Mutations in COX10 result in a defect in mitochondrial heme A biosynthesis and account for multiple, early-onset clinical phenotypes associated with isolated COX deficiency

Hum Mol Genet. 2003 Oct 15;12(20):2693-702. doi: 10.1093/hmg/ddg284. Epub 2003 Aug 19.

Abstract

Deficiencies in the activity of cytochrome c oxidase (COX) are an important cause of autosomal recessive respiratory chain disorders. Patients with isolated COX deficiency are clinically and genetically heterogeneous, and mutations in several different assembly factors have been found to cause specific clinical phenotypes. Two of the most common clinical presentations, Leigh Syndrome and hypertrophic cardiomyopathy, have so far only been associated with mutations in SURF1 or SCO2 and COX15, respectively. Here we show that expression of COX10 from a retroviral vector complements the COX deficiency in a patient with anemia and Leigh Syndrome, and in a patient with anemia, sensorineural deafness and fatal infantile hypertrophic cardiomyopathy. A partial rescue was also obtained following microcell-mediated transfer of mouse chromosomes into patient fibroblasts. COX10 functions in the first step of the mitochondrial heme A biosynthetic pathway, catalyzing the conversion of protoheme (heme B) to heme O via the farnesylation of a vinyl group at position C2. Heme A content was reduced in mitochondria from patient muscle and fibroblasts in proportion to the reduction in COX enzyme activity and the amount of fully assembled enzyme. Mutation analysis of COX10 identified four different missense alleles, predicting amino acid substitutions at evolutionarily conserved residues. A topological model places these residues in regions of the protein shown to have important catalytic functions by mutation analysis of a prokaryotic ortholog. Mutations in COX10 have previously been reported in a single family with tubulopathy and leukodystrophy. This study shows that mutations in this gene can cause nearly the full range of clinical phenotypes associated with early onset isolated COX deficiency.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alkyl and Aryl Transferases / genetics*
  • Amino Acid Sequence
  • Animals
  • Cardiomyopathies / genetics
  • Catalysis
  • Chromatography, High Pressure Liquid
  • Chromosomes / ultrastructure
  • Cloning, Molecular
  • DNA Mutational Analysis
  • Electron Transport Complex IV
  • Electrophoresis, Polyacrylamide Gel
  • Exons
  • Fibroblasts / metabolism
  • Genetic Complementation Test
  • Genome
  • Heme / analogs & derivatives*
  • Heme / chemistry
  • Heme / genetics*
  • Humans
  • Membrane Proteins / genetics*
  • Mice
  • Mitochondria / genetics*
  • Mitochondria / metabolism
  • Molecular Sequence Data
  • Mutation*
  • Phenotype
  • Retroviridae / genetics

Substances

  • Membrane Proteins
  • heme a
  • Heme
  • COX10 protein, human
  • Electron Transport Complex IV
  • Alkyl and Aryl Transferases