{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,12]],"date-time":"2026-04-12T20:14:40Z","timestamp":1776024880771,"version":"3.50.1"},"reference-count":48,"publisher":"Oxford University Press (OUP)","issue":"2","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2008,1,15]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Summary: Unlike tRNAs and microRNAs, both classes of snoRNAs, which direct two distinct types of chemical modifications of uracil residues, have proved to be surprisingly difficult to find in genomic sequences. Most computational approaches so far have explicitly used the fact that snoRNAs predominantly target ribosomal RNAs and spliceosomal RNAs. The target is specified by a short stretch of sequence complementarity between the snoRNA and its target. This sequence complementarity to known targets crucially contributes to sensitivity and specificity of snoRNA gene finding algorithms.<\/jats:p><jats:p>The discovery of \u2018orphan\u2019 snoRNAs, which either have no known target, or which target ordinary protein-coding mRNAs, however, begs the question whether this class of \u2018housekeeping\u2019 non-coding RNAs is much more widespread and might have a diverse set of regulatory functions. In order to approach this question, we present here a combination of RNA secondary structure prediction and machine learning that is designed to recognize the two major classes of snoRNAs, box C\/D and box H\/ACA snoRNAs, among ncRNA candidate sequences. The snoReport approach deliberately avoids any usage of target information. We find that the combination of the conserved sequence boxes and secondary structure constraints as a pre-filter with SVM classifiers based on a small set of structural descriptors are sufficient for a reliable identification of snoRNAs.<\/jats:p><jats:p>Tests of snoReport on data from several recent experimental surveys show that the approach is feasible; the application to a dataset from a large-scale comparative genomics survey for ncRNAs suggests that there are likely hundreds of previously undescribed \u2018orphan\u2019 snoRNAs still hidden in the human genome.<\/jats:p><jats:p>Availability: The snoReport software is implemented in ANSI C. The source code is available under the GNU Public License at http:\/\/www.bioinf.uni-leipzig.de\/Software\/snoReport.<\/jats:p><jats:p>Supplementary Material is available at http:\/\/www.bioinf.uni-leipzig.de\/Publications\/SUPPLEMENTS\/07-015<\/jats:p><jats:p>Contact: \u00a0jana@bioinf.uni-leipzig.de<\/jats:p><jats:p>Supplementary information: Supplementary data are available at Bioinformatics online.<\/jats:p>","DOI":"10.1093\/bioinformatics\/btm464","type":"journal-article","created":{"date-parts":[[2007,9,26]],"date-time":"2007-09-26T02:14:39Z","timestamp":1190772879000},"page":"158-164","source":"Crossref","is-referenced-by-count":105,"title":["<tt>SnoReport<\/tt>: computational identification of snoRNAs with unknown targets"],"prefix":"10.1093","volume":"24","author":[{"given":"Jana","family":"Hertel","sequence":"first","affiliation":[{"name":"1 Institute for Theoretical Chemistry, University of Vienna, W\u00e4hringerstra\u00dfe 17, A-1090 Wien, Austria, 2Bioinformatics Group, Department of Computer Science, and Interdisciplinary Center for Bioinformatics, University of Leipzig, H\u00e4rtelstra\u00dfe 16-18, D-04107 Leipzig, 3Fraunhofer Institut f\u00fcr Zelltherapie und Immunologie Deutscher Platz 5e, 04103 Leipzig, Germany and 4Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501, USA"},{"name":"1 Institute for Theoretical Chemistry, University of Vienna, W\u00e4hringerstra\u00dfe 17, A-1090 Wien, Austria, 2Bioinformatics Group, Department of Computer Science, and Interdisciplinary Center for Bioinformatics, University of Leipzig, H\u00e4rtelstra\u00dfe 16-18, D-04107 Leipzig, 3Fraunhofer Institut f\u00fcr Zelltherapie und Immunologie Deutscher Platz 5e, 04103 Leipzig, Germany and 4Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ivo L.","family":"Hofacker","sequence":"additional","affiliation":[{"name":"1 Institute for Theoretical Chemistry, University of Vienna, W\u00e4hringerstra\u00dfe 17, A-1090 Wien, Austria, 2Bioinformatics Group, Department of Computer Science, and Interdisciplinary Center for Bioinformatics, University of Leipzig, H\u00e4rtelstra\u00dfe 16-18, D-04107 Leipzig, 3Fraunhofer Institut f\u00fcr Zelltherapie und Immunologie Deutscher Platz 5e, 04103 Leipzig, Germany and 4Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Peter F.","family":"Stadler","sequence":"additional","affiliation":[{"name":"1 Institute for Theoretical Chemistry, University of Vienna, W\u00e4hringerstra\u00dfe 17, A-1090 Wien, Austria, 2Bioinformatics Group, Department of Computer Science, and Interdisciplinary Center for Bioinformatics, University of Leipzig, H\u00e4rtelstra\u00dfe 16-18, D-04107 Leipzig, 3Fraunhofer Institut f\u00fcr Zelltherapie und Immunologie Deutscher Platz 5e, 04103 Leipzig, Germany and 4Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2007,9,25]]},"reference":[{"key":"2023020209480523100_B1","doi-asserted-by":"crossref","first-page":"3293","DOI":"10.1093\/bioinformatics\/bth394","article-title":"A computational search for box C\/D snoRNA genes in the Drosophila melanogaster genome","volume":"20","author":"Accardo","year":"2004","journal-title":"Bioinformatics"},{"key":"2023020209480523100_B2","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool","volume":"215","author":"Altschul","year":"1990","journal-title":"J. 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Bioinformatics","author":"Collins","year":"2004"},{"key":"2023020209480523100_B11","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1101\/gr.4139206","article-title":"Organization of the Caenorhabditis elegans small non-coding transcriptome: genomic features, biogenesis, and expression","volume":"16","author":"Deng","year":"2006","journal-title":"Genome Res."},{"key":"2023020209480523100_B12","volume-title":"The Theory Behind Profile HMMS: Biological Sequence Analysis: Probabilistic Models of Proteins and Nucleic Acids","author":"Durbin","year":"1998"},{"key":"2023020209480523100_B13","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1093\/bioinformatics\/btg080","article-title":"A search for H\/ACA snoRNAs in yeast using MFE secondary structure prediction","volume":"19","author":"Edvardsson","year":"2002","journal-title":"Bioinformatics"},{"key":"2023020209480523100_B14","doi-asserted-by":"crossref","first-page":"D109","DOI":"10.1093\/nar\/gkh023","article-title":"The microRNA Registry","volume":"32","author":"Griffiths-Jones","year":"2004","journal-title":"Nucleic Acids Res."},{"key":"2023020209480523100_B15","doi-asserted-by":"crossref","first-page":"D121","DOI":"10.1093\/nar\/gki081","article-title":"Rfam: annotating non-coding RNAs in complete genomes","volume":"33","author":"Griffiths-Jones","year":"2005","journal-title":"Nucleic Acids Res."},{"key":"2023020209480523100_B16","doi-asserted-by":"crossref","first-page":"e197","DOI":"10.1093\/bioinformatics\/btl257","article-title":"Hairpins in a haystack: recognizing microRNA precursors in comparative genomics data","volume":"22","author":"Hertel","year":"2006","journal-title":"Bioinformatics"},{"key":"2023020209480523100_B17","doi-asserted-by":"crossref","first-page":"3429","DOI":"10.1093\/nar\/gkg599","article-title":"Vienna RNA secondary structure server","volume":"31","author":"Hofacker","year":"2003","journal-title":"Nucleic Acids Res."},{"key":"2023020209480523100_B18","doi-asserted-by":"crossref","first-page":"1059","DOI":"10.1016\/S0022-2836(02)00308-X","article-title":"Secondary structure prediction for aligned RNA sequences","volume":"319","author":"Hofacker","year":"2002","journal-title":"J. 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Biol."},{"key":"2023020209480523100_B22","doi-asserted-by":"crossref","first-page":"2943","DOI":"10.1093\/emboj\/20.11.2943","article-title":"RNomics: an experimental approach that identifies 201 candidates for novel, small, non-messenger RNAs in mouse","volume":"20","author":"H\u00fcttenhofer","year":"2001","journal-title":"EMBO J."},{"key":"2023020209480523100_B23","doi-asserted-by":"crossref","first-page":"1484","DOI":"10.1126\/science.1138341","article-title":"RNA maps reveal new RNA classes and a possible function for pervasive transcription","volume":"316","author":"Kapranov","year":"2007","journal-title":"Science"},{"key":"2023020209480523100_B24","doi-asserted-by":"crossref","first-page":"3576","DOI":"10.1093\/nar\/gkg585","article-title":"MATCHTM: a tool for searching transcription factor binding sites in DNA sequences","volume":"31","author":"Kel","year":"2003","journal-title":"Nucleic Acids Res."},{"key":"2023020209480523100_B25","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1016\/S0968-0004(98)01260-2","article-title":"Birth of the snoRNPs: the evolution of the modification-guide snoRNAs","volume":"23","author":"Lafontaine","year":"2002","journal-title":"Trends Biochem. 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Exp. Zool. Mol. Dev. Evol."},{"key":"2023020209480523100_B33","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/S1672-0229(06)60017-X","article-title":"Fragrep: an efficient search tool for fragmented patterns in genomic sequences","volume":"4","author":"Mosig","year":"2006","journal-title":"Genomics Proteomics Bioinformatics"},{"key":"2023020209480523100_B34","doi-asserted-by":"crossref","first-page":"e56","DOI":"10.1371\/journal.pcbi.0030056","article-title":"Query-dependent banding for faster RNA similarity searches","volume":"3","author":"Nawrocki","year":"2007","journal-title":"PLoS Comput. Biol."},{"key":"2023020209480523100_B35","doi-asserted-by":"crossref","first-page":"e33","DOI":"10.1371\/journal.pcbi.0020033","article-title":"Classification of conserved RNA secondary structures in the human genome","volume":"2","author":"Pedersen","year":"2006","journal-title":"PLoS Comput. Biol."},{"key":"2023020209480523100_B36","doi-asserted-by":"crossref","first-page":"4485","DOI":"10.1093\/nar\/gki756","article-title":"Identification and analysis fo ribonuclease P and MRP RNA in a broad range of eukaryotes","volume":"33","author":"Piccinelli","year":"2005","journal-title":"Nucleic Acids Res."},{"key":"2023020209480523100_B37","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1385\/JMN:28:2:103","article-title":"Brain-specific small nucleolar RNAs","volume":"28","author":"Rogelj","year":"2006","journal-title":"J. Mol. Neurosci."},{"key":"2023020209480523100_B38","doi-asserted-by":"crossref","first-page":"1193","DOI":"10.1016\/j.cell.2006.10.040","article-title":"Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in","volume":"127","author":"Ruby","year":"2006","journal-title":"C.elegans. 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Evol."},{"key":"2023020209480523100_B42","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1083\/jcb.200411129","article-title":"ADAR2-mediated editing of RNA substrates in the nucleolus is inhibited by C\/D small nucleolar RNAs","volume":"169","author":"Vitali","year":"2005","journal-title":"J. Cell Biol."},{"key":"2023020209480523100_B43","doi-asserted-by":"crossref","first-page":"1383","DOI":"10.1038\/nbt1144","article-title":"Mapping of conserved RNA secondary structures predicts thousands of functional non-coding RNAs in the human genome","volume":"23","author":"Washietl","year":"2005","journal-title":"Nat. Biotechnol."},{"key":"2023020209480523100_B44","doi-asserted-by":"crossref","first-page":"2454","DOI":"10.1073\/pnas.0409169102","article-title":"Fast and reliable prediction of noncoding RNAs","volume":"102","author":"Washietl","year":"2005","journal-title":"Proc. Natl Acad. Sci. 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C Embryo Today"},{"key":"2023020209480523100_B48","doi-asserted-by":"crossref","first-page":"2676","DOI":"10.1093\/nar\/gkl359","article-title":"Evolution of small nucleolar RNAs in nematodes","volume":"34","author":"Zemann","year":"2006","journal-title":"Nucleic Acids Res."}],"container-title":["Bioinformatics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/24\/2\/158\/49044135\/bioinformatics_24_2_158.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/24\/2\/158\/49044135\/bioinformatics_24_2_158.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,2,18]],"date-time":"2024-02-18T04:00:00Z","timestamp":1708228800000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article\/24\/2\/158\/226808"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2007,9,25]]},"references-count":48,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2008,1,15]]}},"URL":"https:\/\/doi.org\/10.1093\/bioinformatics\/btm464","relation":{},"ISSN":["1367-4811","1367-4803"],"issn-type":[{"value":"1367-4811","type":"electronic"},{"value":"1367-4803","type":"print"}],"subject":[],"published-other":{"date-parts":[[2008,1,15]]},"published":{"date-parts":[[2007,9,25]]}}}