{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T06:21:25Z","timestamp":1772173285500,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1011787","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2024,5,21]],"date-time":"2024-05-21T00:00:00Z","timestamp":1716249600000}}],"reference-count":81,"publisher":"Public Library of Science (PLoS)","issue":"5","license":[{"start":{"date-parts":[[2024,5,7]],"date-time":"2024-05-07T00:00:00Z","timestamp":1715040000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"University of Victoria Department of Computer Science"},{"DOI":"10.13039\/100004318","name":"Microsoft","doi-asserted-by":"publisher","award":["AI4Health Azure Grant"],"award-info":[{"award-number":["AI4Health Azure Grant"]}],"id":[{"id":"10.13039\/100004318","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Understanding and targeting functional RNA structures towards treatment of coronavirus infection can help us to prepare for novel variants of SARS-CoV-2 (the virus causing COVID-19), and any other coronaviruses that could emerge via human-to-human transmission or potential zoonotic (inter-species) events. Leveraging the fact that all coronaviruses use a mechanism known as \u22121 programmed ribosomal frameshifting (\u22121 PRF) to replicate, we apply algorithms to predict the most energetically favourable secondary structures (each nucleotide involved in at most one pairing) that may be involved in regulating the \u22121 PRF event in coronaviruses, especially SARS-CoV-2. We compute previously unknown most stable structure predictions for the frameshift site of coronaviruses via hierarchical folding, a biologically motivated framework where initial non-crossing structure folds first, followed by subsequent, possibly crossing (pseudoknotted), structures. Using mutual information from 181 coronavirus sequences, in conjunction with the algorithm KnotAli, we compute secondary structure predictions for the frameshift site of different coronaviruses. We then utilize the Shapify algorithm to obtain most stable SARS-CoV-2 secondary structure predictions guided by frameshift sequence-specific and genome-wide experimental data. We build on our previous secondary structure investigation of the singular SARS-CoV-2 68 nt frameshift element sequence, by using Shapify to obtain predictions for 132 extended sequences and including covariation information. Previous investigations have not applied hierarchical folding to extended length SARS-CoV-2 frameshift sequences. By doing so, we simulate the effects of ribosome interaction with the frameshift site, providing insight to biological function. We contribute in-depth discussion to contextualize secondary structure dual-graph motifs for SARS-CoV-2, highlighting the energetic stability of the previously identified 3_8 motif alongside the known dominant 3_3 and 3_6 (native-type) \u22121 PRF structures. Using a combination of thermodynamic methods and sequence covariation, our novel predictions suggest function of the attenuator hairpin via previously unknown pseudoknotted base pairing. While certain initial RNA folding is consistent, other pseudoknotted base pairs form which indicate potential conformational switching between the two structures.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1011787","type":"journal-article","created":{"date-parts":[[2024,5,7]],"date-time":"2024-05-07T13:39:17Z","timestamp":1715089157000},"page":"e1011787","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":3,"title":["Tying the knot: Unraveling the intricacies of the coronavirus frameshift 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Hajdin","year":"2013","journal-title":"PNAS"},{"issue":"3","key":"pcbi.1011787.ref034","doi-asserted-by":"crossref","first-page":"584","DOI":"10.1016\/j.molcel.2020.12.041","article-title":"Comprehensive in vivo secondary structure of the SARS-CoV-2 genome reveals novel regulatory motifs and mechanisms","volume":"81","author":"NC Huston","year":"2021","journal-title":"Mol Cell"},{"issue":"22","key":"pcbi.1011787.ref035","doi-asserted-by":"crossref","first-page":"12436","DOI":"10.1093\/nar\/gkaa1053","article-title":"Genome-wide mapping of SARS-CoV-2 RNA structures identifies therapeutically-relevant elements","volume":"48","author":"I Manfredonia","year":"2020","journal-title":"Nucleic Acids Res"},{"issue":"1","key":"pcbi.1011787.ref036","first-page":"1","article-title":"Comprehensive mapping of SARS-CoV-2 interactions in vivo reveals functional virus-host interactions","volume":"12","author":"SL Yang","year":"2021","journal-title":"Nat 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SARS-CoV-2 mutation and lineage tracking by locations and dates of interest","volume":"10","author":"AT Chen","year":"2021","journal-title":"Elife"},{"key":"pcbi.1011787.ref044","doi-asserted-by":"crossref","DOI":"10.1101\/2020.06.26.174193","volume-title":"A cytosine-to-uracil change within the programmed-1 ribosomal frameshift signal of SARS-CoV-2 results in structural similarities with the MERS-CoV signal","author":"D Fourmy","year":"2020"},{"issue":"2","key":"pcbi.1011787.ref045","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1006\/jmbi.1999.3001","article-title":"How RNA folds","volume":"293","author":"I Tinoco","year":"1999","journal-title":"J Mol Biol"},{"issue":"13","key":"pcbi.1011787.ref046","doi-asserted-by":"crossref","first-page":"4659","DOI":"10.1021\/ja0436749","article-title":"RNA SHAPE chemistry reveals nonhierarchical interactions dominate equilibrium structural transitions in tRNAAsp transcripts","volume":"127","author":"KA Wilkinson","year":"2005","journal-title":"J Am Chem Soc"},{"issue":"6","key":"pcbi.1011787.ref047","doi-asserted-by":"crossref","first-page":"1164","DOI":"10.1261\/rna.894608","article-title":"Ab initio RNA folding by discrete molecular dynamics: from structure prediction to folding mechanisms","volume":"14","author":"F Ding","year":"2008","journal-title":"RNA"},{"issue":"41","key":"pcbi.1011787.ref048","doi-asserted-by":"crossref","first-page":"17349","DOI":"10.1073\/pnas.0906625106","article-title":"Assembly mechanisms of RNA pseudoknots are determined by the stabilities of constituent secondary structures","volume":"106","author":"SS Cho","year":"2009","journal-title":"PNAS"},{"issue":"31","key":"pcbi.1011787.ref049","doi-asserted-by":"crossref","first-page":"12706","DOI":"10.1073\/pnas.0905046106","article-title":"Triplex structures in an RNA pseudoknot enhance mechanical stability and increase efficiency of\u20131 ribosomal frameshifting","volume":"106","author":"G Chen","year":"2009","journal-title":"PNAS"},{"issue":"10","key":"pcbi.1011787.ref050","doi-asserted-by":"crossref","first-page":"3072","DOI":"10.1093\/bioinformatics\/btaa080","article-title":"Estimating the power of sequence covariation for detecting conserved RNA structure","volume":"36","author":"E Rivas","year":"2020","journal-title":"Bioinformatics"},{"issue":"4","key":"pcbi.1011787.ref051","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1006\/jmbi.1999.2801","article-title":"RNA secondary structure prediction based on free energy and phylogenetic analysis","volume":"289","author":"V Juan","year":"1999","journal-title":"J Mol Biol"},{"key":"pcbi.1011787.ref052","doi-asserted-by":"crossref","unstructured":"Schroeder SJ, Turner DH. Optical melting measurements of nucleic acid thermodynamics. In: Methods Enzymol.. vol. 468. Elsevier; 2009. p. 371\u2013387.","DOI":"10.1016\/S0076-6879(09)68017-4"},{"issue":"5","key":"pcbi.1011787.ref053","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1006\/jmbi.1999.2700","article-title":"Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure","volume":"288","author":"DH Mathews","year":"1999","journal-title":"J Mol Biol"},{"issue":"19","key":"pcbi.1011787.ref054","doi-asserted-by":"crossref","first-page":"7287","DOI":"10.1073\/pnas.0401799101","article-title":"Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure","volume":"101","author":"DH Mathews","year":"2004","journal-title":"PNAS"},{"issue":"1","key":"pcbi.1011787.ref055","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1261\/rna.1689910","article-title":"Improved free energy parameters for RNA pseudoknotted secondary structure prediction","volume":"16","author":"MS Andronescu","year":"2010","journal-title":"RNA"},{"issue":"1","key":"pcbi.1011787.ref056","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1146\/annurev.bb.17.060188.001123","article-title":"RNA structure prediction","volume":"17","author":"DH Turner","year":"1988","journal-title":"Annu Rev Biophys and Biochem"},{"issue":"17","key":"pcbi.1011787.ref057","doi-asserted-by":"crossref","first-page":"4116","DOI":"10.3390\/ijms20174116","article-title":"3dRNA v2. 0: An Updated Web Server for RNA 3D Structure Prediction","volume":"20","author":"J Wang","year":"2019","journal-title":"Int J Mol Sci"},{"issue":"W1","key":"pcbi.1011787.ref058","doi-asserted-by":"crossref","first-page":"W30","DOI":"10.1093\/nar\/gky314","article-title":"RNApdbee 2.0: multifunctional tool for RNA structure annotation","volume":"46","author":"T Zok","year":"2018","journal-title":"Nucleic Acids Res"},{"issue":"W1","key":"pcbi.1011787.ref059","doi-asserted-by":"crossref","first-page":"W26","DOI":"10.1093\/nar\/gkz394","article-title":"Web 3DNA 2.0 for the analysis, visualization, and modeling of 3D nucleic acid structures","volume":"47","author":"S Li","year":"2019","journal-title":"Nucleic Acids Res"},{"key":"pcbi.1011787.ref060","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1007\/978-1-4939-6433-8_13","volume-title":"RNA Structure Determination","author":"M Biesiada","year":"2016"},{"issue":"7183","key":"pcbi.1011787.ref061","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":"17","key":"pcbi.1011787.ref062","doi-asserted-by":"crossref","first-page":"2891","DOI":"10.1093\/bioinformatics\/btv221","article-title":"iFoldRNA v2: folding RNA with constraints","volume":"31","author":"A Krokhotin","year":"2015","journal-title":"Bioinformatics"},{"key":"pcbi.1011787.ref063","doi-asserted-by":"crossref","first-page":"574485","DOI":"10.3389\/fgene.2020.574485","article-title":"Advances in RNA 3D structure modeling using experimental data","volume":"11","author":"B Li","year":"2020","journal-title":"Front Genet"},{"issue":"1","key":"pcbi.1011787.ref064","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1186\/s12859-022-04673-3","article-title":"KnotAli: informed energy minimization through the use of evolutionary information","volume":"23","author":"M Gray","year":"2022","journal-title":"BMC Bioinf"},{"issue":"4","key":"pcbi.1011787.ref065","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1016\/j.bpj.2009.10.040","article-title":"Free energy profile of RNA hairpins: a molecular dynamics simulation study","volume":"98","author":"NJ Deng","year":"2010","journal-title":"Biophys J"},{"issue":"5038","key":"pcbi.1011787.ref066","doi-asserted-by":"crossref","first-page":"1598","DOI":"10.1126\/science.1749933","article-title":"The energy landscapes and motions of proteins","volume":"254","author":"H Frauenfelder","year":"1991","journal-title":"Science"},{"issue":"1","key":"pcbi.1011787.ref067","doi-asserted-by":"crossref","first-page":"4284","DOI":"10.1038\/s41467-022-31353-w","article-title":"Length-dependent motions of SARS-CoV-2 frameshifting RNA pseudoknot and alternative conformations suggest avenues for frameshifting suppression","volume":"13","author":"S Yan","year":"2022","journal-title":"Nat Commun"},{"issue":"1","key":"pcbi.1011787.ref068","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2105-5-88","article-title":"RAG: RNA-As-Graphs web resource","volume":"5","author":"D Fera","year":"2004","journal-title":"BMC Bioinf"},{"issue":"11","key":"pcbi.1011787.ref069","doi-asserted-by":"crossref","first-page":"2926","DOI":"10.1093\/nar\/gkg365","article-title":"Exploring the repertoire of RNA secondary motifs using graph theory; implications for RNA design","volume":"31","author":"HH Gan","year":"2003","journal-title":"Nucleic Acids Res"},{"issue":"16","key":"pcbi.1011787.ref070","doi-asserted-by":"crossref","first-page":"9249","DOI":"10.3390\/ijms23169249","article-title":"RNA-As-Graphs Motif Atlas\u2014Dual Graph Library of RNA Modules and Viral Frameshifting-Element Applications","volume":"23","author":"Q Zhu","year":"2022","journal-title":"Int J Mol Sci"},{"issue":"10","key":"pcbi.1011787.ref071","doi-asserted-by":"crossref","first-page":"a032433","DOI":"10.1101\/cshperspect.a032433","article-title":"The story of RNA folding, as told in epochs","volume":"10","author":"D Herschlag","year":"2018","journal-title":"Cold Spring Harbor Perspect Biol"},{"issue":"D1","key":"pcbi.1011787.ref072","doi-asserted-by":"crossref","first-page":"D593","DOI":"10.1093\/nar\/gkr859","article-title":"ViPR: an open bioinformatics database and analysis resource for virology research","volume":"40","author":"BE Pickett","year":"2012","journal-title":"Nucleic Acids Res"},{"issue":"23","key":"pcbi.1011787.ref073","doi-asserted-by":"crossref","first-page":"3150","DOI":"10.1093\/bioinformatics\/bts565","article-title":"CD-HIT: accelerated for clustering the next-generation sequencing data","volume":"28","author":"L Fu","year":"2012","journal-title":"Bioinformatics"},{"issue":"22","key":"pcbi.1011787.ref074","doi-asserted-by":"crossref","first-page":"2933","DOI":"10.1093\/bioinformatics\/btt509","article-title":"Infernal 1.1: 100-fold faster RNA homology searches","volume":"29","author":"EP Nawrocki","year":"2013","journal-title":"Bioinformatics"},{"issue":"D1","key":"pcbi.1011787.ref075","doi-asserted-by":"crossref","first-page":"D571","DOI":"10.1093\/nar\/gku1207","article-title":"NCBI viral genomes resource","volume":"43","author":"JR Brister","year":"2015","journal-title":"Nucleic Acids Res"},{"key":"pcbi.1011787.ref076","first-page":"2023","article-title":"CParty: Conditional partition function for density-2 RNA pseudoknots","author":"L Trinity","year":"2023","journal-title":"bioRxiv"},{"issue":"6","key":"pcbi.1011787.ref077","doi-asserted-by":"crossref","first-page":"e172","DOI":"10.1371\/journal.pbio.0030172","article-title":"A three-stemmed mRNA pseudoknot in the SARS coronavirus frameshift signal","volume":"3","author":"EP Plant","year":"2005","journal-title":"PLoS Biol"},{"issue":"2","key":"pcbi.1011787.ref078","doi-asserted-by":"crossref","DOI":"10.1016\/j.celrep.2023.112076","article-title":"CRISPR screening reveals a dependency on ribosome recycling for efficient SARS-CoV-2 programmed ribosomal frameshifting and viral replication","volume":"42","author":"F Rehfeld","year":"2023","journal-title":"Cell Rep"},{"issue":"13","key":"pcbi.1011787.ref079","doi-asserted-by":"crossref","first-page":"i85","DOI":"10.1093\/bioinformatics\/btr215","article-title":"IPknot: fast and accurate prediction of RNA secondary structures with pseudoknots using integer programming","volume":"27","author":"K Sato","year":"2011","journal-title":"Bioinformatics"},{"issue":"10","key":"pcbi.1011787.ref080","doi-asserted-by":"crossref","first-page":"1494","DOI":"10.1261\/rna.7284905","article-title":"HotKnots: heuristic prediction of RNA secondary structures including pseudoknots","volume":"11","author":"J Ren","year":"2005","journal-title":"RNA"},{"issue":"11","key":"pcbi.1011787.ref081","first-page":"1660","article-title":"Unwinding the SARS-CoV-2 Ribosomal Frameshifting Pseudoknot with LNA and G-Clamp-Modified Phosphorothioate Oligonucleotides Inhibits Viral Replication","volume":"13","author":"E Knizhnik","year":"2023","journal-title":"Biomol"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1011787","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2024,5,21]],"date-time":"2024-05-21T00:00:00Z","timestamp":1716249600000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1011787","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,5,21]],"date-time":"2024-05-21T13:49:32Z","timestamp":1716299372000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1011787"}},"subtitle":[],"editor":[{"given":"Arne","family":"Elofsson","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2024,5,7]]},"references-count":81,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2024,5,7]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1011787","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2023.12.28.573501","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,5,7]]}}}