{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,9,20]],"date-time":"2025-09-20T19:34:51Z","timestamp":1758396891397,"version":"3.37.3"},"reference-count":64,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2020,3,24]],"date-time":"2020-03-24T00:00:00Z","timestamp":1585008000000},"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.1007583","type":"journal-article","created":{"date-parts":[[2020,3,24]],"date-time":"2020-03-24T17:24:46Z","timestamp":1585070686000},"page":"e1007583","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":2,"title":["An Evolutionary Trace method defines functionally important bases and sites common to RNA families"],"prefix":"10.1371","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5096-6864","authenticated-orcid":true,"given":"Ilya B.","family":"Novikov","sequence":"first","affiliation":[]},{"given":"Angela D.","family":"Wilkins","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4057-7122","authenticated-orcid":true,"given":"Olivier","family":"Lichtarge","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2020,3,24]]},"reference":[{"issue":"1","key":"pcbi.1007583.ref001","doi-asserted-by":"crossref","first-page":"R17","DOI":"10.1093\/hmg\/ddl046","article-title":"Non-coding RNA","volume":"15","author":"JS Mattick","year":"2006","journal-title":"Hum Mol Genet"},{"issue":"3","key":"pcbi.1007583.ref002","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1038\/nrg2521","article-title":"Long non-coding RNAs: insights into functions","volume":"10","author":"TR Mercer","year":"2009","journal-title":"Nat Rev Genet"},{"issue":"2","key":"pcbi.1007583.ref003","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/S0092-8674(01)00205-7","article-title":"Mutations in the RNA component of RNase MRP cause a pleiotropic human disease, cartilage-hair hypoplasia","volume":"104","author":"M Ridanpaa","year":"2001","journal-title":"Cell"},{"issue":"6","key":"pcbi.1007583.ref004","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1038\/ng.158","article-title":"Prader-Willi phenotype caused by paternal deficiency for the HBII-85 C\/D box small nucleolar RNA cluster","volume":"40","author":"T Sahoo","year":"2008","journal-title":"Nat Genet"},{"issue":"6854","key":"pcbi.1007583.ref005","doi-asserted-by":"crossref","first-page":"432","DOI":"10.1038\/35096585","article-title":"The RNA component of telomerase is mutated in autosomal dominant dyskeratosis congenita","volume":"413","author":"T Vulliamy","year":"2001","journal-title":"Nature"},{"issue":"12","key":"pcbi.1007583.ref006","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1038\/nrg3074","article-title":"Non-coding RNAs in human disease","volume":"12","author":"M Esteller","year":"2011","journal-title":"Nat Rev Genet"},{"issue":"2","key":"pcbi.1007583.ref007","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1002\/path.2638","article-title":"Non-coding RNAs: regulators of disease","volume":"220","author":"RJ Taft","year":"2010","journal-title":"J Pathol"},{"issue":"3","key":"pcbi.1007583.ref008","doi-asserted-by":"crossref","first-page":"1180","DOI":"10.1158\/0008-5472.CAN-12-2850","article-title":"The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells","volume":"73","author":"T Gutschner","year":"2013","journal-title":"Cancer Res"},{"issue":"11","key":"pcbi.1007583.ref009","doi-asserted-by":"crossref","first-page":"12693","DOI":"10.18632\/oncotarget.7281","article-title":"MALAT1 long ncRNA promotes gastric cancer metastasis by suppressing PCDH10","volume":"7","author":"Y Qi","year":"2016","journal-title":"Oncotarget"},{"issue":"7575","key":"pcbi.1007583.ref010","doi-asserted-by":"crossref","first-page":"672","DOI":"10.1038\/nature15542","article-title":"Selective small-molecule inhibition of an RNA structural element","volume":"526","author":"JA Howe","year":"2015","journal-title":"Nature"},{"issue":"1","key":"pcbi.1007583.ref011","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1038\/nrmicro3155","article-title":"Ribosome-targeting antibiotics and mechanisms of bacterial resistance","volume":"12","author":"DN Wilson","year":"2014","journal-title":"Nat Rev Microbiol"},{"key":"pcbi.1007583.ref012","article-title":"The RNA world in the 21st century-a systems approach to finding non-coding keys to clinical questions","author":"U Schmitz","year":"2015","journal-title":"Brief Bioinform"},{"issue":"3","key":"pcbi.1007583.ref013","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1016\/j.sbi.2010.04.001","article-title":"Advances in RNA structure analysis by chemical probing","volume":"20","author":"KM Weeks","year":"2010","journal-title":"Curr Opin Struct Biol"},{"key":"pcbi.1007583.ref014","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/978-1-60327-429-6_1","article-title":"UNAFold: software for nucleic acid folding and hybridization","volume":"453","author":"NR Markham","year":"2008","journal-title":"Methods Mol Biol"},{"issue":"7183","key":"pcbi.1007583.ref015","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1038\/nature06684","article-title":"The MC-Fold and MC-Sym pipeline infers RNA structure from sequence data","volume":"452","author":"M Parisien","year":"2008","journal-title":"Nature"},{"issue":"1","key":"pcbi.1007583.ref016","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.jbiotec.2006.01.034","article-title":"Beyond Mfold: recent advances in RNA bioinformatics","volume":"124","author":"J Reeder","year":"2006","journal-title":"J Biotechnol"},{"issue":"13","key":"pcbi.1007583.ref017","doi-asserted-by":"crossref","first-page":"3406","DOI":"10.1093\/nar\/gkg595","article-title":"Mfold web server for nucleic acid folding and hybridization prediction","volume":"31","author":"M Zuker","year":"2003","journal-title":"Nucleic Acids Res"},{"issue":"1","key":"pcbi.1007583.ref018","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1146\/annurev-biophys-070816-034125","article-title":"RNA Structure: Advances and Assessment of 3D Structure Prediction","volume":"46","author":"Z Miao","year":"2017","journal-title":"Annual Review of Biophysics"},{"issue":"4","key":"pcbi.1007583.ref019","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1261\/rna.912608","article-title":"Hammerhead redux: does the new structure fit the old biochemical data?","volume":"14","author":"JA Nelson","year":"2008","journal-title":"RNA"},{"key":"pcbi.1007583.ref020","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1007\/978-1-61779-465-0_3","article-title":"Evolutionary trace for prediction and redesign of protein functional sites","volume":"819","author":"A Wilkins","year":"2012","journal-title":"Methods Mol Biol"},{"issue":"W1","key":"pcbi.1007583.ref021","doi-asserted-by":"crossref","first-page":"W344","DOI":"10.1093\/nar\/gkw408","article-title":"ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules","volume":"44","author":"H Ashkenazy","year":"2016","journal-title":"Nucleic Acids Res"},{"issue":"12","key":"pcbi.1007583.ref022","doi-asserted-by":"crossref","first-page":"e1001025","DOI":"10.1371\/journal.pcbi.1001025","article-title":"Identifying a high fraction of the human genome to be under selective constraint using GERP++","volume":"6","author":"EV Davydov","year":"2010","journal-title":"PLoS Comput Biol"},{"issue":"8","key":"pcbi.1007583.ref023","doi-asserted-by":"crossref","first-page":"1034","DOI":"10.1101\/gr.3715005","article-title":"Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes","volume":"15","author":"A Siepel","year":"2005","journal-title":"Genome Res"},{"issue":"5221","key":"pcbi.1007583.ref024","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1038\/224759a0","article-title":"Detailed molecular model for transfer ribonucleic acid","volume":"224","author":"M Levitt","year":"1969","journal-title":"Nature"},{"issue":"5517","key":"pcbi.1007583.ref025","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1038\/256505a0","article-title":"5S RNA secondary structure","volume":"256","author":"GE Fox","year":"1975","journal-title":"Nature"},{"issue":"3","key":"pcbi.1007583.ref026","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1016\/0022-2836(90)90386-Z","article-title":"Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis","volume":"216","author":"F Michel","year":"1990","journal-title":"J Mol Biol"},{"issue":"23","key":"pcbi.1007583.ref027","doi-asserted-by":"crossref","first-page":"5112","DOI":"10.1093\/nar\/22.23.5112","article-title":"Stochastic context-free grammars for tRNA modeling","volume":"22","author":"Y Sakakibara","year":"1994","journal-title":"Nucleic Acids Res"},{"issue":"4","key":"pcbi.1007583.ref028","doi-asserted-by":"crossref","first-page":"963","DOI":"10.1016\/j.cell.2016.03.030","article-title":"3D RNA and Functional Interactions from Evolutionary Couplings","volume":"165","author":"C Weinreb","year":"2016","journal-title":"Cell"},{"issue":"2","key":"pcbi.1007583.ref029","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1006\/jmbi.1996.0167","article-title":"An evolutionary trace method defines binding surfaces common to protein families","volume":"257","author":"O Lichtarge","year":"1996","journal-title":"J Mol Biol"},{"issue":"5","key":"pcbi.1007583.ref030","doi-asserted-by":"crossref","first-page":"1265","DOI":"10.1016\/j.jmb.2003.12.078","article-title":"A family of evolution-entropy hybrid methods for ranking protein residues by importance","volume":"336","author":"I Mihalek","year":"2004","journal-title":"J Mol Biol"},{"issue":"12","key":"pcbi.1007583.ref031","doi-asserted-by":"crossref","first-page":"2050","DOI":"10.1101\/gr.176214.114","article-title":"A formal perturbation equation between genotype and phenotype determines the Evolutionary Action of protein-coding variations on fitness","volume":"24","author":"P Katsonis","year":"2014","journal-title":"Genome Res"},{"issue":"2\u20133","key":"pcbi.1007583.ref032","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1023\/A:1026115125950","article-title":"Accurate and scalable identification of functional sites by evolutionary tracing","volume":"4","author":"O Lichtarge","year":"2003","journal-title":"J Struct Funct Genomics"},{"issue":"49","key":"pcbi.1007583.ref033","doi-asserted-by":"crossref","first-page":"12727","DOI":"10.1523\/JNEUROSCI.2734-06.2006","article-title":"Essential helix interactions in the anion transporter domain of prestin revealed by evolutionary trace analysis","volume":"26","author":"L Rajagopalan","year":"2006","journal-title":"J Neurosci"},{"issue":"10","key":"pcbi.1007583.ref034","doi-asserted-by":"crossref","first-page":"2496","DOI":"10.1093\/bioinformatics\/bti340","article-title":"An evolution based classifier for prediction of protein interfaces without using protein structures","volume":"21","author":"I Res","year":"2005","journal-title":"Bioinformatics"},{"issue":"17","key":"pcbi.1007583.ref035","doi-asserted-by":"crossref","first-page":"7787","DOI":"10.1073\/pnas.0914877107","article-title":"Evolution-guided discovery and recoding of allosteric pathway specificity determinants in psychoactive bioamine receptors","volume":"107","author":"GJ Rodriguez","year":"2010","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"4","key":"pcbi.1007583.ref036","doi-asserted-by":"crossref","first-page":"1046","DOI":"10.1002\/prot.21074","article-title":"Evolutionary identification of a subtype specific functional site in the ligand binding domain of steroid receptors","volume":"64","author":"M Raviscioni","year":"2006","journal-title":"Proteins"},{"issue":"36","key":"pcbi.1007583.ref037","doi-asserted-by":"crossref","first-page":"31818","DOI":"10.1074\/jbc.M501924200","article-title":"Evolutionary trace-based peptides identify a novel asymmetric interaction that mediates oligomerization in nuclear receptors","volume":"280","author":"P Gu","year":"2005","journal-title":"J Biol Chem"},{"key":"pcbi.1007583.ref038","doi-asserted-by":"crossref","first-page":"S6","DOI":"10.1186\/1471-2105-14-S3-S6","article-title":"Function prediction from networks of local evolutionary similarity in protein structure","volume":"143","author":"S Erdin","year":"2013","journal-title":"BMC Bioinformatics"},{"key":"pcbi.1007583.ref039","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1186\/1471-2105-9-17","article-title":"Prediction of enzyme function based on 3D templates of evolutionarily important amino acids","volume":"9","author":"DM Kristensen","year":"2008","journal-title":"BMC Bioinformatics"},{"issue":"1","key":"pcbi.1007583.ref040","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1006\/jmbi.2001.5327","article-title":"Structural clusters of evolutionary trace residues are statistically significant and common in proteins","volume":"316","author":"S Madabushi","year":"2002","journal-title":"J Mol Biol"},{"issue":"1","key":"pcbi.1007583.ref041","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1002\/prot.20866","article-title":"Evolutionary and structural feedback on selection of sequences for comparative analysis of proteins","volume":"63","author":"I Mihalek","year":"2006","journal-title":"Proteins"},{"issue":"2","key":"pcbi.1007583.ref042","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1093\/bioinformatics\/bti791","article-title":"A structure and evolution-guided Monte Carlo sequence selection strategy for multiple alignment-based analysis of proteins","volume":"22","author":"I Mihalek","year":"2006","journal-title":"Bioinformatics"},{"issue":"21","key":"pcbi.1007583.ref043","doi-asserted-by":"crossref","first-page":"2714","DOI":"10.1093\/bioinformatics\/btt489","article-title":"Accounting for epistatic interactions improves the functional analysis of protein structures","volume":"29","author":"AD Wilkins","year":"2013","journal-title":"Bioinformatics"},{"issue":"D1","key":"pcbi.1007583.ref044","doi-asserted-by":"crossref","first-page":"D335","DOI":"10.1093\/nar\/gkx1038","article-title":"Rfam 13.0: shifting to a genome-centric resource for non-coding RNA families","volume":"46","author":"I Kalvari","year":"2018","journal-title":"Nucleic Acids Res"},{"issue":"1","key":"pcbi.1007583.ref045","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/S0022-2836(03)00663-6","article-title":"Combining inference from evolution and geometric probability in protein structure evaluation","volume":"331","author":"I Mihalek","year":"2003","journal-title":"J Mol Biol"},{"issue":"5","key":"pcbi.1007583.ref046","doi-asserted-by":"crossref","first-page":"871","DOI":"10.1261\/rna.031401.111","article-title":"The ubiquitous hammerhead ribozyme","volume":"18","author":"C Hammann","year":"2012","journal-title":"RNA"},{"key":"pcbi.1007583.ref047","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1146\/annurev.biophys.050708.133710","article-title":"Comparative enzymology and structural biology of RNA self-cleavage","volume":"38","author":"MJ Fedor","year":"2009","journal-title":"Annu Rev Biophys"},{"issue":"9","key":"pcbi.1007583.ref048","doi-asserted-by":"crossref","first-page":"e234","DOI":"10.1371\/journal.pbio.0060234","article-title":"Capturing hammerhead ribozyme structures in action by modulating general base catalysis","volume":"6","author":"YI Chi","year":"2008","journal-title":"PLoS Biol"},{"issue":"9","key":"pcbi.1007583.ref049","doi-asserted-by":"crossref","first-page":"708","DOI":"10.1038\/nsb959","article-title":"Sequence elements outside the hammerhead ribozyme catalytic core enable intracellular activity","volume":"10","author":"A Khvorova","year":"2003","journal-title":"Nat Struct Biol"},{"issue":"41","key":"pcbi.1007583.ref050","doi-asserted-by":"crossref","first-page":"6369","DOI":"10.1021\/acs.biochem.5b00824","article-title":"Two Divalent Metal Ions and Conformational Changes Play Roles in the Hammerhead Ribozyme Cleavage Reaction","volume":"54","author":"A Mir","year":"2015","journal-title":"Biochemistry"},{"issue":"10","key":"pcbi.1007583.ref051","doi-asserted-by":"crossref","first-page":"5503","DOI":"10.1073\/pnas.091097498","article-title":"Dissection of the ion-induced folding of the hammerhead ribozyme using 19F NMR","volume":"98","author":"C Hammann","year":"2001","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"7393","key":"pcbi.1007583.ref052","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1038\/nature10913","article-title":"A new understanding of the decoding principle on the ribosome","volume":"484","author":"N Demeshkina","year":"2012","journal-title":"Nature"},{"issue":"3","key":"pcbi.1007583.ref053","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1016\/j.molcel.2007.03.015","article-title":"The ribosomal peptidyl transferase","volume":"26","author":"M Beringer","year":"2007","journal-title":"Mol Cell"},{"issue":"5","key":"pcbi.1007583.ref054","doi-asserted-by":"crossref","first-page":"528","DOI":"10.1038\/nsmb.1577","article-title":"Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome","volume":"16","author":"RM Voorhees","year":"2009","journal-title":"Nat Struct Mol Biol"},{"issue":"28","key":"pcbi.1007583.ref055","doi-asserted-by":"crossref","first-page":"10251","DOI":"10.1073\/pnas.1407205111","article-title":"Evolution of the ribosome at atomic resolution","volume":"111","author":"AS Petrov","year":"2014","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"4076","key":"pcbi.1007583.ref056","doi-asserted-by":"crossref","first-page":"864","DOI":"10.1126\/science.179.4076.864","article-title":"Assembly of bacterial ribosomes","volume":"179","author":"M Nomura","year":"1973","journal-title":"Science"},{"issue":"10","key":"pcbi.1007583.ref057","doi-asserted-by":"crossref","first-page":"2146","DOI":"10.1016\/j.jmb.2016.02.009","article-title":"Intersubunit Bridges of the Bacterial Ribosome","volume":"428","author":"Q Liu","year":"2016","journal-title":"J Mol Biol"},{"issue":"30","key":"pcbi.1007583.ref058","doi-asserted-by":"crossref","first-page":"17758","DOI":"10.1074\/jbc.270.30.17758","article-title":"Posttranscriptional modification of the central loop of domain V in Escherichia coli 23 S ribosomal RNA","volume":"270","author":"JA Kowalak","year":"1995","journal-title":"J Biol Chem"},{"issue":"8","key":"pcbi.1007583.ref059","doi-asserted-by":"crossref","first-page":"2353","DOI":"10.1021\/bi00382a042","article-title":"In vitro synthesis of 16S ribosomal RNA containing single base changes and assembly into a functional 30S ribosome","volume":"26","author":"W Krzyzosiak","year":"1987","journal-title":"Biochemistry"},{"key":"pcbi.1007583.ref060","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1186\/1471-2105-3-2","article-title":"The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs","volume":"3","author":"JJ Cannone","year":"2002","journal-title":"BMC Bioinformatics"},{"issue":"6977","key":"pcbi.1007583.ref061","doi-asserted-by":"crossref","first-page":"862","DOI":"10.1038\/nature02332","article-title":"Visualization of release factor 3 on the ribosome during termination of protein synthesis","volume":"427","author":"BP Klaholz","year":"2004","journal-title":"Nature"},{"issue":"7","key":"pcbi.1007583.ref062","doi-asserted-by":"crossref","first-page":"e1001095","DOI":"10.1371\/journal.pbio.1001095","article-title":"The Cryo-EM structure of a complete 30S translation initiation complex from Escherichia coli","volume":"9","author":"P Julian","year":"2011","journal-title":"PLoS Biol"},{"issue":"2","key":"pcbi.1007583.ref063","first-page":"202","article-title":"RNA in evolution. Wiley Interdisciplinary Reviews","volume":"1","author":"N Lehman","year":"2010","journal-title":"RNA"},{"issue":"1","key":"pcbi.1007583.ref064","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1038\/nmeth.4066","article-title":"A statistical test for conserved RNA structure shows lack of evidence for structure in lncRNAs","volume":"14","author":"E Rivas","year":"2017","journal-title":"Nat Methods"}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1007583","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,3,5]],"date-time":"2021-03-05T22:52:37Z","timestamp":1614984757000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1007583"}},"subtitle":[],"editor":[{"given":"Francois","family":"Major","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2020,3,24]]},"references-count":64,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2020,3,24]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1007583","relation":{},"ISSN":["1553-7358"],"issn-type":[{"type":"electronic","value":"1553-7358"}],"subject":[],"published":{"date-parts":[[2020,3,24]]}}}