The key role of solvent in condensation: Mapping water in liquid-liquid phase-separated FUS

Biophysical Journal - Tập 120 - Trang 1266-1275 - 2021
Jonas Ahlers1, Ellen M. Adams1, Verian Bader2, Simone Pezzotti1, Konstanze F. Winklhofer2, Jörg Tatzelt3, Martina Havenith1
1Department Physical Chemistry, Ruhr-University Bochum, Bochum, Germany
2Department Molecular Cell Biology, Institute of Biochemistry and Pathobiochemistry, Ruhr-University Bochum, Bochum, Germany
3Department Biochemistry of Neurodegenerative Diseases, Institute of Biochemistry and Pathobiochemistry, Ruhr-University Bochum, Bochum, Germany

Tài liệu tham khảo

Riback, 2017, Stress-triggered phase separation is an adaptive, evolutionarily tuned response, Cell, 168, 1028, 10.1016/j.cell.2017.02.027 Shin, 2017, Liquid phase condensation in cell physiology and disease, Science, 357, eaaf4382, 10.1126/science.aaf4382 Strom, 2017, Phase separation drives heterochromatin domain formation, Nature, 547, 241, 10.1038/nature22989 Wang, 2018, A single N-terminal phosphomimic disrupts TDP-43 polymerization, phase separation, and RNA splicing, EMBO J, 37, e97452, 10.15252/embj.201797452 Woodruff, 2018, Assembly of mitotic structures through phase separation, J. Mol. Biol, 430, 4762, 10.1016/j.jmb.2018.04.041 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 Larson, 2017, Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin, Nature, 547, 236, 10.1038/nature22822 Franzmann, 2018, Phase separation of a yeast prion protein promotes cellular fitness, Science, 359, eaao5654, 10.1126/science.aao5654 Banjade, 2014, Phase transitions of multivalent proteins can promote clustering of membrane receptors, eLife, 3, e04123, 10.7554/eLife.04123 Banani, 2017, Biomolecular condensates: organizers of cellular biochemistry, Nat. Rev. Mol. Cell Biol, 18, 285, 10.1038/nrm.2017.7 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 Conicella, 2016, ALS mutations disrupt phase separation mediated by α-helical structure in the TDP-43 low-complexity C-terminal domain, Structure, 24, 1537, 10.1016/j.str.2016.07.007 Guo, 2018, Nuclear-import receptors reverse aberrant phase transitions of RNA-binding proteins with prion-like domains, Cell, 173, 677, 10.1016/j.cell.2018.03.002 Wegmann, 2018, Tau protein liquid-liquid phase separation can initiate tau aggregation, EMBO J, 37, e98049, 10.15252/embj.201798049 Hofweber, 2018, Phase separation of FUS is suppressed by its nuclear import receptor and arginine methylation, Cell, 173, 706, 10.1016/j.cell.2018.03.004 Qamar, 2018, FUS phase separation is modulated by a molecular chaperone and methylation of arginine cation-π interactions, Cell, 173, 720, 10.1016/j.cell.2018.03.056 Alberti, 2019, Liquid-liquid phase separation in disease, Annu. Rev. Genet, 53, 171, 10.1146/annurev-genet-112618-043527 Guo, 2017, HDAC6 inhibition reverses axonal transport defects in motor neurons derived from FUS-ALS patients, Nat. Commun, 8, 861, 10.1038/s41467-017-00911-y Kamelgarn, 2018, ALS mutations of FUS suppress protein translation and disrupt the regulation of nonsense-mediated decay, Proc. Natl. Acad. Sci. USA, 115, E11904, 10.1073/pnas.1810413115 Morlando, 2012, FUS stimulates microRNA biogenesis by facilitating co-transcriptional Drosha recruitment, EMBO J, 31, 4502, 10.1038/emboj.2012.319 Rulten, 2014, PARP-1 dependent recruitment of the amyotrophic lateral sclerosis-associated protein FUS/TLS to sites of oxidative DNA damage, Nucleic Acids Res, 42, 307, 10.1093/nar/gkt835 Wang, 2013, Interaction of FUS and HDAC1 regulates DNA damage response and repair in neurons, Nat. Neurosci, 16, 1383, 10.1038/nn.3514 Yasuda, 2013, The RNA-binding protein Fus directs translation of localized mRNAs in APC-RNP granules, J. Cell Biol, 203, 737, 10.1083/jcb.201306058 Zhang, 2018, FUS regulates activity of MicroRNA-mediated gene silencing, Mol. Cell, 69, 787, 10.1016/j.molcel.2018.02.001 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 Kang, 2019, A unified mechanism for LLPS of ALS/FTLD-causing FUS as well as its modulation by ATP and oligonucleic acids, PLoS Biol, 17, e3000327, 10.1371/journal.pbio.3000327 Murthy, 2020, The (un)structural biology of biomolecular liquid-liquid phase separation using NMR spectroscopy, J. Biol. Chem, 295, 2375, 10.1074/jbc.REV119.009847 Dao, 2018, Ubiquitin modulates liquid-liquid phase separation of UBQLN2 via disruption of multivalent interactions, Mol. Cell, 69, 965, 10.1016/j.molcel.2018.02.004 Conicella, 2020, TDP-43 α-helical structure tunes liquid-liquid phase separation and function, Proc. Natl. Acad. Sci. USA, 117, 5883, 10.1073/pnas.1912055117 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 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 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 Murthy, 2019, Molecular interactions underlying liquid-liquid phase separation of the FUS low-complexity domain, Nat. Struct. Mol. Biol, 26, 637, 10.1038/s41594-019-0250-x Dormann, 2010, ALS-associated fused in sarcoma (FUS) mutations disrupt Transportin-mediated nuclear import, EMBO J, 29, 2841, 10.1038/emboj.2010.143 Marrone, 2019, FUS pathology in ALS is linked to alterations in multiple ALS-associated proteins and rescued by drugs stimulating autophagy, Acta Neuropathol, 138, 67, 10.1007/s00401-019-01998-x Cinar, 2019, Pressure-sensitive and osmolyte-modulated liquid-liquid phase separation of eye-lens γ-crystallins, J. Am. Chem. Soc, 141, 7347, 10.1021/jacs.8b13636 Maharana, 2018, RNA buffers the phase separation behavior of prion-like RNA binding proteins, Science, 360, 918, 10.1126/science.aar7366 Cinar, 2018, Pressure-induced dissolution and reentrant formation of condensed, liquid-liquid phase-separated elastomeric α-elastin, Chemistry, 24, 8286, 10.1002/chem.201801643 Ribeiro, 2019, The synergic effect of water and biomolecules in intracellular phase separation, Nat. Rev. Chem, 3, 552, 10.1038/s41570-019-0120-4 Reddy, 2010, Dry amyloid fibril assembly in a yeast prion peptide is mediated by long-lived structures containing water wires, Proc. Natl. Acad. Sci. USA, 107, 21459, 10.1073/pnas.1008616107 Tros, 2017, Picosecond orientational dynamics of water in living cells, Nat. Commun, 8, 904, 10.1038/s41467-017-00858-0 Arya, 2018, Femtosecond hydration map of intrinsically disordered α-synuclein, Biophys. J, 114, 2540, 10.1016/j.bpj.2018.04.028 Fisette, 2016, Hydration dynamics of a peripheral membrane protein, J. Am. Chem. Soc, 138, 11526, 10.1021/jacs.6b07005 Zaslavsky, 2018, The solvent side of proteinaceous membrane-less organelles in light of aqueous two-phase systems, Int. J. Biol. Macromol, 117, 1224, 10.1016/j.ijbiomac.2018.06.030 Zaslavsky, 2018, In aqua veritas: the indispensable yet mostly ignored role of water in phase separation and membrane-less organelles, Biochemistry, 57, 2437, 10.1021/acs.biochem.7b01215 Chandler, 2005, Interfaces and the driving force of hydrophobic assembly, Nature, 437, 640, 10.1038/nature04162 Sarupria, 2009, Quantifying water density fluctuations and compressibility of hydration shells of hydrophobic solutes and proteins, Phys. Rev. Lett, 103, 037803, 10.1103/PhysRevLett.103.037803 Jamadagni, 2011, Hydrophobicity of proteins and interfaces: insights from density fluctuations, Annu. Rev. Chem. Biomol. Eng, 2, 147, 10.1146/annurev-chembioeng-061010-114156 Monroe, 2018, Computational discovery of chemically patterned surfaces that effect unique hydration water dynamics, Proc. Natl. Acad. Sci. USA, 115, 8093, 10.1073/pnas.1807208115 Monroe, 2020, Water structure and properties at hydrophilic and hydrophobic surfaces, Annu. Rev. Chem. Biomol. Eng, 11, 523, 10.1146/annurev-chembioeng-120919-114657 Xi, 2017, Hydrophobicity of proteins and nanostructured solutes is governed by topographical and chemical context, Proc. Natl. Acad. Sci. USA, 114, 13345, 10.1073/pnas.1700092114 Cyran, 2019, Molecular hydrophobicity at a macroscopically hydrophilic surface, Proc. Natl. Acad. Sci. USA, 116, 1520, 10.1073/pnas.1819000116 Shin, 2018, Characterizing hydration properties based on the orientational structure of interfacial water molecules, J. Chem. Theory Comput, 14, 461, 10.1021/acs.jctc.7b00898 Conti Nibali, 2014, New insights into the role of water in biological function: studying solvated biomolecules using terahertz absorption spectroscopy in conjunction with molecular dynamics simulations, J. Am. Chem. Soc, 136, 12800, 10.1021/ja504441h Ebbinghaus, 2010, Antifreeze glycoprotein activity correlates with long-range protein-water dynamics, J. Am. Chem. Soc, 132, 12210, 10.1021/ja1051632 Png, 2016, Tracking aggregation and fibrillation of globular proteins using terahertz and far-infrared spectroscopies, IEEE Trans. Terahertz Sci. Technol, 6, 45, 10.1109/TTHZ.2015.2505900 Novelli, 2017, Time-domain THz spectroscopy reveals coupled protein-hydration dielectric response in solutions of native and fibrils of human lysozyme, J. Phys. Chem. B, 121, 4810, 10.1021/acs.jpcb.7b02724 Adams, 2020, Solvent dynamics play a decisive role in the complex formation of biologically relevant redox proteins, Phys. Chem. Chem. Phys, 22, 7451, 10.1039/D0CP00267D Böhm, 2017, Mapping hydration water around alcohol chains by THz calorimetry, Angew. Chem. Int. Ed. Engl, 56, 9981, 10.1002/anie.201612162 Conti Nibali, 2020, Wrapping up hydrophobic hydration: locality matters, J. Phys. Chem. Lett, 11, 4809, 10.1021/acs.jpclett.0c00846 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 Park, 2020, Dehydration entropy drives liquid-liquid phase separation by molecular crowding, Commun. Chem, 3, 83, 10.1038/s42004-020-0328-8 Wang, 2018, A molecular grammar governing the driving forces for phase separation of prion-like RNA binding proteins, Cell, 174, 688, 10.1016/j.cell.2018.06.006 Zeng, 2018, Reconstituted postsynaptic density as a molecular platform for understanding synapse formation and plasticity, Cell, 174, 1172, 10.1016/j.cell.2018.06.047 Jo, 2020, Interplay between intrinsically disordered proteins inside membraneless protein liquid droplets, Chem. Sci. (Camb.), 11, 1269, 10.1039/C9SC03191J 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 Wei, 2017, Phase behaviour of disordered proteins underlying low density and high permeability of liquid organelles, Nat. Chem, 9, 1118, 10.1038/nchem.2803 Morawietz, 2018, The interplay of structure and dynamics in the Raman spectrum of liquid water over the full frequency and temperature range, J. Phys. Chem. Lett, 9, 851, 10.1021/acs.jpclett.8b00133 Maréchal, 1991, Infrared spectra of water. I. Effect of temperature and of H/D isotopic dilution, J. Chem. Phys, 95, 5565, 10.1063/1.461630 Maréchal, 2011, The molecular structure of liquid water delivered by absorption spectroscopy in the whole IR region completed with thermodynamics data, J. Mol. Struct, 1004, 146, 10.1016/j.molstruc.2011.07.054 Myatt, 2017, Monomeric green fluorescent protein as a protein standard for small angle scattering, Biomed. Spectrosc. Imaging, 6, 123, 10.3233/BSI-170167 Bernadó, 2009, A self-consistent description of the conformational behavior of chemically denatured proteins from NMR and small angle scattering, Biophys. J, 97, 2839, 10.1016/j.bpj.2009.08.044 Reichheld, 2017, Direct observation of structure and dynamics during phase separation of an elastomeric protein, Proc. Natl. Acad. Sci. USA, 114, E4408, 10.1073/pnas.1701877114 Choi, 2020, Physical principles underlying the complex biology of intracellular phase transitions, Annu. Rev. Biophys, 49, 107, 10.1146/annurev-biophys-121219-081629 Choi, 2019, LASSI: a lattice model for simulating phase transitions of multivalent proteins, PLoS Comput. Biol, 15, e1007028, 10.1371/journal.pcbi.1007028 Schindelin, 2012, Fiji: an open-source platform for biological-image analysis, Nat. Methods, 9, 676, 10.1038/nmeth.2019 Schwaab, 2019, Ion hydration and ion pairing as probed by THz spectroscopy, Angew. Chem. Int. Ed. Engl, 58, 3000, 10.1002/anie.201805261 Bertie, 1996, Infrared intensities of liquids XX: the intensity of the OH stretching band of liquid water revisited, and the best current values of the optical constants of H2O(l) at 25°C between 15,000 and 1 cm−1, Appl. Spectrosc, 50, 1047, 10.1366/0003702963905385 Ebbinghaus, 2007, An extended dynamical hydration shell around proteins, Proc. Natl. Acad. Sci. USA, 104, 20749, 10.1073/pnas.0709207104