Expression of an expanded CGG-repeat RNA in a single pair of primary sensory neurons impairs olfactory adaptation in Caenorhabditis elegans

Hum Mol Genet. 2014 Sep 15;23(18):4945-59. doi: 10.1093/hmg/ddu210. Epub 2014 May 12.

Abstract

Fragile X-associated tremor/ataxia syndrome (FXTAS) is a severe neurodegenerative disorder that affects carriers of premutation CGG-repeat expansion alleles of the fragile X mental retardation 1 (FMR1) gene; current evidence supports a causal role of the expanded CGG repeat within the FMR1 mRNA in the pathogenesis of FXTAS. Though the mRNA has been observed to induce cellular toxicity in FXTAS, the mechanisms are unclear. One common neurophysiological characteristic of FXTAS patients is their inability to properly attenuate their response to an auditory stimulus upon receipt of a small pre-stimulus. Therefore, to gain genetic and cell biological insight into FXTAS, we examined the effect of expanded CGG repeats on the plasticity of the olfactory response of the genetically tractable nematode, Caenorhabditis elegans (C. elegans). While C. elegans is innately attracted to odors, this response can be downregulated if the odor is paired with starvation. We found that expressing expanded CGG repeats in olfactory neurons interfered with this plasticity without affecting either the innate odor-seeking response or the olfactory neuronal morphology. Interrogation of three RNA regulatory pathways indicated that the expanded CGG repeats act via the C. elegans microRNA (miRNA)-specific Argonaute ALG-2 to diminish olfactory plasticity. This observation suggests that the miRNA-Argonaute pathway may play a pathogenic role in subverting neuronal function in FXTAS.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Argonaute Proteins / genetics
  • Ataxia / genetics
  • Ataxia / pathology
  • Butanones / pharmacology*
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / physiology*
  • Disease Models, Animal
  • Fragile X Mental Retardation Protein / genetics*
  • Fragile X Syndrome / genetics
  • Fragile X Syndrome / pathology
  • Humans
  • Neuronal Plasticity
  • Olfactory Receptor Neurons / metabolism*
  • Sensory Receptor Cells / metabolism*
  • Smell
  • Tremor / genetics
  • Tremor / pathology
  • Trinucleotide Repeat Expansion

Substances

  • Argonaute Proteins
  • Butanones
  • FMR1 protein, human
  • Fragile X Mental Retardation Protein

Supplementary concepts

  • Fragile X Tremor Ataxia Syndrome