Protein disorder and autoinhibition: The role of multivalency and effective concentration

Pufall, 2002, Autoinhibitory domains: modular effectors of cellular regulation, Annu Rev Cell Dev Biol, 18, 421, 10.1146/annurev.cellbio.18.031502.133614 Khan, 2019, Adhesions assemble!-autoinhibition as a major regulatory mechanism of integrin-mediated adhesion, Front Mol Biosci, 6, 144, 10.3389/fmolb.2019.00144 Nussinov, 2020, Autoinhibition can identify rare driver mutations and advise pharmacology, Faseb J, 34, 16, 10.1096/fj.201901341R Boggon, 2004, Structure and regulation of Src family kinases, Oncogene, 23, 7918, 10.1038/sj.onc.1208081 Bollhagen, 2022, Discovering autoinhibition as a design principle for the control of biological mechanisms, Stud Hist Philos Sci, 95, 145, 10.1016/j.shpsa.2022.08.008 Goksoy, 2008, Structural basis for the autoinhibition of talin in regulating integrin activation, Mol Cell, 31, 124, 10.1016/j.molcel.2008.06.011 Trudeau, 2013, Structure and intrinsic disorder in protein autoinhibition, Structure, 21, 332, 10.1016/j.str.2012.12.013 Majumdar, 2019, Liquid-liquid phase separation is driven by large-scale conformational unwinding and fluctuations of intrinsically disordered protein molecules, J Phys Chem Lett, 10, 3929, 10.1021/acs.jpclett.9b01731 Her, 2022, Molecular interactions underlying the phase separation of HP1alpha: role of phosphorylation, ligand and nucleic acid binding, Nucleic Acids Res, 50, 12702, 10.1093/nar/gkac1194 Chakrabarti, 2022, Intrinsically disordered proteins/regions and insight into their biomolecular interactions, Biophys Chem, 283, 10.1016/j.bpc.2022.106769 Bugge, 2020, Interactions by disorder - a matter of context, Front Mol Biosci, 7, 110, 10.3389/fmolb.2020.00110 Arbesu, 2018, Intramolecular fuzzy interactions involving intrinsically disordered domains, Front Mol Biosci, 5, 39, 10.3389/fmolb.2018.00039 Brown, 2011, Evolution and disorder, Curr Opin Struct Biol, 21, 441, 10.1016/j.sbi.2011.02.005 Koh, 2021, Probing coupled conformational transitions of intrinsically disordered proteins in their interactions with target proteins, Anal Biochem, 619, 114126, 10.1016/j.ab.2021.114126 Guo, 2012, Intrinsic disorder within and flanking the DNA-binding domains of human transcription factors, Pac Symp Biocomput, 104 Malagrino, 2022, On the effects of disordered tails, supertertiary structure and quinary interactions on the folding and function of protein domains, Biomolecules, 12, 10.3390/biom12020209 Prestel, 2019, The PCNA interaction motifs revisited: thinking outside the PIP-box, Cell Mol Life Sci, 76, 4923, 10.1007/s00018-019-03150-0 Tompa, 2014, A million peptide motifs for the molecular biologist, Mol Cell, 55, 161, 10.1016/j.molcel.2014.05.032 Kumar, 2022, The eukaryotic linear motif resource: 2022 release, Nucleic Acids Res, 50, D497, 10.1093/nar/gkab975 Desjardins, 2014, Synergy of aromatic residues and phosphoserines within the intrinsically disordered DNA-binding inhibitory elements of the Ets-1 transcription factor, Proc Natl Acad Sci USA, 111, 11019, 10.1073/pnas.1401891111 Kang, 2020, An autoinhibitory intramolecular interaction proof-reads RNA recognition by the essential splicing factor U2AF2, Proc Natl Acad Sci U S A, 117, 7140, 10.1073/pnas.1913483117 Cheng, 2022, Structural Insight into the MCM double hexamer activation by Dbf4-Cdc7 kinase, Nat Commun, 13, 1396, 10.1038/s41467-022-29070-5 Stott, 2014, Structural insights into the mechanism of negative regulation of single-box high mobility group proteins by the acidic tail domain, J Biol Chem, 289, 29817, 10.1074/jbc.M114.591115 Basu, 2020, The C-terminal tails of the mitochondrial transcription factors Mtf1 and TFB2M are part of an autoinhibitory mechanism that regulates DNA binding, J Biol Chem, 295, 6823, 10.1074/jbc.RA120.013338 Schweibenz, 2022, The intrinsically disordered CARDs-Helicase linker in RIG-I is a molecular gate for RNA proofreading, EMBO J, 41, 10.15252/embj.2021109782 Coucke, 2016, Direct coevolutionary couplings reflect biophysical residue interactions in proteins, J Chem Phys, 145, 174102 Jumper, 2021, Highly accurate protein structure prediction with AlphaFold, Nature, 596, 583, 10.1038/s41586-021-03819-2 Varadi, 2021, AlphaFold Protein Structure Database: massively expanding the structural coverage of protein-sequence space with high-accuracy models, Nucleic Acids Res, 50, D439, 10.1093/nar/gkab1061 Burke, 2012, Structures of inactive retinoblastoma protein reveal multiple mechanisms for cell cycle control, Genes Dev, 26, 1156, 10.1101/gad.189837.112 Fang, 2016, Hemi-methylated DNA opens a closed conformation of UHRF1 to facilitate its histone recognition, Nat Commun, 7, 11197, 10.1038/ncomms11197 Fenton, 2022, The MDMX acidic domain uses allovalency to bind both p53 and MDMX, J Mol Biol, 434, 167844, 10.1016/j.jmb.2022.167844 He, 2019, Interaction between p53 N terminus and core domain regulates specific and nonspecific DNA binding, Proc Natl Acad Sci U S A, 116, 8859, 10.1073/pnas.1903077116 Wang, 2023, Negatively charged, intrinsically disordered regions can accelerate target search by DNA-binding proteins, Nucleic Acids Res, 10 Bourgeois, 2021, Multiple regulatory intrinsically disordered motifs control FOXO4 transcription factor binding and function, Cell Rep, 36, 109446, 10.1016/j.celrep.2021.109446 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 Gong, 2021, Structural insight into chromatin recognition by multiple domains of the tumor suppressor RBBP1, J Mol Biol, 433, 10.1016/j.jmb.2021.167224 Esquina, 2019, Intramolecular electrostatic interactions contribute to phospholipase Cbeta3 autoinhibition, Cell Signal, 62, 109349, 10.1016/j.cellsig.2019.109349 Kjaergaard, 2021, Predicting the effect of disordered linkers on effective concentrations and avidity with the "C(eff) calculator" app, Methods Enzymol, 647, 145, 10.1016/bs.mie.2020.09.012 Spreitzer, 2022, FOXO transcription factors differ in their dynamics and intra/intermolecular interactions, Curr Res Struct Biol, 4, 118, 10.1016/j.crstbi.2022.04.001 Gregory, 2022, Sequence properties of an intramolecular interaction that inhibits p53 DNA binding, Biomolecules, 12, 10.3390/biom12111558 Sun, 2021, A phosphorylation-dependent switch in the disordered p53 transactivation domain regulates DNA binding, Proc Natl Acad Sci U S A, 118, 10.1073/pnas.2021456118 Gianni, 2021, Fuzziness and frustration in the energy landscape of protein folding, function, and assembly, Acc Chem Res, 54, 1251, 10.1021/acs.accounts.0c00813 Wei, 2016, Secondary interaction between MDMX and p53 core domain inhibits p53 DNA binding, Proc Natl Acad Sci U S A, 113, E2558, 10.1073/pnas.1603838113 Troilo, 2019, Understanding intramolecular crosstalk in an intrinsically disordered protein, ACS Chem Biol, 14, 337, 10.1021/acschembio.8b01055 Malaby, 2018, Structural dynamics control allosteric activation of cytohesin family arf GTPase exchange factors, Structure, 26, 106, 10.1016/j.str.2017.11.019 Li, 2018, Disordered linkers in multidomain allosteric proteins: entropic effect to favor the open state or enhanced local concentration to favor the closed state?, Protein Sci, 27, 1600, 10.1002/pro.3475 Ortega-Alarcon, 2021, Stabilization effect of intrinsically disordered regions on multidomain proteins: the case of the methyl-CpG protein 2, MeCP2, Biomolecules, 11, 10.3390/biom11081216 Yu, 2010, Structural and energetic mechanisms of cooperative autoinhibition and activation of Vav1, Cell, 140, 246, 10.1016/j.cell.2009.12.033 Zhong, 2022, The role of auxiliary domains in modulating CHD4 activity suggests mechanistic commonality between enzyme families, Nat Commun, 13, 7524, 10.1038/s41467-022-35002-0 Schwamberger, 2015, Combining SAXS and DLS for simultaneous measurements and time-resolved monitoring of nanoparticle synthesis, Nucl Instrum Methods Phys Res Sect B Beam Interact Mater Atoms, 343, 116, 10.1016/j.nimb.2014.11.049 Shannon, 2019, Evolutionary drivers of protein shape, Sci Rep, 9, 11873, 10.1038/s41598-019-47337-8 Argudo, 2021, Folding and self-assembly of short intrinsically disordered peptides and protein regions, Nanoscale Adv, 3, 1789, 10.1039/D0NA00941E Sorrell, 2019, Solution structures and biophysical analysis of full-length group A PAKs reveal they are monomeric and auto-inhibited in cis, Biochem J, 476, 1037, 10.1042/BCJ20180867 Bernado, 2007, Structural characterization of flexible proteins using small-angle X-ray scattering, J Am Chem Soc, 129, 5656, 10.1021/ja069124n Gomes, 2021, Conformational landscape of multidomain SMAD proteins, Comput Struct Biotechnol J, 19, 5210, 10.1016/j.csbj.2021.09.009 Ha, 2018, CDC42 binds PAK4 via an extended GTPase-effector interface, Proc Natl Acad Sci U S A, 115, 531, 10.1073/pnas.1717437115 Kleckner, 2011, An introduction to NMR-based approaches for measuring protein dynamics, Biochim Biophys Acta, 1814, 942, 10.1016/j.bbapap.2010.10.012 Borgia, 2018, Extreme disorder in an ultrahigh-affinity protein complex, Nature, 555, 61, 10.1038/nature25762 Kim, 2021, FOXO4 transactivation domain interaction with Forkhead DNA binding domain and effect on selective DNA recognition for transcription initiation, J Mol Biol, 433, 166808, 10.1016/j.jmb.2021.166808 Kim, 2022, Biophysical investigation of the dual binding surfaces of human transcription factors FOXO4 and p53, FEBS J, 289, 3163, 10.1111/febs.16333 Borcherds, 2018, Using NMR chemical shifts to determine residue-specific secondary structure populations for intrinsically disordered proteins, Methods Enzymol, 611, 101, 10.1016/bs.mie.2018.09.011 Greenfield, 2006, Using circular dichroism spectra to estimate protein secondary structure, Nat Protoc, 1, 2876, 10.1038/nprot.2006.202 Kodera, 2022, Visualization of intrinsically disordered proteins by high-speed atomic force microscopy, Curr Opin Struct Biol, 72, 260, 10.1016/j.sbi.2021.11.014 Kodera, 2021, Structural and dynamics analysis of intrinsically disordered proteins by high-speed atomic force microscopy, Nat Nanotechnol, 16, 181, 10.1038/s41565-020-00798-9 Shrestha, 2021, Full structural ensembles of intrinsically disordered proteins from unbiased molecular dynamics simulations, Commun Biol, 4, 243, 10.1038/s42003-021-01759-1 Tan, 2017, Anatomy of Mdm2 and Mdm4 in evolution, J Mol Cell Biol, 9, 3