The ETFDH c.158A>G variation disrupts the balanced interplay of ESE- and ESS-binding proteins thereby causing missplicing and multiple Acyl-CoA dehydrogenation deficiency

Hum Mutat. 2014 Jan;35(1):86-95. doi: 10.1002/humu.22455. Epub 2013 Oct 28.

Abstract

Multiple acyl-CoA dehydrogenation deficiency is a disorder of fatty acid and amino acid oxidation caused by defects of electron transfer flavoprotein (ETF) or its dehydrogenase (ETFDH). A clear relationship between genotype and phenotype makes genotyping of patients important not only diagnostically but also for prognosis and for assessment of treatment. In the present study, we show that a predicted benign ETFDH missense variation (c.158A>G/p.Lys53Arg) in exon 2 causes exon skipping and degradation of ETFDH protein in patient samples. Using splicing reporter minigenes and RNA pull-down of nuclear proteins, we show that the c.158A>G variation increases the strength of a preexisting exonic splicing silencer (ESS) motif UAGGGA. This ESS motif binds splice inhibitory hnRNP A1, hnRNP A2/B1, and hnRNP H proteins. Binding of these inhibitory proteins prevents binding of the positive splicing regulatory SRSF1 and SRSF5 proteins to nearby and overlapping exonic splicing enhancer elements and this causes exon skipping. We further suggest that binding of hnRNP proteins to UAGGGA is increased by triggering synergistic hnRNP H binding to GGG triplets located upstream and downsteam of the UAGGGA motif. A number of disease-causing exonic elements that induce exon skipping in other genes have a similar architecture as the one in ETFDH exon 2.

Keywords: ETFDH; MADD; exonic splicing enhancer; exonic splicing silencer; pre-mRNA splicing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine / metabolism*
  • Amino Acid Motifs
  • Cadaver
  • Electron-Transferring Flavoproteins / genetics*
  • Electron-Transferring Flavoproteins / metabolism*
  • Enhancer Elements, Genetic
  • Exons
  • Gene Expression Regulation
  • Genetic Variation
  • Guanine / metabolism*
  • HEK293 Cells
  • HeLa Cells
  • Heterogeneous Nuclear Ribonucleoprotein A1
  • Heterogeneous-Nuclear Ribonucleoprotein Group A-B / metabolism
  • Heterogeneous-Nuclear Ribonucleoprotein Group F-H / metabolism
  • Humans
  • Infant, Newborn
  • Iron-Sulfur Proteins / genetics*
  • Iron-Sulfur Proteins / metabolism*
  • Multiple Acyl Coenzyme A Dehydrogenase Deficiency / diagnosis
  • Multiple Acyl Coenzyme A Dehydrogenase Deficiency / genetics*
  • Mutation, Missense
  • Nuclear Proteins / metabolism
  • Oxidoreductases Acting on CH-NH Group Donors / genetics*
  • Oxidoreductases Acting on CH-NH Group Donors / metabolism*
  • Protein Binding
  • RNA Splicing*
  • RNA-Binding Proteins / metabolism
  • Sequence Analysis, DNA
  • Serine-Arginine Splicing Factors
  • Silencer Elements, Transcriptional
  • Trinucleotide Repeats

Substances

  • Electron-Transferring Flavoproteins
  • Heterogeneous Nuclear Ribonucleoprotein A1
  • Heterogeneous-Nuclear Ribonucleoprotein Group A-B
  • Heterogeneous-Nuclear Ribonucleoprotein Group F-H
  • Iron-Sulfur Proteins
  • Nuclear Proteins
  • RNA-Binding Proteins
  • Serine-Arginine Splicing Factors
  • Guanine
  • Oxidoreductases Acting on CH-NH Group Donors
  • electron-transferring-flavoprotein dehydrogenase
  • Adenosine