A complex V ATP5A1 defect causes fatal neonatal mitochondrial encephalopathy

Brain. 2013 May;136(Pt 5):1544-54. doi: 10.1093/brain/awt086. Epub 2013 Apr 18.

Abstract

Whole exome sequencing is a powerful tool to detect novel pathogenic mutations in patients with suspected mitochondrial disease. However, the interpretation of novel genetic variants is not always straightforward. Here, we present two siblings with a severe neonatal encephalopathy caused by complex V deficiency. The aim of this study was to uncover the underlying genetic defect using the combination of enzymatic testing and whole exome sequence analysis, and to provide evidence for causality by functional follow-up. Measurement of the oxygen consumption rate and enzyme analysis in fibroblasts were performed. Immunoblotting techniques were applied to study complex V assembly. The coding regions of the genome were analysed. Three-dimensional modelling was applied. Exome sequencing of the two siblings with complex V deficiency revealed a heterozygous mutation in the ATP5A1 gene, coding for complex V subunit α. The father carried the variant heterozygously. At the messenger RNA level, only the mutated allele was expressed in the patients, whereas the father expressed both the wild-type and the mutant allele. Gene expression data indicate that the maternal allele is not expressed, which is supported by the observation that the ATP5A1 expression levels in the patients and their mother are reduced to ∼50%. Complementation with wild-type ATP5A1 restored complex V in the patient fibroblasts, confirming pathogenicity of the defect. At the protein level, the mutation results in a disturbed interaction of the α-subunit with the β-subunit of complex V, which interferes with the stability of the complex. This study demonstrates the important value of functional studies in the diagnostic work-up of mitochondrial patients, in order to guide genetic variant prioritization, and to validate gene defects.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cells, Cultured
  • Humans
  • Infant, Newborn
  • Mitochondrial Encephalomyopathies / enzymology*
  • Mitochondrial Encephalomyopathies / genetics*
  • Mitochondrial Encephalomyopathies / mortality
  • Mitochondrial Proton-Translocating ATPases / chemistry
  • Mitochondrial Proton-Translocating ATPases / genetics*
  • Oxidative Phosphorylation Coupling Factors / chemistry
  • Oxidative Phosphorylation Coupling Factors / genetics
  • Protein Structure, Secondary

Substances

  • Oxidative Phosphorylation Coupling Factors
  • complex V (mitochondrial oxidative phosphorylation system)
  • F(6) ATPase
  • Mitochondrial Proton-Translocating ATPases

Supplementary concepts

  • Mitochondrial encephalopathy