{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T06:09:09Z","timestamp":1772172549494,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1007630","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2020,3,12]],"date-time":"2020-03-12T00:00:00Z","timestamp":1583971200000}}],"reference-count":60,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2020,3,2]],"date-time":"2020-03-02T00:00:00Z","timestamp":1583107200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"DOI":"10.1371\/journal.pcbi.1007630","type":"journal-article","created":{"date-parts":[[2020,3,2]],"date-time":"2020-03-02T13:35:00Z","timestamp":1583156100000},"page":"e1007630","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":18,"title":["Direct coupling analysis of epistasis in allosteric materials"],"prefix":"10.1371","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4860-7584","authenticated-orcid":true,"given":"Barbara","family":"Bravi","sequence":"first","affiliation":[]},{"given":"Riccardo","family":"Ravasio","sequence":"additional","affiliation":[]},{"given":"Carolina","family":"Brito","sequence":"additional","affiliation":[]},{"given":"Matthieu","family":"Wyart","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2020,3,2]]},"reference":[{"issue":"11","key":"pcbi.1007630.ref001","doi-asserted-by":"crossref","first-page":"6503","DOI":"10.1021\/acs.chemrev.5b00590","article-title":"Protein Allostery and Conformational Dynamics","volume":"116","author":"G Jingjing","year":"2016","journal-title":"Chem Rev"},{"issue":"11","key":"pcbi.1007630.ref002","doi-asserted-by":"crossref","first-page":"6463","DOI":"10.1021\/acs.chemrev.5b00544","article-title":"Controlling Allosteric Networks in Proteins","volume":"116","author":"NV Dokholyan","year":"2016","journal-title":"Chem Rev"},{"key":"pcbi.1007630.ref003","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.sbi.2015.10.004","article-title":"Allosteric sites: remote control in regulation of protein activity","volume":"37","author":"E Guarnera","year":"2016","journal-title":"Curr Opin Struct Biol"},{"key":"pcbi.1007630.ref004","doi-asserted-by":"crossref","first-page":"1132","DOI":"10.1002\/humu.23231","article-title":"Whole protein alanine-scanning mutagenesis of allostery: A large percentage of a protein can contribute to mechanism","volume":"38","author":"Q Tang","year":"2017","journal-title":"Human Mutation"},{"issue":"6","key":"pcbi.1007630.ref005","doi-asserted-by":"crossref","first-page":"E931","DOI":"10.1073\/pnas.1620667114","article-title":"Mutation of a kinase allosteric node uncouples dynamics linked to phosphotransfer","volume":"114","author":"LG Ahuja","year":"2017","journal-title":"Proc Natl Acad Sci USA"},{"issue":"22","key":"pcbi.1007630.ref006","doi-asserted-by":"crossref","first-page":"2643","DOI":"10.1016\/j.cub.2014.09.072","article-title":"A Comprehensive Biophysical Description of Pairwise Epistasis throughout an Entire Protein Domain","volume":"24","author":"CA Olson","year":"2014","journal-title":"Curr Biol"},{"issue":"1725","key":"pcbi.1007630.ref007","doi-asserted-by":"crossref","first-page":"3617","DOI":"10.1098\/rspb.2011.1537","article-title":"The causes of epistasis","volume":"278","author":"JAGM De Visser","year":"2011","journal-title":"Proc R Soc B"},{"key":"pcbi.1007630.ref008","doi-asserted-by":"crossref","first-page":"1204","DOI":"10.1002\/pro.2897","article-title":"Epistasis in protein evolution","volume":"25","author":"TN Starr","year":"2016","journal-title":"Protein Sci"},{"issue":"5844","key":"pcbi.1007630.ref009","doi-asserted-by":"crossref","first-page":"1544","DOI":"10.1126\/science.1142819","article-title":"Crystal Structure of an Ancient Protein: Evolution by Conformational Epistasis","volume":"317","author":"EA Ortlund","year":"2007","journal-title":"Science"},{"issue":"6138","key":"pcbi.1007630.ref010","doi-asserted-by":"crossref","first-page":"1324","DOI":"10.1126\/science.1236862","article-title":"Epistasis Among Adaptive Mutations in Deer Mouse Hemoglobin","volume":"340","author":"C Natarajan","year":"2013","journal-title":"Science"},{"issue":"8","key":"pcbi.1007630.ref011","doi-asserted-by":"crossref","first-page":"1779","DOI":"10.1093\/molbev\/mst096","article-title":"Patterns of Epistasis between Beneficial Mutations in an Antibiotic Resistance Gene","volume":"30","author":"MF Schenk","year":"2013","journal-title":"Mol Biol Evol"},{"key":"pcbi.1007630.ref012","doi-asserted-by":"crossref","first-page":"e34300","DOI":"10.7554\/eLife.34300","article-title":"Coevolution-based inference of amino acid interactions underlying protein function","volume":"7","author":"VH Salinas","year":"2018","journal-title":"eLife"},{"key":"pcbi.1007630.ref013","doi-asserted-by":"crossref","DOI":"10.1017\/CBO9780511790492","volume-title":"Biological sequence analysis: probabilistic models of proteins and nucleic acids","author":"R Durbin","year":"1998"},{"key":"pcbi.1007630.ref014","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/nsb881","article-title":"Evolutionarily conserved networks of residues mediate allosteric communication in proteins","volume":"10","author":"GM S\u00fcel","year":"2003","journal-title":"Nat Struct Mol Biol"},{"issue":"7","key":"pcbi.1007630.ref015","doi-asserted-by":"crossref","first-page":"1564","DOI":"10.1016\/j.cell.2011.10.049","article-title":"Hot Spots for Allosteric Regulation on Protein Surfaces","volume":"147","author":"KA Reynolds","year":"2011","journal-title":"Cell"},{"issue":"49","key":"pcbi.1007630.ref016","doi-asserted-by":"crossref","first-page":"E1293","DOI":"10.1073\/pnas.1111471108","article-title":"Direct-coupling analysis of residue coevolution captures native contacts across many protein families","volume":"108","author":"F Morcos","year":"2011","journal-title":"Proc Natl Acad Sci USA"},{"issue":"6322","key":"pcbi.1007630.ref017","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1126\/science.aah4043","article-title":"Protein Structure Determination using Metagenome sequence data","volume":"355","author":"S Ovchinnikov","year":"2017","journal-title":"Science"},{"issue":"3","key":"pcbi.1007630.ref018","doi-asserted-by":"crossref","first-page":"606","DOI":"10.1016\/j.immuni.2012.11.022","article-title":"Translating HIV Sequences into Quantitative Fitness Landscapes Predicts Viral Vulnerabilities for Rational Immunogen Design","volume":"38","author":"AL Ferguson","year":"2013","journal-title":"Immunity"},{"issue":"8","key":"pcbi.1007630.ref019","doi-asserted-by":"crossref","first-page":"e1003776","DOI":"10.1371\/journal.pcbi.1003776","article-title":"The Fitness Landscape of HIV-1 Gag: Advanced Modeling Approaches and Validation of Model Predictions by In Vitro Testing","volume":"10","author":"JK Mann","year":"2014","journal-title":"PLOS Computational Biology"},{"key":"pcbi.1007630.ref020","doi-asserted-by":"crossref","first-page":"37812","DOI":"10.1038\/srep37812","article-title":"Improving landscape inference by integrating heterogeneous data in the inverse Ising problem","volume":"6","author":"P Barrat-Charlaix","year":"2016","journal-title":"Scientific Reports"},{"issue":"1","key":"pcbi.1007630.ref021","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1093\/molbev\/msv211","article-title":"Coevolutionary Landscape Inference and the Context-Dependence of Mutations in Beta-Lactamase TEM-1","volume":"33","author":"M Figliuzzi","year":"2016","journal-title":"Mol Biol Evol"},{"issue":"2","key":"pcbi.1007630.ref022","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1038\/nbt.3769","article-title":"Mutation Effects Predicted from Sequence Co-Variation","volume":"35","author":"TA Hopf","year":"2017","journal-title":"Nature Biotechnology"},{"key":"pcbi.1007630.ref023","doi-asserted-by":"crossref","DOI":"10.1103\/PhysRevE.97.062404","article-title":"Inference of epistatic effects in a key mitochondrial protein","volume":"97","author":"ED Nelson","year":"2018","journal-title":"Phys Rev E"},{"key":"pcbi.1007630.ref024","article-title":"Learning the pattern of epistasis linking genotype and phenotype in a protein","author":"FJ Poelwijk","year":"2017","journal-title":"Bioarxiv"},{"issue":"34","key":"pcbi.1007630.ref025","doi-asserted-by":"crossref","first-page":"9122","DOI":"10.1073\/pnas.1702664114","article-title":"Origins of coevolution between residues distant in protein 3D structures","volume":"114","author":"I Anishchenko","year":"2017","journal-title":"Proc Natl Acad Sci USA"},{"issue":"4","key":"pcbi.1007630.ref026","doi-asserted-by":"crossref","first-page":"042704","DOI":"10.1103\/PhysRevE.91.042704","article-title":"Evolution of sparsity and modularity in a model of protein allostery","volume":"91","author":"M Hemery","year":"2015","journal-title":"Phys Rev E"},{"issue":"10","key":"pcbi.1007630.ref027","doi-asserted-by":"crossref","first-page":"2520","DOI":"10.1073\/pnas.1612139114","article-title":"Designing allostery-inspired response in mechanical networks","volume":"114","author":"JW Rocks","year":"2017","journal-title":"Proc Natl Acad Sci USA"},{"issue":"3","key":"pcbi.1007630.ref028","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1016\/j.bpj.2017.06.043","article-title":"Design of elastic networks with evolutionary optimised long-range communication as mechanical models of allosteric proteins","volume":"113","author":"H Flechsig","year":"2017","journal-title":"Biophys J"},{"issue":"10","key":"pcbi.1007630.ref029","doi-asserted-by":"crossref","first-page":"2526","DOI":"10.1073\/pnas.1615536114","article-title":"Architecture and coevolution of allosteric materials","volume":"114","author":"L Yan","year":"2017","journal-title":"Proc Natl Acad Sci USA"},{"issue":"12","key":"pcbi.1007630.ref030","doi-asserted-by":"crossref","first-page":"2787","DOI":"10.1016\/j.bpj.2018.05.015","article-title":"Principles for optimal cooperativity in allosteric materials","volume":"114","author":"L Yan","year":"2018","journal-title":"Biophys J"},{"key":"pcbi.1007630.ref031","article-title":"Physical model of the sequence-to-function map of proteins","volume":"7","author":"T Tlusty","year":"2017","journal-title":"Phys Rev X"},{"key":"pcbi.1007630.ref032","article-title":"Green function of correlated genes in a minimal mechanical model of protein evolution","author":"S Dutta","year":"2018","journal-title":"Proc Natl Acad Sci USA"},{"issue":"6034","key":"pcbi.1007630.ref033","doi-asserted-by":"crossref","first-page":"1190","DOI":"10.1126\/science.1203799","article-title":"Diminishing Returns Epistasis Among Beneficial Mutations Decelerates Adaptation","volume":"332","author":"HH Chou","year":"2011","journal-title":"Science"},{"key":"pcbi.1007630.ref034","doi-asserted-by":"crossref","DOI":"10.1098\/rspb.2016.1376","article-title":"Diminishing-returns epistasis among random beneficial mutations in a multicellular fungus","volume":"283","author":"S Schoustra","year":"2016","journal-title":"Proc R Soc B"},{"key":"pcbi.1007630.ref035","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1534\/genetics.107.075812","article-title":"Evolution Can Favor Antagonistic Epistasis","volume":"177","author":"MM Desai","year":"2007","journal-title":"Genetics"},{"issue":"2","key":"pcbi.1007630.ref036","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1038\/hdy.2012.15","article-title":"Magnitude and sign epistasis among deleterious mutations in a positive-sense plant RNA virus","volume":"109","author":"J Lali\u0107","year":"2012","journal-title":"Heredity"},{"issue":"3","key":"pcbi.1007630.ref037","doi-asserted-by":"crossref","first-page":"032601","DOI":"10.1088\/1361-6633\/aa9965","article-title":"Inverse statistical physics of protein sequences: a key issues review","volume":"81","author":"S Cocco","year":"2018","journal-title":"Rep Prog Phys"},{"key":"pcbi.1007630.ref038","doi-asserted-by":"crossref","first-page":"090601","DOI":"10.1103\/PhysRevLett.106.090601","article-title":"Adaptive Cluster Expansion for Inferring Boltzmann Machines with Noisy Data","volume":"106","author":"S Cocco","year":"2011","journal-title":"Phys Rev Lett"},{"key":"pcbi.1007630.ref039","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1007\/s10955-012-0463-4","article-title":"Adaptive cluster expansion for the inverse Ising problem: convergence, algorithm and tests","volume":"147","author":"S Cocco","year":"2012","journal-title":"J Stat Phys"},{"issue":"5","key":"pcbi.1007630.ref040","doi-asserted-by":"crossref","first-page":"e1004889","DOI":"10.1371\/journal.pcbi.1004889","article-title":"Benchmarking Inverse Statistical Approaches for Protein Structure and Design with Exactly Solvable Models","volume":"12","author":"H Jacquin","year":"2016","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1007630.ref041","first-page":"1018","article-title":"How Pairwise Coevolutionary Models Capture the Collective Residue Variability in Proteins?","volume":"354","author":"M Figliuzzi","year":"2017","journal-title":"Mol Biol Evol"},{"issue":"20","key":"pcbi.1007630.ref042","doi-asserted-by":"crossref","first-page":"3089","DOI":"10.1093\/bioinformatics\/btw328","article-title":"ACE: adaptive cluster expansion for maximum entropy graphical model inference","volume":"32","author":"JP Barton","year":"2016","journal-title":"Bioinformatics"},{"key":"pcbi.1007630.ref043","doi-asserted-by":"crossref","first-page":"012707","DOI":"10.1103\/PhysRevE.87.012707","article-title":"Improved contact prediction in proteins: Using pseudolikelihoods to infer Potts models","volume":"87","author":"M Ekeberg","year":"2013","journal-title":"Phys Rev E"},{"issue":"5438","key":"pcbi.1007630.ref044","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1126\/science.286.5438.295","article-title":"Evolutionarily conserved pathways of energetic connectivity in protein families","volume":"286","author":"SW Lockless","year":"1999","journal-title":"Science"},{"issue":"4","key":"pcbi.1007630.ref045","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1016\/j.cell.2009.07.038","article-title":"Protein sectors: evolutionary units of three-dimensional structure","volume":"138","author":"N Halabi","year":"2009","journal-title":"Cell"},{"issue":"4","key":"pcbi.1007630.ref046","doi-asserted-by":"crossref","first-page":"e1007010","DOI":"10.1371\/journal.pcbi.1007010","article-title":"Revealing evolutionary constraints on proteins through sequence analysis","volume":"15","author":"SW Wang","year":"2019","journal-title":"PLoS Comput Biol"},{"issue":"40","key":"pcbi.1007630.ref047","doi-asserted-by":"crossref","first-page":"5847","DOI":"10.1073\/pnas.1609462113","article-title":"Strain analysis of protein structures and low dimensionality of mechanical allosteric couplings","volume":"113","author":"MR Mitchell","year":"2016","journal-title":"Proc Natl Acad Sci USA"},{"issue":"1","key":"pcbi.1007630.ref048","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1529\/biophysj.104.055004","article-title":"Functional dynamics of PDZ binding domains: a normal-mode analysis","volume":"89","author":"P De Los Rios","year":"2005","journal-title":"Biophys J"},{"issue":"20","key":"pcbi.1007630.ref049","doi-asserted-by":"crossref","first-page":"7664","DOI":"10.1073\/pnas.0510426103","article-title":"Low-frequency normal modes that describe allosteric transitions in biological nanomachines are robust to sequence variations","volume":"103","author":"W Zheng","year":"2006","journal-title":"Proc Natl Acad Sci USA"},{"issue":"1475","key":"pcbi.1007630.ref050","doi-asserted-by":"crossref","first-page":"1469","DOI":"10.1098\/rspb.2001.1690","article-title":"Interaction between directional epistasis and average mutational effects","volume":"268","author":"CO Wilke","year":"2001","journal-title":"Proc R Soc B"},{"issue":"801","key":"pcbi.1007630.ref051","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1038\/nmeth.3027","article-title":"Deep mutational scanning: a new style of protein science","volume":"11","author":"DM Fowler","year":"2014","journal-title":"Nat Methods"},{"key":"pcbi.1007630.ref052","doi-asserted-by":"crossref","first-page":"e39397","DOI":"10.7554\/eLife.39397","article-title":"Learning Protein Constitutive Motifs from Sequence Data","volume":"8","author":"J Tubiana","year":"2019","journal-title":"eLife"},{"issue":"9","key":"pcbi.1007630.ref053","doi-asserted-by":"crossref","first-page":"e1005763","DOI":"10.1371\/journal.pcbi.1005763","article-title":"Probabilistic models for neural populations that naturally capture global coupling and criticality","volume":"13","author":"J Humplik","year":"2017","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1007630.ref054","doi-asserted-by":"crossref","first-page":"E7550","DOI":"10.1073\/pnas.1804015115","article-title":"Inferring the shape of global epistasis","volume":"115","author":"J Otwinowski","year":"2018","journal-title":"Proc Natl Acad Sci USA"},{"issue":"10","key":"pcbi.1007630.ref055","doi-asserted-by":"crossref","first-page":"816","DOI":"10.1038\/s41592-018-0138-4","article-title":"Deep Generative Models of Genetic Variation Capture the Effects of Mutations","volume":"15","author":"AJ Riesselman","year":"2018","journal-title":"Nature Methods"},{"issue":"12","key":"pcbi.1007630.ref056","doi-asserted-by":"crossref","first-page":"1315","DOI":"10.1038\/s41592-019-0598-1","article-title":"Unified Rational Protein Engineering with Sequence-Based Deep Representation Learning","volume":"16","author":"EC Alley","year":"2019","journal-title":"Nature Methods"},{"issue":"3","key":"pcbi.1007630.ref057","first-page":"1","article-title":"Inverse statistical problems: from the inverse Ising problem to data science","volume":"66","author":"RHC Nguyen","year":"2017","journal-title":"Adv Phys"},{"issue":"6","key":"pcbi.1007630.ref058","doi-asserted-by":"crossref","first-page":"063406","DOI":"10.1088\/1742-5468\/aa727d","article-title":"A statistical physics approach to learning curves for the inverse Ising problem","volume":"2017","author":"L Bachschmid-Romano","year":"2017","journal-title":"J Stat Mech Theory Exp"},{"key":"pcbi.1007630.ref059","doi-asserted-by":"crossref","first-page":"012132","DOI":"10.1103\/PhysRevE.90.012132","article-title":"Large pseudocounts and L2-norm penalties are necessary for the mean-field inference of Ising and Potts models","volume":"90","author":"JP Barton","year":"2014","journal-title":"Phys Rev E"},{"key":"pcbi.1007630.ref060","doi-asserted-by":"crossref","first-page":"1073","DOI":"10.1038\/nprot.2009.86","article-title":"Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm","volume":"4","author":"P Kumar","year":"2009","journal-title":"Nat Protoc"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1007630","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2020,3,12]],"date-time":"2020-03-12T00:00:00Z","timestamp":1583971200000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1007630","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,3,12]],"date-time":"2020-03-12T13:55:33Z","timestamp":1584021333000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1007630"}},"subtitle":[],"editor":[{"given":"Alexandre V.","family":"Morozov","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2020,3,2]]},"references-count":60,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2020,3,2]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1007630","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/519116","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,3,2]]}}}