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Cited by 992Genomics and Chromatin DynamicsChromatin Remodeling and CancerEpigenetics and DNA Methylation

YY1 Is a Structural Regulator of Enhancer-Promoter Loops

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Weintraub, Abraham S., Li, Charles H., Zamudio, Alicia V., Sigova, Alla A., Hannett, Nancy M., Day, Daniel S., Abraham, Brian J., Cohen, Malkiel A. +8 more·2017·Cell
DOI 10.1016/j.cell.2017.11.008PMC PMC5785279
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Abstract

There is considerable evidence that chromosome structure plays important roles in gene control, but we have limited understanding of the proteins that contribute to structural interactions between gene promoters and their enhancer elements. Large DNA loops that encompass genes and their regulatory elements depend on CTCF-CTCF interactions, but most enhancer-promoter interactions do not employ this structural protein. Here, we show that the ubiquitously expressed transcription factor Yin Yang 1 (YY1) contributes to enhancer-promoter structural interactions in a manner analogous to DNA interactions mediated by CTCF. YY1 binds to active enhancers and promoter-proximal elements and forms dimers that facilitate the interaction of these DNA elements. Deletion of YY1 binding sites or depletion of YY1 protein disrupts enhancer-promoter looping and gene expression. We propose that YY1-mediated enhancer-promoter interactions are a general feature of mammalian gene control.

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  • Using techniques with antibodies to enhancer- and promoter-associated histone modifications or RNA polymerase has revealed large numbers of 3D enhancer-promoter contacts.

    “Using these techniques with antibodies to enhancer- and promoter-associated histone modifications or those to RNA polymerase has also revealed large numbers of 3D enhancer–promoter contacts [244, 295–301].”

    From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [295]

    The Results section (“Enhancer-Promoter Interactions Depend on YY1 in Living Cells”; page unavailable) reports that H3K27ac HiChIP detected enhancer–promoter interactions; H3K27ac is a modification present at both enhancers and promoters. The paper therefore supports the histone-modification part of the claim, but the passages found do not show contacts detected using antibodies to RNA polymerase. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Long-term depletion of YY1 or ZNF143 in mammalian cells causes a significant reduction of enhancer-promoter loops, coupled with substantial changes in gene expression.

    “Unlike CTCF and cohesin, long-term depletion of YY1 or ZNF143 in mammalian cells causes a significant reduction of enhancer–promoter loops, coupled with substantial changes in gene expression [295, 368, 369]”

    From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [295]

    The Results section reports that YY1 depletion in mouse embryonic stem cells significantly reduced interactions between YY1-occupied enhancers and promoters, while 60% of genes connected by those loops showed significant expression changes. The Methods specify 24 hours of YY1 depletion. Our copy does not establish the claimed effect for ZNF143 or characterize this experiment as long-term depletion. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • YY1 and ZNF143 are zinc finger TFs with DNA binding domains that have been implicated as looping factors mediating interactions between active regulatory elements.

    “YY1 and ZNF143 are both zinc finger TFs with DNA binding domains that have recently been implicated as looping factors mediating interactions between active regulatory elements [295, 362–365].”

    From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [295]

    The Introduction and Discussion (page numbers unavailable) identify YY1 as a DNA-binding zinc-finger factor that facilitates enhancer–promoter loops. Our copy does not establish the corresponding claim about ZNF143; a search for ZNF143 returned no relevant passage. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • Many enhancers are spatially proximate to their target promoter in 3D, but exceptions have been described.

    “Many enhancers are spatially proximate to their target promoter in 3D109,110, but exceptions have been described111-114.”

    From Towards a comprehensive catalogue of validated and target-linked human enhancers (2020) · cites this paper as [110]

  • YY1 has a global role in connecting cell type-specific active enhancers and promoters in a range of mammalian cell types including mESCs and neural progenitor cells.

    “Recent studies have confirmed its global role in connecting cell type-specific active enhancers and promoters in a range of mammalian cell types including mESCs [295] and neural progenitor cells [365].”

    From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [295]

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Authors
Weintraub, A. S., Li, C. H., Zamudio, A. V., Sigova, A. A., Hannett, N. M., Day, D. S., Abraham, B. J., Cohen, M. A., Nabet, B., Buckley, D. L., Guo, Y. E., Hnisz, D., Jaenisch, R., Bradner, J. E., Gray, N. S., & Young, R. A.
Affiliations
  • Whitehead Institute for Biomedical Research (US)
  • Harvard University (US)
  • Dana-Farber Cancer Institute (US)
Corresponding author
Young, Richard A.
ORCID
Venue
Cell
Publisher
Elsevier BV
Published
2017-12
Volume
171
Issue
7
Pages
1573-1588.e28
ISSN
0092-8674 (ISSN-L)
DOI
10.1016/j.cell.2017.11.008
PMC
PMC5785279
OpenAlex
W2774733631
Cited by
992
References
24
Citations by year
2026: 73 · 2025: 118 · 2024: 113 · 2023: 118 · 2022: 116 · 2021: 124 · 2020: 124 · 2019: 124 · 2018: 79 · 2017: 2 · 2014: 1
FWCI
36.77
Type
journal article
Language
en
Open access
Licence
Locations
  • Cell (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • NIH (HG002668/GM123511, R37HD045022/R01-NS088538/R01-MH104610)
  • Ludwig Graduate Fellowship
  • NSF GRFP
  • American Cancer Society New England Division Postdoctoral Fellowship (PF-16-146-01-DMC)
  • Margaret and Herman Sokol Postdoctoral Award
  • ACS Postdoctoral Fellowship (PF-17-010-01-CDD)
  • Merck Fellow of the Damon Runyon Cancer Research Foundation (DRG-2196-14)
  • Hope Funds for Cancer Research Grillo-Marxuach Family Fellowship
  • Emerald Foundation
  • Cancer Research Institute Irvington Fellowship
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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Keywords
YY1, enhancer-promoter looping, chromatin looping, CTCF, enhancer-promoter interactions, gene expression regulation, chromatin structure
MeSH terms
CCCTC-Binding Factor, Animals, Enhancer Elements, Genetic, Humans, Promoter Regions, Genetic, YY1 Transcription Factor, Mice, Embryonic Stem Cells

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