Mutations in the mitochondrial complex I assembly factor NDUFAF6 cause isolated bilateral striatal necrosis and progressive dystonia in childhood

Mol Genet Metab. 2019 Mar;126(3):250-258. doi: 10.1016/j.ymgme.2019.01.001. Epub 2019 Jan 5.

Abstract

Aim: To perform a deep phenotype characterisation in a pedigree of 3 siblings with Leigh syndrome and compound heterozygous NDUFAF6 mutations.

Method: A multi-gene panel of childhood-onset basal ganglia neurodegeneration inherited conditions was analysed followed by functional studies in fibroblasts.

Results: Three siblings developed gait dystonia in infancy followed by rapid progression to generalised dystonia and psychomotor regression. Brain magnetic resonance showed symmetric and bilateral cytotoxic lesions in the putamen and proliferation of the lenticular-striate arteries, latter spreading to the caudate and progressing to cavitation and volume loss. We identified a frameshift novel change (c.554_558delTTCTT; p.Tyr187AsnfsTer65) and a pathogenic missense change (c.371T>C; p.Ile124Thr) in the NDUFAF6 gene, which segregated with an autosomal recessive inheritance within the family. Patient mutations were associated with the absence of the NDUFAF6 protein and reduced activity and assembly of mature complex I in fibroblasts. By functional complementation assay, the mutant phenotype was rescued by the canonical version of the NDUFAF6. A literature review of 14 NDUFAF6 patients showed a consistent phenotype of an early childhood insidious onset neurological regression with prominent dystonia associated with basal ganglia degeneration and long survival.

Interpretation: NDUFAF6-related Leigh syndrome is a relevant cause of childhood onset dystonia and isolated bilateral striatal necrosis. By genetic complementation, we could demonstrate the pathogenicity of novel genetic variants in NDUFAF6.

Keywords: Bilateral striatal necrosis; Complex I deficiency; Dystonia; Leigh syndrome; Mitochondrial disease; NDUFAF6.

Publication types

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

MeSH terms

  • Biopsy
  • Child
  • Cohort Studies
  • Dystonic Disorders / genetics*
  • Electron Transport Complex I / genetics*
  • Female
  • Fibroblasts
  • Gene Expression
  • Genetic Variation
  • Humans
  • Leigh Disease / complications
  • Leigh Disease / genetics*
  • Male
  • Mitochondrial Proteins / genetics*
  • Muscles / pathology
  • Mutation
  • Pedigree
  • Siblings
  • Striatonigral Degeneration / congenital*
  • Striatonigral Degeneration / genetics

Substances

  • Mitochondrial Proteins
  • NDUFAF6 protein, human
  • Electron Transport Complex I

Supplementary concepts

  • Striatonigral Degeneration, Infantile, Mitochondrial