Loss of holocytochrome c-type synthetase causes the male lethality of X-linked dominant microphthalmia with linear skin defects (MLS) syndrome

Hum Mol Genet. 2002 Dec 1;11(25):3237-48. doi: 10.1093/hmg/11.25.3237.

Abstract

Girls with MLS syndrome have microphthalmia with linear skin defects of face and neck, sclerocornea, corpus callosum agenesis and other brain anomalies. This X-linked dominant, male-lethal condition is associated with heterozygous deletions of a critical region in Xp22.31, from the 5' untranslated region of MID1 at the telomeric boundary to the ARHGAP6 gene at the centromeric boundary. HCCS, encoding human holocytochrome c-type synthetase, is the only gene located entirely inside the critical region. Because single gene analysis is not feasible in MLS patients (all have deletions), we generated a deletion of the equivalent region in the mouse to study the molecular basis of this syndrome. This deletion inactivates mouse Hccs, whose homologs in lower organisms (cytochrome c or c1 heme lyases) are essential for function of cytochrome c or c1 in the mitochondrial respiratory chain. Ubiquitous deletions generated in vivo lead to lethality of hemizygous, homozygous and heterozygous embryos early in development. This lethality is rescued by expression of the human HCCS gene from a transgenic BAC, resulting in viable homozygous, heterozygous and hemizygous deleted mice with no apparent phenotype. In the presence of the HCCS transgene, the deletion is easily transmitted to subsequent generations. We did obtain a single heterozygous deleted female that does not express human HCCS, which is analogous to the low prevalence of the heterozygous MLS deletion in humans. Through the study of these genetically engineered mice we demonstrate that loss of HCCS causes the male lethality of MLS syndrome.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • 5' Untranslated Regions / genetics
  • Animals
  • Blastocyst / chemistry
  • Blastocyst / metabolism
  • Cell Survival / genetics
  • Disease Models, Animal
  • Exons / genetics
  • Female
  • Gene Deletion
  • Genes, Dominant / genetics*
  • Genes, Lethal / genetics
  • Genetic Linkage*
  • Genetic Variation
  • Holoenzymes / deficiency
  • Holoenzymes / genetics
  • Holoenzymes / physiology
  • Humans
  • Lyases / deficiency*
  • Lyases / genetics
  • Lyases / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Microphthalmos / genetics*
  • Mosaicism / genetics
  • Phenotype
  • Sequence Homology, Nucleic Acid
  • Skin Abnormalities / genetics*
  • Syndrome
  • Totipotent Stem Cells / chemistry
  • Totipotent Stem Cells / metabolism
  • Transgenes
  • X Chromosome / genetics*

Substances

  • 5' Untranslated Regions
  • Holoenzymes
  • Lyases
  • cytochrome C synthetase