An atlas of human long non-coding RNAs with accurate 5′ ends

Handle URI:
http://hdl.handle.net/10754/623789
Title:
An atlas of human long non-coding RNAs with accurate 5′ ends
Authors:
Hon, Chung-Chau; Ramilowski, Jordan A.; Harshbarger, Jayson; Bertin, Nicolas; Rackham, Owen J. L.; Gough, Julian; Denisenko, Elena; Schmeier, Sebastian; Poulsen, Thomas M.; Severin, Jessica; Lizio, Marina; Kawaji, Hideya; Kasukawa, Takeya; Itoh, Masayoshi; Burroughs, A. Maxwell; Noma, Shohei; Djebali, Sarah; Alam, Tanvir ( 0000-0003-4844-0171 ) ; Medvedeva, Yulia A.; Testa, Alison C.; Lipovich, Leonard; Yip, Chi-Wai; Abugessaisa, Imad; Mendez, Mickaël; Hasegawa, Akira; Tang, Dave; Lassmann, Timo; Heutink, Peter; Babina, Magda; Wells, Christine A.; Kojima, Soichi; Nakamura, Yukio; Suzuki, Harukazu; Daub, Carsten O.; Hoon, Michiel J. L. de; Arner, Erik; Hayashizaki, Yoshihide; Carninci, Piero; Forrest, Alistair R. R.
Abstract:
Long non-coding RNAs (lncRNAs) are largely heterogeneous and functionally uncharacterized. Here, using FANTOM5 cap analysis of gene expression (CAGE) data, we integrate multiple transcript collections to generate a comprehensive atlas of 27,919 human lncRNA genes with high-confidence 5′ ends and expression profiles across 1,829 samples from the major human primary cell types and tissues. Genomic and epigenomic classification of these lncRNAs reveals that most intergenic lncRNAs originate from enhancers rather than from promoters. Incorporating genetic and expression data, we show that lncRNAs overlapping trait-associated single nucleotide polymorphisms are specifically expressed in cell types relevant to the traits, implicating these lncRNAs in multiple diseases. We further demonstrate that lncRNAs overlapping expression quantitative trait loci (eQTL)-associated single nucleotide polymorphisms of messenger RNAs are co-expressed with the corresponding messenger RNAs, suggesting their potential roles in transcriptional regulation. Combining these findings with conservation data, we identify 19,175 potentially functional lncRNAs in the human genome.
KAUST Department:
Computational Bioscience Research Center (CBRC); Computer, Electrical and Mathematical Sciences and Engineering (CEMSE) Division
Citation:
Hon C-C, Ramilowski JA, Harshbarger J, Bertin N, Rackham OJL, et al. (2017) An atlas of human long non-coding RNAs with accurate 5′ ends. Nature 543: 199–204. Available: http://dx.doi.org/10.1038/nature21374.
Publisher:
Springer Nature
Journal:
Nature
Issue Date:
28-Feb-2017
DOI:
10.1038/nature21374
Type:
Article
ISSN:
0028-0836; 1476-4687
Sponsors:
FANTOM5 was made possible by research grants for the RIKEN Omics Science Center and the Innovative Cell Biology by Innovative Technology (Cell Innovation Program) from the MEXT to Y.H. It was also supported by research grants for the RIKEN Preventive Medicine and Diagnosis Innovation Program (RIKEN PMI) to Y.H. and the RIKEN Centre for Life Science Technologies, Division of Genomic Technologies (RIKEN CLST (DGT)) from the MEXT, Japan. A.R.R.F. is supported by a Senior Cancer Research Fellowship from the Cancer Research Trust, the MACA Ride to Conquer Cancer and the Australian Research Council’s Discovery Projects funding scheme (DP160101960). S.D. is supported by award number U54HG007004 from the National Human Genome Research Institute of the National Institutes of Health, funding from the Ministry of Economy and Competitiveness (MINECO) under grant number BIO2011-26205, and SEV-2012-0208 from the Spanish Ministry of Economy and Competitiveness. Y.A.M. is supported by the Russian Science Foundation, grant 15-14-30002. We thank RIKEN GeNAS for generation of the CAGE and RNA-seq libraries, the Netherlands Brain Bank for brain materials, the RIKEN BioResource Centre for providing cell lines and all members of the FANTOM5 consortium for discussions, in particular H. Ashoor, M. Frith, R. Guigo, A. Tanzer, E. Wood, H. Jia, K. Bailie, J. Harrow, E. Valen, R. Andersson, K. Vitting-Seerup, A. Sandelin, M. Taylor, J. Shin, R. Mori, C. Mungall and T. Meehan.
Additional Links:
http://www.nature.com/nature/journal/v543/n7644/full/nature21374.html
Appears in Collections:
Articles; Computational Bioscience Research Center (CBRC); Computer, Electrical and Mathematical Sciences and Engineering (CEMSE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorHon, Chung-Chauen
dc.contributor.authorRamilowski, Jordan A.en
dc.contributor.authorHarshbarger, Jaysonen
dc.contributor.authorBertin, Nicolasen
dc.contributor.authorRackham, Owen J. L.en
dc.contributor.authorGough, Julianen
dc.contributor.authorDenisenko, Elenaen
dc.contributor.authorSchmeier, Sebastianen
dc.contributor.authorPoulsen, Thomas M.en
dc.contributor.authorSeverin, Jessicaen
dc.contributor.authorLizio, Marinaen
dc.contributor.authorKawaji, Hideyaen
dc.contributor.authorKasukawa, Takeyaen
dc.contributor.authorItoh, Masayoshien
dc.contributor.authorBurroughs, A. Maxwellen
dc.contributor.authorNoma, Shoheien
dc.contributor.authorDjebali, Sarahen
dc.contributor.authorAlam, Tanviren
dc.contributor.authorMedvedeva, Yulia A.en
dc.contributor.authorTesta, Alison C.en
dc.contributor.authorLipovich, Leonarden
dc.contributor.authorYip, Chi-Waien
dc.contributor.authorAbugessaisa, Imaden
dc.contributor.authorMendez, Mickaëlen
dc.contributor.authorHasegawa, Akiraen
dc.contributor.authorTang, Daveen
dc.contributor.authorLassmann, Timoen
dc.contributor.authorHeutink, Peteren
dc.contributor.authorBabina, Magdaen
dc.contributor.authorWells, Christine A.en
dc.contributor.authorKojima, Soichien
dc.contributor.authorNakamura, Yukioen
dc.contributor.authorSuzuki, Harukazuen
dc.contributor.authorDaub, Carsten O.en
dc.contributor.authorHoon, Michiel J. L. deen
dc.contributor.authorArner, Eriken
dc.contributor.authorHayashizaki, Yoshihideen
dc.contributor.authorCarninci, Pieroen
dc.contributor.authorForrest, Alistair R. R.en
dc.date.accessioned2017-05-31T11:23:05Z-
dc.date.available2017-05-31T11:23:05Z-
dc.date.issued2017-02-28en
dc.identifier.citationHon C-C, Ramilowski JA, Harshbarger J, Bertin N, Rackham OJL, et al. (2017) An atlas of human long non-coding RNAs with accurate 5′ ends. Nature 543: 199–204. Available: http://dx.doi.org/10.1038/nature21374.en
dc.identifier.issn0028-0836en
dc.identifier.issn1476-4687en
dc.identifier.doi10.1038/nature21374en
dc.identifier.urihttp://hdl.handle.net/10754/623789-
dc.description.abstractLong non-coding RNAs (lncRNAs) are largely heterogeneous and functionally uncharacterized. Here, using FANTOM5 cap analysis of gene expression (CAGE) data, we integrate multiple transcript collections to generate a comprehensive atlas of 27,919 human lncRNA genes with high-confidence 5′ ends and expression profiles across 1,829 samples from the major human primary cell types and tissues. Genomic and epigenomic classification of these lncRNAs reveals that most intergenic lncRNAs originate from enhancers rather than from promoters. Incorporating genetic and expression data, we show that lncRNAs overlapping trait-associated single nucleotide polymorphisms are specifically expressed in cell types relevant to the traits, implicating these lncRNAs in multiple diseases. We further demonstrate that lncRNAs overlapping expression quantitative trait loci (eQTL)-associated single nucleotide polymorphisms of messenger RNAs are co-expressed with the corresponding messenger RNAs, suggesting their potential roles in transcriptional regulation. Combining these findings with conservation data, we identify 19,175 potentially functional lncRNAs in the human genome.en
dc.description.sponsorshipFANTOM5 was made possible by research grants for the RIKEN Omics Science Center and the Innovative Cell Biology by Innovative Technology (Cell Innovation Program) from the MEXT to Y.H. It was also supported by research grants for the RIKEN Preventive Medicine and Diagnosis Innovation Program (RIKEN PMI) to Y.H. and the RIKEN Centre for Life Science Technologies, Division of Genomic Technologies (RIKEN CLST (DGT)) from the MEXT, Japan. A.R.R.F. is supported by a Senior Cancer Research Fellowship from the Cancer Research Trust, the MACA Ride to Conquer Cancer and the Australian Research Council’s Discovery Projects funding scheme (DP160101960). S.D. is supported by award number U54HG007004 from the National Human Genome Research Institute of the National Institutes of Health, funding from the Ministry of Economy and Competitiveness (MINECO) under grant number BIO2011-26205, and SEV-2012-0208 from the Spanish Ministry of Economy and Competitiveness. Y.A.M. is supported by the Russian Science Foundation, grant 15-14-30002. We thank RIKEN GeNAS for generation of the CAGE and RNA-seq libraries, the Netherlands Brain Bank for brain materials, the RIKEN BioResource Centre for providing cell lines and all members of the FANTOM5 consortium for discussions, in particular H. Ashoor, M. Frith, R. Guigo, A. Tanzer, E. Wood, H. Jia, K. Bailie, J. Harrow, E. Valen, R. Andersson, K. Vitting-Seerup, A. Sandelin, M. Taylor, J. Shin, R. Mori, C. Mungall and T. Meehan.en
dc.publisherSpringer Natureen
dc.relation.urlhttp://www.nature.com/nature/journal/v543/n7644/full/nature21374.htmlen
dc.titleAn atlas of human long non-coding RNAs with accurate 5′ endsen
dc.typeArticleen
dc.contributor.departmentComputational Bioscience Research Center (CBRC)en
dc.contributor.departmentComputer, Electrical and Mathematical Sciences and Engineering (CEMSE) Divisionen
dc.identifier.journalNatureen
dc.contributor.institutionRIKEN Center for Life Science Technologies, Division of Genomic Technologies, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, 230-0045, , Japanen
dc.contributor.institutionRIKEN Omics Science Center (OSC), 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, 230-0045, , Japanen
dc.contributor.institutionCancer Science Institute of Singapore, National University of Singapore, Centre for Translational Medicine, 14 Medical Drive, #12-01, Singapore, 117599, , Singaporeen
dc.contributor.institutionHuman Longevity Singapore Pte. Ltd., Singapore, , Singaporeen
dc.contributor.institutionUniversity of Bristol, Department of Computer Science, 24 Tyndall Avenue, Bristol, BS8 1TQ, , United Kingdomen
dc.contributor.institutionProgram in Cardiovascular and Metabolic Disorders, Duke-NUS Medical School, 8 College Road, Singapore, 169857, , Singaporeen
dc.contributor.institutionInstitute of Natural and Mathematical Sciences, Massey University Auckland, Albany, 0632, , New Zealanden
dc.contributor.institutionBiotechnology Research Institute for Drug Discovery (BRD), National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba Central 2, 1-1-1 Umezono, Tsukuba, Ibaraki, 305-8568, , Japanen
dc.contributor.institutionRIKEN Preventive Medicine and Diagnosis Innovation Program, 2-1 Hirosawa, Wako, Saitama, 351-0198, , Japanen
dc.contributor.institutionNational Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, , United Statesen
dc.contributor.institutionCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, Barcelona, 08003, , Spainen
dc.contributor.institutionUniversitat Pompeu Fabra (UPF), Barcelona Biomedical Research Park (PRBB), Dr Aiguader 88, Barcelona, 08003, , Spainen
dc.contributor.institutionGenPhySE, Université de Toulouse, INRA, Castanet Tolosan, , Franceen
dc.contributor.institutionInstitute of Bioengineering, Research Center of Biotechnology RAS, Moscow, 119071, , Russian Federationen
dc.contributor.institutionVavilov Institute of General Genetic, RAS, Moscow, 119991, , Russian Federationen
dc.contributor.institutionHarry Perkins Institute of Medical Research, QEII Medical Centre and Centre for Medical Research, University of Western Australia, Nedlands, Western Australia, 6009, , Australiaen
dc.contributor.institutionCenter for Molecular Medicine and Genetics, Wayne State University, Detroit, MI, 48201, , United Statesen
dc.contributor.institutionDepartment of Neurology, School of Medicine, Wayne State University, Detroit, MI, 48201, , United Statesen
dc.contributor.institutionDepartment of Computer Science, University of Toronto, Toronto, ON, , Canadaen
dc.contributor.institutionTelethon Kids Institute, University of Western Australia, 100 Roberts Road, Subiaco, Subiaco, Western Australia, 6008, , Australiaen
dc.contributor.institutionGerman Center for Neurodegenerative Diseases (DZNE), Tübingen, D-72076, , Germanyen
dc.contributor.institutionDepartment of Dermatology and Allergy, Charité Universitätsmedizin Berlin, Berlin, 10117, , Germanyen
dc.contributor.institutionAustralian Institute for Bioengineering and Nanotechnology, University of Queensland, Brisbane, 4072, , Australiaen
dc.contributor.institutionFaculty of Medicine, Department of Anatomy and Neuroscience, University of Melbourne, 3010, , Australiaen
dc.contributor.institutionRIKEN CLST (Division of Bio-Function Dynamics Imaging), Wako, Saitama, 351-0198, , Japanen
dc.contributor.institutionCell Engineering Division, RIKEN BioResource Center, Tsukuba, Ibaraki, 305-0074, , Japanen
dc.contributor.institutionFaculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki, 305-8577, , Japanen
dc.contributor.institutionDepartment of Biosciences and Nutrition, Karolinska Institutet, Huddinge, 141 83, , Swedenen
kaust.authorAlam, Tanviren
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