Recurrent De Novo and Biallelic Variation of ATAD3A, Encoding a Mitochondrial Membrane Protein, Results in Distinct Neurological Syndromes

Am J Hum Genet. 2016 Oct 6;99(4):831-845. doi: 10.1016/j.ajhg.2016.08.007. Epub 2016 Sep 15.

Abstract

ATPase family AAA-domain containing protein 3A (ATAD3A) is a nuclear-encoded mitochondrial membrane protein implicated in mitochondrial dynamics, nucleoid organization, protein translation, cell growth, and cholesterol metabolism. We identified a recurrent de novo ATAD3A c.1582C>T (p.Arg528Trp) variant by whole-exome sequencing (WES) in five unrelated individuals with a core phenotype of global developmental delay, hypotonia, optic atrophy, axonal neuropathy, and hypertrophic cardiomyopathy. We also describe two families with biallelic variants in ATAD3A, including a homozygous variant in two siblings, and biallelic ATAD3A deletions mediated by nonallelic homologous recombination (NAHR) between ATAD3A and gene family members ATAD3B and ATAD3C. Tissue-specific overexpression of borR534W, the Drosophila mutation homologous to the human c.1582C>T (p.Arg528Trp) variant, resulted in a dramatic decrease in mitochondrial content, aberrant mitochondrial morphology, and increased autophagy. Homozygous null bor larvae showed a significant decrease of mitochondria, while overexpression of borWT resulted in larger, elongated mitochondria. Finally, fibroblasts of an affected individual exhibited increased mitophagy. We conclude that the p.Arg528Trp variant functions through a dominant-negative mechanism that results in small mitochondria that trigger mitophagy, resulting in a reduction in mitochondrial content. ATAD3A variation represents an additional link between mitochondrial dynamics and recognizable neurological syndromes, as seen with MFN2, OPA1, DNM1L, and STAT2 mutations.

Keywords: ATAD3A; CNV; cardiomyopathy; de novo variant; dominant negative; mitochondrial dynamics; neuropathy; optic atrophy; whole-exome sequencing.

MeSH terms

  • ATPases Associated with Diverse Cellular Activities
  • Adenosine Triphosphatases / genetics*
  • Adult
  • Alleles*
  • Animals
  • Axons / pathology
  • Cardiomyopathies / genetics
  • Child
  • Child, Preschool
  • DNA Copy Number Variations / genetics
  • Developmental Disabilities / genetics
  • Drosophila melanogaster / genetics
  • Female
  • Fibroblasts
  • Homozygote
  • Humans
  • Infant
  • Infant, Newborn
  • Male
  • Membrane Proteins / genetics*
  • Mitochondria / metabolism*
  • Mitochondria / pathology*
  • Mitochondrial Proteins / genetics*
  • Muscle Hypotonia / genetics
  • Muscles / pathology
  • Mutation*
  • Nervous System Diseases / genetics*
  • Nervous System Diseases / metabolism
  • Nervous System Diseases / pathology
  • Neurons / pathology
  • Optic Atrophy / genetics
  • Phenotype
  • Polymorphism, Single Nucleotide / genetics
  • Syndrome
  • Young Adult

Substances

  • ATAD3A protein, human
  • Membrane Proteins
  • Mitochondrial Proteins
  • Adenosine Triphosphatases
  • ATPases Associated with Diverse Cellular Activities