Integration-independent Transgenic Huntington Disease Fragment Mouse Models Reveal Distinct Phenotypes and Life Span in Vivo

J Biol Chem. 2015 Jul 31;290(31):19287-306. doi: 10.1074/jbc.M114.623561. Epub 2015 May 29.

Abstract

The cascade of events that lead to cognitive decline, motor deficits, and psychiatric symptoms in patients with Huntington disease (HD) is triggered by a polyglutamine expansion in the N-terminal region of the huntingtin (HTT) protein. A significant mechanism in HD is the generation of mutant HTT fragments, which are generally more toxic than the full-length HTT. The protein fragments observed in human HD tissue and mouse models of HD are formed by proteolysis or aberrant splicing of HTT. To systematically investigate the relative contribution of the various HTT protein proteolysis events observed in vivo, we generated transgenic mouse models of HD representing five distinct proteolysis fragments ending at amino acids 171, 463, 536, 552, and 586 with a polyglutamine length of 148. All lines contain a single integration at the ROSA26 locus, with expression of the fragments driven by the chicken β-actin promoter at nearly identical levels. The transgenic mice N171-Q148 and N552-Q148 display significantly accelerated phenotypes and a shortened life span when compared with N463-Q148, N536-Q148, and N586-Q148 transgenic mice. We hypothesized that the accelerated phenotype was due to altered HTT protein interactions/complexes that accumulate with age. We found evidence for altered HTT complexes in caspase-2 fragment transgenic mice (N552-Q148) and a stronger interaction with the endogenous HTT protein. These findings correlate with an altered HTT molecular complex and distinct proteins in the HTT interactome set identified by mass spectrometry. In particular, we identified HSP90AA1 (HSP86) as a potential modulator of the distinct neurotoxicity of the caspase-2 fragment mice (N552-Q148) when compared with the caspase-6 transgenic mice (N586-Q148).

Keywords: caspase; neurodegenerative disease; polyglutamine disease; proteolysis; transgenic mice.

Publication types

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

MeSH terms

  • Animals
  • Brain / pathology
  • Codon, Nonsense
  • Disease Models, Animal
  • Female
  • HEK293 Cells
  • HSP90 Heat-Shock Proteins / metabolism
  • Humans
  • Huntingtin Protein
  • Huntington Disease / genetics*
  • Huntington Disease / physiopathology
  • Longevity
  • Male
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Motor Activity
  • Nerve Tissue Proteins / genetics*
  • Nerve Tissue Proteins / metabolism
  • Phenotype
  • Protein Interaction Mapping
  • Proteolysis

Substances

  • Codon, Nonsense
  • HSP90 Heat-Shock Proteins
  • HTT protein, human
  • Hsp86 protein, human
  • Huntingtin Protein
  • Nerve Tissue Proteins