RNA interference mitigates motor and neuropathological deficits in a cerebellar mouse model of Machado-Joseph disease

PLoS One. 2014 Aug 21;9(8):e100086. doi: 10.1371/journal.pone.0100086. eCollection 2014.

Abstract

Machado-Joseph disease or Spinocerebellar ataxia type 3 is a progressive fatal neurodegenerative disorder caused by the polyglutamine-expanded protein ataxin-3. Recent studies demonstrate that RNA interference is a promising approach for the treatment of Machado-Joseph disease. However, whether gene silencing at an early time-point is able to prevent the appearance of motor behavior deficits typical of the disease when initiated before onset of the disease had not been explored. Here, using a lentiviral-mediated allele-specific silencing of mutant ataxin-3 in an early pre-symptomatic cerebellar mouse model of Machado-Joseph disease we show that this strategy hampers the development of the motor and neuropathological phenotypic characteristics of the disease. At the histological level, the RNA-specific silencing of mutant ataxin-3 decreased formation of mutant ataxin-3 aggregates, preserved Purkinje cell morphology and expression of neuronal markers while reducing cell death. Importantly, gene silencing prevented the development of impairments in balance, motor coordination, gait and hyperactivity observed in control mice. These data support the therapeutic potential of RNA interference for Machado-Joseph disease and constitute a proof of principle of the beneficial effects of early allele-specific silencing for therapy of this disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Ataxin-3
  • Cerebellum / metabolism
  • Cerebellum / pathology
  • Disease Models, Animal
  • Gene Silencing
  • Machado-Joseph Disease / genetics*
  • Machado-Joseph Disease / metabolism
  • Machado-Joseph Disease / pathology*
  • Mice
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • RNA Interference / physiology*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Nuclear Proteins
  • Transcription Factors
  • Ataxin-3
  • Atxn3 protein, mouse

Grants and funding

We thank the Portuguese Foundation for Science and Technology and FEDER funds by Programa Operacional Factores de Competitividade – COMPETE (PTDC/SAU-NEU/099307/2008, PTDC/SAU-FAR/116535/2010 and PEst-C/SAU/LA0001/2013-2014), the Richard Chin and Lily Lock Machado-Joseph Research Fund, the National Ataxia Foundation, and the Association Française pour les Myopathies (SB/NF/2010/2008 Number 15079CA) for funding. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.