Loss of seryl-tRNA synthetase (SARS1) causes complex spastic paraplegia and cellular senescence

J Med Genet. 2022 Dec;59(12):1227-1233. doi: 10.1136/jmg-2022-108529. Epub 2022 Aug 30.

Abstract

Background: Aminoacyl-tRNA synthetases (ARS) are key enzymes catalysing the first reactions in protein synthesis, with increasingly recognised pleiotropic roles in tumourgenesis, angiogenesis, immune response and lifespan. Germline mutations in several ARS genes have been associated with both recessive and dominant neurological diseases. Recently, patients affected with microcephaly, intellectual disability and ataxia harbouring biallelic variants in the seryl-tRNA synthetase encoded by seryl-tRNA synthetase 1 (SARS1) were reported.

Methods: We used exome sequencing to identify the causal variant in a patient affected by complex spastic paraplegia with ataxia, intellectual disability, developmental delay and seizures, but without microcephaly. Complementation and serylation assays using patient's fibroblasts and an Saccharomyces cerevisiae model were performed to examine this variant's pathogenicity.

Results: A de novo splice site deletion in SARS1 was identified in our patient, resulting in a 5-amino acid in-frame insertion near its active site. Complementation assays in S. cerevisiae and serylation assays in both yeast strains and patient fibroblasts proved a loss-of-function, dominant negative effect. Fibroblasts showed an abnormal cell shape, arrested division and increased beta-galactosidase staining along with a senescence-associated secretory phenotype (raised interleukin-6, p21, p16 and p53 levels).

Conclusion: We refine the phenotypic spectrum and modes of inheritance of a newly described, ultrarare neurodevelopmental disorder, while unveiling the role of SARS1 as a regulator of cell growth, division and senescence.

Keywords: genetic research; nervous system diseases; neurology; pediatrics; sequence analysis, RNA.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acyl-tRNA Synthetases* / genetics
  • Ataxia
  • Cellular Senescence / genetics
  • Humans
  • Intellectual Disability* / genetics
  • Ligases
  • Microcephaly* / genetics
  • Paraplegia / genetics
  • Saccharomyces cerevisiae / genetics
  • Serine-tRNA Ligase* / chemistry
  • Serine-tRNA Ligase* / metabolism

Substances

  • Amino Acyl-tRNA Synthetases
  • Ligases
  • Serine-tRNA Ligase