CGG repeat-associated translation mediates neurodegeneration in fragile X tremor ataxia syndrome

Neuron. 2013 May 8;78(3):440-55. doi: 10.1016/j.neuron.2013.03.026. Epub 2013 Apr 18.

Abstract

Fragile X-associated tremor ataxia syndrome (FXTAS) results from a CGG repeat expansion in the 5' UTR of FMR1. This repeat is thought to elicit toxicity as RNA, yet disease brains contain ubiquitin-positive neuronal inclusions, a pathologic hallmark of protein-mediated neurodegeneration. We explain this paradox by demonstrating that CGG repeats trigger repeat-associated non-AUG-initiated (RAN) translation of a cryptic polyglycine-containing protein, FMRpolyG. FMRpolyG accumulates in ubiquitin-positive inclusions in Drosophila, cell culture, mouse disease models, and FXTAS patient brains. CGG RAN translation occurs in at least two of three possible reading frames at repeat sizes ranging from normal (25) to pathogenic (90), but inclusion formation only occurs with expanded repeats. In Drosophila, CGG repeat toxicity is suppressed by eliminating RAN translation and enhanced by increased polyglycine protein production. These studies expand the growing list of nucleotide repeat disorders in which RAN translation occurs and provide evidence that RAN translation contributes to neurodegeneration.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Ataxia / genetics*
  • Ataxia / metabolism
  • Ataxia / pathology
  • Brain / metabolism*
  • Brain / pathology
  • Cells, Cultured
  • Disease Models, Animal
  • Drosophila
  • Fragile X Mental Retardation Protein / genetics*
  • Fragile X Mental Retardation Protein / metabolism
  • Fragile X Syndrome / genetics*
  • Fragile X Syndrome / metabolism
  • Fragile X Syndrome / pathology
  • Humans
  • Nerve Degeneration / genetics*
  • Nerve Degeneration / metabolism
  • Nerve Degeneration / pathology
  • Neurons / metabolism
  • Neurons / pathology
  • Protein Biosynthesis
  • Tremor / genetics*
  • Tremor / metabolism
  • Tremor / pathology
  • Trinucleotide Repeat Expansion / genetics*

Substances

  • Fragile X Mental Retardation Protein

Supplementary concepts

  • Fragile X Tremor Ataxia Syndrome