{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,23]],"date-time":"2026-06-23T00:50:47Z","timestamp":1782175847819,"version":"3.54.5"},"reference-count":69,"publisher":"Public Library of Science (PLoS)","issue":"4","license":[{"start":{"date-parts":[[2024,4,22]],"date-time":"2024-04-22T00:00:00Z","timestamp":1713744000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Cambridge Centre for Mathematics in Healthcare Hub, Centre for Mathematical Sciences, University of Cambridge"},{"DOI":"10.13039\/501100000648","name":"King\u2019s College Cambridge, University of Cambridge","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000648","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000272","name":"National Institute for Health and Care Research","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000272","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Influenza A virus contains regions of its segmented genome associated with ability to package the segments into virions, but many such regions are poorly characterised. We provide detailed predictions of the key locations within these packaging-associated regions, and their structures, by applying a recently-improved pipeline for delineating constrained regions in RNA viruses and applying structural prediction algorithms. We find and characterise other known constrained regions within influenza A genomes, including the region associated with the PA-X frameshift, regions associated with alternative splicing, and constraint around the initiation motif for a truncated PB1 protein, PB1-N92, associated with avian viruses. We further predict the presence of constrained regions that have not previously been described. The extra characterisation our work provides allows investigation of these key regions for drug target potential, and points towards determinants of packaging compatibility between segments.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1012009","type":"journal-article","created":{"date-parts":[[2024,4,22]],"date-time":"2024-04-22T17:23:38Z","timestamp":1713806618000},"page":"e1012009","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":3,"title":["Locations and structures of influenza A virus packaging-associated signals and other functional elements via an in silico pipeline for predicting constrained features in RNA viruses"],"prefix":"10.1371","volume":"20","author":[{"given":"Emma","family":"Beniston","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8228-3758","authenticated-orcid":true,"given":"Jordan 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Ozawa","year":"2009","journal-title":"Journal of Virology"},{"issue":"11","key":"pcbi.1012009.ref042","doi-asserted-by":"crossref","first-page":"e1002998","DOI":"10.1371\/journal.ppat.1002998","article-title":"Identification of a novel splice variant form of the influenza A virus M2 ion channel with an antigenically distinct ectodomain","volume":"8","author":"HM Wise","year":"2012","journal-title":"PLoS Pathogens"},{"key":"pcbi.1012009.ref043","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1261\/rna.2619511","article-title":"Identification of potential conserved RNA secondary structure throughout influenza A coding regions","volume":"17","author":"WN Moss","year":"2011","journal-title":"RNA"},{"key":"pcbi.1012009.ref044","doi-asserted-by":"crossref","first-page":"5236","DOI":"10.1021\/bi500611j","article-title":"Secondary structure of a conserved domain in an intron of influenza A M1 mRNA","volume":"53","author":"T 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