Mutations in COX15 produce a defect in the mitochondrial heme biosynthetic pathway, causing early-onset fatal hypertrophic cardiomyopathy

Am J Hum Genet. 2003 Jan;72(1):101-14. doi: 10.1086/345489. Epub 2002 Dec 9.

Abstract

Deficiencies in the activity of cytochrome c oxidase (COX), the terminal enzyme in the respiratory chain, are a frequent cause of autosomal recessive mitochondrial disease in infants. These patients are clinically and genetically heterogeneous, and all defects so far identified in this group have been found in genes coding for accessory proteins that play important roles in the assembly of the COX holoenzyme complex. Many patients, however, remain without a molecular diagnosis. We have used a panel of retroviral vectors expressing human COX assembly factors in these patients to identify the molecular basis for the COX deficiency by functional complementation. Here we show that overexpression of COX15, a protein involved in the synthesis of heme A, the heme prosthetic group for COX, can functionally complement the isolated COX deficiency in fibroblasts from a patient with fatal, infantile hypertrophic cardiomyopathy. Mutation analysis of COX15 in the patient identified a missense mutation (C700T) on one allele, changing a conserved arginine to tryptophan (R217W), and a splice-site mutation in intron 3 on the other allele (C447-3G), resulting in a deletion of exon 4. This splicing error introduces a frameshift and a premature stop codon, resulting in an unstable mRNA and, likely, a null allele. Mitochondrial heme A content was reduced in the patient's heart and fibroblast mitochondria, and levels of heme O were increased in the patient's heart. COX activity and the total amount of fully assembled enzyme were reduced by 50%-70% in patient fibroblasts. Expression of COX15 increased heme A content and rescued COX activity. These results suggest that reduced availability of heme A stalls the assembly of COX. This study establishes COX15 as an additional cause, along with SCO2, of fatal infantile, hypertrophic cardiomyopathy associated with isolated COX deficiency.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Age of Onset
  • Amino Acid Sequence
  • Animals
  • Base Sequence
  • Cardiomyopathy, Hypertrophic / enzymology
  • Cardiomyopathy, Hypertrophic / genetics*
  • Cardiomyopathy, Hypertrophic / metabolism*
  • Cardiomyopathy, Hypertrophic / pathology
  • DNA Mutational Analysis
  • Fibroblasts
  • Heme / analogs & derivatives*
  • Heme / biosynthesis*
  • Humans
  • Membrane Proteins / biosynthesis
  • Membrane Proteins / genetics*
  • Membrane Proteins / metabolism
  • Mitochondria, Heart / enzymology
  • Mitochondria, Heart / metabolism*
  • Molecular Sequence Data
  • Mutation / genetics*
  • Myocardium / enzymology
  • Myocardium / metabolism
  • Myocardium / pathology
  • Saccharomyces cerevisiae Proteins*

Substances

  • COX15 protein, S cerevisiae
  • Membrane Proteins
  • Saccharomyces cerevisiae Proteins
  • heme O
  • heme a
  • Heme

Associated data

  • OMIM/220110
  • OMIM/602472
  • OMIM/603646
  • OMIM/604377