Mutations in FBXL4 cause mitochondrial encephalopathy and a disorder of mitochondrial DNA maintenance

Am J Hum Genet. 2013 Sep 5;93(3):471-81. doi: 10.1016/j.ajhg.2013.07.017. Epub 2013 Aug 29.

Abstract

Nuclear genetic disorders causing mitochondrial DNA (mtDNA) depletion are clinically and genetically heterogeneous, and the molecular etiology remains undiagnosed in the majority of cases. Through whole-exome sequencing, we identified recessive nonsense and splicing mutations in FBXL4 segregating in three unrelated consanguineous kindreds in which affected children present with a fatal encephalopathy, lactic acidosis, and severe mtDNA depletion in muscle. We show that FBXL4 is an F-box protein that colocalizes with mitochondria and that loss-of-function and splice mutations in this protein result in a severe respiratory chain deficiency, loss of mitochondrial membrane potential, and a disturbance of the dynamic mitochondrial network and nucleoid distribution in fibroblasts from affected individuals. Expression of the wild-type FBXL4 transcript in cell lines from two subjects fully rescued the levels of mtDNA copy number, leading to a correction of the mitochondrial biochemical deficit. Together our data demonstrate that mutations in FBXL4 are disease causing and establish FBXL4 as a mitochondrial protein with a possible role in maintaining mtDNA integrity and stability.

Publication types

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

MeSH terms

  • Acidosis, Lactic / complications
  • Acidosis, Lactic / genetics
  • Acidosis, Lactic / pathology
  • Base Sequence
  • Child
  • Child, Preschool
  • Chromosome Segregation / genetics
  • DNA, Mitochondrial / genetics*
  • Electron Transport / genetics
  • F-Box Proteins / chemistry
  • F-Box Proteins / genetics*
  • Female
  • Fibroblasts / metabolism
  • Fibroblasts / pathology
  • Gene Dosage / genetics
  • Genes, Recessive / genetics
  • Genetic Predisposition to Disease*
  • Humans
  • Infant
  • Infant, Newborn
  • Male
  • Mitochondrial Encephalomyopathies / complications
  • Mitochondrial Encephalomyopathies / genetics*
  • Mitochondrial Encephalomyopathies / pathology
  • Molecular Sequence Data
  • Muscle, Skeletal / pathology
  • Mutation / genetics*
  • Oxidative Phosphorylation
  • Pedigree
  • Protein Transport
  • Ubiquitin-Protein Ligases / chemistry
  • Ubiquitin-Protein Ligases / genetics*

Substances

  • DNA, Mitochondrial
  • F-Box Proteins
  • Ubiquitin-Protein Ligases
  • FbxL4 protein, human

Supplementary concepts

  • Mitochondrial encephalopathy