Mistargeting of peroxisomal EHHADH and inherited renal Fanconi's syndrome

N Engl J Med. 2014 Jan 9;370(2):129-38. doi: 10.1056/NEJMoa1307581.

Abstract

Background: In renal Fanconi's syndrome, dysfunction in proximal tubular cells leads to renal losses of water, electrolytes, and low-molecular-weight nutrients. For most types of isolated Fanconi's syndrome, the genetic cause and underlying defect remain unknown.

Methods: We clinically and genetically characterized members of a five-generation black family with isolated autosomal dominant Fanconi's syndrome. We performed genomewide linkage analysis, gene sequencing, biochemical and cell-biologic investigations of renal proximal tubular cells, studies in knockout mice, and functional evaluations of mitochondria. Urine was studied with the use of proton nuclear magnetic resonance ((1)H-NMR) spectroscopy.

Results: We linked the phenotype of this family's Fanconi's syndrome to a single locus on chromosome 3q27, where a heterozygous missense mutation in EHHADH segregated with the disease. The p.E3K mutation created a new mitochondrial targeting motif in the N-terminal portion of EHHADH, an enzyme that is involved in peroxisomal oxidation of fatty acids and is expressed in the proximal tubule. Immunocytofluorescence studies showed mistargeting of the mutant EHHADH to mitochondria. Studies of proximal tubular cells revealed impaired mitochondrial oxidative phosphorylation and defects in the transport of fluids and a glucose analogue across the epithelium. (1)H-NMR spectroscopy showed elevated levels of mitochondrial metabolites in urine from affected family members. Ehhadh knockout mice showed no abnormalities in renal tubular cells, a finding that indicates a dominant negative nature of the mutation rather than haploinsufficiency.

Conclusions: Mistargeting of peroxisomal EHHADH disrupts mitochondrial metabolism and leads to renal Fanconi's syndrome; this indicates a central role of mitochondria in proximal tubular function. The dominant negative effect of the mistargeted protein adds to the spectrum of monogenic mechanisms of Fanconi's syndrome. (Funded by the European Commission Seventh Framework Programme and others.).

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Black People
  • Chromosomes, Human, Pair 3
  • Disease Models, Animal
  • Fanconi Syndrome / ethnology
  • Fanconi Syndrome / genetics*
  • Female
  • Genetic Linkage
  • Humans
  • Kidney Tubules, Proximal / metabolism*
  • Male
  • Mice
  • Mice, Knockout
  • Mitochondria / metabolism*
  • Molecular Sequence Data
  • Mutation, Missense*
  • Pedigree
  • Peroxisomal Bifunctional Enzyme / chemistry
  • Peroxisomal Bifunctional Enzyme / genetics*
  • Peroxisomal Bifunctional Enzyme / metabolism
  • Phenotype
  • Sequence Analysis, DNA

Substances

  • EHHADH protein, human
  • Peroxisomal Bifunctional Enzyme