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MEG3 long noncoding RNA regulates the TGF-β pathway genes through formation of RNA–DNA triplex structures

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  • Tanmoy Mondal

    (Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg)

  • Santhilal Subhash

    (Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg)

  • Roshan Vaid

    (Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg)

  • Stefan Enroth

    (Genetics and Pathology, Biomedical Center, SciLifeLab Uppsala, Uppsala University)

  • Sireesha Uday

    (Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg)

  • Björn Reinius

    (Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg)

  • Sanhita Mitra

    (Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg)

  • Arif Mohammed

    (Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg)

  • Alva Rani James

    (Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg)

  • Emily Hoberg

    (University of Gothenburg)

  • Aristidis Moustakas

    (Science for Life Laboratory, Uppsala University
    Ludwig Institute for Cancer Research, Science for Life Laboratory, Uppsala University)

  • Ulf Gyllensten

    (Genetics and Pathology, Biomedical Center, SciLifeLab Uppsala, Uppsala University)

  • Steven J.M. Jones

    (Genome Sciences Centre, British Columbia Cancer Agency)

  • Claes M Gustafsson

    (University of Gothenburg)

  • Andrew H Sims

    (Applied Bioinformatics of Cancer, University of Edinburgh Cancer Research UK Centre)

  • Fredrik Westerlund

    (Chalmers University of Technology)

  • Eduardo Gorab

    (Instituto de Biociências, Universidade de São Paulo)

  • Chandrasekhar Kanduri

    (Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg)

Abstract

Long noncoding RNAs (lncRNAs) regulate gene expression by association with chromatin, but how they target chromatin remains poorly understood. We have used chromatin RNA immunoprecipitation-coupled high-throughput sequencing to identify 276 lncRNAs enriched in repressive chromatin from breast cancer cells. Using one of the chromatin-interacting lncRNAs, MEG3, we explore the mechanisms by which lncRNAs target chromatin. Here we show that MEG3 and EZH2 share common target genes, including the TGF-β pathway genes. Genome-wide mapping of MEG3 binding sites reveals that MEG3 modulates the activity of TGF-β genes by binding to distal regulatory elements. MEG3 binding sites have GA-rich sequences, which guide MEG3 to the chromatin through RNA–DNA triplex formation. We have found that RNA–DNA triplex structures are widespread and are present over the MEG3 binding sites associated with the TGF-β pathway genes. Our findings suggest that RNA–DNA triplex formation could be a general characteristic of target gene recognition by the chromatin-interacting lncRNAs.

Suggested Citation

  • Tanmoy Mondal & Santhilal Subhash & Roshan Vaid & Stefan Enroth & Sireesha Uday & Björn Reinius & Sanhita Mitra & Arif Mohammed & Alva Rani James & Emily Hoberg & Aristidis Moustakas & Ulf Gyllensten , 2015. "MEG3 long noncoding RNA regulates the TGF-β pathway genes through formation of RNA–DNA triplex structures," Nature Communications, Nature, vol. 6(1), pages 1-17, November.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms8743
    DOI: 10.1038/ncomms8743
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    Cited by:

    1. Matthias S. Leisegang & Jasleen Kaur Bains & Sandra Seredinski & James A. Oo & Nina M. Krause & Chao-Chung Kuo & Stefan Günther & Nevcin Sentürk Cetin & Timothy Warwick & Can Cao & Frederike Boos & Ju, 2022. "HIF1α-AS1 is a DNA:DNA:RNA triplex-forming lncRNA interacting with the HUSH complex," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    2. Elizabeth A. Werren & Geneva R. LaForce & Anshika Srivastava & Delia R. Perillo & Shaokun Li & Katherine Johnson & Safa Baris & Brandon Berger & Samantha L. Regan & Christian D. Pfennig & Sonja Munnik, 2024. "TREX tetramer disruption alters RNA processing necessary for corticogenesis in THOC6 Intellectual Disability Syndrome," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

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