Insights into RNA-mediated pathology in new mouse models of Huntington's disease

FASEB J. 2024 Dec 15;38(23):e70182. doi: 10.1096/fj.202401465R.

Abstract

Huntington's disease (HD) is a neurodegenerative polyglutamine (polyQ) disease resulting from the expansion of CAG repeats located in the ORF of the huntingtin gene (HTT). The extent to which mutant mRNA-driven disruptions contribute to HD pathogenesis, particularly in comparison to the dominant mechanisms related to the gain-of-function effects of the mutant polyQ protein, is still debatable. To evaluate this contribution in vivo, we generated two mouse models through a knock-in strategy at the Rosa26 locus. These models expressed distinct variants of human mutant HTT cDNA fragment: a translated variant (HD/100Q model, serving as a reference) and a nontranslated variant (HD/100CAG model). The cohorts of animals were subjected to a broad spectrum of molecular, behavioral, and cognitive analysis for 21 months. Behavioral testing revealed alterations in both models, with the HD/100Q model exhibiting late disease phenotype. The rotarod, static rod, and open-field tests showed some motor deficits in HD/100CAG and HD/100Q model mice during the light phase, while ActiMot indicated hyperkinesis during the dark phase. Both models also exhibited certain gene deregulations in the striatum that are related to disrupted pathways and phenotype alterations observed in HD. In conclusion, we provide in vivo evidence for a minor contributory role of mutant RNA in HD pathogenesis. The separated effects resulting from the presence of mutant RNA in the HD/100CAG model led to less severe but, to some extent, similar types of impairments as in the HD/100Q model. Increased anxiety was one of the most substantial effects caused by mutant HTT RNA.

Keywords: Huntington's disease; RNA toxicity; mouse model; neurodegenerative diseases; polyglutamine disorders.

MeSH terms

  • Animals
  • Behavior, Animal
  • Disease Models, Animal*
  • Gene Knock-In Techniques
  • Humans
  • Huntingtin Protein* / genetics
  • Huntingtin Protein* / metabolism
  • Huntington Disease* / genetics
  • Huntington Disease* / metabolism
  • Huntington Disease* / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Motor Activity
  • RNA / genetics
  • RNA / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism

Substances

  • Huntingtin Protein
  • HTT protein, human
  • RNA
  • RNA, Messenger