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 · 01 April 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

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Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); NIH; NIGMS; Howard Hughes Medical Institute HCIA; Welch Foundation

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1548416

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

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (72)

TDP-43 and FUS en route from the nucleus to the cytoplasm Ederle, Helena; Dormann, Dorothee FEBS Letters, Vol. 591, Issue 11 https://doi.org/10.1002/1873-3468.12646	journal	April 2017
Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: A historical perspective Guex, Nicolas; Peitsch, Manuel C.; Schwede, Torsten ELECTROPHORESIS, Vol. 30, Issue S1 https://doi.org/10.1002/elps.200900140	journal	June 2009
The CCPN data model for NMR spectroscopy: Development of a software pipeline Vranken, Wim F.; Boucher, Wayne; Stevens, Tim J. Proteins: Structure, Function, and Bioinformatics, Vol. 59, Issue 4 https://doi.org/10.1002/prot.20449	journal	April 2005
CRM1 Mediates Nuclear Export of Nonstructural Protein 2 from Parvovirus Minute Virus of Mice Ohshima, Takayuki; Nakajima, Toshihiro; Oishi, Takayuki Biochemical and Biophysical Research Communications, Vol. 264, Issue 1 https://doi.org/10.1006/bbrc.1999.1478	journal	October 1999
Complete Relaxation and Conformational Exchange Matrix (CORCEMA) Analysis of Intermolecular Saturation Transfer Effects in Reversibly Forming Ligand–Receptor Complexes Jayalakshmi, V.; Krishna, N. Rama Journal of Magnetic Resonance, Vol. 155, Issue 1 https://doi.org/10.1006/jmre.2001.2499	journal	March 2002
NMRPipe: A multidimensional spectral processing system based on UNIX pipes Delaglio, Frank; Grzesiek, Stephan; Vuister, GeertenW. Journal of Biomolecular NMR, Vol. 6, Issue 3 https://doi.org/10.1007/BF00197809	journal	November 1995
Size and Shape of Protein Molecules at the Nanometer Level Determined by Sedimentation, Gel Filtration, and Electron Microscopy Erickson, Harold P. Biological Procedures Online, Vol. 11, Issue 1 https://doi.org/10.1007/s12575-009-9008-x	journal	May 2009
Analysis of edge birefringence Oldenbourg, R. Biophysical Journal, Vol. 60, Issue 3 https://doi.org/10.1016/S0006-3495(91)82092-6	journal	September 1991
Nucleocytoplasmic transport enters the atomic age Conti, Elena; Izaurralde, Elisa Current Opinion in Cell Biology, Vol. 13, Issue 3 https://doi.org/10.1016/S0955-0674(00)00213-1	journal	June 2001
Calculations and Publication-Quality Illustrations for Analytical Ultracentrifugation Data Brautigam, Chad A. Methods in Enzymology https://doi.org/10.1016/bs.mie.2015.05.001	book	January 2015
Nuclear import by karyopherin-βs: Recognition and inhibition Chook, Yuh Min; Süel, Katherine E. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1813, Issue 9 https://doi.org/10.1016/j.bbamcr.2010.10.014	journal	September 2011
Weak Interactions Govern the Viscosity of Concentrated Antibody Solutions: High-Throughput Analysis Using the Diffusion Interaction Parameter Connolly, Brian D.; Petry, Chris; Yadav, Sandeep Biophysical Journal, Vol. 103, Issue 1 https://doi.org/10.1016/j.bpj.2012.04.047	journal	July 2012
The tip of the iceberg: RNA-binding proteins with prion-like domains in neurodegenerative disease King, Oliver D.; Gitler, Aaron D.; Shorter, James Brain Research, Vol. 1462 https://doi.org/10.1016/j.brainres.2012.01.016	journal	June 2012
Rules for Nuclear Localization Sequence Recognition by Karyopherinβ2 Lee, Brittany J.; Cansizoglu, Ahmet E.; Süel, Katherine E. Cell, Vol. 126, Issue 3 https://doi.org/10.1016/j.cell.2006.05.049	journal	August 2006
Cell-free Formation of RNA Granules: Low Complexity Sequence Domains Form Dynamic Fibers within Hydrogels Kato, Masato; Han, Tina W.; Xie, Shanhai Cell, Vol. 149, Issue 4 https://doi.org/10.1016/j.cell.2012.04.017	journal	May 2012
A Liquid-to-Solid Phase Transition of the ALS Protein FUS Accelerated by Disease Mutation Patel, Avinash; Lee, Hyun O.; Jawerth, Louise Cell, Vol. 162, Issue 5 https://doi.org/10.1016/j.cell.2015.07.047	journal	August 2015
Phase Separation by Low Complexity Domains Promotes Stress Granule Assembly and Drives Pathological Fibrillization Molliex, Amandine; Temirov, Jamshid; Lee, Jihun Cell, Vol. 163, Issue 1 https://doi.org/10.1016/j.cell.2015.09.015	journal	September 2015
Plasticity of an Ultrafast Interaction between Nucleoporins and Nuclear Transport Receptors Milles, Sigrid; Mercadante, Davide; Aramburu, Iker Valle Cell, Vol. 163, Issue 3 https://doi.org/10.1016/j.cell.2015.09.047	journal	October 2015
The LC Domain of hnRNPA2 Adopts Similar Conformations in Hydrogel Polymers, Liquid-like Droplets, and Nuclei Xiang, Siheng; Kato, Masato; Wu, Leeju C. Cell, Vol. 163, Issue 4 https://doi.org/10.1016/j.cell.2015.10.040	journal	November 2015
Structure of FUS Protein Fibrils and Its Relevance to Self-Assembly and Phase Separation of Low-Complexity Domains Murray, Dylan T.; Kato, Masato; Lin, Yi Cell, Vol. 171, Issue 3 https://doi.org/10.1016/j.cell.2017.08.048	journal	October 2017
Nuclear-Import Receptors Reverse Aberrant Phase Transitions of RNA-Binding Proteins with Prion-like Domains Guo, Lin; Kim, Hong Joo; Wang, Hejia Cell, Vol. 173, Issue 3 https://doi.org/10.1016/j.cell.2018.03.002	journal	April 2018
Phase Separation of FUS Is Suppressed by Its Nuclear Import Receptor and Arginine Methylation Hofweber, Mario; Hutten, Saskia; Bourgeois, Benjamin Cell, Vol. 173, Issue 3 https://doi.org/10.1016/j.cell.2018.03.004	journal	April 2018
RNA Seeds Higher-Order Assembly of FUS Protein Schwartz, Jacob C.; Wang, Xueyin; Podell, Elaine R. Cell Reports, Vol. 5, Issue 4 https://doi.org/10.1016/j.celrep.2013.11.017	journal	November 2013
Structural and Functional Characterization of CRM1-Nup214 Interactions Reveals Multiple FG-Binding Sites Involved in Nuclear Export Port, Sarah A.; Monecke, Thomas; Dickmanns, Achim Cell Reports, Vol. 13, Issue 4 https://doi.org/10.1016/j.celrep.2015.09.042	journal	October 2015
A practical guide to small angle X-ray scattering (SAXS) of flexible and intrinsically disordered proteins Kikhney, Alexey G.; Svergun, Dmitri I. FEBS Letters, Vol. 589, Issue 19PartA https://doi.org/10.1016/j.febslet.2015.08.027	journal	August 2015
Structural Basis for Cell-Cycle-Dependent Nuclear Import Mediated by the Karyopherin Kap121p Kobayashi, Junya; Matsuura, Yoshiyuki Journal of Molecular Biology, Vol. 425, Issue 11 https://doi.org/10.1016/j.jmb.2013.02.035	journal	June 2013
Formation and Maturation of Phase-Separated Liquid Droplets by RNA-Binding Proteins Lin, Yuan; Protter, David S. W.; Rosen, Michael K. Molecular Cell, Vol. 60, Issue 2 https://doi.org/10.1016/j.molcel.2015.08.018	journal	October 2015
Residue-by-Residue View of In Vitro FUS Granules that Bind the C-Terminal Domain of RNA Polymerase II Burke, Kathleen A.; Janke, Abigail M.; Rhine, Christy L. Molecular Cell, Vol. 60, Issue 2 https://doi.org/10.1016/j.molcel.2015.09.006	journal	October 2015
Autophagy regulates amyotrophic lateral sclerosis-linked fused in sarcoma-positive stress granules in neurons Ryu, Hyun-Hee; Jun, Mi-Hee; Min, Kyung-Jin Neurobiology of Aging, Vol. 35, Issue 12 https://doi.org/10.1016/j.neurobiolaging.2014.07.026	journal	December 2014
ALS/FTD Mutation-Induced Phase Transition of FUS Liquid Droplets and Reversible Hydrogels into Irreversible Hydrogels Impairs RNP Granule Function Murakami, Tetsuro; Qamar, Seema; Lin, Julie Qiaojin Neuron, Vol. 88, Issue 4 https://doi.org/10.1016/j.neuron.2015.10.030	journal	November 2015
Atomic basis of CRM1-cargo recognition, release and inhibition Fung, Ho Yee Joyce; Chook, Yuh Min Seminars in Cancer Biology, Vol. 27 https://doi.org/10.1016/j.semcancer.2014.03.002	journal	August 2014
Conformational Heterogeneity of Karyopherinβ2 Is Segmental Cansizoglu, Ahmet E.; Chook, Yuh Min Structure, Vol. 15, Issue 11 https://doi.org/10.1016/j.str.2007.09.009	journal	November 2007
Karyopherin-β2 Recognition of a PY-NLS Variant that Lacks the Proline-Tyrosine Motif Soniat, Michael; Chook, Yuh Min Structure, Vol. 24, Issue 10 https://doi.org/10.1016/j.str.2016.07.018	journal	October 2016
TDP-43 and FUS: a nuclear affair Dormann, Dorothee; Haass, Christian Trends in Neurosciences, Vol. 34, Issue 7 https://doi.org/10.1016/j.tins.2011.05.002	journal	July 2011
SEDPHAT – A platform for global ITC analysis and global multi-method analysis of molecular interactions Zhao, Huaying; Piszczek, Grzegorz; Schuck, Peter Methods, Vol. 76 https://doi.org/10.1016/j.ymeth.2014.11.012	journal	April 2015
High-precision, automated integration of multiple isothermal titration calorimetric thermograms: New features of NITPIC Scheuermann, Thomas H.; Brautigam, Chad A. Methods, Vol. 76 https://doi.org/10.1016/j.ymeth.2014.11.024	journal	April 2015
Cross-saturation and transferred cross-saturation experiments Ueda, Takumi; Takeuchi, Koh; Nishida, Noritaka Quarterly Reviews of Biophysics, Vol. 47, Issue 2 https://doi.org/10.1017/S0033583514000043	journal	April 2014
Uncoupling Kapβ2 Substrate Dissociation and Ran Binding Chook, Yuh Min; Jung, Astrid; Rosen, Michael K. Biochemistry, Vol. 41, Issue 22 https://doi.org/10.1021/bi012122p	journal	June 2002
Specific Binding of Modified RGG Domain in TLS/FUS to G-Quadruplex RNA: Tyrosines in RGG Domain Recognize 2′-OH of the Riboses of Loops in G-Quadruplex Takahama, Kentaro; Oyoshi, Takanori Journal of the American Chemical Society, Vol. 135, Issue 48 https://doi.org/10.1021/ja4086929	journal	November 2013
Structure of the nuclear transport complex karyopherin-β2–Ran˙GppNHp Chook, Yuh Min; Blobel, Günter Nature, Vol. 399, Issue 6733 https://doi.org/10.1038/20375	journal	May 1999
Fusion of CHOP to a novel RNA-binding protein in human myxoid liposarcoma Crozat, Anne; Åman, Pierre; Mandahl, Nils Nature, Vol. 363, Issue 6430 https://doi.org/10.1038/363640a0	journal	June 1993
ALS-associated fused in sarcoma (FUS) mutations disrupt Transportin-mediated nuclear import Dormann, Dorothee; Rodde, Ramona; Edbauer, Dieter The EMBO Journal, Vol. 29, Issue 16 https://doi.org/10.1038/emboj.2010.143	journal	July 2010
Structural basis for leucine-rich nuclear export signal recognition by CRM1 Dong, Xiuhua; Biswas, Anindita; Süel, Katherine E. Nature, Vol. 458, Issue 7242 https://doi.org/10.1038/nature07975	journal	April 2009
Polymer physics of intracellular phase transitions Brangwynne, Clifford P.; Tompa, Peter; Pappu, Rohit V. Nature Physics, Vol. 11, Issue 11 https://doi.org/10.1038/nphys3532	journal	November 2015
Integration and global analysis of isothermal titration calorimetry data for studying macromolecular interactions Brautigam, Chad A.; Zhao, Huaying; Vargas, Carolyn Nature Protocols, Vol. 11, Issue 5 https://doi.org/10.1038/nprot.2016.044	journal	April 2016
Biomolecular condensates: organizers of cellular biochemistry Banani, Salman F.; Lee, Hyun O.; Hyman, Anthony A. Nature Reviews Molecular Cell Biology, Vol. 18, Issue 5 https://doi.org/10.1038/nrm.2017.7	journal	February 2017
Structure-based design of a pathway-specific nuclear import inhibitor Cansizoglu, Ahmet E.; Lee, Brittany J.; Zhang, Zi Chao Nature Structural & Molecular Biology, Vol. 14, Issue 5 https://doi.org/10.1038/nsmb1229	journal	April 2007
RNA-binding proteins with prion-like domains in health and disease Harrison, Alice Ford; Shorter, James Biochemical Journal, Vol. 474, Issue 8 https://doi.org/10.1042/BCJ20160499	journal	April 2017
The zinc fingers of the SR-like protein ZRANB2 are single-stranded RNA-binding domains that recognize 5' splice site-like sequences Loughlin, F. E.; Mansfield, R. E.; Vaz, P. M. Proceedings of the National Academy of Sciences, Vol. 106, Issue 14 https://doi.org/10.1073/pnas.0802466106	journal	March 2009
Dynamic equilibrium engagement of a polyvalent ligand with a single-site receptor Mittag, Tanja; Orlicky, Stephen; Choy, Wing-Yiu Proceedings of the National Academy of Sciences, Vol. 105, Issue 46 https://doi.org/10.1073/pnas.0809222105	journal	November 2008
Structural and energetic basis of ALS-causing mutations in the atypical proline–tyrosine nuclear localization signal of the Fused in Sarcoma protein (FUS) Zhang, Zi Chao; Chook, Yuh Min Proceedings of the National Academy of Sciences, Vol. 109, Issue 30 https://doi.org/10.1073/pnas.1207247109	journal	July 2012
Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution Pervushin, K.; Riek, R.; Wider, G. Proceedings of the National Academy of Sciences, Vol. 94, Issue 23 https://doi.org/10.1073/pnas.94.23.12366	journal	November 1997
Intrinsically disordered sequences enable modulation of protein phase separation through distributed tyrosine motifs Lin, Yuan; Currie, Simon L.; Rosen, Michael K. Journal of Biological Chemistry, Vol. 292, Issue 46 https://doi.org/10.1074/jbc.M117.800466	journal	September 2017
Domain Architectures and Characterization of an RNA-binding Protein, TLS Iko, Yuko; Kodama, Takashi S.; Kasai, Nobuyuki Journal of Biological Chemistry, Vol. 279, Issue 43 https://doi.org/10.1074/jbc.M408552200	journal	October 2004
Integrative Structure–Function Mapping of the Nucleoporin Nup133 Suggests a Conserved Mechanism for Membrane Anchoring of the Nuclear Pore Complex Kim, Seung Joong; Fernandez-Martinez, Javier; Sampathkumar, Parthasarathy Molecular & Cellular Proteomics, Vol. 13, Issue 11 https://doi.org/10.1074/mcp.M114.040915	journal	August 2014
Stress granules as crucibles of ALS pathogenesis Li, Yun R.; King, Oliver D.; Shorter, James The Journal of Cell Biology, Vol. 201, Issue 3 https://doi.org/10.1083/jcb.201302044	journal	April 2013
Importins fulfil a dual function as nuclear import receptors and cytoplasmic chaperones for exposed basic domains Jäkel, Stefan; Mingot, José-Manuel; Schwarzmaier, Petra The EMBO Journal, Vol. 21, Issue 3 https://doi.org/10.1093/emboj/21.3.377	journal	February 2002
Intrinsically disordered RGG/RG domains mediate degenerate specificity in RNA binding Ozdilek, Bagdeser A.; Thompson, Valery F.; Ahmed, Nasiha S. Nucleic Acids Research, Vol. 45, Issue 13 https://doi.org/10.1093/nar/gkx460	journal	May 2017
Determination of the molecular weight of proteins in solution from a single small-angle X-ray scattering measurement on a relative scale Fischer, H.; de Oliveira Neto, M.; Napolitano, H. B. Journal of Applied Crystallography, Vol. 43, Issue 1 https://doi.org/10.1107/S0021889809043076	journal	December 2009
New developments in the ATSAS program package for small-angle scattering data analysis Petoukhov, Maxim V.; Franke, Daniel; Shkumatov, Alexander V. Journal of Applied Crystallography, Vol. 45, Issue 2 https://doi.org/10.1107/S0021889812007662	journal	March 2012
HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes Minor, Wladek; Cymborowski, Marcin; Otwinowski, Zbyszek Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 8 https://doi.org/10.1107/S0907444906019949	journal	July 2006
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
ATSAS 2.8 : a comprehensive data analysis suite for small-angle scattering from macromolecular solutions Franke, D.; Petoukhov, M. V.; Konarev, P. V. Journal of Applied Crystallography, Vol. 50, Issue 4 https://doi.org/10.1107/S1600576717007786	journal	June 2017
New polarized light microscope with precision universal compensator Oldenbourg, R.; Mei, G. Journal of Microscopy, Vol. 180, Issue 2 https://doi.org/10.1111/j.1365-2818.1995.tb03669.x	journal	November 1995
Biochemical Properties and Biological Functions of FET Proteins Schwartz, Jacob C.; Cech, Thomas R.; Parker, Roy R. Annual Review of Biochemistry, Vol. 84, Issue 1 https://doi.org/10.1146/annurev-biochem-060614-034325	journal	June 2015
Molecular Determinants and Genetic Modifiers of Aggregation and Toxicity for the ALS Disease Protein FUS/TLS Sun, Zhihui; Diaz, Zamia; Fang, Xiaodong PLoS Biology, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pbio.1000614	journal	April 2011
A Yeast Model of FUS/TLS-Dependent Cytotoxicity Ju, Shulin; Tardiff, Daniel F.; Han, Haesun PLoS Biology, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pbio.1001052	journal	April 2011
Phosphorylation of the FUS low‐complexity domain disrupts phase separation, aggregation, and toxicity Monahan, Zachary; Ryan, Veronica H.; Janke, Abigail M. The EMBO Journal, Vol. 36, Issue 20 https://doi.org/10.15252/embj.201696394	journal	August 2017
The molecular mechanism of nuclear transport revealed by atomic-scale measurements Hough, Loren E.; Dutta, Kaushik; Sparks, Samuel eLife, Vol. 4 https://doi.org/10.7554/eLife.10027	journal	September 2015

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