C9ORF72 poly(GA) aggregates sequester and impair HR23 and nucleocytoplasmic transport proteins

Nat Neurosci. 2016 May;19(5):668-677. doi: 10.1038/nn.4272. Epub 2016 Mar 21.

Abstract

Neuronal inclusions of poly(GA), a protein unconventionally translated from G4C2 repeat expansions in C9ORF72, are abundant in patients with frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS) caused by this mutation. To investigate poly(GA) toxicity, we generated mice that exhibit poly(GA) pathology, neurodegeneration and behavioral abnormalities reminiscent of FTD and ALS. These phenotypes occurred in the absence of TDP-43 pathology and required poly(GA) aggregation. HR23 proteins involved in proteasomal degradation and proteins involved in nucleocytoplasmic transport were sequestered by poly(GA) in these mice. HR23A and HR23B similarly colocalized to poly(GA) inclusions in C9ORF72 expansion carriers. Sequestration was accompanied by an accumulation of ubiquitinated proteins and decreased xeroderma pigmentosum C (XPC) levels in mice, indicative of HR23A and HR23B dysfunction. Restoring HR23B levels attenuated poly(GA) aggregation and rescued poly(GA)-induced toxicity in neuronal cultures. These data demonstrate that sequestration and impairment of nuclear HR23 and nucleocytoplasmic transport proteins is an outcome of, and a contributor to, poly(GA) pathology.

MeSH terms

  • Amyotrophic Lateral Sclerosis / metabolism
  • Amyotrophic Lateral Sclerosis / pathology
  • Animals
  • Atrophy / pathology
  • Behavior, Animal
  • Brain / metabolism
  • Brain / pathology
  • Brain / ultrastructure
  • C9orf72 Protein
  • Carrier Proteins / metabolism*
  • DNA-Binding Proteins / metabolism*
  • Frontotemporal Dementia / metabolism
  • Frontotemporal Dementia / pathology
  • Gene Expression / genetics
  • Guanine Nucleotide Exchange Factors / metabolism*
  • Humans
  • Inclusion Bodies / metabolism
  • Inclusion Bodies / ultrastructure
  • Mice
  • Mutation
  • Nerve Degeneration / pathology
  • Neurons / metabolism
  • Neurons / pathology*
  • Primary Cell Culture
  • Proteins / genetics
  • Proteins / metabolism
  • Proteins / toxicity*
  • Ubiquitinated Proteins / metabolism

Substances

  • C9orf72 Protein
  • C9orf72 protein, mouse
  • Carrier Proteins
  • DNA-Binding Proteins
  • Guanine Nucleotide Exchange Factors
  • Proteins
  • Rad23a protein, mouse
  • Rad23b protein, mouse
  • TDP-43 protein, mouse
  • Ubiquitinated Proteins
  • Xpc protein, mouse
  • poly(glycyl-alanyl)