Metabolic impact of pathogenic variants in the mitochondrial glutamyl-tRNA synthetase EARS2

J Inherit Metab Dis. 2021 Jul;44(4):949-960. doi: 10.1002/jimd.12387. Epub 2021 Apr 27.

Abstract

Glutamyl-tRNA synthetase 2 (encoded by EARS2) is a mitochondrial aminoacyl-tRNA synthetase required to translate the 13 subunits of the electron transport chain encoded by the mitochondrial DNA. Pathogenic EARS2 variants cause combined oxidative phosphorylation deficiency, subtype 12 (COXPD12), an autosomal recessive disorder involving lactic acidosis, intellectual disability, and other features of mitochondrial compromise. Patients with EARS2 deficiency present with variable phenotypes ranging from neonatal lethality to a mitigated disease with clinical improvement in early childhood. Here, we report a neonate homozygous for a rare pathogenic variant in EARS2 (c.949G>T; p.G317C). Metabolomics in primary fibroblasts from this patient revealed expected abnormalities in TCA cycle metabolites, as well as numerous changes in purine, pyrimidine, and fatty acid metabolism. To examine genotype-phenotype correlations in COXPD12, we compared the metabolic impact of reconstituting these fibroblasts with wild-type EARS2 versus four additional EARS2 variants from COXPD12 patients with varying clinical severity. Metabolomics identified a group of signature metabolites, mostly from the TCA cycle and amino acid metabolism, that discriminate between EARS2 variants causing relatively mild and severe COXPD12. Taken together, these findings indicate that metabolomics in patient-derived fibroblasts may help establish genotype-phenotype correlations in EARS2 deficiency and likely other mitochondrial disorders.

Keywords: EARS2; genotype-phenotype correlation; inborn errors of metabolism; lactic acidosis; metabolomics; mitochondria.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acidosis, Lactic / etiology
  • Amino Acyl-tRNA Synthetases / genetics
  • Child
  • Child, Preschool
  • Female
  • Genetic Association Studies
  • Genetic Variation / genetics*
  • Glutamate-tRNA Ligase / genetics*
  • Glutamate-tRNA Ligase / metabolism
  • Humans
  • Infant
  • Infant, Newborn
  • Intellectual Disability / etiology
  • Leukoencephalopathies / genetics*
  • Leukoencephalopathies / metabolism
  • Male
  • Metabolism, Inborn Errors / genetics*
  • Metabolism, Inborn Errors / metabolism
  • Mitochondria / genetics
  • Mitochondria / metabolism
  • Mutation

Substances

  • Amino Acyl-tRNA Synthetases
  • Glutamate-tRNA Ligase