The in vivo mitochondrial two-step maturation of human frataxin

Hum Mol Genet. 2008 Nov 15;17(22):3521-31. doi: 10.1093/hmg/ddn244. Epub 2008 Aug 25.

Abstract

Deficiency in the nuclear-encoded mitochondrial protein frataxin causes Friedreich ataxia (FRDA), a progressive neurodegenerative disorder associating spinocerebellar ataxia and cardiomyopathy. Although the exact function of frataxin is still a matter of debate, it is widely accepted that frataxin is a mitochondrial iron chaperone involved in iron-sulfur cluster and heme biosynthesis. Frataxin is synthesized as a precursor polypeptide, directed to the mitochondrial matrix where it is proteolytically cleaved by the mitochondrial processing peptidase to the mature form via a processing intermediate. The mature form was initially reported to be encoded by amino acids 56-210 (m(56)-FXN). However, two independent reports have challenged these studies describing two different forms encoded by amino acids 78-210 (m(78)-FXN) and 81-210 (m(81)-FXN). Here, we provide evidence that mature human frataxin corresponds to m(81)-FXN, and can rescue the lethal phenotype of fibroblasts completely deleted for frataxin. Furthermore, our data demonstrate that the migration profile of frataxin depends on the experimental conditions, a behavior which most likely contributed to the confusion concerning the endogenous mature frataxin. Interestingly, we show that m(56)-FXN and m(78)-FXN can be generated when the normal maturation process of frataxin is impaired, although the physiological relevance is not clear. Furthermore, we determine that the d-FXN form, previously reported to be a degradation product, corresponds to m(78)-FXN. Finally, we demonstrate that all frataxin isoforms are generated and localized within the mitochondria. The clear identification of the N-terminus of mature FXN is an important step for designing therapeutic approaches for FRDA based on frataxin replacement.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Electrophoresis, Polyacrylamide Gel
  • Fibroblasts
  • Frataxin
  • Friedreich Ataxia / genetics
  • Friedreich Ataxia / metabolism
  • Humans
  • Iron-Binding Proteins / chemistry
  • Iron-Binding Proteins / genetics
  • Iron-Binding Proteins / metabolism*
  • Mice
  • Mitochondria / genetics
  • Mitochondria / metabolism*
  • Mitochondrial Proteins / metabolism
  • Mutagenesis, Site-Directed
  • Peptide Mapping
  • Protein Processing, Post-Translational*
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization

Substances

  • Iron-Binding Proteins
  • Mitochondrial Proteins
  • Recombinant Proteins