GATA3-dependent cellular reprogramming requires activation-domain dependent recruitment of a chromatin remodeler
Open accessAbstract
BACKGROUND: Transcription factor-dependent cellular reprogramming is integral to normal development and is central to production of induced pluripotent stem cells. This process typically requires pioneer transcription factors (TFs) to induce de novo formation of enhancers at previously closed chromatin. Mechanistic information on this process is currently sparse. RESULTS: Here we explore the mechanistic basis by which GATA3 functions as a pioneer TF in a cellular reprogramming event relevant to breast cancer, the mesenchymal to epithelial transition (MET). In some instances, GATA3 binds previously inaccessible chromatin, characterized by stable, positioned nucleosomes where it induces nucleosome eviction, alters local histone modifications, and remodels local chromatin architecture. At other loci, GATA3 binding induces nucleosome sliding without concomitant generation of accessible chromatin. Deletion of the transactivation domain retains the chromatin binding ability of GATA3 but cripples chromatin reprogramming ability, resulting in failure to induce MET. CONCLUSIONS: These data provide mechanistic insights into GATA3-mediated chromatin reprogramming during MET, and suggest unexpected complexity to TF pioneering. Successful reprogramming requires stable binding to a nucleosomal site; activation domain-dependent recruitment of co-factors including BRG1, the ATPase subunit of the SWI/SNF chromatin remodeling complex; and appropriate genomic context. The resulting model provides a new conceptual framework for de novo enhancer establishment by a pioneer TF.
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SOX9 harbours the pioneer TF ability to engage target sites in closed chromatin.
“Our results suggests that SOX9 harbours this ability but, as observed with other pioneer TFs (47,69,70), not all SOX9 binding events result in opening of chromatin.”
From SOX9 reprograms endothelial cells by altering the chromatin landscape (2022) · cites this paper as [69]
Many pioneer factors recruit chromatin remodelers.
“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 [49]
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- Authors
- Takaku, M., Grimm, S. A., Shimbo, T., Perera, L., Menafra, R., Stunnenberg, H. G., Archer, T. K., Machida, S., Kurumizaka, H., & Wade, P. A.
- Affiliations
- National Institutes of Health (US)
- National Institute of Environmental Health Sciences (US)
- Radboud University Nijmegen (NL)
- Waseda University (JP)
- Corresponding author
- Wade, Paul A.
- ORCID
- Venue
- Genome Biology
- Published
- 2016-02-27
- Volume
- 17
- Issue
- 1
- Pages
- 36-36
- ISSN
- 1465-6906 (ISSN-L)
- 1474-760X
- PMC
- PMC4769547
- OpenAlex
- W2281053309
- Cited by
- 151
- References
- 69
- Citations by year
- 2026: 6 · 2025: 11 · 2024: 18 · 2023: 22 · 2022: 14 · 2021: 16 · 2020: 16 · 2019: 18 · 2018: 20 · 2017: 6 · 2016: 4
- FWCI
- 8.32
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Genome biology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion, other-oa)
- Funders
- National Institute of Environmental Health Sciences (ES101965, ES071006, ES043010)
- Ministry of Education, Culture, Sports, Science, and Technology (25116002)
- Japan Society for the Promotion of Science
- 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
- GATA3, pioneer transcription factors, cellular reprogramming, mesenchymal-epithelial transition, chromatin remodeling, SWI/SNF complex, SMARCA4, nucleosome eviction, nucleosome sliding, histone modifications, transactivation domain, breast cancer, chromatin accessibility
- MeSH terms
- Breast Neoplasms, Chromatin, Chromosomal Proteins, Non-Histone, Female, Humans, Nucleosomes, Transcription Factors, Chromatin Assembly and Disassembly, GATA3 Transcription Factor, Induced Pluripotent Stem Cells, Epithelial-Mesenchymal Transition, Cellular Reprogramming
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