Uninterrupted CAG repeat drives striatum-selective transcriptionopathy and nuclear pathogenesis in human Huntingtin BAC mice

Neuron. 2022 Apr 6;110(7):1173-1192.e7. doi: 10.1016/j.neuron.2022.01.006. Epub 2022 Feb 2.

Abstract

In Huntington's disease (HD), the uninterrupted CAG repeat length, but not the polyglutamine length, predicts disease onset. However, the underlying pathobiology remains unclear. Here, we developed bacterial artificial chromosome (BAC) transgenic mice expressing human mutant huntingtin (mHTT) with uninterrupted, and somatically unstable, CAG repeats that exhibit progressive disease-related phenotypes. Unlike prior mHTT transgenic models with stable, CAA-interrupted, polyglutamine-encoding repeats, BAC-CAG mice show robust striatum-selective nuclear inclusions and transcriptional dysregulation resembling those in murine huntingtin knockin models and HD patients. Importantly, the striatal transcriptionopathy in HD models is significantly correlated with their uninterrupted CAG repeat length but not polyglutamine length. Finally, among the pathogenic entities originating from mHTT genomic transgenes and only present or enriched in the uninterrupted CAG repeat model, somatic CAG repeat instability and nuclear mHTT aggregation are best correlated with early-onset striatum-selective molecular pathogenesis and locomotor and sleep deficits, while repeat RNA-associated pathologies and repeat-associated non-AUG (RAN) translation may play less selective or late pathogenic roles, respectively.

Keywords: BAC transgenic; BAC-CAG; BACHD; CAG repeat; HD; Huntingtin; Huntington’s disease; RAN translation; RNA foci; RNA-seq; aggregation; instability; knockin; motor deficits; muscleblind; mutant huntingtin; nuclear inclusions; polyglutamine; striatum; transcriptional dysregulation; transcriptionopathy.

Publication types

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

MeSH terms

  • Animals
  • Chromosomes, Artificial, Bacterial / genetics
  • Chromosomes, Artificial, Bacterial / metabolism
  • Disease Models, Animal
  • Humans
  • Huntingtin Protein / genetics
  • Huntington Disease* / genetics
  • Huntington Disease* / pathology
  • Mice
  • Mice, Transgenic
  • Nerve Tissue Proteins* / genetics
  • Neurons / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Trinucleotide Repeat Expansion / genetics

Substances

  • Huntingtin Protein
  • Nerve Tissue Proteins
  • Nuclear Proteins