A Molecular Grammar Governing the Driving Forces for Phase Separation of Prion-like RNA Binding Proteins

Alberti, 2009, A systematic survey identifies prions and illuminates sequence features of prionogenic proteins, Cell, 137, 146, 10.1016/j.cell.2009.02.044 Aleksandrov, 2018, Protein dynamics in complex DNA lesions, Mol. Cell, 69, 1046, 10.1016/j.molcel.2018.02.016 Altmeyer, 2015, Liquid demixing of intrinsically disordered proteins is seeded by poly(ADP-ribose), Nat. Commun., 6, 8088, 10.1038/ncomms9088 Banani, 2016, Compositional control of phase-separated cellular bodies, Cell, 166, 651, 10.1016/j.cell.2016.06.010 Banani, 2017, Biomolecular condensates: organizers of cellular biochemistry, Nat. Rev. Mol. Cell Biol., 18, 285, 10.1038/nrm.2017.7 Berchowitz, 2015, Regulated formation of an amyloid-like translational repressor governs gametogenesis, Cell, 163, 406, 10.1016/j.cell.2015.08.060 Bergeron-Sandoval, 2016, Mechanisms and consequences of macromolecular phase separation, Cell, 165, 1067, 10.1016/j.cell.2016.05.026 Boeynaems, 2017, Phase Separation of C9orf72 Dipeptide Repeats Perturbs Stress Granule Dynamics, Mol Cell, 65, 1044, 10.1016/j.molcel.2017.02.013 Boke, 2016, Amyloid-like self-assembly of a cellular compartment, Cell, 166, 637, 10.1016/j.cell.2016.06.051 Brady, 2017, Structural and hydrodynamic properties of an intrinsically disordered region of a germ cell-specific protein on phase separation, Proc. Natl. Acad. Sci. USA, 114, E8194, 10.1073/pnas.1706197114 Brangwynne, 2009, Germline P granules are liquid droplets that localize by controlled dissolution/condensation, Science, 324, 1729, 10.1126/science.1172046 Burke, 2015, Residue-by-residue view of in vitro fus granules that bind the C-terminal domain of RNA polymerase II, Mol. Cell, 60, 231, 10.1016/j.molcel.2015.09.006 Burley, 1988, Weakly polar interactions in proteins, Adv. Protein Chem., 39, 125, 10.1016/S0065-3233(08)60376-9 Crozat, 1993, Fusion of CHOP to a novel RNA-binding protein in human myxoid liposarcoma, Nature, 363, 640, 10.1038/363640a0 Dougherty, 1996, Cation-pi interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp, Science, 271, 163, 10.1126/science.271.5246.163 Dougherty, 2013, The cation-π interaction, Acc. Chem. Res., 46, 885, 10.1021/ar300265y Elbaum-Garfinkle, 2015, The disordered P granule protein LAF-1 drives phase separation into droplets with tunable viscosity and dynamics, Proc. Natl. Acad. Sci. USA, 112, 7189, 10.1073/pnas.1504822112 Fei, 2017, Quantitative analysis of multilayer organization of proteins and RNA in nuclear speckles at super resolution, J. Cell Sci., 130, 4180 Feric, 2016, Coexisting liquid phases underlie nucleolar subcompartments, Cell, 165, 1686, 10.1016/j.cell.2016.04.047 Flory, 1941, Molecular size distribution in three dimensional polymers. I. Gelation, J. Am. Chem. Soc., 63, 3083, 10.1021/ja01856a061 Franzmann, 2018, Phase separation of a yeast prion protein promotes cellular fitness, Science, 359, aao5654, 10.1126/science.aao5654 Gallivan, 1999, Cation-pi interactions in structural biology, Proc. Natl. Acad. Sci. USA, 96, 9459, 10.1073/pnas.96.17.9459 Gobbi, 1993, Y-conjugated compounds: the equilibrium geometries and electronic structures of guanidine, guanidinium cation, urea, and 1,1-diaminoethylene, J. Am. Chem. Soc., 115, 2362, 10.1021/ja00059a035 Han, 2012, Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies, Cell, 149, 768, 10.1016/j.cell.2012.04.016 Hein, 2015, A human interactome in three quantitative dimensions organized by stoichiometries and abundances, Cell, 163, 712, 10.1016/j.cell.2015.09.053 Hernández-Vega, 2017, Local nucleation of microtubule bundles through tubulin concentration into a condensed tau phase, Cell Rep., 20, 2304, 10.1016/j.celrep.2017.08.042 Holehouse, 2017, CIDER: resources to analyze sequence-ensemble relationships of intrinsically disordered proteins, Biophys. J., 112, 16, 10.1016/j.bpj.2016.11.3200 Hughes, 2018, Atomic structures of low-complexity protein segments reveal kinked β sheets that assemble networks, Science, 359, 698, 10.1126/science.aan6398 Hyman, 2011, Beyond stereospecificity: liquids and mesoscale organization of cytoplasm, Dev. Cell, 21, 14, 10.1016/j.devcel.2011.06.013 Hyman, 2014, Liquid-liquid phase separation in biology, Annu. Rev. Cell Dev. Biol., 30, 39, 10.1146/annurev-cellbio-100913-013325 Jahnel, 2011, Measuring the complete force field of an optical trap, Opt. Lett., 36, 1260, 10.1364/OL.36.001260 Kato, 2012, Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels, Cell, 149, 753, 10.1016/j.cell.2012.04.017 King, 2012, The tip of the iceberg: RNA-binding proteins with prion-like domains in neurodegenerative disease, Brain Res., 1462, 61, 10.1016/j.brainres.2012.01.016 Kwon, 2013, Phosphorylation-regulated binding of RNA polymerase II to fibrous polymers of low-complexity domains, Cell, 155, 1049, 10.1016/j.cell.2013.10.033 Lancaster, 2014, PLAAC: a web and command-line application to identify proteins with prion-like amino acid composition, Bioinformatics, 30, 2501, 10.1093/bioinformatics/btu310 Lee, 2016, C9orf72 Dipeptide Repeats Impair the Assembly, Dynamics, and Function of Membrane-Less Organelles, Cell, 167, 774, 10.1016/j.cell.2016.10.002 Lin, 2015, Formation and maturation of phase-separated liquid droplets by RNA-binding proteins, Mol. Cell, 60, 208, 10.1016/j.molcel.2015.08.018 Lin, 2016, Sequence-specific polyampholyte phase separation in membraneless organelles, Phys. Rev. Lett., 117, 178101, 10.1103/PhysRevLett.117.178101 Lin, 2017, Intrinsically disordered sequences enable modulation of protein phase separation through distributed tyrosine motifs, J. Biol. Chem., 292, 19110, 10.1074/jbc.M117.800466 Liu, 2015, IBS: an illustrator for the presentation and visualization of biological sequences, Bioinformatics, 31, 3359, 10.1093/bioinformatics/btv362 Luo, 2018, Atomic structures of FUS LC domain segments reveal bases for reversible amyloid fibril formation, Nat. Struct. Mol. Biol., 25, 341, 10.1038/s41594-018-0050-8 Maharana, 2018, RNA buffers the phase separation behavior of prion-like RNA binding proteins, Science, 360, 918, 10.1126/science.aar7366 Malinovska, 2013, Protein disorder, prion propensities, and self-organizing macromolecular collectives, Biochim. Biophys. Acta, 1834, 918, 10.1016/j.bbapap.2013.01.003 Malinovska, 2015, Dictyostelium discoideum has a highly Q/N-rich proteome and shows an unusual resilience to protein aggregation, Proc. Natl. Acad. Sci. USA, 112, E2620, 10.1073/pnas.1504459112 Mateju, 2017, An aberrant phase transition of stress granules triggered by misfolded protein and prevented by chaperone function, EMBO J, 36, 1669, 10.15252/embj.201695957 Molliex, 2015, Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization, Cell, 163, 123, 10.1016/j.cell.2015.09.015 Monahan, 2017, Phosphorylation of the FUS low-complexity domain disrupts phase separation, aggregation, and toxicity, EMBO J., 36, 2951, 10.15252/embj.201696394 Murakami, 2015, ALS/FTD mutation-induced phase transition of FUS liquid droplets and reversible hydrogels into irreversible hydrogels impairs RNP granule function, Neuron, 88, 678, 10.1016/j.neuron.2015.10.030 Murray, 2017, Structure of FUS protein fibrils and its relevance to self-assembly and phase separation of low-complexity domains, Cell, 171, 615, 10.1016/j.cell.2017.08.048 Necci, 2017, MobiDB-lite: fast and highly specific consensus prediction of intrinsic disorder in proteins, Bioinformatics, 33, 1402, 10.1093/bioinformatics/btx015 Nott, 2015, Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles, Mol. Cell, 57, 936, 10.1016/j.molcel.2015.01.013 Pak, 2016, Sequence determinants of intracellular phase separation by complex coacervation of a disordered protein, Mol. Cell, 63, 72, 10.1016/j.molcel.2016.05.042 Patel, 2015, A liquid-to-solid phase transition of the ALS protein FUS accelerated by disease mutation, Cell, 162, 1066, 10.1016/j.cell.2015.07.047 Poser, 2008, BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals, Nat Methods, 5, 409, 10.1038/nmeth.1199 Protter, 2016, Principles and properties of stress granules, Trends Cell Biol., 26, 668, 10.1016/j.tcb.2016.05.004 Ramachandran, 1963, Stereochemistry of polypeptide chain configurations, J. Mol. Biol., 7, 95, 10.1016/S0022-2836(63)80023-6 Riback, 2017, Stress-triggered phase separation is an adaptive, evolutionarily tuned response, Cell, 168, 1028, 10.1016/j.cell.2017.02.027 Rubinstein, 1997, Solutions of associative polymers, Trends Polym. Sci. (Regul.), 5, 181 Schwartz, 2015, Biochemical properties and biological functions of FET proteins, Annu. Rev. Biochem., 84, 355, 10.1146/annurev-biochem-060614-034325 Schwartz, 2013, RNA seeds higher-order assembly of FUS protein, Cell Rep, 5, 918, 10.1016/j.celrep.2013.11.017 Semenov, 1998, Thermoreversible gelation in solutions of associative polymers. 1. Statics, Macromolecules, 31, 1373, 10.1021/ma970616h Shin, 2017, Liquid phase condensation in cell physiology and disease, Science, 357, eaaf4382, 10.1126/science.aaf4382 Simon, 2017, Programming molecular self-assembly of intrinsically disordered proteins containing sequences of low complexity, Nat. Chem., 9, 509, 10.1038/nchem.2715 Stockmayer, 1943, Theory of molecular size distribution and gel formation in branched-chain polymers, J. Chem. Phys., 11, 45, 10.1063/1.1723803 Wei, 2017, Phase behaviour of disordered proteins underlying low density and high permeability of liquid organelles, Nat. Chem, 9, 1118, 10.1038/nchem.2803 Woodruff, 2017, The centrosome is a selective condensate that nucleates microtubules by concentrating tubulin, Cell, 169, 1066, 10.1016/j.cell.2017.05.028 Woodruff, 2018, Organization and function of non-dynamic biomolecular condensates, Trends Biochem. Sci., 43, 81, 10.1016/j.tibs.2017.11.005 Zhang, 2015, RNA controls PolyQ protein phase transitions, Mol. Cell, 60, 220, 10.1016/j.molcel.2015.09.017