Pathological variants in TOP3A cause distinct disorders of mitochondrial and nuclear genome stability

EMBO Mol Med. 2023 May 8;15(5):e16775. doi: 10.15252/emmm.202216775. Epub 2023 Apr 4.

Abstract

Topoisomerase 3α (TOP3A) is an enzyme that removes torsional strain and interlinks between DNA molecules. TOP3A localises to both the nucleus and mitochondria, with the two isoforms playing specialised roles in DNA recombination and replication respectively. Pathogenic variants in TOP3A can cause a disorder similar to Bloom syndrome, which results from bi-allelic pathogenic variants in BLM, encoding a nuclear-binding partner of TOP3A. In this work, we describe 11 individuals from 9 families with an adult-onset mitochondrial disease resulting from bi-allelic TOP3A gene variants. The majority of patients have a consistent clinical phenotype characterised by bilateral ptosis, ophthalmoplegia, myopathy and axonal sensory-motor neuropathy. We present a comprehensive characterisation of the effect of TOP3A variants, from individuals with mitochondrial disease and Bloom-like syndrome, upon mtDNA maintenance and different aspects of enzyme function. Based on these results, we suggest a model whereby the overall severity of the TOP3A catalytic defect determines the clinical outcome, with milder variants causing adult-onset mitochondrial disease and more severe variants causing a Bloom-like syndrome with mitochondrial dysfunction in childhood.

Keywords: Bloom syndrome; TOP3A; mitochondrial disease; mtDNA.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • DNA, Mitochondrial / genetics
  • Genomic Instability
  • Humans
  • Mitochondria / genetics
  • Mitochondrial Diseases* / genetics
  • Muscular Diseases*
  • Syndrome

Substances

  • DNA, Mitochondrial