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Cited by 114Genomics and Chromatin DynamicsEpigenetics and DNA MethylationChromatin Remodeling and Cancer

Occupancy by key transcription factors is a more accurate predictor of enhancer activity than histone modifications or chromatin accessibility

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Dogan, Nergiz, Wu, Weisheng, Morrissey, Christapher S, Chen, Kuan-Bei, Stonestrom, Aaron, Long, Maria, Keller, Cheryl A, Cheng, Yong +6 more·2015·Epigenetics & Chromatin
DOI 10.1186/s13072-015-0009-5PMC PMC4432502
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Abstract

BACKGROUND: Regulated gene expression controls organismal development, and variation in regulatory patterns has been implicated in complex traits. Thus accurate prediction of enhancers is important for further understanding of these processes. Genome-wide measurement of epigenetic features, such as histone modifications and occupancy by transcription factors, is improving enhancer predictions, but the contribution of these features to prediction accuracy is not known. Given the importance of the hematopoietic transcription factor TAL1 for erythroid gene activation, we predicted candidate enhancers based on genomic occupancy by TAL1 and measured their activity. Contributions of multiple features to enhancer prediction were evaluated based on the results of these and other studies. RESULTS: TAL1-bound DNA segments were active enhancers at a high rate both in transient transfections of cultured cells (39 of 79, or 56%) and transgenic mice (43 of 66, or 65%). The level of binding signal for TAL1 or GATA1 did not help distinguish TAL1-bound DNA segments as active versus inactive enhancers, nor did the density of regulation-related histone modifications. A meta-analysis of results from this and other studies (273 tested predicted enhancers) showed that the presence of TAL1, GATA1, EP300, SMAD1, H3K4 methylation, H3K27ac, and CAGE tags at DNase hypersensitive sites gave the most accurate predictors of enhancer activity, with a success rate over 80% and a median threefold increase in activity. Chromatin accessibility assays and the histone modifications H3K4me1 and H3K27ac were sensitive for finding enhancers, but they have high false positive rates unless transcription factor occupancy is also included. CONCLUSIONS: Occupancy by key transcription factors such as TAL1, GATA1, SMAD1, and EP300, along with evidence of transcription, improves the accuracy of enhancer predictions based on epigenetic features.

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  • The observation that p300 catalytic activity does not contribute to destabilization is inconsistent with a model by which histone acetylation reduces nucleosome-DNA affinity to facilitate TF binding.

    “appears inconsistent with a model by which histone acetylation reduces nucleosome-DNA affinity to facilitate TF binding29,49,50”

    From Single-molecule states link transcription factor binding to gene expression (2024) · cites this paper as [50]

    The Background describes TF-bound enhancers as flanked by nucleosomes bearing H3K27ac, and the Results and Discussion compare TF occupancy and histone marks as predictors of enhancer activity. No passage found addresses the cited model that acetylation reduces nucleosome–DNA affinity to facilitate TF binding; searches for nucleosome affinity, acetylation-mediated binding, and p300 catalytic activity did not resolve it. (LLM, conf=0.73)

    Experimental — accuracy not yet measured

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Authors
Dogan, N., Wu, W., Morrissey, C. S., Chen, K.-B., Stonestrom, A., Long, M., Keller, C. A., Cheng, Y., Jain, D., Visel, A., Pennacchio, L. A., Weiss, M. J., Blobel, G. A., & Hardison, R. C.
Affiliations
  • Pennsylvania State University (US)
  • Children's Hospital of Philadelphia (US)
  • Stanford University (US)
  • Lawrence Berkeley National Laboratory (US)
  • St. Jude Children's Research Hospital (US)
Corresponding author
Hardison, Ross C
ORCID
Venue
Epigenetics & Chromatin
Publisher
Springer Science and Business Media LLC
Published
2015-04-23
Volume
8
Issue
1
Pages
16-16
ISSN
1756-8935 (ISSN-L)
DOI
10.1186/s13072-015-0009-5
PMC
PMC4432502
OpenAlex
W1988760117
Cited by
114
References
12
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FWCI
6.81
Type
journal article
Language
en
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  • Epigenetics & Chromatin (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion, other-oa)
  • eScholarship (California Digital Library) (submittedVersion, cc-by)
Funders
  • National Science Foundation (0821527)
  • University of Pennsylvania
  • Pennsylvania State University (OCI-0821527)
  • National Institutes of Health (R01DK58044)
  • National Heart, Lung, and Blood Institute (U01HL099656)
  • National Human Genome Research Institute (RC2HG005573, U54HG006998, R01HG003988)
  • National Institute of Diabetes and Digestive and Kidney Diseases (R37DK058044, P30DK090969, R01DK065806, R56DK065806, R01DK058044, R01DK054937)
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
enhancer prediction, transcription factor occupancy, TAL1, GATA-1, Smad1, EP300, histone modifications, H3K4me1, H3K27ac, chromatin accessibility, DNase I hypersensitive sites, hematopoietic transcription factors, enhancer activity

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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