Cited by 551Genomics and Chromatin DynamicsEpigenetics and DNA MethylationChromatin Remodeling and Cancer

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H3K4me3 Breadth Is Linked to Cell Identity and Transcriptional Consistency

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Benayoun, Bérénice A., Pollina, Elizabeth A., Ucar, Duygu, Mahmoudi, Salah, Karra, Kalpana, Wong, Edith D., Devarajan, Keerthana, Daugherty, Aaron C., Kundaje, Anshul B., Mancini, Elena, Hitz, Benjamin C., Gupta, Rakhi, Rando, Thomas A., Baker, Julie C., Snyder, Michael P., Cherry, J. Michael, Brunet, Anne·2014·Cell

DOI 10.1016/j.cell.2014.06.027PMC PMC4137894

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Abstract

Trimethylation of histone H3 at lysine 4 (H3K4me3) is a chromatin modification known to mark the transcription start sites of active genes. Here, we show that H3K4me3 domains that spread more broadly over genes in a given cell type preferentially mark genes that are essential for the identity and function of that cell type. Using the broadest H3K4me3 domains as a discovery tool in neural progenitor cells, we identify novel regulators of these cells. Machine learning models reveal that the broadest H3K4me3 domains represent a distinct entity, characterized by increased marks of elongation. The broadest H3K4me3 domains also have more paused polymerase at their promoters, suggesting a unique transcriptional output. Indeed, genes marked by the broadest H3K4me3 domains exhibit enhanced transcriptional consistency and [corrected] increased transcriptional levels, and perturbation of H3K4me3 breadth leads to changes in transcriptional consistency. Thus, H3K4me3 breadth contains information that could ensure transcriptional precision at key cell identity/function genes.

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Additional file 4 of Swd2/Cps35 determines H3K4 tri-methylation via interactions with Set1 and Rad6
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Additional file 1 of Synergising single-cell resolution and 4sU labelling boosts inference of transcriptional bursting
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Additional file 6 of Chromatin profiling and state predictions reveal insights into epigenetic regulation during early porcine development
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Additional file 1 of Chromatin profiling and state predictions reveal insights into epigenetic regulation during early porcine development
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Additional file 10 of Epigenetic regulation of H3K27me3 in laying hens with fatty liver hemorrhagic syndrome induced by high-energy and low-protein diets
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Additional file 1 of Inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo
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Additional file 1 of Altered H3K4me3 profile at the TFAM promoter causes mitochondrial alterations in preadipocytes from first-degree relatives of type 2 diabetics
Longo, M., Zatterale, F., Spinelli, R., Naderi, J., Parrillo, L., Florese, P., Nigro, C., Leone, A., Moccia, A., Desiderio, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26615680
Additional file 3 of Epigenetic regulation of H3K27me3 in laying hens with fatty liver hemorrhagic syndrome induced by high-energy and low-protein diets
Cui, Y., Ru, M., Wang, Y., Weng, L., Haji, R. A., Liang, H., Zeng, Q., Wei, Q., Xie, X., Yin, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26707808
Additional file 2 of Epigenetic regulation of H3K27me3 in laying hens with fatty liver hemorrhagic syndrome induced by high-energy and low-protein diets
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Additional file 4 of Chromatin profiling and state predictions reveal insights into epigenetic regulation during early porcine development
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Additional file 3 of Chromatin profiling and state predictions reveal insights into epigenetic regulation during early porcine development
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Additional file 3 of Swd2/Cps35 determines H3K4 tri-methylation via interactions with Set1 and Rad6
Oh, J., Park, S., Kim, J., Yeom, S., Lee, E., Lee, E., Cho, Y.-J., & Lee, J. (2024) · Figshare · doi:10.6084/m9.figshare.26715958
Additional file 5 of Chromatin profiling and state predictions reveal insights into epigenetic regulation during early porcine development
Innis, S. M., & Cabot, R. A. (2024) · Figshare · doi:10.6084/m9.figshare.26723325
Additional file 2 of Inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo
Liu, J., Frochaux, M., Gardeux, V., Deplancke, B., & Robinson‐Rechavi, M. (2020) · Figshare · doi:10.6084/m9.figshare.12980262
Additional file 2 of Swd2/Cps35 determines H3K4 tri-methylation via interactions with Set1 and Rad6
Oh, J., Park, S., Kim, J., Yeom, S., Lee, E., Lee, E., Cho, Y.-J., & Lee, J. (2024) · Figshare · doi:10.6084/m9.figshare.25750152
Additional file 8 of Epigenetic regulation of H3K27me3 in laying hens with fatty liver hemorrhagic syndrome induced by high-energy and low-protein diets
Cui, Y., Ru, M., Wang, Y., Weng, L., Haji, R. A., Liang, H., Zeng, Q., Wei, Q., Xie, X., Yin, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26707823
Additional file 3 of Altered H3K4me3 profile at the TFAM promoter causes mitochondrial alterations in preadipocytes from first-degree relatives of type 2 diabetics
Longo, M., Zatterale, F., Spinelli, R., Naderi, J., Parrillo, L., Florese, P., Nigro, C., Leone, A., Moccia, A., Desiderio, A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26615686
Additional file 3 of Synergising single-cell resolution and 4sU labelling boosts inference of transcriptional bursting
Edwards, D. M., Davies, P., & Hebenstreit, D. (2023) · Figshare · doi:10.6084/m9.figshare.23536053
Additional file 5 of Epigenetic regulation of H3K27me3 in laying hens with fatty liver hemorrhagic syndrome induced by high-energy and low-protein diets
Cui, Y., Ru, M., Wang, Y., Weng, L., Haji, R. A., Liang, H., Zeng, Q., Wei, Q., Xie, X., Yin, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26707814
Additional file 5 of Swd2/Cps35 determines H3K4 tri-methylation via interactions with Set1 and Rad6
Oh, J., Park, S., Kim, J., Yeom, S., Lee, E., Lee, E., Cho, Y.-J., & Lee, J. (2024) · Figshare · doi:10.6084/m9.figshare.26715964
Additional file 2 of Chromatin profiling and state predictions reveal insights into epigenetic regulation during early porcine development
Innis, S. M., & Cabot, R. A. (2024) · Figshare · doi:10.6084/m9.figshare.26723316
Additional file 1 of Swd2/Cps35 determines H3K4 tri-methylation via interactions with Set1 and Rad6
Oh, J., Park, S., Kim, J., Yeom, S., Lee, E., Lee, E., Cho, Y.-J., & Lee, J. (2024) · Figshare · doi:10.6084/m9.figshare.25749933
Additional file 7 of Epigenetic regulation of H3K27me3 in laying hens with fatty liver hemorrhagic syndrome induced by high-energy and low-protein diets
Cui, Y., Ru, M., Wang, Y., Weng, L., Haji, R. A., Liang, H., Zeng, Q., Wei, Q., Xie, X., Yin, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26707820
Additional file 6 of Epigenetic regulation of H3K27me3 in laying hens with fatty liver hemorrhagic syndrome induced by high-energy and low-protein diets
Cui, Y., Ru, M., Wang, Y., Weng, L., Haji, R. A., Liang, H., Zeng, Q., Wei, Q., Xie, X., Yin, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26707817
Additional file 9 of Epigenetic regulation of H3K27me3 in laying hens with fatty liver hemorrhagic syndrome induced by high-energy and low-protein diets
Cui, Y., Ru, M., Wang, Y., Weng, L., Haji, R. A., Liang, H., Zeng, Q., Wei, Q., Xie, X., Yin, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26707826
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Authors: Benayoun, B. A., Pollina, E. A., Ucar, D., Mahmoudi, S., Karra, K., Wong, E. D., Devarajan, K., Daugherty, A. C., Kundaje, A. B., Mancini, E., Hitz, B. C., Gupta, R., Rando, T. A., Baker, J. C., Snyder, M. P., Cherry, J. M., & Brunet, A.
Affiliations: Stanford University (US)
Stanford Medicine (US)
VA Palo Alto Health Care System (US)
Corresponding author: Brunet, Anne
ORCID: Benayoun, Bérénice A.
Pollina, Elizabeth A.
Ucar, Duygu
Karra, Kalpana
Wong, Edith D.
Devarajan, Keerthana
Kundaje, Anshul B.
Hitz, Benjamin C.
Rando, Thomas A.
Baker, Julie C.
Snyder, Michael P.
Cherry, J. Michael
Brunet, Anne
Venue: Cell
Publisher: Elsevier BV
Published: 2014-07
Volume: 158
Issue: 3
Pages: 673-688
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2014.06.027
PMC: PMC4137894
OpenAlex: W1984173288
Cited by: 536
References: 105
Citations by year: 2026: 28 · 2025: 53 · 2024: 52 · 2023: 50 · 2022: 41 · 2021: 57 · 2020: 40 · 2019: 44 · 2018: 32 · 2017: 51 · 2016: 47 · 2015: 38 · 2014: 3
FWCI: 4.36
Type: journal article
Language: en
Update notices: erratum (2015-11-19)
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 395 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
Funders: National Institute on Aging (F31AG043232, DP1AG044848, P01AG036695)
National Cancer Institute (T32CA009302)
National Institute of General Medical Sciences (P01GM099130, R01GM103787, T32GM007790)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Keywords: H3K4me3, histone trimethylation, chromatin modification, transcription start sites, cell identity, neural progenitor cells, gene expression regulation, RNA polymerase II elongation, cell type-specific genes, machine learning
MeSH terms: Animals, Artificial Intelligence, Cells, Histones, Humans, Lysine, Methylation, Mice, Inbred C57BL, RNA Polymerase II, Transcription, Genetic, Genomics, Histone Code, Neural Stem Cells

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H3K4me3 Breadth Is Linked to Cell Identity and Transcriptional Consistency

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