A mutant ataxin-3 putative-cleavage fragment in brains of Machado-Joseph disease patients and transgenic mice is cytotoxic above a critical concentration

J Neurosci. 2004 Nov 10;24(45):10266-79. doi: 10.1523/JNEUROSCI.2734-04.2004.

Abstract

Machado-Joseph disease (MJD) is an inherited neurodegenerative disorder caused by ataxin-3 with a polyglutamine expansion. It is proposed that a toxic cleavage fragment of mutant ataxin-3 alternatively spliced isoform mjd1a triggers neurodegeneration, although this fragment has not yet been detected in the brains of MJD patients or in animal models. We have now generated transgenic mice expressing human mutant (Q71) or normal (Q20) ataxin-3 mjd1a under the control of the mouse prion promoter. Q71 transgenic mice expressing mutant ataxin-3 mjd1a above a critical level developed a phenotype similar to MJD including progressive postural instability, gait and limb ataxia, weight loss, premature death, neuronal intranuclear inclusions, and decreased tyrosine hydroxylase-positive neurons in the substantia nigra (determined by unbiased stereology). Q20 transgenic mice had normal behavior and pathology. Brains from sick Q71 transgenic mice contained an abundant mutant ataxin-3 mjd1a putative-cleavage fragment (Fragment), which was scarce in normal Q71 transgenic mice. Reactivity of the Fragment with a panel of antibodies and comigration with truncations of mutant ataxin-3 revealed that it contained residues C terminal to amino acid 221 to include the polyglutamine expansion. A similar portion of mutant ataxin-3 mjd1a expressed in transfected neuroblastoma cells was toxic above a critical concentration. The Fragment was more abundant in two affected brain regions of MJD patients. Thus, we have developed a murine model for mutant ataxin-3 mjd1a toxicity and identified a putative-cleavage fragment of the disease protein in the brains of these transgenic mice and MJD patients that is cytotoxic above a critical concentration.

Publication types

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

MeSH terms

  • Adult
  • Alternative Splicing
  • Amino Acid Sequence
  • Animals
  • Ataxin-3
  • Brain Chemistry*
  • Cell Line, Tumor / drug effects
  • Dose-Response Relationship, Drug
  • Exploratory Behavior
  • Female
  • Hand Strength
  • Humans
  • Intranuclear Inclusion Bodies
  • Machado-Joseph Disease / metabolism*
  • Machado-Joseph Disease / pathology
  • Male
  • Mice
  • Mice, Transgenic
  • Middle Aged
  • Minisatellite Repeats
  • Molecular Sequence Data
  • Nerve Tissue Proteins / analysis
  • Nerve Tissue Proteins / chemistry*
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / physiology
  • Neuroblastoma / pathology
  • Neurons / pathology
  • Nuclear Proteins
  • Peptide Fragments / analysis
  • Peptide Fragments / toxicity*
  • Phenotype
  • Postural Balance
  • Reflex
  • Repressor Proteins
  • Subcellular Fractions
  • Substantia Nigra / pathology
  • Transcription Factors
  • Transfection

Substances

  • Nerve Tissue Proteins
  • Nuclear Proteins
  • Peptide Fragments
  • Repressor Proteins
  • Transcription Factors
  • ATXN3 protein, human
  • Ataxin-3
  • Atxn3 protein, mouse