Dominant, toxic gain-of-function mutations in gars lead to non-cell autonomous neuropathology

Hum Mol Genet. 2015 Aug 1;24(15):4397-406. doi: 10.1093/hmg/ddv176. Epub 2015 May 13.

Abstract

Charcot-Marie-Tooth (CMT) neuropathies are collectively the most common hereditary neurological condition and a major health burden for society. Dominant mutations in the gene GARS, encoding the ubiquitous enzyme, glycyl-tRNA synthetase (GlyRS), cause peripheral nerve degeneration and lead to CMT disease type 2D. This genetic disorder exemplifies a recurring motif in neurodegeneration, whereby mutations in essential, widely expressed genes have selective deleterious consequences for the nervous system. Here, using novel Drosophila models, we show a potential solution to this phenomenon. Ubiquitous expression of mutant GlyRS leads to motor deficits, progressive neuromuscular junction (NMJ) denervation and pre-synaptic build-up of mutant GlyRS. Intriguingly, neuronal toxicity is, at least in part, non-cell autonomous, as expression of mutant GlyRS in mesoderm or muscle alone results in similar pathology. This mutant GlyRS toxic gain-of-function, which is WHEP domain-dependent, coincides with abnormal NMJ assembly, leading to synaptic degeneration, and, ultimately, reduced viability. Our findings suggest that mutant GlyRS gains access to ectopic sub-compartments of the motor neuron, providing a possible explanation for the selective neuropathology caused by mutations in a widely expressed gene.

Publication types

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

MeSH terms

  • Animals
  • Charcot-Marie-Tooth Disease / genetics*
  • Charcot-Marie-Tooth Disease / pathology
  • Disease Models, Animal
  • Drosophila melanogaster / genetics
  • Gene Expression Regulation
  • Glycine-tRNA Ligase / biosynthesis
  • Glycine-tRNA Ligase / genetics*
  • Humans
  • Mushroom Bodies / pathology
  • Mutation
  • Nerve Degeneration / genetics*
  • Nerve Degeneration / pathology
  • Neuromuscular Junction / genetics*
  • Neuromuscular Junction / growth & development
  • Neuromuscular Junction / pathology
  • Olfactory Bulb / pathology
  • Peripheral Nerves / pathology

Substances

  • Glycine-tRNA Ligase

Supplementary concepts

  • Charcot-Marie-Tooth disease, Type 2D