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Widespread transcription at neuronal activity-regulated enhancers

Author

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  • Tae-Kyung Kim

    (Harvard Medical School, 220 Longwood Avenue, Boston, Massachusetts 02115, USA
    Present addresses: University of Texas Southwestern Medical Center, Department of Neuroscience, 5323 Harry Hines Blvd, Dallas, Texas 75390-9111, USA (T.-K.K.); Graduate Program in Neuroscience, University of California San Francisco, 1550 4th Street, San Francisco, California 94158, USA (E.M.-P.).)

  • Martin Hemberg

    (Children’s Hospital Boston, Center for Brain Science and Swartz Center for Theoretical Neuroscience, Harvard University, 300 Longwood Avenue, Boston, Massachusetts 02115, USA)

  • Jesse M. Gray

    (Harvard Medical School, 220 Longwood Avenue, Boston, Massachusetts 02115, USA)

  • Allen M. Costa

    (Harvard Medical School, 220 Longwood Avenue, Boston, Massachusetts 02115, USA)

  • Daniel M. Bear

    (Harvard Medical School, 220 Longwood Avenue, Boston, Massachusetts 02115, USA)

  • Jing Wu

    (Johns Hopkins University School of Medicine, 725 North Wolfe Street, Baltimore, Maryland 21205, USA)

  • David A. Harmin

    (Harvard Medical School, 220 Longwood Avenue, Boston, Massachusetts 02115, USA
    300 Longwood Avenue, Boston, Massachusetts 02115, USA)

  • Mike Laptewicz

    (Harvard Medical School, 220 Longwood Avenue, Boston, Massachusetts 02115, USA)

  • Kellie Barbara-Haley

    (Molecular Genetics Core facility, Children’s Hospital Boston, 300 Longwood Avenue, Boston, Massachusetts 02115, USA)

  • Scott Kuersten

    (Epicentre Biotechnologies, 726 Post Road, Madison, Wisconsin 53713, USA)

  • Eirene Markenscoff-Papadimitriou

    (Harvard Medical School, 220 Longwood Avenue, Boston, Massachusetts 02115, USA
    Present addresses: University of Texas Southwestern Medical Center, Department of Neuroscience, 5323 Harry Hines Blvd, Dallas, Texas 75390-9111, USA (T.-K.K.); Graduate Program in Neuroscience, University of California San Francisco, 1550 4th Street, San Francisco, California 94158, USA (E.M.-P.).)

  • Dietmar Kuhl

    (Institute for Molecular and Cellular Cognition (IMCC), Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg-Eppendorf (UKE), Falkenried 94, 20251 Hamburg, Germany)

  • Haruhiko Bito

    (Graduate School of Medicine, University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan)

  • Paul F. Worley

    (Johns Hopkins University School of Medicine, 725 North Wolfe Street, Baltimore, Maryland 21205, USA)

  • Gabriel Kreiman

    (Children’s Hospital Boston, Center for Brain Science and Swartz Center for Theoretical Neuroscience, Harvard University, 300 Longwood Avenue, Boston, Massachusetts 02115, USA)

  • Michael E. Greenberg

    (Harvard Medical School, 220 Longwood Avenue, Boston, Massachusetts 02115, USA)

Abstract

We used genome-wide sequencing methods to study stimulus-dependent enhancer function in mouse cortical neurons. We identified ∼12,000 neuronal activity-regulated enhancers that are bound by the general transcriptional co-activator CBP in an activity-dependent manner. A function of CBP at enhancers may be to recruit RNA polymerase II (RNAPII), as we also observed activity-regulated RNAPII binding to thousands of enhancers. Notably, RNAPII at enhancers transcribes bi-directionally a novel class of enhancer RNAs (eRNAs) within enhancer domains defined by the presence of histone H3 monomethylated at lysine 4. The level of eRNA expression at neuronal enhancers positively correlates with the level of messenger RNA synthesis at nearby genes, suggesting that eRNA synthesis occurs specifically at enhancers that are actively engaged in promoting mRNA synthesis. These findings reveal that a widespread mechanism of enhancer activation involves RNAPII binding and eRNA synthesis.

Suggested Citation

  • Tae-Kyung Kim & Martin Hemberg & Jesse M. Gray & Allen M. Costa & Daniel M. Bear & Jing Wu & David A. Harmin & Mike Laptewicz & Kellie Barbara-Haley & Scott Kuersten & Eirene Markenscoff-Papadimitriou, 2010. "Widespread transcription at neuronal activity-regulated enhancers," Nature, Nature, vol. 465(7295), pages 182-187, May.
    • Handle: RePEc:nat:nature:v:465:y:2010:i:7295:d:10.1038_nature09033
    DOI: 10.1038/nature09033
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    Cited by:

    1. Lauren A. Choate & Gilad Barshad & Pierce W. McMahon & Iskander Said & Edward J. Rice & Paul R. Munn & James J. Lewis & Charles G. Danko, 2021. "Multiple stages of evolutionary change in anthrax toxin receptor expression in humans," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
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    4. Kota Hamamoto & Yusuke Umemura & Shiho Makino & Takashi Fukaya, 2023. "Dynamic interplay between non-coding enhancer transcription and gene activity in development," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    5. B. Edginton-White & A. Maytum & S. G. Kellaway & D. K. Goode & P. Keane & I. Pagnuco & S. A. Assi & L. Ames & M. Clarke & P. N. Cockerill & B. Göttgens & J. B. Cazier & C. Bonifer, 2023. "A genome-wide relay of signalling-responsive enhancers drives hematopoietic specification," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    6. Vladyslava Gorbovytska & Seung-Kyoon Kim & Filiz Kuybu & Michael Götze & Dahun Um & Keunsoo Kang & Andreas Pittroff & Theresia Brennecke & Lisa-Marie Schneider & Alexander Leitner & Tae-Kyung Kim & Cl, 2022. "Enhancer RNAs stimulate Pol II pause release by harnessing multivalent interactions to NELF," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    7. Charles Limouse & Owen K. Smith & David Jukam & Kelsey A. Fryer & William J. Greenleaf & Aaron F. Straight, 2023. "Global mapping of RNA-chromatin contacts reveals a proximity-dominated connectivity model for ncRNA-gene interactions," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    8. Annkatrin Bressin & Olga Jasnovidova & Mirjam Arnold & Elisabeth Altendorfer & Filip Trajkovski & Thomas A. Kratz & Joanna E. Handzlik & Denes Hnisz & Andreas Mayer, 2023. "High-sensitive nascent transcript sequencing reveals BRD4-specific control of widespread enhancer and target gene transcription," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

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