C9orf72 arginine-rich dipeptide repeat proteins disrupt karyopherin-mediated nuclear import

Elife. 2020 Mar 2:9:e51685. doi: 10.7554/eLife.51685.

Abstract

Disruption of nucleocytoplasmic transport is increasingly implicated in the pathogenesis of neurodegenerative diseases, including ALS caused by a C9orf72 hexanucleotide repeat expansion. However, the mechanism(s) remain unclear. Karyopherins, including importin β and its cargo adaptors, have been shown to co-precipitate with the C9orf72 arginine-containing dipeptide repeat proteins (R-DPRs), poly-glycine arginine (GR) and poly-proline arginine (PR), and are protective in genetic modifier screens. Here, we show that R-DPRs interact with importin β, disrupt its cargo loading, and inhibit nuclear import of importin β, importin α/β, and transportin cargoes in permeabilized mouse neurons and HeLa cells, in a manner that can be rescued by RNA. Although R-DPRs induce widespread protein aggregation in this in vitro system, transport disruption is not due to nucleocytoplasmic transport protein sequestration, nor blockade of the phenylalanine-glycine (FG)-rich nuclear pore complex. Our results support a model in which R-DPRs interfere with cargo loading on karyopherins.

Keywords: C9orf72; amyotrophic lateral sclerosis; cell biology; dipeptide repeat proteins; human; importin beta; karyopherins; mouse; neuroscience; nucleocytoplasmic transport.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Active Transport, Cell Nucleus
  • Amyotrophic Lateral Sclerosis / metabolism
  • Animals
  • Arginine / metabolism*
  • C9orf72 Protein / chemistry
  • C9orf72 Protein / metabolism*
  • Dipeptides / metabolism*
  • Humans
  • Karyopherins / metabolism*
  • Mice
  • Protein Binding
  • beta Karyopherins / metabolism

Substances

  • C9orf72 Protein
  • Dipeptides
  • Karyopherins
  • beta Karyopherins
  • Arginine