Cited by 2,450Genomics and Chromatin DynamicsCancer-related molecular mechanisms researchRNA Research and Splicing

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Widespread transcription at neuronal activity-regulated enhancers

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Kim, Tae-Kyung, Hemberg, Martin, Gray, Jesse M., Costa, Allen M., Bear, Daniel M., Wu, Jing, Harmin, David A., Laptewicz, Mike, Barbara-Haley, Kellie, Kuersten, Scott, Markenscoff-Papadimitriou, Eirene, Kuhl, Dietmar, Bito, Haruhiko, Worley, Paul F., Kreiman, Gabriel, Greenberg, Michael E.·2010·Nature

DOI 10.1038/nature09033PMC PMC3020079

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Abstract

We used genome-wide sequencing methods to study stimulus-dependent enhancer function in mouse cortical neurons. We identified approximately 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.

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Authors: Kim, T.-K., Hemberg, M., Gray, J. M., Costa, A. M., Bear, D. M., Wu, J., Harmin, D. A., Laptewicz, M., Barbara-Haley, K., Kuersten, S., Markenscoff-Papadimitriou, E., Kuhl, D., Bito, H., Worley, P. F., Kreiman, G., & Greenberg, M. E.
Affiliations: Harvard University (US)
Boston Children's Hospital (US)
Johns Hopkins University (US)
Epicentre (FR)
Universität Hamburg (DE)
The University of Tokyo (JP)
Corresponding author: Greenberg, Michael E.
ORCID: Kim, Tae-Kyung
Hemberg, Martin
Gray, Jesse M.
Costa, Allen M.
Wu, Jing
Kuersten, Scott
Markenscoff-Papadimitriou, Eirene
Kuhl, Dietmar
Bito, Haruhiko
Worley, Paul F.
Kreiman, Gabriel
Greenberg, Michael E.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2010-04-14
Volume: 465
Issue: 7295
Pages: 182-187
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature09033
PMC: PMC3020079
OpenAlex: W2014787267
Cited by: 2,450
References: 38
Citations by year: 2026: 70 · 2025: 126 · 2024: 138 · 2023: 121 · 2022: 152 · 2021: 180 · 2020: 169 · 2019: 151 · 2018: 158 · 2017: 167 · 2016: 155 · 2015: 204 · 2014: 175 · 2013: 187 · 2012: 140
FWCI: 62.71
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
RePEc: Research Papers in Economics (submittedVersion)
Open Access System for Information Sharing (Pohang University of Science and Technology) (submittedVersion)
Funders: National Institutes of Health (1dp2od006461-01)
National Institute of Mental Health (R01MH053608, MH-053608)
National Eye Institute (R21EY019710)
National Institute of Neurological Disorders and Stroke (NS028829, R01NS028829, R37NS028829)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD018655)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
Keywords: enhancer RNA, CBP, RNA polymerase II, enhancer activation, H3K4 monomethylation, cortical neurons, electrical activity, gene expression regulation, mouse brain
MeSH terms: Animals, Cytoskeletal Proteins, Enhancer Elements, Genetic, Gene Expression Regulation, Histones, Methylation, Mice, Inbred C57BL, Nerve Tissue Proteins, Neurons, RNA Polymerase II, Transcription, Genetic, Consensus Sequence, Genes, fos, Genes, Reporter, RNA, Untranslated, CREB-Binding Protein, Mice, Basic Helix-Loop-Helix Proteins, Basic Helix-Loop-Helix Transcription Factors

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Widespread transcription at neuronal activity-regulated enhancers

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