Silencing mutant ataxin-3 rescues motor deficits and neuropathology in Machado-Joseph disease transgenic mice

PLoS One. 2013;8(1):e52396. doi: 10.1371/journal.pone.0052396. Epub 2013 Jan 22.

Abstract

Machado-Joseph disease (MJD) or spinocerebellar ataxia type 3 (SCA3) is an autosomal dominantly-inherited neurodegenerative disorder caused by the over-repetition of a CAG codon in the MJD1 gene. This expansion translates into a polyglutamine tract that confers a toxic gain-of-function to the mutant protein--ataxin-3, leading to neurodegeneration in specific brain regions, with particular severity in the cerebellum. No treatment able to modify the disease progression is available. However, gene silencing by RNA interference has shown promising results. Therefore, in this study we investigated whether lentiviral-mediated allele-specific silencing of the mutant ataxin-3 gene, after disease onset, would rescue the motor behavior deficits and neuropathological features in a severely impaired transgenic mouse model of MJD. For this purpose, we injected lentiviral vectors encoding allele-specific silencing-sequences (shAtx3) into the cerebellum of diseased transgenic mice expressing the targeted C-variant of mutant ataxin-3 present in 70% of MJD patients. This variation permits to discriminate between the wild-type and mutant forms, maintaining the normal function of the wild-type allele and silencing only the mutant form. Quantitative analysis of rotarod performance, footprint and activity patterns revealed significant and robust alleviation of gait, balance (average 3-fold increase of rotarod test time), locomotor and exploratory activity impairments in shAtx3-injected mice, as compared to control ones injected with shGFP. An important improvement of neuropathology was also observed, regarding the number of intranuclear inclusions, calbindin and DARPP-32 immunoreactivity, fluorojade B and Golgi staining and molecular and granular layers thickness. These data demonstrate for the first time the efficacy of gene silencing in blocking the MJD-associated motor-behavior and neuropathological abnormalities after the onset of the disease, supporting the use of this strategy for therapy of MJD.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Animals
  • Anxiety / complications
  • Ataxin-3
  • Exploratory Behavior
  • Gene Silencing*
  • Humans
  • Intranuclear Inclusion Bodies / pathology
  • Locomotion / genetics
  • Machado-Joseph Disease / complications
  • Machado-Joseph Disease / genetics
  • Machado-Joseph Disease / pathology*
  • Machado-Joseph Disease / physiopathology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Motor Activity / genetics*
  • Mutation*
  • Nerve Tissue Proteins / deficiency*
  • Nerve Tissue Proteins / genetics*
  • Nuclear Proteins / deficiency*
  • Nuclear Proteins / genetics*
  • Purkinje Cells / pathology
  • Repressor Proteins / deficiency*
  • Repressor Proteins / genetics*

Substances

  • Nerve Tissue Proteins
  • Nuclear Proteins
  • Repressor Proteins
  • ATXN3 protein, human
  • Ataxin-3

Grants and funding

This work was supported by the Portuguese Foundation for Science and Technology (grants PTDC/SAU-NEU/099307/2008 and PTDC/SAU-FAR/116535/2010 and fellowships to CN, INF, IO and DA), the Center for Science and Technology of Madeira (CN), the National Ataxia Foundation and the Richard Chin and Lily Lock Machado-Joseph disease Research Fund. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.