Neuronal expression of TATA box-binding protein containing expanded polyglutamine in knock-in mice reduces chaperone protein response by impairing the function of nuclear factor-Y transcription factor

Brain. 2011 Jul;134(Pt 7):1943-58. doi: 10.1093/brain/awr146.

Abstract

The polyglutamine diseases consist of nine neurodegenerative disorders including spinocerebellar ataxia type 17 that is caused by a polyglutamine tract expansion in the TATA box-binding protein. In all polyglutamine diseases, polyglutamine-expanded proteins are ubiquitously expressed throughout the body but cause selective neurodegeneration. Understanding the specific effects of polyglutamine-expanded proteins, when expressed at the endogenous levels, in neurons is important for unravelling the pathogenesis of polyglutamine diseases. However, addressing this important issue using mouse models that either overly or ubiquitously express mutant polyglutamine proteins in the brain and body has proved difficult. To investigate the pathogenesis of spinocerebellar ataxia 17, we generated a conditional knock-in mouse model that expresses one copy of the mutant TATA box-binding protein gene, which encodes a 105-glutamine repeat, selectively in neuronal cells at the endogenous level. Neuronal expression of mutant TATA box-binding protein causes age-dependent neurological symptoms in mice and the degeneration of cerebellar Purkinje cells. Mutant TATA box-binding protein binds more tightly to the transcription factor nuclear factor-Y, inhibits its association with the chaperone protein promoter, as well as the promoter activity and reduces the expression of the chaperones Hsp70, Hsp25 and HspA5, and their response to stress. These findings demonstrate how mutant TATA box-binding protein at the endogenous level affects neuronal function, with important implications for the pathogenesis and treatment of polyglutamine diseases.

Publication types

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

MeSH terms

  • Age Factors
  • Animals
  • Body Weight / genetics
  • Brain / metabolism
  • Brain / pathology*
  • CCAAT-Binding Factor / genetics
  • CCAAT-Binding Factor / metabolism*
  • Cell Line, Transformed
  • Chromatin Immunoprecipitation / methods
  • Disease Models, Animal
  • Endoplasmic Reticulum Chaperone BiP
  • Female
  • Gene Expression Regulation / genetics
  • Humans
  • Intermediate Filament Proteins / deficiency
  • Male
  • Mice
  • Mice, Transgenic
  • Molecular Chaperones / genetics
  • Molecular Chaperones / metabolism*
  • Nerve Tissue Proteins / deficiency
  • Nestin
  • Neurodegenerative Diseases / genetics
  • Neurodegenerative Diseases / pathology*
  • Neurons / metabolism*
  • Neurons / pathology
  • Peptides / genetics
  • Peptides / metabolism*
  • TATA-Box Binding Protein / genetics
  • TATA-Box Binding Protein / metabolism*
  • Transfection

Substances

  • CCAAT-Binding Factor
  • Endoplasmic Reticulum Chaperone BiP
  • HSPA5 protein, human
  • Hspa5 protein, mouse
  • Intermediate Filament Proteins
  • Molecular Chaperones
  • NES protein, human
  • Nerve Tissue Proteins
  • Nes protein, mouse
  • Nestin
  • Peptides
  • TATA-Box Binding Protein
  • TBP protein, human
  • nuclear factor Y
  • polyglutamine