Mutations in LYRM4, encoding iron-sulfur cluster biogenesis factor ISD11, cause deficiency of multiple respiratory chain complexes

Hum Mol Genet. 2013 Nov 15;22(22):4460-73. doi: 10.1093/hmg/ddt295. Epub 2013 Jun 28.

Abstract

Iron-sulfur clusters (ISCs) are important prosthetic groups that define the functions of many proteins. Proteins with ISCs (called iron-sulfur or Fe-S proteins) are present in mitochondria, the cytosol, the endoplasmic reticulum and the nucleus. They participate in various biological pathways including oxidative phosphorylation (OXPHOS), the citric acid cycle, iron homeostasis, heme biosynthesis and DNA repair. Here, we report a homozygous mutation in LYRM4 in two patients with combined OXPHOS deficiency. LYRM4 encodes the ISD11 protein, which forms a complex with, and stabilizes, the sulfur donor NFS1. The homozygous mutation (c.203G>T, p.R68L) was identified via massively parallel sequencing of >1000 mitochondrial genes (MitoExome sequencing) in a patient with deficiency of complexes I, II and III in muscle and liver. These three complexes contain ISCs. Sanger sequencing identified the same mutation in his similarly affected cousin, who had a more severe phenotype and died while a neonate. Complex IV was also deficient in her skeletal muscle. Several other Fe-S proteins were also affected in both patients, including the aconitases and ferrochelatase. Mutant ISD11 only partially complemented for an ISD11 deletion in yeast. Our in vitro studies showed that the l-cysteine desulfurase activity of NFS1 was barely present when co-expressed with mutant ISD11. Our findings are consistent with a defect in the early step of ISC assembly affecting a broad variety of Fe-S proteins. The differences in biochemical and clinical features between the two patients may relate to limited availability of cysteine in the newborn period and suggest a potential approach to therapy.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Electron Transport
  • Female
  • Genes, Mitochondrial
  • Homozygote
  • Humans
  • Infant, Newborn
  • Iron-Regulatory Proteins / chemistry
  • Iron-Regulatory Proteins / genetics*
  • Iron-Regulatory Proteins / metabolism
  • Iron-Sulfur Proteins / deficiency*
  • Iron-Sulfur Proteins / genetics
  • Iron-Sulfur Proteins / metabolism
  • Liver / metabolism
  • Male
  • Mitochondria / genetics*
  • Mitochondria / metabolism
  • Mitochondrial Diseases / genetics*
  • Mitochondrial Diseases / metabolism*
  • Mitochondrial Diseases / pathology
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism
  • Molecular Sequence Data
  • Muscles / metabolism
  • Mutagenesis, Site-Directed
  • N-Ethylmaleimide-Sensitive Proteins / genetics
  • N-Ethylmaleimide-Sensitive Proteins / metabolism
  • Oxidative Phosphorylation
  • Point Mutation
  • Polymorphism, Single Nucleotide
  • Sequence Alignment
  • Sequence Analysis, DNA

Substances

  • Iron-Regulatory Proteins
  • Iron-Sulfur Proteins
  • LYRM4 protein, human
  • Mitochondrial Proteins
  • N-Ethylmaleimide-Sensitive Proteins