Widespread transcription at neuronal activity-regulated enhancers

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, Dietmar Kuhl, Haruhiko Bito, Paul F. Worley, Gabriel Kreiman and Michael E. Greenberg ()
Additional contact information
Tae-Kyung Kim: Harvard Medical School, 220 Longwood Avenue, Boston, Massachusetts 02115, USA
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
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
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

Nature, 2010, vol. 465, issue 7295, 182-187

Abstract: 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.

Date: 2010
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DOI: 10.1038/nature09033

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