Overexpression of the autophagic beclin-1 protein clears mutant ataxin-3 and alleviates Machado-Joseph disease

Brain. 2011 May;134(Pt 5):1400-15. doi: 10.1093/brain/awr047. Epub 2011 Apr 7.

Abstract

Machado-Joseph disease, also known as spinocerebellar ataxia type 3, is the most common of the dominantly inherited ataxias worldwide and is characterized by mutant ataxin-3 misfolding, intracellular accumulation of aggregates and neuronal degeneration. Here we investigated the implication of autophagy, the major pathway for organelle and protein turnover, in the accumulation of mutant ataxin-3 aggregates and neurodegeneration found in Machado-Joseph disease and we assessed whether specific stimulation of this pathway could mitigate the disease. Using tissue from patients with Machado-Joseph disease, transgenic mice and a lentiviral-based rat model, we found an abnormal expression of endogenous autophagic markers, accumulation of autophagosomes and decreased levels of beclin-1, a crucial protein in the early nucleation step of autophagy. Lentiviral vector-mediated overexpression of beclin-1 led to stimulation of autophagic flux, mutant ataxin-3 clearance and overall neuroprotective effects in neuronal cultures and in a lentiviral-based rat model of Machado-Joseph disease. These data demonstrate that autophagy is a key degradation pathway, with beclin-1 playing a significant role in alleviating Machado-Joseph disease pathogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Aged
  • Animals
  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism*
  • Ataxin-3
  • Autophagy / genetics*
  • Autophagy-Related Proteins
  • Beclin-1
  • Brain / metabolism
  • Brain / pathology
  • Carrier Proteins / genetics
  • Cell Line, Tumor
  • Female
  • Flow Cytometry
  • Gene Expression Regulation / genetics
  • Humans
  • Machado-Joseph Disease / genetics*
  • Machado-Joseph Disease / pathology
  • Machado-Joseph Disease / physiopathology
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Middle Aged
  • Mutation / genetics*
  • Nerve Tissue Proteins / genetics*
  • Nuclear Proteins / genetics*
  • Rats
  • Rats, Wistar
  • Repressor Proteins / genetics*
  • Sequestosome-1 Protein
  • Transfection / methods
  • Trinucleotide Repeat Expansion / genetics

Substances

  • ATG16L1 protein, human
  • Adaptor Proteins, Signal Transducing
  • Apoptosis Regulatory Proteins
  • Autophagy-Related Proteins
  • BECN1 protein, human
  • Beclin-1
  • Carrier Proteins
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Nuclear Proteins
  • Repressor Proteins
  • SQSTM1 protein, human
  • Sequestosome-1 Protein
  • ATXN3 protein, human
  • Ataxin-3