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

Author

Listed:
  • Chung-Chau Hon

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies))

  • Jordan A. Ramilowski

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC))

  • Jayson Harshbarger

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC))

  • Nicolas Bertin

    (RIKEN Omics Science Center (OSC)
    Cancer Science Institute of Singapore, National University of Singapore, Centre for Translational Medicine
    † Present addresses: Human Longevity Singapore Pte. Ltd., Singapore (N.B.); GenPhySE, Université de Toulouse, INRA, INPT, ENVT, Castanet Tolosan, France (S.D.); Department of Computer Science, University of Toronto, Ontario, Canada (M.M.).)

  • Owen J. L. Rackham

    (University of Bristol, Life Sciences building
    Program in Cardiovascular and Metabolic Disorders, Duke-NUS Medical School)

  • Julian Gough

    (University of Bristol, Life Sciences building)

  • Elena Denisenko

    (Institute of Natural and Mathematical Sciences, Massey University Auckland)

  • Sebastian Schmeier

    (Institute of Natural and Mathematical Sciences, Massey University Auckland)

  • Thomas M. Poulsen

    (Biotechnology Research Institute for Drug Discovery (BRD), National Institute of Advanced Industrial Science and Technology (AIST))

  • Jessica Severin

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC))

  • Marina Lizio

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC))

  • Hideya Kawaji

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC)
    RIKEN Preventive Medicine and Diagnosis Innovation Program)

  • Takeya Kasukawa

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies))

  • Masayoshi Itoh

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC)
    RIKEN Preventive Medicine and Diagnosis Innovation Program)

  • A. Maxwell Burroughs

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC)
    National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health)

  • Shohei Noma

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC))

  • Sarah Djebali

    (Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology
    Universitat Pompeu Fabra (UPF), Barcelona Biomedical Research Park (PRBB)
    † Present addresses: Human Longevity Singapore Pte. Ltd., Singapore (N.B.); GenPhySE, Université de Toulouse, INRA, INPT, ENVT, Castanet Tolosan, France (S.D.); Department of Computer Science, University of Toronto, Ontario, Canada (M.M.).)

  • Tanvir Alam

    (Computational Bioscience Research Center; Computer, King Abdullah University of Science and Technology (KAUST)
    Computer, King Abdullah University of Science and Technology (KAUST))

  • Yulia A. Medvedeva

    (Institute of Bioengineering, Research Center of Biotechnology RAS
    Vavilov Institute of General Genetic, RAS)

  • Alison C. Testa

    (Harry Perkins Institute of Medical Research, QEII Medical Centre and Centre for Medical Research, the University of Western Australia)

  • Leonard Lipovich

    (Center for Molecular Medicine and Genetics, Wayne State University
    School of Medicine, Wayne State University)

  • Chi-Wai Yip

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies))

  • Imad Abugessaisa

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies))

  • Mickaël Mendez

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC)
    † Present addresses: Human Longevity Singapore Pte. Ltd., Singapore (N.B.); GenPhySE, Université de Toulouse, INRA, INPT, ENVT, Castanet Tolosan, France (S.D.); Department of Computer Science, University of Toronto, Ontario, Canada (M.M.).)

  • Akira Hasegawa

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC))

  • Dave Tang

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC)
    Telethon Kids Institute, The University of Western Australia)

  • Timo Lassmann

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC)
    Telethon Kids Institute, The University of Western Australia)

  • Peter Heutink

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    German Center for Neurodegenerative Diseases (DZNE))

  • Magda Babina

    (Charité Universitätsmedizin Berlin)

  • Christine A. Wells

    (Australian Institute for Bioengineering and Nanotechnology, The University of Queensland
    Faculty of Medicine, The University of Melbourne)

  • Soichi Kojima

    (RIKEN CLST (Division of Bio-Function Dynamics Imaging))

  • Yukio Nakamura

    (RIKEN BioResource Center
    Faculty of Medicine, University of Tsukuba)

  • Harukazu Suzuki

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC))

  • Carsten O. Daub

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC)
    Karolinska Institutet)

  • Michiel J. L. de Hoon

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC))

  • Erik Arner

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC))

  • Yoshihide Hayashizaki

    (RIKEN Omics Science Center (OSC)
    RIKEN Preventive Medicine and Diagnosis Innovation Program)

  • Piero Carninci

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC))

  • Alistair R. R. Forrest

    (RIKEN Center for Life Science Technologies (Division of Genomic Technologies)
    RIKEN Omics Science Center (OSC)
    Harry Perkins Institute of Medical Research, QEII Medical Centre and Centre for Medical Research, the University of Western Australia)

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.

Suggested Citation

  • Chung-Chau Hon & Jordan A. Ramilowski & Jayson Harshbarger & Nicolas Bertin & Owen J. L. Rackham & Julian Gough & Elena Denisenko & Sebastian Schmeier & Thomas M. Poulsen & Jessica Severin & Marina Li, 2017. "An atlas of human long non-coding RNAs with accurate 5′ ends," Nature, Nature, vol. 543(7644), pages 199-204, March.
  • Handle: RePEc:nat:nature:v:543:y:2017:i:7644:d:10.1038_nature21374
    DOI: 10.1038/nature21374
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    Citations

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    Cited by:

    1. Zhao Wang & Qian Liang & Xinyi Qian & Bolang Hu & Zhanye Zheng & Jianhua Wang & Yuelin Hu & Zhengkai Bao & Ke Zhao & Yao Zhou & Xiangling Feng & Xianfu Yi & Jin Li & Jiandang Shi & Zhe Liu & Jihui Hao, 2023. "An autoimmune pleiotropic SNP modulates IRF5 alternative promoter usage through ZBTB3-mediated chromatin looping," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    2. Wojciech Barczak & Simon M. Carr & Geng Liu & Shonagh Munro & Annalisa Nicastri & Lian Ni Lee & Claire Hutchings & Nicola Ternette & Paul Klenerman & Alexander Kanapin & Anastasia Samsonova & Nicholas, 2023. "Long non-coding RNA-derived peptides are immunogenic and drive a potent anti-tumour response," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Chirag Nepal & Jesper B. Andersen, 2023. "Alternative promoters in CpG depleted regions are prevalently associated with epigenetic misregulation of liver cancer transcriptomes," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Alastair G. Kerr & Zuoneng Wang & Na Wang & Kelvin H. M. Kwok & Jutta Jalkanen & Alison Ludzki & Simon Lecoutre & Dominique Langin & Martin O. Bergo & Ingrid Dahlman & Carsten Mim & Peter Arner & Hui , 2022. "The long noncoding RNA ADIPINT regulates human adipocyte metabolism via pyruvate carboxylase," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Sandra Rogala & Tamer Ali & Maria-Theodora Melissari & Sandra Währisch & Peggy Schuster & Alexandre Sarre & Rebeca Cordellini Emídio & Thomas Boettger & Eva-Maria Rogg & Jaskiran Kaur & Jaya Krishnan , 2023. "The lncRNA Sweetheart regulates compensatory cardiac hypertrophy after myocardial injury in murine males," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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