Huntington's disease mice and human brain tissue exhibit increased G3BP1 granules and TDP43 mislocalization

J Clin Invest. 2021 Jun 15;131(12):e140723. doi: 10.1172/JCI140723.

Abstract

Chronic cellular stress associated with neurodegenerative disease can result in the persistence of stress granule (SG) structures, membraneless organelles that form in response to cellular stress. In Huntington's disease (HD), chronic expression of mutant huntingtin generates various forms of cellular stress, including activation of the unfolded protein response and oxidative stress. However, it has yet to be determined whether SGs are a feature of HD neuropathology. We examined the miRNA composition of extracellular vesicles (EVs) present in the cerebrospinal fluid (CSF) of patients with HD and show that a subset of their target mRNAs were differentially expressed in the prefrontal cortex. Of these targets, SG components were enriched, including the SG-nucleating Ras GTPase-activating protein-binding protein 1 (G3BP1). We investigated localization and levels of G3BP1 and found a significant increase in the density of G3BP1-positive granules in the cortex and hippocampus of R6/2 transgenic mice and in the superior frontal cortex of the brains of patients with HD. Intriguingly, we also observed that the SG-associated TAR DNA-binding protein 43 (TDP43), a nuclear RNA/DNA binding protein, was mislocalized to the cytoplasm of G3BP1 granule-positive HD cortical neurons. These findings suggest that G3BP1 SG dynamics may play a role in the pathophysiology of HD.

Keywords: Neurodegeneration; Neuroscience.

Publication types

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

MeSH terms

  • Animals
  • Cytoplasmic Granules / metabolism*
  • Cytoplasmic Granules / pathology
  • DNA Helicases / genetics
  • DNA Helicases / metabolism*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Female
  • Hippocampus / metabolism*
  • Hippocampus / pathology
  • Humans
  • Huntington Disease / genetics
  • Huntington Disease / metabolism*
  • Huntington Disease / pathology
  • Male
  • Mice
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Neurons / metabolism*
  • Neurons / pathology
  • Poly-ADP-Ribose Binding Proteins / genetics
  • Poly-ADP-Ribose Binding Proteins / metabolism*
  • Prefrontal Cortex / metabolism*
  • Prefrontal Cortex / pathology
  • Protein Transport / genetics
  • RNA Helicases / genetics
  • RNA Helicases / metabolism*
  • RNA Recognition Motif Proteins / genetics
  • RNA Recognition Motif Proteins / metabolism*

Substances

  • DNA-Binding Proteins
  • MicroRNAs
  • Poly-ADP-Ribose Binding Proteins
  • RNA Recognition Motif Proteins
  • TARDBP protein, human
  • DNA Helicases
  • G3BP1 protein, human
  • G3bp1 protein, mouse
  • RNA Helicases