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Pioneer Transcription Factors Target Partial DNA Motifs on Nucleosomes to Initiate Reprogramming
Open accessAbstract
SUMMARY Pioneer transcription factors (TFs) access silent chromatin and initiate cell fate changes, using diverse types of DNA binding domains (DBDs). FoxA, the paradigm pioneer TF, has a winged helix DBD that resembles linker histone and thereby binds its target sites on nucleosomes and in compacted chromatin. Herein we compare the nucleosome and chromatin targeting activities of Oct4 (POU DBD), Sox2 (HMG box DBD), Klf4 (zinc finger DBD), and c-Myc (bHLH DBD), which together reprogram somatic cells to pluripotency. Purified Oct4, Sox2, and Klf4 proteins can bind nucleosomes in vitro, and in vivo they preferentially target silent sites enriched for nucleosomes. Pioneer activity relates simply to the ability of a given DBD to target partial motifs displayed on the nucleosome surface. Such partial motif recognition can occur by coordinate binding between factors. Our findings provide insight into how pioneer factors can target naïve chromatin sites.
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“The pioneering model of reprogramming has been proposed for OSKM based on their ability to bind to chromatin not normally accessible by transcription factors60–62.”
From The NuRD complex cooperates with SALL4 to orchestrate reprogramming (2023) · cites this paper as [60]
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“We show here that JGES reprogramming differs markedly from the classic Yamanaka factors OSKM in that JGES relies on Sall4 to engage endogenous NuRD to close open chromatin in MEFs while OSKM relies on pioneering factors to open chromatin in MEFs10,60.”
From The NuRD complex cooperates with SALL4 to orchestrate reprogramming (2023) · cites this paper as [60]
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“The pluripotency factors OCT4, SOX2, and KLF4, when acting as pioneer TFs, bind nucleosomes in vitro by targeting partial and degenerate DNA motifs displayed on the nucleosome surface (64).”
From SOX9 reprograms endothelial cells by altering the chromatin landscape (2022) · cites this paper as [64]
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“which has also been observed at sites of nucleosomal binding by the pioneer and pluripotency factor SOX2 (64).”
From SOX9 reprograms endothelial cells by altering the chromatin landscape (2022) · cites this paper as [64]
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“In contrast with the OSK factors, which function synergistically as pioneer factors during reprogramming, MYC (Fig. 1d) does not exert this function 55 .”
From Mechanisms, pathways and strategies for rejuvenation through epigenetic reprogramming (2023) · cites this paper as [55]
In the citing paper
“For example, a handful pioneer TFs (such as OCT4, SOX2 and KLF4) were shown to bind only partial motifs displayed on the nucleosome surface107.”
From Transcription factors as readers and effectors of DNA methylation (2016) · cites this paper as [107]
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Citations
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Self-citationTranscriptional Amplification in Tumor Cells with Elevated c-Myc
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BackgroundMolecular Basis of Cell Reprogramming into iPSCs with Exogenous Transcription Factors
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The regulatory role of pioneer factors during cardiovascular lineage specification – A mini review
Sierra-Pagán, J. E., & Garry, D. J. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.972591 · Cited by 2
“Perhaps, the most recognized examples of pioneer factors are OCT4, SOX2 and KLF4 (OSK), which promote the reprogramming of terminally differentiated fibroblasts to induced pluripotent stem cells (iPSCs) (32, 33).”
BackgroundTranscriptional Regulation of Early B-Cell Development
Ng, A. P., Morris, R., & Nutt, S. L. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-95895-0.00014-3 · Cited by 2
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“Accordingly, Zelda opens inaccessible genomic regions to permit binding by other TFs (Schulz et al., 2015; Sun et al., 2015) and both Oct4/Pou5f1 and Sox proteins also possess pioneer activity (Soufi et al., 2012; Soufi et al., 2015).”
BackgroundA dual mechanism of enhancer activation by FOXA pioneer factors induces endodermal organ fatesPreprint
Geusz, R. J., Wang, A., Lam, D. K., Vinckier, N. K., Alysandratos, K., Roberts, D. A., Wang, J., Kefalopoulou, S., Qiu, Y., Chiou, J., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.28.263020 · Cited by 2
“In vitro assays have shown that FOXA1/2 can engage target sites on nucleosomal DNA, which is referred to as pioneering activity (Cirillo et al., 2002; Iwafuchi-Doi et al., 2016; Soufi et al., 2015).”
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“The pluripotency factors OCT4, SOX2 and KLF4,when acting as pioneer TFs, bind nucleosomes in vitro by targeting partial DNA motifs displayed on the nucleosome surface (Soufi et al. 2015).”
BackgroundSeATAC: a tool for exploring the chromatin landscape and the role of pioneer factorsPreprint
Dsouza, N., Gong, W., & Garry, D. J. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.04.25.489439 · Cited by 2
ASCL1 interacts with the mSWI/SNF at distal regulatory elements to regulate neural differentiationPreprint
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“…recognize binding sites in regulatory elements embedded in closed chromatin, i.e. in DNA wrapped around nucleosomes, and to open chromatin, thus facilitating the binding of other transcription factors and the transcription of the associated genes (Iwafuchi-Doi and Zaret, 2014; Soufi et al., 2015).”
BackgroundInfluentialPhysiological reprogramming in vivo mediated by Sox4 pioneer factor activityPreprint
Katsuda, T., Sussman, J., Ito, K., Katznelson, A., Yuan, S., Li, J., Merrell, A. J., Takenaka, N., Cure, H., Li, Q., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.14.528556 · Cited by 2
Self-citationHistone modifications regulate pioneer transcription factor binding and cooperativityPreprint
Sinha, K. K., Bilokapić, S., Du, Y., Malik, D., & Halić, M. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.14.532583 · Cited by 2
The pioneer transcription factor ELF2 remodels the nucleosome near transcription start sitesPreprint
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Cells Transit Through a Quiescent-Like State to Convert to Neurons at High RatesPreprint
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Multiple lineage-specific epigenetic landscapes at the antigen receptor loci
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“…and Yamanaka (2006) has been applied to basic stem cell research and clinical treatment (Huangfu et al. 2008), including developmental biology (Soufi et al. 2015), disease treat-ment (Ang et al. 2011), drug development (Marchetto et al. 2010; Ryan et al. 2013), gene therapy (Yamanaka 2020),…”
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“Reprogramming factors can convert transcriptionally silent chromatin into an active state by recruiting chromatin remodelers and transcriptional complexes [81, 82].”
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“22,66 Thus, the vast majority of mapped motifs, including those with lower PWM scores, showed independent experimental evidence for being functional.”
How to Be a Pioneer: A One-Sided View
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“This is especially interesting in light of a recent proposal that pioneer function might be helped by the ability of these proteins to recognize half-sites in the genome (Soufi et al., 2015).”
BackgroundPioneers conquer core histones at the chromatin frontier
Murawska, M., Ladurner, A. G., & Margulies, C. E. (2023) · Nature Structural & Molecular Biology · doi:10.1038/s41594-023-01058-9 · Cited by 1
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“So-called “ pioneer transcription factors ” that bind to DNA within heterochromatic regions have been demonstrated in numerous contexts with chromatin immunoprecipitation (ChIP) among other methods (Zaret & Carroll, 2011; Sou fi et al, 2015).”
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“The bICP0 E promoter is synergistically transactivated by two pioneer transcription factors GR and KLF4, which can specifically bind silent chromatin [36,40,41].”
Akerman, İ., Maestro, M. A., De Franco, E., Grau, V., Flanagan, S. E., García-Hurtado, J., Mittler, G., Ravassard, P., Piemonti, L., Ellard, S., et al. (2021) · Yearbook of pediatric endocrinology · doi:10.1530/ey.18.2.12 · Cited by 1
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“It has been suggested that recognition of partial motifs on one face of nucleosomal DNA is the discerning feature of a pioneer factor.(44) Further studies are needed to delineate the Satb1-nucleosme binding interface at high resolution and to temporally resolve the changes in chromatin architecture upon binding of Sat…”
BackgroundOzden, B., Boopathi, R., Barlas, A. B., Lone, I. N., Bednář, J., Petosa, C., Kale, S., Hamiche, A., Angelov, D., Dimitrov, S. I., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.12.07.471700 · Cited by 1
“The two orders of magnitude higher concentrations (R=50 nM) of the constant component (DNA or nucleosomes) with respect to the true Kd <1 nM (62)and the unavoidable presence of several lower-affinity binding sites per ∼200 bp DNA fragment (due binding motif degeneracy) precluded the true Kd determination under our exp…”
BackgroundLerner, J., Katznelson, A., Zhang, J., & Zaret, K. S. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.12.22.521655 · Cited by 1
Self-citationDetection of new pioneer transcription factors as cell-type specific nucleosome bindersPreprint
Peng, Y., Song, W., Teif, V. B., Ovcharenko, I., Landsman, D., & Panchenko, A. R. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.10.540098 · Cited by 1
“It has been previously shown that Yamanaka pioneer factors might target partial sequence motifs on nucleosomal DNA and require other factors for their binding to nucleosomes 16 and therefore their enrichment score might not be expected to be high.”
Detection of new pioneer transcription factors as cell-type specific nucleosome bindersPreprint
Peng, Y., Song, W., Teif, V. B., Ovcharenko, I., Landsman, D., & Panchenko, A. R. (2023) · eLife · doi:10.7554/elife.88936.1 · Cited by 1
Detection of new pioneer transcription factors as cell-type specific nucleosome bindersPreprint
Peng, Y., Song, W., Teif, V. B., Ovcharenko, I., Landsman, D., & Panchenko, A. R. (2023) · eLife · doi:10.7554/elife.88936.2 · Cited by 1
Endogenous variability in transcription factor concentrations shapes their genome-wide occupancyPreprint
Mizeret, R., Tollenaere, A., Deluz, C., & Suter, D. M. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.24.678270 · Cited by 1
Oct4 clusters promote DNA accessibility by enhancing chromatin plasticityPreprint
Huertas, J., Maristany, M. J., & Collepardo‐Guevara, R. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.20.683403 · Cited by 1
“Notably, three of these factors (Oct4, Sox2, and Klf4) are pioneer tran-63 scription factors [46,47] , underscoring that the ability to engage closed chromatin is crucial for cellular reprogramming [48] .”
Essential genes are dominantly activated by single transcription factorsPreprint
Capriati, M., Nestmann, S., Akan, I. S., Tuschmann, F., Druffel‐Augustin, S., & Grand, R. S. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.04.27.721063 · Cited by 2
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Genetic Mechanisms during Terminal Cell Fate Specification in the Drosophila CNS
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Lamparter, D., Marbach, D., Rueedi, R., Bergmann, S., & Kutalik, Z. (2016)
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“By investigating OSKM binding at 48 hours of reprogramming, previous studies have begun to elucidate the patterns and regulatory roles of OSKM in early reprogramming in the human and mouse systems (Chronis et al., 2017; Soufi, Donahue, & Zaret, 2012; Soufi et al., 2015).”
BackgroundSelf-citationElucidating Blood Origin: From Reprogramming to Ontogeny
Gomes, A. M. (2018) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
Zviran, A., Mor, N., Rais, Y., Gingold, H., Peles, S., Chomsky, E., Viukov, S. V., Buenrostro, J. D., Scognamiglio, R., Weinberger, L., et al. (2018) · SSRN Electronic Journal · doi:10.2139/ssrn.3155731
Novel Approaches for Pluripotent Reprogramming
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“However, things may turn out to be more complex, as OSKM factors have been described to not only induce reprogramming into iPSCs, but also cause apoptosis in fibroblasts.(8) In addition, Klf4 has been described to behave as an antiapoptotic oncogene in some cellular contexts and as an apoptosisinducing suppressor gene…”
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Wright, G. M., & Cui, F. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/207167
“Several cis and trans determinants of the translational positioning of nucleosomes have been reviewed in literature (Struhl and Segal 2013).”
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How to Find Targets That Are Always Hidden: Nucleosome-Covered DNA and Pioneer Transcription Factors
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Metadata
- Authors
- Soufi, A., Garcia, M. F., Jaroszewicz, A., Osman, N., Pellegrini, M., & Zaret, K. S.
- Affiliations
- University of Pennsylvania (US)
- University of California, Los Angeles (US)
- Corresponding author
- Zaret, Kenneth S.
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2015-04
- Volume
- 161
- Issue
- 3
- Pages
- 555-568
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4409934
- OpenAlex
- W1971451591
- Semantic Scholar
- 0a23a104294ce4318a90a1c70248de6cc65b2f1f
- Cited by
- 780
- References
- 85
- Citations by year
- 2026: 54 · 2025: 57 · 2024: 67 · 2023: 78 · 2022: 82 · 2021: 89 · 2020: 77 · 2019: 66 · 2018: 72 · 2017: 59 · 2016: 54 · 2015: 23
- FWCI
- 30.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institutes of Health
- National Human Genome Research Institute (T32HG002536)
- National Institute of General Medical Sciences (P01GM099134)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- pioneer transcription factors, nucleosome binding, DNA-binding domain, chromatin accessibility, cellular reprogramming, pluripotency, Oct4, SOX2, KLF4, c-Myc, HMG box, bHLH, zinc finger, silent chromatin, chromatin remodeling
- MeSH terms
- Kruppel-Like Factor 4, Amino Acid Sequence, DNA, Fibroblasts, Humans, Models, Molecular, Nucleosomes, Transcription Factors, Sequence Alignment, Protein Structure, Tertiary, Octamer Transcription Factor-3, Cell Dedifferentiation, Induced Pluripotent Stem Cells, Nucleotide Motifs, Cellular Reprogramming
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