Phosphorylation of the FUS low-complexity domain disrupts phase separation, aggregation, and toxicity

EMBO J. 2017 Oct 16;36(20):2951-2967. doi: 10.15252/embj.201696394. Epub 2017 Aug 8.

Abstract

Neuronal inclusions of aggregated RNA-binding protein fused in sarcoma (FUS) are hallmarks of ALS and frontotemporal dementia subtypes. Intriguingly, FUS's nearly uncharged, aggregation-prone, yeast prion-like, low sequence-complexity domain (LC) is known to be targeted for phosphorylation. Here we map in vitro and in-cell phosphorylation sites across FUS LC We show that both phosphorylation and phosphomimetic variants reduce its aggregation-prone/prion-like character, disrupting FUS phase separation in the presence of RNA or salt and reducing FUS propensity to aggregate. Nuclear magnetic resonance spectroscopy demonstrates the intrinsically disordered structure of FUS LC is preserved after phosphorylation; however, transient domain collapse and self-interaction are reduced by phosphomimetics. Moreover, we show that phosphomimetic FUS reduces aggregation in human and yeast cell models, and can ameliorate FUS-associated cytotoxicity. Hence, post-translational modification may be a mechanism by which cells control physiological assembly and prevent pathological protein aggregation, suggesting a potential treatment pathway amenable to pharmacologic modulation.

Keywords: amyotrophic lateral sclerosis; frontotemporal dementia; intrinsically disordered protein; prion; ribonucleoprotein granule.

Publication types

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

MeSH terms

  • Amyotrophic Lateral Sclerosis / pathology
  • Cell Line
  • Frontotemporal Dementia / pathology
  • Humans
  • Magnetic Resonance Spectroscopy
  • Phosphorylation
  • Protein Aggregation, Pathological
  • Protein Conformation
  • Protein Processing, Post-Translational*
  • RNA-Binding Protein FUS / chemistry
  • RNA-Binding Protein FUS / metabolism*

Substances

  • FUS protein, human
  • RNA-Binding Protein FUS