition and that, consequently, intronic mutations may cause exon skipping by a novel mechanism, where they disrupt stimulatory U1 snRNP binding close to the 5' splice site. Notably, our results provide further understanding of the reported therapeutic effect of exon specific U1 snRNA for splicing mutations in disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Base Sequence
  • Computer Simulation
  • Exons
  • Hep G2 Cells
  • Humans
  • Introns
  • Mutation*
  • Phenylalanine Hydroxylase / genetics*
  • Phenylketonurias / genetics
  • Phenylketonurias / metabolism
  • RNA Splice Sites / genetics*
  • RNA Splicing / genetics*
  • RNA, Small Nuclear / genetics
  • RNA, Small Nuclear / metabolism
  • Ribonucleoprotein, U1 Small Nuclear / genetics*
  • Ribonucleoprotein, U1 Small Nuclear / metabolism*

Substances

  • RNA Splice Sites
  • RNA, Small Nuclear
  • Ribonucleoprotein, U1 Small Nuclear
  • U1 small nuclear RNA
  • Phenylalanine Hydroxylase

Grants and funding

This work was supported by Fundación Ramón Areces (http://www.fundacionareces.es/fundacionareces/, Grant XVII CN to LRD), European Cooperation in Science And Technology (http://www.cost.eu/, Action BM1207 to LRD), Natur og Univers, Det Frie Forskningsråd (https://dff.dk/ Grant 4181-00515 to BSA) and Novo Nordisk Fonden (DK) (http://novonordiskfonden.dk/en, Grant 61310-0128 to BSA). Centro de Biología Molecular Severo Ochoa receives an institutional grant from Fundación Ramón Areces (http://www.fundacionareces.es/fundacionareces). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.