The first enhancer in an enhancer chain safeguards subsequent enhancer-promoter contacts from a distance
Open accessAbstract
Background: Robustness and evolutionary stability of gene expression in the human genome are established by an array of redundant enhancers. Results: Using Hi-C data in multiple cell lines, we report a comprehensive map of promoters and active enhancers connected by chromatin contacts, spanning 9000 enhancer chains in 4 human cell lines associated with 2600 human genes. We find that the first enhancer in a chain that directly contacts the target promoter is commonly located at a greater genomic distance from the promoter than the second enhancer in a chain, 96 kb vs. 45 kb, respectively. The first enhancer also features higher similarity to the promoter in terms of tissue specificity and higher enrichment of loop factors, suggestive of a stable primary contact with the promoter. In contrast, a chain of enhancers which connects to the target promoter through a neutral DNA segment instead of an enhancer is associated with a significant decrease in target gene expression, suggesting an important role of the first enhancer in initiating transcription using the target promoter and bridging the promoter with other regulatory elements in the locus. Conclusions: The widespread chained structure of gene enhancers in humans reveals that the primary, critical enhancer is distal, commonly located further away than other enhancers. This first, distal enhancer establishes contacts with multiple regulatory elements and safeguards a complex regulatory program of its target gene.
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Evidence from Hi-C data analysis suggests that the first enhancer in the chain is often more distal than the second enhancer, attracts more tissue-specific factors and is more enriched for eQTLs than other enhancers within the chain.
“Evidence from Hi-C data analysis has suggested that the “first” enhancer in the chain, i.e. the enhancer with direct looping to the gene promoter, is often more distal than the “second” enhancer, attracts more tissue-specific factors and is more enriched for eQTLs than other enhancers within the chain [490].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [490]
The Abstract (Results) reports that the first enhancer directly contacts the promoter and is commonly farther from it than the second; the Results section on baseline gene regulation reports higher tissue-specific eQTL density in first enhancers. The factor claim is less well supported: the Results report enrichment of loop factors in first enhancers, but do not establish that they attract more tissue-specific factors than other chain enhancers. A separate Results comparison says overall bound-transcription-factor enrichment is similar across chain enhancers. (LLM, conf=0.87)
Experimental — accuracy not yet measuredAnalysis of enhancer chains suggests that the promoter-connected enhancer is often more distal than downstream enhancers in the same chain, yet binds more tissue-appropriate TFs, suggesting that enhancer chains might involve pioneer enhancers.
“Analysis of enhancer chains suggests that the promoter-connected enhancer is often more distal than downstream enhancers in the same chain, yet binds more tissue-appropriate TFs, suggesting that enhancer chains might involve pioneer enhancers [490].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [490]
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Additional file 1 of Mechanisms of enhancer action: the known and the unknown
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Cao, H., Wu, Z., Ji, B., Yang, S., Gonzalez-Smith, L., Vu, A. H., & Rhie, S. K. (2026) · Genome biology · doi:10.1186/s13059-026-04178-9
- Authors
- Song, W., Sharan, R., & Ovcharenko, I.
- Affiliations
- National Institutes of Health (US)
- Tel Aviv University (IL)
- Corresponding author
- Ovcharenko, Ivan
- Venue
- Genome Biology
- Published
- 2019-09-12
- Volume
- 20
- Issue
- 1
- Pages
- 197-197
- ISSN
- 1465-6906 (ISSN-L)
- 1474-760X
- PMC
- PMC6739990
- OpenAlex
- W2972483091
- Cited by
- 28
- References
- 47
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 5 · 2023: 6 · 2022: 8 · 2021: 3 · 2020: 3
- FWCI
- 1.16
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Genome biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- U.S. National Library of Medicine (Intramural Research Program)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- enhancer-promoter interactions, chromatin looping, 3D genome organization, distal enhancers, gene expression regulation, tissue specificity, human cell lines
- MeSH terms
- Cell Line, Chromatin, Enhancer Elements, Genetic, Gene Expression Regulation, Humans, Promoter Regions, Genetic
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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