Nuclear Import Receptor Inhibits Phase Separation of FUS through Binding to Multiple Sites

Yoshizawa, Takuya; Ali, Rustam; Jiou, Jenny; Fung, Ho Yee Joyce; Burke, Kathleen A.; Kim, Seung Joong; Lin, Yuan; Peeples, William B.; Saltzberg, Daniel; Soniat, Michael; Baumhardt, Jordan M.; Oldenbourg, Rudolf; Sali, Andrej; Fawzi, Nicolas L.; Rosen, Michael K.; Chook, Yuh Min

doi:10.1016/j.cell.2018.03.003

Title: Nuclear Import Receptor Inhibits Phase Separation of FUS through Binding to Multiple Sites

Journal Article · Sun Apr 01 00:00:00 EDT 2018 · Cell

DOI:https://doi.org/10.1016/j.cell.2018.03.003· OSTI ID:1548416

Yoshizawa, Takuya; Ali, Rustam; Jiou, Jenny; Fung, Ho Yee Joyce; Burke, Kathleen A.; Kim, Seung Joong; Lin, Yuan; Peeples, William B.; Saltzberg, Daniel; Soniat, Michael; Baumhardt, Jordan M.; Oldenbourg, Rudolf; Sali, Andrej; Fawzi, Nicolas L.; Rosen, Michael K.; Chook, Yuh Min

Liquid-liquid phase separation (LLPS) is believed to underlie formation of biomolecular condensates, cellular compartments that concentrate macromolecules without surrounding membranes. Physical mechanisms that control condensate formation/dissolution are poorly understood. The RNA-binding protein fused in sarcoma (FUS) undergoes LLPS in vitro and associates with condensates in cells. We show that the importin karyopherin-β2/transportin-1 inhibits LLPS of FUS. This activity depends on tight binding of karyopherin-β2 to the C-terminal proline-tyrosine nuclear localization signal (PY-NLS) of FUS. Nuclear magnetic resonance (NMR) analyses reveal weak interactions of karyopherin-β2 with sequence elements and structural domains distributed throughout the entirety of FUS. Biochemical analyses demonstrate that most of these same regions also contribute to LLPS of FUS. Here, the data lead to a model where high-affinity binding of karyopherin-β2 to the FUS PY-NLS tethers the proteins together, allowing multiple, distributed weak intermolecular contacts to disrupt FUS self-association, blocking LLPS. Karyopherin-β2 may act analogously to control condensates in diverse cellular contexts.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); NIGMS; Howard Hughes Medical Institute HCIA; Welch Foundation

Grant/Contract Number:: AC02-06CH11357; 1S10RR26461-1; 1S10OD018027-01; R01GM069909; U01GM98256-01; R01GM56322; R01GM118530; R01GM083960; P41GM109824; R01GM112108; R01GM114274; T32GM008203; T32GM008297

OSTI ID:: 1548416

Alternate ID(s):: OSTI ID: 1440606

Journal Information:: Cell, Journal Name: Cell Vol. 173 Journal Issue: 3; ISSN 0092-8674

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 198 works

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59 BASIC BIOLOGICAL SCIENCES
karyopherin-β2
transportin-1
PY-NLS
FUS
amyotrophic lateral sclerosis
liquid-liquid phase separation
biomolecular condensate
low-complexity sequences
intrinsically disordered protein
RNA granule

Title: Nuclear Import Receptor Inhibits Phase Separation of FUS through Binding to Multiple Sites

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