CMT-associated mutations in glycyl- and tyrosyl-tRNA synthetases exhibit similar pattern of toxicity and share common genetic modifiers in Drosophila

Neurobiol Dis. 2014 Aug:68:180-9. doi: 10.1016/j.nbd.2014.04.020. Epub 2014 May 5.

Abstract

Aminoacyl-tRNA synthetases are ubiquitously expressed proteins that charge tRNAs with their cognate amino acids. By ensuring the fidelity of protein synthesis, these enzymes are essential for the viability of every cell. Yet, mutations in six tRNA synthetases specifically affect the peripheral nerves and cause Charcot-Marie-Tooth (CMT) disease. The CMT-causing mutations in tyrosyl- and glycyl-tRNA synthetases (YARS and GARS, respectively) alter the activity of the proteins in a range of ways (some mutations do not impact charging function, while others abrogate it), making a loss of function in tRNA charging unlikely to be the cause of disease pathology. It is currently unknown which cellular mechanisms are triggered by the mutant enzymes and how this leads to neurodegeneration. Here, by expressing two pathogenic mutations (G240R, P234KY) in Drosophila, we generated a model for GARS-associated neuropathy. We observed compromised viability, and behavioral, electrophysiological and morphological impairment in flies expressing the cytoplasmic isoform of mutant GARS. Their features recapitulated several hallmarks of CMT pathophysiology and were similar to the phenotypes identified in our previously described Drosophila model of YARS-associated neuropathy. Furthermore, CG8316 and CG15599 - genes identified in a retinal degeneration screen to modify mutant YARS, also modified the mutant GARS phenotypes. Our study presents genetic evidence for common mutant-specific interactions between two CMT-associated aminoacyl-tRNA synthetases, lending support for a shared mechanism responsible for the synthetase-induced peripheral neuropathies.

Keywords: Aminoacyl-tRNA synthetase; Charcot–Marie–Tooth disease; Drosophila.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Charcot-Marie-Tooth Disease / complications*
  • Charcot-Marie-Tooth Disease / genetics*
  • Charcot-Marie-Tooth Disease / pathology
  • Dextrans
  • Disease Models, Animal
  • Drosophila
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Female
  • Glycine-tRNA Ligase / genetics*
  • Humans
  • Male
  • Membrane Potentials / genetics
  • Membrane Potentials / physiology
  • Mutation / genetics*
  • Nerve Fibers / physiology
  • Neurons / pathology
  • Neurons / physiology
  • Peripheral Nervous System Diseases / etiology*
  • Peripheral Nervous System Diseases / genetics
  • Retina / pathology
  • Retina / ultrastructure
  • Retinal Degeneration / diagnosis
  • Retinal Degeneration / etiology
  • Retinal Degeneration / genetics
  • Rhodamines
  • Tyrosine-tRNA Ligase / genetics*
  • Wings, Animal / pathology
  • Wings, Animal / ultrastructure

Substances

  • Dextrans
  • Drosophila Proteins
  • Fluoro-Ruby
  • Rhodamines
  • Tyrosine-tRNA Ligase
  • Glycine-tRNA Ligase