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Pioneer Transcription Factors Target Partial DNA Motifs on Nucleosomes to Initiate Reprogramming
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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]
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“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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Reprogramming of Human Fibroblasts to Pluripotency with Lineage Specifiers
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“Other TFs involved in cell reprogramming can target their sites in silent chromatin (Montserrat et al., 2013; Soufi et al., 2012; Takahashi andYamanaka, 2006;Wapinski et al., 2013), but they possess DBDs that differ from that of FoxA.”
Acquisition of myogenic specificity by replacement of three amino acid residues from MyoD into E12
Davis, R., & Weintraub, H. M. (1992) · Science · doi:10.1126/science.1317057 · Cited by 147 · cited 1×
“Interestingly, the mutation of two amino acids within the basic helix-1 that interacts with central E-box makes the non-myogenic bHLH factor E12 able to convert fibroblasts to muscle cells (Davis and Weintraub, 1992).”
Murphy, E. C., Zhurkin, V. B., Louis, J. M., Cornilescu, G., & Clore, G. M. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.4977 · Cited by 146
Differential genomic targeting of the transcription factor TAL1 in alternate haematopoietic lineages
Palii, C. G., Perez‐Iratxeta, C., Yao, Z., Cao, Y., Dai, F., Davison, J., Atkins, H. L., Allan, D., Dilworth, F. J., Gentleman, R. C., et al. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.342 · Cited by 143 · cited 1×
“Various examples have been reported on the overexpression of bHLH factors in cancer, including c-Myc,Tal1, andOlig2 (Lin et al., 2012; Nie et al., 2012; Palii et al., 2011; Sanda et al., 2012; Suvà et al., 2014).”
Assa‐Munt, N. (1993) · Cell · doi:10.1016/0092-8674(93)90171-l · Cited by 138
Pogenberg, V., Ögmundsdóttir, M. H., Bergsteinsdóttir, K., Schepsky, A., Phung, B., Deineko, V., Milewski, M., Steingrímsson, E., & Wilmanns, M. (2012) · Genes & Development · doi:10.1101/gad.198192.112 · Cited by 137 · cited 1×
“crystallography for Mitf, which shares 86% sequence homology across the basic region with c-Myc (Figure S6C) (Pogenberg et al., 2012).”
Pbx homeodomain proteins direct Myod activity to promote fast-muscle differentiation
Maves, L., Waskiewicz, A. J., Paul, B., Cao, Y., Tyler, A. E., Moens, C. B., & Tapscott, S. J. (2007) · Development · doi:10.1242/dev.003905 · Cited by 133 · cited 1×
“The homeodomain factor PBX primesMyoD targets to inducemyogenic potential (Maves et al., 2007).”
Spatially Precise DNA Bending Is an Essential Activity of the Sox2 Transcription Factor
Scaffidi, P., & Bianchi, M. E. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m107619200 · Cited by 126 · cited 3×
“Furthermore, mutation of the ‘‘G’’ nucleotide in the sixth position of the motif has the unique ability, among all mutations tested, to abolish DNA bending by wild-type Sox2 (Scaffidi and Bianchi, 2001).”
InfluentialLongo, A., Guanga, G. P., & Rose, R. B. (2007) · Biochemistry · doi:10.1021/bi701527r · Cited by 104 · cited 1×
“Predicting Pioneer Activity among Different bHLH Factors in Reprogramming To gain insights on how bHLH proteins may differentially target nucleosomes in reprogramming, we examined the 3D structures of a range of bHLH-DNA complexes that have been used in reprogramming experiments (Longo et al., 2008; Ma et al., 1994; E…”
The structure of the Klf4 DNA-binding domain links to self-renewal and macrophage differentiation
Schuetz, A., Nana, D., Rose, C., Zocher, G., Milanovic, M., Koenigsmann, J., Blasig, R., Heinemann, U., & Carstanjen, D. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0618-x · Cited by 84 · cited 2×
“Klf4 recognizes the nonameric DNA motif using all three C2H2-type ZFs (three nucleotides per ZF) located at the C terminus (Schuetz et al., 2011) (Figure 4F).”
The nucleosome map of the mammalian liver
Li, Z., Schug, J., Tuteja, G., White, P., & Kaestner, K. H. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2060 · Cited by 80 · cited 1×
“This is different from what was observed for FoxA1, which recognizes the same motif on free DNA and nucleosomes (Cirillo et al., 1998; Li et al., 2011).”
Identification and analysis of murine pancreatic islet enhancers
Tennant, B., Robertson, A. G., Kramer, M. M., Li, L., Zhang, X., Beach, M., Thiessen, N., Chiu, R., Mungall, K. L., Whiting, C. J., et al. (2012) · Diabetologia · doi:10.1007/s00125-012-2797-5 · Cited by 72
Key regulators control distinct transcriptional programmes in blood progenitor and mast cells
Calero‐Nieto, F. J., Ng, F. S., Wilson, N. K., Hannah, R., Moignard, V., Leal-Cervantes, A. I., Jimenez-Madrid, I., Diamanti, E., Wernisch, L., & Göttgens, B. (2014) · The EMBO Journal · doi:10.1002/embj.201386825 · Cited by 71
Omari, K. E., Hoosdally, S., Tuladhar, K., Karia, D., Hall-Ponselé, E., Platonova, O., Vyas, P., Patient, R. K., Porcher, C., & Mancini, E. J. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.06.008 · Cited by 67
MacQuarrie, K. L., Yao, Z., Fong, A. P., Diede, S. J., Rudzinski, E. R., Hawkins, D. S., & Tapscott, S. J. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.00916-12 · Cited by 66
Differential Binding of c-Myc and Max to Nucleosomal DNA
Wechsler, D. S., Papoulas, O., Dang, C. V., & Kingston, R. E. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.6.4097-4107.1994 · Cited by 60
Sauvé, S., Tremblay, L., & Lavigne, P. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.07.058 · Cited by 58 · cited 1×
“The basic region of bHLH domain, not bound to DNA, appears to be unfolded in solution (Sauvé et al., 2004) (Figure 6A; Figure S6A).”
Privalov, P. L., Dragan, A. I., & Crane‐Robinson, C. (2009) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2009.05.005 · Cited by 49 · cited 1×
“While bending naked DNA by Sox2 requires minimal work (Privalov et al., 2009), the energy cost would impede Sox2 to further bend DNA on nucleosomes.”
Function of GATA Factors in the Adult Mouse Liver
Zheng, R., Rebolledo‐Jaramillo, B., Zong, Y., Wang, L., Russo, P., Hancock, W. W., Stanger, B. Z., Hardison, R. C., & Blobel, G. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083723 · Cited by 47 · cited 1×
“The pioneer factor GATA4 binds nucleosomes modestly in vitro (Cirillo and Zaret, 1999) and targets a hexamericmotif in vivo (Zheng et al., 2013).”
Solution structure of the Oct-1 POU homeodomain determined by NMR and restrained molecular dynamics
Cox, M., van Tilborg, P. J. A., de Laat, W. L., Boelens, R., van Leeuwen, H. C., van der Vliet, P. C., & Kaptein, R. (1995) · Journal of Biomolecular NMR · doi:10.1007/bf00417488 · Cited by 35
Farina, A. N., Faiola, F., & Martinez, E. (2004) · Protein Expression and Purification · doi:10.1016/j.pep.2003.11.021 · Cited by 29 · cited 1×
“) expressed, recombinant O, S, K, and M proteins bound to DNA probes containing canonical motifs, as previously reported for the purified DBDs (Farina et al., 2004; Nakatake et al., 2006; Rodda et al., 2005) (Figure S1B; Table 1), and bound with much lower affinity to non-specific DNA sequences of the same length (Fig…”
Mechanisms for enhancing cellular reprogramming
Soufi, A. (2014) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2013.12.007 · Cited by 14 · cited 1×
“In an attempt to increase the efficiency of reprogramming, efforts have focused on explaining how somatic cells respond to the ectopic expression of OSKM (Buganim et al., 2013; Papp and Plath, 2013; Soufi, 2014).”
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The Human Transcription Factors
Lambert, S. A., Jolma, A., Campitelli, L. F., Das, P. K., Yin, Y., Albu, M., Chen, X., Taipale, J., Hughes, T. R., & Weirauch, M. T. (2018) · Cell · doi:10.1016/j.cell.2018.01.029 · Cited by 3,399
Chromatin accessibility and the regulatory epigenome
Klemm, S. L., Shipony, Z., & Greenleaf, W. J. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-018-0089-8 · Cited by 1,793
Stine, Z. E., Walton, Z. E., Altman, B. J., Hsieh, A. L., & Dang, C. V. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-0507 · Cited by 1,435
“Indeed, recent work suggests a centrally degenerate E-box motif in closed chromatin may be accessible to MYC using a partially unfolded DNA-binding domain when assisted by other factors, adding a structural rationale to the idea that MYC’s ability to affect gene expression is a confluence of DNA consensus sequence aff…”
BackgroundTranscription factors as readers and effectors of DNA methylation
Zhu, H., Wang, G., & Qian, J. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.83 · Cited by 649
Cooperative Binding of Transcription Factors Orchestrates Reprogramming
Chronis, C., Fiziev, P., Papp, B., Butz, S., Bonora, G., Sabri, S., Ernst, J., & Plath, K. (2017) · Cell · doi:10.1016/j.cell.2016.12.016 · Cited by 555
“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript for human somatic cell reprogramming (Soufi et al., 2012; Soufi et al., 2015) does not act at enhancers in mouse cell reprogramming.”
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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