Folded domain charge properties influence the conformational behavior of disordered tails

Current Research in Structural Biology - Tập 3 - Trang 216-228 - 2021
Ishan Taneja1,2, Alex S. Holehouse1,2
1Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, 660 S. Euclid Ave., St. Louis, MO, 63110, USA
2Center for Science and Engineering of Living Systems (CSELS), Washington University in St. Louis, St. Louis, MO 63130, USA

Tài liệu tham khảo

Arbesú, 2018, Intramolecular fuzzy interactions involving intrinsically disordered domains, Front Mol Biosci, 5, 39, 10.3389/fmolb.2018.00039 Baker, 2001, Electrostatics of nanosystems: application to microtubules and the ribosome, Proc. Natl. Acad. Sci. U.S.A., 98, 10037, 10.1073/pnas.181342398 Berlow, 2017, Hypersensitive termination of the hypoxic response by a disordered protein switch, Nature, 543, 447, 10.1038/nature21705 Borcherds, 2014, Disorder and residual helicity alter p53-Mdm2 binding affinity and signaling in cells, Nat. Chem. Biol., 10, 1000, 10.1038/nchembio.1668 Borg, 2007, Polyelectrostatic interactions of disordered ligands suggest a physical basis for ultrasensitivity, Proc. Natl. Acad. Sci. U.S.A., 104, 9650, 10.1073/pnas.0702580104 Borgia, 2018, Extreme disorder in an ultrahigh-affinity protein complex, Nature, 555, 61, 10.1038/nature25762 Bowman, 2020, Properties of protein unfolded states suggest broad selection for expanded conformational ensembles, Proc. Natl. Acad. Sci. U.S.A., 117, 23356, 10.1073/pnas.2003773117 Cubuk, 2021, The SARS-CoV-2 nucleocapsid protein is dynamic, disordered, and phase separates with RNA, Nat. Commun., 12, 1, 10.1038/s41467-021-21953-3 Cummings, 2018, Phase separation behavior of supercharged proteins and polyelectrolytes, Biochemistry, 57, 314, 10.1021/acs.biochem.7b00990 Das, 2013, Conformations of intrinsically disordered proteins are influenced by linear sequence distributions of oppositely charged residues, Proc. Natl. Acad. Sci. U.S.A., 110, 13392, 10.1073/pnas.1304749110 Das, 2015, Relating sequence encoded information to form and function of intrinsically disordered proteins, Curr. Opin. Struct. Biol., 32, 102, 10.1016/j.sbi.2015.03.008 Das, 2020, Comparative roles of charge, π, and hydrophobic interactions in sequence-dependent phase separation of intrinsically disordered proteins, Proc. Natl. Acad. Sci. U.S.A., 117, 28795, 10.1073/pnas.2008122117 Davey, 2019, The functional importance of structure in unstructured protein regions, Curr. Opin. Struct. Biol., 56, 155, 10.1016/j.sbi.2019.03.009 Dignon, 2018, Relation between single-molecule properties and phase behavior of intrinsically disordered proteins, Proc. Natl. Acad. Sci. U.S.A., 115, 9929, 10.1073/pnas.1804177115 Dolinsky, 2004, PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations, Nucleic Acids Res., 32, W665, 10.1093/nar/gkh381 Duong, 2007, Kernel density estimation and kernel discriminant analysis for multivariate data inR, J. Stat. Software, 21 Dyla, 2020, Intrinsically disordered linkers control tethered kinases via effective concentration, Proc. Natl. Acad. Sci. U.S.A., 117, 21413, 10.1073/pnas.2006382117 Fuxreiter, 2020, Fuzzy protein theory for disordered proteins, Biochem. Soc. Trans., 10.1042/BST20200239 Ganguly, 2012, Electrostatically accelerated coupled binding and folding of intrinsically disordered proteins, J. Mol. Biol., 422, 674, 10.1016/j.jmb.2012.06.019 Ginell, 2020, Analyzing the sequences of intrinsically disordered regions with CIDER and localCIDER, 103 Graña-Montes, 2014, N-terminal protein tails act as aggregation protective entropic bristles: the SUMO case, Biomacromolecules, 15, 1194, 10.1021/bm401776z Hofmann, 2012, Polymer scaling laws of unfolded and intrinsically disordered proteins quantified with single-molecule spectroscopy, Proc. Natl. Acad. Sci. U.S.A., 109, 16155, 10.1073/pnas.1207719109 Holehouse, 2017, CIDER: Resources to Analyze Sequence-Ensemble Relationships of Intrinsically Disordered Proteins, Biophysical Journal, 112, 16, 10.1016/j.bpj.2016.11.3200 Holehouse, 2015, Quantitative assessments of the distinct contributions of polypeptide backbone amides versus side chain groups to chain expansion via chemical denaturation, J. Am. Chem. Soc., 137, 2984, 10.1021/ja512062h Huang, 2020, Allostery of multidomain proteins with disordered linkers, Curr. Opin. Struct. Biol., 62, 175, 10.1016/j.sbi.2020.01.017 Jurrus, 2018, Improvements to the APBS biomolecular solvation software suite: improvements to the APBS Software Suite, Protein Sci., 27, 112, 10.1002/pro.3280 Keul, 2018, The entropic force generated by intrinsically disordered segments tunes protein function, Nature, 563, 584, 10.1038/s41586-018-0699-5 Kim, 2020, Effect of protein surface charge distribution on protein-polyelectrolyte complexation, Biomacromolecules, 21, 3026, 10.1021/acs.biomac.0c00346 Krois, 2018, Long-range regulation of p53 DNA binding by its intrinsically disordered N-terminal transactivation domain, Proc. Natl. Acad. Sci. U.S.A., 115, E11302, 10.1073/pnas.1814051115 Laber, 2017, Charge shielding prevents aggregation of supercharged GFP variants at high protein concentration, Mol. Pharm., 14, 3269, 10.1021/acs.molpharmaceut.7b00322 Lawrence, 2007, Supercharging proteins can impart unusual resilience, J. Am. Chem. Soc., 129, 10110, 10.1021/ja071641y Lecoq, 2017, Structural characterization of interactions between transactivation domain 1 of the p65 subunit of NF-κB and transcription regulatory factors, Nucleic Acids Res., 45, 5564, 10.1093/nar/gkx146 Lin, 2018, Theories for sequence-dependent phase behaviors of biomolecular condensates, Biochemistry, 57, 2499, 10.1021/acs.biochem.8b00058 Ma, 2011, Dynamic allostery: linkers are not merely flexible, Structure, 19, 907, 10.1016/j.str.2011.06.002 Mao, 2010, Net charge per residue modulates conformational ensembles of intrinsically disordered proteins, Proc. Natl. Acad. Sci. U.S.A., 107, 8183, 10.1073/pnas.0911107107 Mao, 2013, Describing sequence-ensemble relationships for intrinsically disordered proteins, Biochem. J., 449, 307, 10.1042/BJ20121346 Marsh, 2010, Sequence determinants of compaction in intrinsically disordered proteins, Biophys. J., 98, 2383, 10.1016/j.bpj.2010.02.006 Martin, 2020, Intrinsically disordered protein regions and phase separation: sequence determinants of assembly or lack thereof, Emerg Top Life Sci, 4, 307, 10.1042/ETLS20190164 Martin, 2016, Sequence determinants of the conformational properties of an intrinsically disordered protein prior to and upon multisite phosphorylation, J. Am. Chem. Soc., 138, 15323, 10.1021/jacs.6b10272 Martin, 2020, Valence and patterning of aromatic residues determine the phase behavior of prion-like domains, Science, 367, 694, 10.1126/science.aaw8653 Martin, 2021, Interplay of folded domains and the disordered low-complexity domain in mediating hnRNPA1 phase separation, Nucleic Acids Res., 10.1093/nar/gkab063 Masters, 2019, Coronavirus genomic RNA packaging, Virology, 537, 198, 10.1016/j.virol.2019.08.031 McCann, 2014, Reconstitution of multivalent PDZ domain binding to the scaffold protein PSD-95 reveals ternary-complex specificity of combinatorial inhibition, Structure, 22, 1458, 10.1016/j.str.2014.08.006 McGibbon, 2015, A modern, open library for the analysis of molecular dynamics trajectories, Biophys. J., 109, 1528, 10.1016/j.bpj.2015.08.015 Mittag, 2007, Atomic-level characterization of disordered protein ensembles, Curr. Opin. Struct. Biol., 17, 3, 10.1016/j.sbi.2007.01.009 Mittag, 2010, Protein dynamics and conformational disorder in molecular recognition, J. Mol. Recogn., 23, 105, 10.1002/jmr.961 Mittag, 2010, Structure/function implications in a dynamic complex of the intrinsically disordered Sic 1 with the Cdc 4 subunit of an SCF ubiquitin ligase, Structure, 18, 494, 10.1016/j.str.2010.01.020 Mittal, 2018, Sequence-to-Conformation relationships of disordered regions tethered to folded domains of proteins, J. Mol. Biol., 430, 2403, 10.1016/j.jmb.2018.05.012 Moses, 2020, Revealing the hidden sensitivity of intrinsically disordered proteins to their chemical environment, J. Phys. Chem. Lett., 11, 10131, 10.1021/acs.jpclett.0c02822 Müller-Späth, 2010, Charge interactions can dominate the dimensions of intrinsically disordered proteins, Proc. Natl. Acad. Sci. U.S.A., 107, 14609, 10.1073/pnas.1001743107 Ortega, 2018, Transcription factor dimerization activates the p300 acetyltransferase, Nature, 562, 538, 10.1038/s41586-018-0621-1 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 Patil, 2006, Disordered domains and high surface charge confer hubs with the ability to interact with multiple proteins in interaction networks, FEBS Lett., 580, 2041, 10.1016/j.febslet.2006.03.003 Portz, 2017, Structural heterogeneity in the intrinsically disordered RNA polymerase II C-terminal domain, Nat. Commun., 8, 15231, 10.1038/ncomms15231 Receveur-Bréchot, 2006, Assessing protein disorder and induced folding, Proteins: Struct. Funct. Bioinf., 62, 24, 10.1002/prot.20750 Saikatendu, 2007, Ribonucleocapsid formation of severe acute respiratory syndrome coronavirus through molecular action of the N-terminal domain of N protein, J. Virol., 81, 3913, 10.1128/JVI.02236-06 Sambi, 2010, How disorder influences order and vice versa - mutual effects in fusion proteins containing an intrinsically disordered and a globular protein: ordered and disordered protein domains, FEBS J., 277, 4438, 10.1111/j.1742-4658.2010.07825.x Sankaranarayanan, 2021, The arrested state of processing bodies supports mRNA regulation in early development, Cold Spring Harbor Laboratory, 2021 Sawle, 2015, A theoretical method to compute sequence dependent configurational properties in charged polymers and proteins, J. Chem. Phys., 143 Sherry, 2017, Control of transcriptional activity by design of charge patterning in the intrinsically disordered RAM region of the Notch receptor, Proc. Natl. Acad. Sci. U.S.A., 114, E9243, 10.1073/pnas.1706083114 Sing, 2020, Recent progress in the science of complex coacervation, Soft Matter, 16, 2885, 10.1039/D0SM00001A Sørensen, 2019, Effective concentrations enforced by intrinsically disordered linkers are governed by polymer physics, Proc. Natl. Acad. Sci. U.S.A., 116, 23124, 10.1073/pnas.1904813116 Staby, 2020, Disorder in a two-domain neuronal Ca2+-binding protein regulates domain stability and dynamics using ligand mimicry, Cell. Mol. Life Sci. Sun, 2018, Electrostatic control of calcineurin's intrinsically-disordered regulatory domain binding to calmodulin, Biochim. Biophys. Acta Gen. Subj., 1862, 2651, 10.1016/j.bbagen.2018.07.027 Tompa, 2008, Fuzzy complexes: polymorphism and structural disorder in protein–protein interactions, Trends Biochem. Sci., 33, 2, 10.1016/j.tibs.2007.10.003 Uversky, 2013, The most important thing is the tail: multitudinous functionalities of intrinsically disordered protein termini, FEBS Lett., 587, 1891, 10.1016/j.febslet.2013.04.042 van der Lee, 2014, Classification of intrinsically disordered regions and proteins, Chem. Rev., 114, 6589, 10.1021/cr400525m Vitalis, 2009, ABSINTH: a new continuum solvation model for simulations of polypeptides in aqueous solutions, J. Comput. Chem., 30, 673, 10.1002/jcc.21005 Vuzman, 2010, DNA search efficiency is modulated by charge composition and distribution in the intrinsically disordered tail, Proc. Natl. Acad. Sci. U.S.A., 107, 21004, 10.1073/pnas.1011775107 Waterhouse, 2018, SWISS-MODEL: homology modelling of protein structures and complexes, Nucleic Acids Res., 46, W296, 10.1093/nar/gky427 Wright, 1999, Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm, J. Mol. Biol., 293, 321, 10.1006/jmbi.1999.3110 Wright, 2015, Intrinsically disordered proteins in cellular signalling and regulation, Nat. Rev. Mol. Cell Biol., 16, 18, 10.1038/nrm3920 Xu, 2009, Generating triangulated macromolecular surfaces by euclidean distance transform, PloS One, 4, 10.1371/journal.pone.0008140 Yanez Orozco, 2018, Identifying weak interdomain interactions that stabilize the supertertiary structure of the N-terminal tandem PDZ domains of PSD-95, Nat. Commun., 9, 3724, 10.1038/s41467-018-06133-0 Zerze, 2015, Sequence- and temperature-dependent properties of unfolded and disordered proteins from atomistic simulations, J. Phys. Chem. B, 119, 14622, 10.1021/acs.jpcb.5b08619 Zheng, 2021, Previously uncharacterized interactions between the folded and intrinsically disordered domains impart asymmetric effects on UBQLN2 phase separation, bioRxiv. (2021) Zheng, 2018, Inferring properties of disordered chains from FRET transfer efficiencies, J. Chem. Phys., 148, 123329, 10.1063/1.5006954 Zheng, 2020, Hydropathy patterning complements charge patterning to describe conformational preferences of disordered proteins, J. Phys. Chem. Lett.