Altered zinc transport disrupts mitochondrial protein processing/import in fragile X-associated tremor/ataxia syndrome

Hum Mol Genet. 2011 Aug 1;20(15):3079-92. doi: 10.1093/hmg/ddr211. Epub 2011 May 10.

Abstract

Fragile X-associated tremor/ataxia syndrome (FXTAS) is a late-onset neurodegenerative disorder that affects individuals who are carriers of small CGG premutation expansions in the fragile X mental retardation 1 (FMR1) gene. Mitochondrial dysfunction was observed as an incipient pathological process occurring in individuals who do not display overt features of FXTAS (1). Fibroblasts from premutation carriers had lower oxidative phosphorylation capacity (35% of controls) and Complex IV activity (45%), and higher precursor-to-mature ratios (P:M) of nDNA-encoded mitochondrial proteins (3.1-fold). However, fibroblasts from carriers with FXTAS symptoms presented higher FMR1 mRNA expression (3-fold) and lower Complex V (38%) and aconitase activities (43%). Higher P:M of ATPase β-subunit (ATPB) and frataxin were also observed in cortex from patients that died with FXTAS symptoms. Biochemical findings observed in FXTAS cells (lower mature frataxin, lower Complex IV and aconitase activities) along with common phenotypic traits shared by Friedreich's ataxia and FXTAS carriers (e.g. gait ataxia, loss of coordination) are consistent with a defective iron homeostasis in both diseases. Higher P:M, and lower ZnT6 and mature frataxin protein expression suggested defective zinc and iron metabolism arising from altered ZnT protein expression, which in turn impairs the activity of mitochondrial Zn-dependent proteases, critical for the import and processing of cytosolic precursors, such as frataxin. In support of this hypothesis, Zn-treated fibroblasts showed a significant recovery of ATPB P:M, ATPase activity and doubling time, whereas Zn and desferrioxamine extended these recoveries and rescued Complex IV activity.

Publication types

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

MeSH terms

  • Aged
  • Blotting, Western
  • Cells, Cultured
  • DNA, Mitochondrial / genetics
  • Female
  • Fragile X Mental Retardation Protein / genetics
  • Fragile X Mental Retardation Protein / metabolism
  • Fragile X Syndrome / genetics
  • Fragile X Syndrome / metabolism*
  • Gene Dosage / genetics
  • Humans
  • Hydrogen Peroxide / metabolism
  • In Vitro Techniques
  • Ion Transport / genetics
  • Ion Transport / physiology*
  • Male
  • Mitochondrial Proteins / genetics*
  • Mitochondrial Proteins / metabolism*
  • Zinc / metabolism*

Substances

  • DNA, Mitochondrial
  • FMR1 protein, human
  • Mitochondrial Proteins
  • Fragile X Mental Retardation Protein
  • Hydrogen Peroxide
  • Zinc