Sequence determinants of protein phase behavior from a coarse-grained model

Dignon, Gregory L.; Zheng, Wenwei; Kim, Young C.; Best, Robert B.; Mittal, Jeetain; Ofran, ed., Yanay

doi:10.1371/journal.pcbi.1005941

Title: Sequence determinants of protein phase behavior from a coarse-grained model

Journal Article · Wed Jan 24 00:00:00 UTC 2018 · PLoS Computational Biology (Online)

DOI: https://doi.org/10.1371/journal.pcbi.1005941 · OSTI ID:1419611

; Zheng, Wenwei; Kim, Young C.; Best, Robert B.;

; Ofran, ed., Yanay

Not Available

View Journal Article

Cite

Export

Save

Research Organization:: Lehigh Univ., Bethlehem, PA (United States); Univ. of California, Berkeley, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231; SC0013979

OSTI ID:: 1419611

Journal Information:: PLoS Computational Biology (Online), Journal Name: PLoS Computational Biology (Online) Journal Issue: 1 Vol. 14; ISSN 1553-7358

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (79)

Why are ?natively unfolded? proteins unstructured under physiologic conditions? Uversky, Vladimir N.; Gillespie, Joel R.; Fink, Anthony L. Proteins: Structure, Function, and Genetics, Vol. 41, Issue 3 https://doi.org/10.1002/1097-0134(20001115)41:3<415::AID-PROT130>3.0.CO;2-7	journal	January 2000
In Vitro Reconstitution of a Cellular Phase-Transition Process that Involves the mRNA Decapping Machinery Fromm, Simon A.; Kamenz, Julia; Nöldeke, Erik R. Angewandte Chemie International Edition, Vol. 53, Issue 28 https://doi.org/10.1002/anie.201402885	journal	May 2014
Fast Parallel Algorithms for Short-Range Molecular Dynamics Plimpton, Steve Journal of Computational Physics, Vol. 117, Issue 1 https://doi.org/10.1006/jcph.1995.1039	journal	March 1995
Comparative Protein Modelling by Satisfaction of Spatial Restraints Šali, Andrej; Blundell, Tom L. Journal of Molecular Biology, Vol. 234, Issue 3 https://doi.org/10.1006/jmbi.1993.1626	journal	December 1993
Residue – Residue Potentials with a Favorable Contact Pair Term and an Unfavorable High Packing Density Term, for Simulation and Threading Miyazawa, Sanzo; Jernigan, Robert L. Journal of Molecular Biology, Vol. 256, Issue 3 https://doi.org/10.1006/jmbi.1996.0114	journal	March 1996
A simple method for displaying the hydropathic character of a protein Kyte, Jack; Doolittle, Russell F. Journal of Molecular Biology, Vol. 157, Issue 1, p. 105-132 https://doi.org/10.1016/0022-2836(82)90515-0	journal	May 1982
How Hofmeister ion interactions affect protein stability Baldwin, R. L. Biophysical Journal, Vol. 71, Issue 4, p. 2056-2063 https://doi.org/10.1016/S0006-3495(96)79404-3	journal	October 1996
Protein Composition Determines the Effect of Crowding on the Properties of Disordered Proteins Miller, Cayla M.; Kim, Young C.; Mittal, Jeetain Biophysical Journal, Vol. 111, Issue 1 https://doi.org/10.1016/j.bpj.2016.05.033	journal	July 2016
Phase Transitions in Biological Systems with Many Components Jacobs, William M.; Frenkel, Daan Biophysical Journal, Vol. 112, Issue 4 https://doi.org/10.1016/j.bpj.2016.10.043	journal	February 2017
Conformational Heterogeneity and FRET Data Interpretation for Dimensions of Unfolded Proteins Song, Jianhui; Gomes, Gregory-Neal; Shi, Tongfei Biophysical Journal, Vol. 113, Issue 5 https://doi.org/10.1016/j.bpj.2017.07.023	journal	September 2017
Structural Basis for RNA Unwinding by the DEAD-Box Protein Drosophila Vasa Sengoku, Toru; Nureki, Osamu; Nakamura, Akira Cell, Vol. 125, Issue 2 https://doi.org/10.1016/j.cell.2006.01.054	journal	April 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
Dual Specificity Kinase DYRK3 Couples Stress Granule Condensation/Dissolution to mTORC1 Signaling Wippich, Frank; Bodenmiller, Bernd; Trajkovska, Maria Gustafsson Cell, Vol. 152, Issue 4 https://doi.org/10.1016/j.cell.2013.01.033	journal	February 2013
Phosphorylation-Regulated Binding of RNA Polymerase II to Fibrous Polymers of Low-Complexity Domains Kwon, Ilmin; Kato, Masato; Xiang, Siheng Cell, Vol. 155, Issue 5 https://doi.org/10.1016/j.cell.2013.10.033	journal	November 2013
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 Transition of Spindle-Associated Protein Regulate Spindle Apparatus Assembly Jiang, Hao; Wang, Shusheng; Huang, Yuejia Cell, Vol. 163, Issue 1 https://doi.org/10.1016/j.cell.2015.08.010	journal	September 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
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
Coexisting Liquid Phases Underlie Nucleolar Subcompartments Feric, Marina; Vaidya, Nilesh; Harmon, Tyler S. Cell, Vol. 165, Issue 7 https://doi.org/10.1016/j.cell.2016.04.047	journal	June 2016
Spatiotemporal Control of Intracellular Phase Transitions Using Light-Activated optoDroplets Shin, Yongdae; Berry, Joel; Pannucci, Nicole Cell, Vol. 168, Issue 1-2 https://doi.org/10.1016/j.cell.2016.11.054	journal	January 2017
A Phase Separation Model for Transcriptional Control Hnisz, Denes; Shrinivas, Krishna; Young, Richard A. Cell, Vol. 169, Issue 1 https://doi.org/10.1016/j.cell.2017.02.007	journal	March 2017
Stress-Triggered Phase Separation Is an Adaptive, Evolutionarily Tuned Response Riback, Joshua A.; Katanski, Christopher D.; Kear-Scott, Jamie L. Cell, Vol. 168, Issue 6 https://doi.org/10.1016/j.cell.2017.02.027	journal	March 2017
Protein intrinsic disorder-based liquid–liquid phase transitions in biological systems: Complex coacervates and membrane-less organelles Uversky, Vladimir N. Advances in Colloid and Interface Science, Vol. 239 https://doi.org/10.1016/j.cis.2016.05.012	journal	January 2017
Intrinsically disordered proteins as crucial constituents of cellular aqueous two phase systems and coacervates Uversky, Vladimir N.; Kuznetsova, Irina M.; Turoverov, Konstantin K. FEBS Letters, Vol. 589, Issue 1 https://doi.org/10.1016/j.febslet.2014.11.028	journal	November 2014
General purpose molecular dynamics simulations fully implemented on graphics processing units Anderson, Joshua A.; Lorenz, Chris D.; Travesset, A. Journal of Computational Physics, Vol. 227, Issue 10 https://doi.org/10.1016/j.jcp.2008.01.047	journal	May 2008
Coarse-grained Models for Simulations of Multiprotein Complexes: Application to Ubiquitin Binding Kim, Young C.; Hummer, Gerhard Journal of Molecular Biology, Vol. 375, Issue 5 https://doi.org/10.1016/j.jmb.2007.11.063	journal	February 2008
A Simple Atomic-Level Hydrophobicity Scale Reveals Protein Interfacial Structure Kapcha, Lauren H.; Rossky, Peter J. Journal of Molecular Biology, Vol. 426, Issue 2 https://doi.org/10.1016/j.jmb.2013.09.039	journal	January 2014
Phase Transition of a Disordered Nuage Protein Generates Environmentally Responsive Membraneless Organelles Nott, Timothy J.; Petsalaki, Evangelia; Farber, Patrick Molecular Cell, Vol. 57, Issue 5 https://doi.org/10.1016/j.molcel.2015.01.013	journal	March 2015
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
RNA Controls PolyQ Protein Phase Transitions Zhang, Huaiying; Elbaum-Garfinkle, Shana; Langdon, Erin M. Molecular Cell, Vol. 60, Issue 2 https://doi.org/10.1016/j.molcel.2015.09.017	journal	October 2015
Sequence Determinants of Intracellular Phase Separation by Complex Coacervation of a Disordered Protein Pak, Chi W.; Kosno, Martyna; Holehouse, Alex S. Molecular Cell, Vol. 63, Issue 1 https://doi.org/10.1016/j.molcel.2016.05.042	journal	July 2016
RNA Remodeling Activity of DEAD Box Proteins Tuned by Protein Concentration, RNA Length, and ATP Kim, Younghoon; Myong, Sua Molecular Cell, Vol. 63, Issue 5 https://doi.org/10.1016/j.molcel.2016.07.010	journal	September 2016
Random-phase-approximation theory for sequence-dependent, biologically functional liquid-liquid phase separation of intrinsically disordered proteins Lin, Yi-Hsuan; Song, Jianhui; Forman-Kay, Julie D. Journal of Molecular Liquids, Vol. 228 https://doi.org/10.1016/j.molliq.2016.09.090	journal	February 2017
ALS Mutations Disrupt Phase Separation Mediated by α-Helical Structure in the TDP-43 Low-Complexity C-Terminal Domain Conicella, Alexander E.; Zerze, Gül H.; Mittal, Jeetain Structure, Vol. 24, Issue 9 https://doi.org/10.1016/j.str.2016.07.007	journal	September 2016
Protein crystallization and phase diagrams Asherie, N. Methods, Vol. 34, Issue 3 https://doi.org/10.1016/j.ymeth.2004.03.028	journal	November 2004
Balanced Protein–Water Interactions Improve Properties of Disordered Proteins and Non-Specific Protein Association Best, Robert B.; Zheng, Wenwei; Mittal, Jeetain Journal of Chemical Theory and Computation, Vol. 10, Issue 11 https://doi.org/10.1021/ct500569b	journal	October 2014
The salting-out behavior of amides and its relation to the denaturation of proteins by salts Schrier, Eugene E.; Schrier, Evelyn B. The Journal of Physical Chemistry, Vol. 71, Issue 6 https://doi.org/10.1021/j100865a049	journal	May 1967
Some Properties of Solutions of Long-chain Compounds. Huggins, Maurice L. The Journal of Physical Chemistry, Vol. 46, Issue 1 https://doi.org/10.1021/j150415a018	journal	January 1942
Effects of salts on the free energy of the peptide group Nandi, Pradip K.; Robinson, Dwight R. Journal of the American Chemical Society, Vol. 94, Issue 4 https://doi.org/10.1021/ja00759a042	journal	February 1972
Effects of salts on the free energies of nonpolar groups in model peptides Nandi, Pradip K.; Robinson, Dwight R. Journal of the American Chemical Society, Vol. 94, Issue 4 https://doi.org/10.1021/ja00759a043	journal	February 1972
Natively Unfolded Protein Stability as a Coil-to-Globule Transition in Charge/Hydropathy Space Ashbaugh, Henry S.; Hatch, Harold W. Journal of the American Chemical Society, Vol. 130, Issue 29 https://doi.org/10.1021/ja802124e	journal	July 2008
Probing the Action of Chemical Denaturant on an Intrinsically Disordered Protein by Simulation and Experiment Zheng, Wenwei; Borgia, Alessandro; Buholzer, Karin Journal of the American Chemical Society, Vol. 138, Issue 36 https://doi.org/10.1021/jacs.6b05443	journal	September 2016
Consistent View of Polypeptide Chain Expansion in Chemical Denaturants from Multiple Experimental Methods Borgia, Alessandro; Zheng, Wenwei; Buholzer, Karin Journal of the American Chemical Society, Vol. 138, Issue 36 https://doi.org/10.1021/jacs.6b05917	journal	September 2016
Water Dispersion Interactions Strongly Influence Simulated Structural Properties of Disordered Protein States Piana, Stefano; Donchev, Alexander G.; Robustelli, Paul The Journal of Physical Chemistry B, Vol. 119, Issue 16 https://doi.org/10.1021/jp508971m	journal	April 2015
Phase transitions in the assembly of multivalent signalling proteins Li, Pilong; Banjade, Sudeep; Cheng, Hui-Chun Nature, Vol. 483, Issue 7389 https://doi.org/10.1038/nature10879	journal	March 2012
Membraneless organelles can melt nucleic acid duplexes and act as biomolecular filters Nott, Timothy J.; Craggs, Timothy D.; Baldwin, Andrew J. Nature Chemistry, Vol. 8, Issue 6 https://doi.org/10.1038/nchem.2519	journal	May 2016
Phase behaviour of disordered proteins underlying low density and high permeability of liquid organelles Wei, Ming-Tzo; Elbaum-Garfinkle, Shana; Holehouse, Alex S. Nature Chemistry, Vol. 9, Issue 11 https://doi.org/10.1038/nchem.2803	journal	June 2017
Liquid demixing of intrinsically disordered proteins is seeded by poly(ADP-ribose) Altmeyer, Matthias; Neelsen, Kai J.; Teloni, Federico Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9088	journal	August 2015
Sequence heuristics to encode phase behaviour in intrinsically disordered protein polymers Quiroz, Felipe García; Chilkoti, Ashutosh Nature Materials, Vol. 14, Issue 11 https://doi.org/10.1038/nmat4418	journal	September 2015
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
Role of Repulsive Forces in Determining the Equilibrium Structure of Simple Liquids Weeks, John D.; Chandler, David; Andersen, Hans C. The Journal of Chemical Physics, Vol. 54, Issue 12 https://doi.org/10.1063/1.1674820	journal	June 1971
Thermodynamics of High Polymer Solutions Flory, Paul J. The Journal of Chemical Physics, Vol. 10, Issue 1 https://doi.org/10.1063/1.1723621	journal	January 1942
Vapor-liquid interfacial properties of fully flexible Lennard-Jones chains Blas, Felipe J.; MacDowell, Luis G.; de Miguel, Enrique The Journal of Chemical Physics, Vol. 129, Issue 14 https://doi.org/10.1063/1.2989115	journal	October 2008
How accurate are polymer models in the analysis of Förster resonance energy transfer experiments on proteins? O’Brien, Edward P.; Morrison, Greg; Brooks, Bernard R. The Journal of Chemical Physics, Vol. 130, Issue 12 https://doi.org/10.1063/1.3082151	journal	March 2009
Polymorphic transitions in single crystals: A new molecular dynamics method Parrinello, M.; Rahman, A. Journal of Applied Physics, Vol. 52, Issue 12 https://doi.org/10.1063/1.328693	journal	December 1981
Generalized Replica Exchange Method Kim, Jaegil; Keyes, Thomas; Straub, John E. The Journal of Chemical Physics, Vol. 132, Issue 22 https://doi.org/10.1063/1.3432176	journal	June 2010
A theoretical method to compute sequence dependent configurational properties in charged polymers and proteins Sawle, Lucas; Ghosh, Kingshuk The Journal of Chemical Physics, Vol. 143, Issue 8 https://doi.org/10.1063/1.4929391	journal	August 2015
Net charge per residue modulates conformational ensembles of intrinsically disordered proteins Mao, A. H.; Crick, S. L.; Vitalis, A. Proceedings of the National Academy of Sciences, Vol. 107, Issue 18 https://doi.org/10.1073/pnas.0911107107	journal	April 2010
Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes Brangwynne, C. P.; Mitchison, T. J.; Hyman, A. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue 11 https://doi.org/10.1073/pnas.1017150108	journal	February 2011
Polymer scaling laws of unfolded and intrinsically disordered proteins quantified with single-molecule spectroscopy Hofmann, H.; Soranno, A.; Borgia, A. Proceedings of the National Academy of Sciences, Vol. 109, Issue 40 https://doi.org/10.1073/pnas.1207719109	journal	September 2012
The disordered P granule protein LAF-1 drives phase separation into droplets with tunable viscosity and dynamics Elbaum-Garfinkle, Shana; Kim, Younghoon; Szczepaniak, Krzysztof Proceedings of the National Academy of Sciences, Vol. 112, Issue 23 https://doi.org/10.1073/pnas.1504822112	journal	May 2015
RNA transcription modulates phase transition-driven nuclear body assembly Berry, Joel; Weber, Stephanie C.; Vaidya, Nilesh Proceedings of the National Academy of Sciences, Vol. 112, Issue 38 https://doi.org/10.1073/pnas.1509317112	journal	September 2015
Decoupling of size and shape fluctuations in heteropolymeric sequences reconciles discrepancies in SAXS vs. FRET measurements Fuertes, Gustavo; Banterle, Niccolò; Ruff, Kiersten M. Proceedings of the National Academy of Sciences, Vol. 114, Issue 31 https://doi.org/10.1073/pnas.1704692114	journal	July 2017
Structural and hydrodynamic properties of an intrinsically disordered region of a germ cell-specific protein on phase separation Brady, Jacob P.; Farber, Patrick J.; Sekhar, Ashok Proceedings of the National Academy of Sciences, Vol. 114, Issue 39 https://doi.org/10.1073/pnas.1706197114	journal	September 2017
Vapour–liquid phase equilibrium and surface tension of fully flexible Lennard–Jones chains Silmore, Kevin S.; Howard, Michael P.; Panagiotopoulos, Athanassios Z. Molecular Physics, Vol. 115, Issue 3 https://doi.org/10.1080/00268976.2016.1262075	journal	December 2016
Nuclear Stress Bodies Biamonti, G.; Vourc'h, C. Cold Spring Harbor Perspectives in Biology, Vol. 2, Issue 6 https://doi.org/10.1101/cshperspect.a000695	journal	April 2010
Sequence-Specific Polyampholyte Phase Separation in Membraneless Organelles Lin, Yi-Hsuan; Forman-Kay, Julie D.; Chan, Hue Sun Physical Review Letters, Vol. 117, Issue 17 https://doi.org/10.1103/PhysRevLett.117.178101	journal	October 2016
Reversible Compartmentalization of de Novo Purine Biosynthetic Complexes in Living Cells An, S.; Kumar, R.; Sheets, E. D. Science, Vol. 320, Issue 5872 https://doi.org/10.1126/science.1152241	journal	April 2008
Mutations in FUS, an RNA Processing Protein, Cause Familial Amyotrophic Lateral Sclerosis Type 6 Vance, C.; Rogelj, B.; Hortobagyi, T. Science, Vol. 323, Issue 5918 https://doi.org/10.1126/science.1165942	journal	February 2009
Mutations in the FUS/TLS Gene on Chromosome 16 Cause Familial Amyotrophic Lateral Sclerosis Kwiatkowski, T. J.; Bosco, D. A.; LeClerc, A. L. Science, Vol. 323, Issue 5918 https://doi.org/10.1126/science.1166066	journal	February 2009
Germline P Granules Are Liquid Droplets That Localize by Controlled Dissolution/Condensation Brangwynne, C. P.; Eckmann, C. R.; Courson, D. S. Science, Vol. 324, Issue 5935 https://doi.org/10.1126/science.1172046	journal	May 2009
Atomic-Level Characterization of the Structural Dynamics of Proteins Shaw, D. E.; Maragakis, P.; Lindorff-Larsen, K. Science, Vol. 330, Issue 6002 https://doi.org/10.1126/science.1187409	journal	October 2010
How Fast-Folding Proteins Fold Lindorff-Larsen, K.; Piana, S.; Dror, R. O. Science, Vol. 334, Issue 6055 https://doi.org/10.1126/science.1208351	journal	October 2011
Polymer-Polymer Phase Behavior Bates, Frank S. Science, Vol. 251, Issue 4996, p. 898-905 https://doi.org/10.1126/science.251.4996.898	journal	February 1991
Phase separation of signaling molecules promotes T cell receptor signal transduction Su, Xiaolei; Ditlev, Jonathon A.; Hui, Enfu Science, Vol. 352, Issue 6285 https://doi.org/10.1126/science.aad9964	journal	April 2016
Innovative scattering analysis shows that hydrophobic disordered proteins are expanded in water Riback, Joshua A.; Bowman, Micayla A.; Zmyslowski, Adam M. Science, Vol. 358, Issue 6360 https://doi.org/10.1126/science.aan5774	journal	October 2017
The Role of Nuclear Bodies in Gene Expression and Disease Morimoto, Marie; Boerkoel, Cornelius Biology, Vol. 2, Issue 3 https://doi.org/10.3390/biology2030976	journal	July 2013
Regulation of RNA granule dynamics by phosphorylation of serine-rich, intrinsically disordered proteins in C. elegans Wang, Jennifer T.; Smith, Jarrett; Chen, Bi-Chang eLife, Vol. 3 https://doi.org/10.7554/eLife.04591	journal	December 2014

Similar Records

Coarse-grained sequences for protein folding and design

Journal Article · Mon Mar 31 04:00:00 UTC 2003 · Proceedings of the National Academy ofSciences · OSTI ID:927172

Brown, Scott; Fawzi, Nicolas J; Head-Gordon, Teresa

Temperature-Controlled Liquid–Liquid Phase Separation of Disordered Proteins

Journal Article · Wed May 01 00:00:00 UTC 2019 · ACS Central Science · OSTI ID:1510159

Dignon, Gregory L.; Zheng, Wenwei; Kim, Young C.; +1 more

Relation between single-molecule properties and phase behavior of intrinsically disordered proteins

Journal Article · Fri Sep 14 00:00:00 UTC 2018 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1470803

Dignon, Gregory L.; Zheng, Wenwei; Best, Robert B.; +2 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Sequence determinants of protein phase behavior from a coarse-grained model

Citation Formats

References (79)

Similar Records

Related Subjects