The Pioneer Transcription Factor FoxA Maintains an Accessible Nucleosome Configuration at Enhancers for Tissue-Specific Gene Activation
Open accessAbstract
Nuclear DNA wraps around core histones to form nucleosomes, which restricts the binding of transcription factors to gene regulatory sequences. Pioneer transcription factors can bind DNA sites on nucleosomes and initiate gene regulatory events, often leading to the local opening of chromatin. However, the nucleosomal configuration of open chromatin and the basis for its regulation is unclear. We combined low and high levels of micrococcal nuclease (MNase) digestion along with core histone mapping to assess the nucleosomal configuration at enhancers and promoters in mouse liver. We find that MNase-accessible nucleosomes, bound by transcription factors, are retained more at liver-specific enhancers than at promoters and ubiquitous enhancers. The pioneer factor FoxA displaces linker histone H1, thereby keeping enhancer nucleosomes accessible in chromatin and allowing other liver-specific transcription factors to bind and stimulate transcription. Thus, nucleosomes are not exclusively repressive to gene regulation when they are retained with, and exposed by, pioneer factors.
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FOXA2 can be bound to closed or unmarked regions, suggesting additional factors may be required to activate these regions when needed.
“As FOXA2 is a known pioneer factor51, it can be bound to closed or unmarked regions, suggesting additional factors may be required to activate these regions when needed.”
From HNF4A guides the MLL4 complex to establish and maintain H3K4me1 at gene regulatory elements (2024) · cites this paper as [51]
The Results section on FoxA2 binding identifies it as a pioneer factor, and the Discussion describes pioneer factors helping other transcription factors access their sites. But the Results report that most FoxA2 sites overlap DNase-hypersensitive regions and that FoxA did not bind the silent enhancers examined. Our copy does not establish FOXA2 binding at closed or unmarked regions, or that additional factors are required to activate those regions. (LLM, conf=0.86)
Experimental — accuracy not yet measuredFOXA factors are not always required for accessibility at HBRs.
“Furthermore, although FOXA factors act as pioneer factors in hepatocytes51,52, we show that FOXA factors are not always required for accessibility at HBRs.”
From HNF4A guides the MLL4 complex to establish and maintain H3K4me1 at gene regulatory elements (2024) · cites this paper as [51]
At least some pioneer factors, such as FOXA, OCT4 and SOX2/SOX11, initiate chromatin opening by direct displacement of histones.
“The mechanisms of pioneer factor action are still being established [37], but at least some of them (such as FOXA, OCT4 and SOX2/SOX11) have been shown to initiate chromatin opening by direct displacement of histones [38–41], whilst many others recruit chromatin remodelers [42–50].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [38]
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Cites
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Pioneer Transcription Factors Target Partial DNA Motifs on Nucleosomes to Initiate Reprogramming
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“Although most TFs cannot access nucleosomal DNA on their own, a subset of TFs possess a special ability to engage their target sites on nucleosomal DNA and are thus referred to as ‘‘pioneer’’ factors (Iwafuchi-Doi and Zaret, 2014; Soufi et al., 2015).”
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“, 2013), and HNF4a (Hoffman et al., 2010) binding events (Figure 3E), and these motifs focused around the nucleosome dyad axis (Figure 3F).”
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“(11) As a pioneer factor, FOXA family members are capable of altering epigenetic modifications to regulate gene expression.(24,34) We therefore speculated that a high level of H3K4me1 and H3K27ac at HBRs could be attributed to FOXA2 occupancy at those sites.”
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- Authors
- Iwafuchi-Doi, M., Donahue, G., Kakumanu, A., Watts, J. A., Mahony, S., Pugh, B. F., Lee, D., Kaestner, K. H., & Zaret, K. S.
- Affiliations
- University of Pennsylvania (US)
- Pennsylvania State University (US)
- Corresponding author
- Zaret, Kenneth S.
- ORCID
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2016-04
- Volume
- 62
- Issue
- 1
- Pages
- 79-91
- ISSN
- 1097-2765 (ISSN-L)
- PMC
- PMC4826471
- OpenAlex
- W2331147307
- Cited by
- 390
- References
- 8
- Citations by year
- 2026: 39 · 2025: 26 · 2024: 40 · 2023: 40 · 2022: 38 · 2021: 43 · 2020: 42 · 2019: 43 · 2018: 38 · 2017: 30 · 2016: 11
- FWCI
- 17.37
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Human Genome Research Institute (HG004160, R56HG004160, R01HG004160)
- National Institute of General Medical Sciences (R01GM036477, R37GM036477)
- National Institute of Diabetes and Digestive and Kidney Diseases (P01DK049210)
- 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 › Nuclear Structure and Function
- Keywords
- FoxA, pioneer transcription factors, enhancers, chromatin accessibility, histone H1, tissue-specific gene regulation, promoter accessibility
- MeSH terms
- Animals, Enhancer Elements, Genetic, Histones, Liver, Nucleosomes, Organ Specificity, Promoter Regions, Genetic, Transcription, Genetic, Mice, Hepatocyte Nuclear Factor 3-alpha, Hepatocyte Nuclear Factor 3-beta, Hepatocyte Nuclear Factor 3-gamma
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