Phase Separation of FUS Is Suppressed by Its Nuclear Import Receptor and Arginine Methylation

Cell. 2018 Apr 19;173(3):706-719.e13. doi: 10.1016/j.cell.2018.03.004.

Abstract

Cytoplasmic FUS aggregates are a pathological hallmark in a subset of patients with frontotemporal dementia (FTD) or amyotrophic lateral sclerosis (ALS). A key step that is disrupted in these patients is nuclear import of FUS mediated by the import receptor Transportin/Karyopherin-β2. In ALS-FUS patients, this is caused by mutations in the nuclear localization signal (NLS) of FUS that weaken Transportin binding. In FTD-FUS patients, Transportin is aggregated, and post-translational arginine methylation, which regulates the FUS-Transportin interaction, is lost. Here, we show that Transportin and arginine methylation have a crucial function beyond nuclear import-namely to suppress RGG/RG-driven phase separation and stress granule association of FUS. ALS-associated FUS-NLS mutations weaken the chaperone activity of Transportin and loss of FUS arginine methylation, as seen in FTD-FUS, promote phase separation, and stress granule partitioning of FUS. Our findings reveal two regulatory mechanisms of liquid-phase homeostasis that are disrupted in FUS-associated neurodegeneration.

Keywords: ALS; FTD; Karyopherin-β2 (Kapβ2); Transportin (TNPO1); arginine methylation; fused in sarcoma (FUS); neurodegeneration; nuclear import; phase separation; stress granules.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus
  • Amino Acid Motifs
  • Arginine / chemistry*
  • Cytoplasm / metabolism
  • DNA Methylation
  • DNA, Complementary / metabolism
  • Densitometry
  • Frontotemporal Lobar Degeneration / metabolism
  • HeLa Cells
  • Homeostasis
  • Humans
  • Karyopherins / chemistry
  • Magnetic Resonance Spectroscopy
  • Methylation
  • Molecular Chaperones / chemistry
  • Mutation
  • Neurodegenerative Diseases / metabolism
  • Protein Binding
  • Protein Domains
  • RNA-Binding Protein FUS / chemistry*
  • beta Karyopherins / chemistry*

Substances

  • DNA, Complementary
  • FUS protein, human
  • Karyopherins
  • Molecular Chaperones
  • RNA-Binding Protein FUS
  • TNPO1 protein, human
  • beta Karyopherins
  • Arginine