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 factors.
“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]
The Introduction (p. 3) says Oct4, Sox2 and Klf4 can function as pioneers because they target closed, DNase I-resistant chromatin. It explicitly excludes c-Myc from that finding; the paper later describes c-Myc targeting nucleosomal sites with assistance from other factors (p. 9). Thus the claim is supported for three OSKM factors, but overstates their shared ability. (LLM, conf=0.88)
Experimental — accuracy not yet measuredJGES reprogramming differs markedly from 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 MEFs.
“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]
The Introduction (p. 3) identifies Oct4, Sox2, and Klf4—but not c-Myc—as pioneer factors that target closed chromatin, and the Discussion (p. 11) reports their ability to target nucleosomal sites during reprogramming. The paper studies human fibroblasts and initial access to closed chromatin; these passages do not establish that OSKM opens chromatin in mouse embryonic fibroblasts (MEFs). The JGES–Sall4–NuRD comparison is presented as the citing authors’ own finding, not as a finding attributed to this source. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe 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.
“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]
A half-site lacking the 'G' nucleotide from the canonical Ca/tTTGT motif has been observed at sites of nucleosomal binding by SOX2.
“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]
A few pioneer transcription factors, including OCT4, SOX2 and KLF4, were shown to recognize only partial motifs exposed on nucleosomes.
“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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Budry, L., Balsalobre, A., Gauthier, Y., Khetchoumian, K., L’honoré, A., Vallette-Kasic, S., Brue, T. C., Figarella-Branger, D. F., Meij, B. P., & Drouin, J. (2012) · Genes & Development · doi:10.1101/gad.200436.112 · Cited by 157 · cited 2× · see citing works
“1 have emerged as pioneer transcription factors based on targeting closed chromatin and their ability to reprogram cells, though assessments of direct interaction with nucleosomes has been lacking (Barozzi et al., 2014; Budry et al., 2012;Wapinski et al., 2013).”
A unique Oct4 interface is crucial for reprogramming to pluripotency
Esch, D., Vahokoski, J., Groves, M. R., Pogenberg, V., Cojocaru, V., Bruch, H. V., Han, D., Drexler, H. C. A., Araúzo-Bravo, M. J., Ng, C. K. L., et al. (2013) · Nature Cell Biology · doi:10.1038/ncb2680 · Cited by 156 · cited 1× · see citing works
“The X-ray structure of Oct4-POU-DNA complex confirms that the POUS and POUHD each bind one-half of the octameric motif on DNA (Esch et al., 2013) (Figure 4G, lower panels).”
Reprogramming of Human Fibroblasts to Pluripotency with Lineage Specifiers
Montserrat, N., Nivet, E., Sancho-Martinez, I., Hishida, T., Kumar, S., Miquel‐Serra, L., Cortina, C., Hishida, Y., Xia, Y. F., Esteban, C. R., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.06.019 · Cited by 150 · cited 1× · see citing works
“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× · see citing works
“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 · see citing works
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 140 · cited 1× · see citing works
“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 · see citing works
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× · see citing works
“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× · see citing works
“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× · see citing works
“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× · see citing works
“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 100 · cited 2× · see citing works
“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 78 · cited 1× · see citing works
“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).”
Key regulators control distinct transcriptional programmes in blood progenitor and mast cells
Calero-Nieto, F., Ng, F. S. L., Wilson, N. K., Hannah, R., Moignard, V., Leal-Cervantes, A. I., Jimenez-Madrid, I., Diamanti, E., Wernisch, L., & Göttgens, B. (2014) · EMBO Journal · doi:10.1002/embj.201386825 · Cited by 77 · see citing works
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 71 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Sauvé, S., Tremblay, L., & Lavigne, P. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.07.058 · Cited by 58 · cited 1× · see citing works
“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× · see citing works
“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 46 · cited 1× · see citing works
“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 · see citing works
Farina, A. N., Faiola, F., & Martinez, E. (2004) · Protein Expression and Purification · doi:10.1016/j.pep.2003.11.021 · Cited by 27 · cited 1× · see citing works
“) 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× · see citing works
“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 · see citing works
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 · see citing works
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 1,375 · see citing works
“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 · see citing works
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 · see citing works
“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.”
Base-resolution models of transcription-factor binding reveal soft motif syntax
Avsec, Ž., Weilert, M., Shrikumar, A., Krueger, S., Alexandari, A., Dalal, K., Fropf, R., McAnany, C., Gagneur, J., Kundaje, A., et al. (2021) · Nature Genetics · doi:10.1038/s41588-021-00782-6 · Cited by 610 · see citing works
Mechanisms regulating zygotic genome activation
Schulz, K. N., & Harrison, M. M. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0087-x · Cited by 543 · see citing works
MYC: Connecting selective transcriptional control to global RNA production
Kress, T. R., Sabò, A., & Amati, B. (2015) · Nature reviews. Cancer · doi:10.1038/nrc3984 · Cited by 521 · see citing works
H3K9me3-Dependent Heterochromatin: Barrier to Cell Fate Changes
Becker, J. S., Nicetto, D., & Zaret, K. S. (2015) · Trends in Genetics · doi:10.1016/j.tig.2015.11.001 · Cited by 480 · see citing works
“All four factors target open chromatin sites, but only OSK, while not M, also target sites containing nucleosomes and lacking evident histone marks, making them pioneer factors [32,46,47].”
BackgroundSelf-citationThe Genetics of Transcription Factor DNA Binding Variation
Deplancke, B., Alpern, D., & Gardeux, V. (2016) · Cell · doi:10.1016/j.cell.2016.07.012 · Cited by 390 · see citing works
“More generally, epigenomic properties such as nucleosome location (Soufi et al., 2015) or density (Barozzi et al.”
Induced pluripotent stem cells (iPSCs): molecular mechanisms of induction and applications
Cerneckis, J., Cai, H., & Shi, Y. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01809-0 · Cited by 452 · see citing works
“54,55 Through concerted action, OSKM expel somatic cell-speci fi c transcription factors from somatic enhancers and activate pluripotency enhancers; silencing of somatic cell-speci fi c enhancers is initiated early in reprogramming, whereas activation of pluripotency-speci fi c enhancers occurs later…”
BackgroundDirect cell reprogramming: approaches, mechanisms and progress
Wang, H., Yang, Y., Liu, J., & Li, Q. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00335-z · Cited by 438 · see citing works
Pioneer Transcription Factors Initiating Gene Network Changes
Zaret, K. S. (2020) · Annual Review of Genetics · doi:10.1146/annurev-genet-030220-015007 · Cited by 398 · see citing works
Self-citationIwafuchi-Doi, M., Donahue, G., Kakumanu, A., Watts, J. A., Mahony, S., Pugh, B. F., Lee, D., Kaestner, K. H., & Zaret, K. S. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.03.001 · Cited by 390 · see citing works
“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).”
BackgroundInfluentialSelf-citationThe interaction landscape between transcription factors and the nucleosome
Zhu, F., Farnung, L., Kaasinen, E., Sahu, B., Yin, Y., Wei, B., Dodonova, S., Nitta, K. R., Morgunova, E. Y., Taipale, M., et al. (2018) · Nature · doi:10.1038/s41586-018-0549-5 · Cited by 348 · see citing works
Combinatorial function of transcription factors and cofactors
Reiter, F., Wienerroither, S., & Stark, A. (2017) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.12.007 · Cited by 354 · see citing works
Pioneer transcription factors, chromatin dynamics, and cell fate control
Zaret, K. S., & Mango, S. E. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2015.12.003 · Cited by 337 · see citing works
“Oct4 and Klf4 were found to target a reduced sequence motif on nucleosomal sites, consistent with the idea that the pioneer factors tolerate reduced proteinDNA interactions during the initial nucleosome targeting (Soufi et al., 2015).”
BackgroundSelf-citationCell fate control by pioneer transcription factors
Iwafuchi-Doi, M., & Zaret, K. S. (2016) · Development · doi:10.1242/dev.133900 · Cited by 304 · see citing works
“By contrast, c-Myc alone prefers to bind to active chromatin, but can also bind low signal chromatin sites when cooperating with the other factors (Soufi et al., 2012, 2015).”
BackgroundInfluentialSelf-citationEvaluating cell reprogramming, differentiation and conversion technologies in neuroscience
Mertens, J., Marchetto, M. C., Bardy, C., & Gage, F. H. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.46 · Cited by 301 · see citing works
Deciphering the multi-scale, quantitative cis-regulatory code
Kim, S., & Wysocka, J. (2023) · Molecular Cell · doi:10.1016/j.molcel.2022.12.032 · Cited by 282 · see citing works
Nucleosome-bound SOX2 and SOX11 structures elucidate pioneer factor function
Dodonova, S. O., Zhu, F., Dienemann, C., Taipale, J., & Cramer, P. (2020) · Nature · doi:10.1038/s41586-020-2195-y · Cited by 265 · see citing works
King, H. W., & Klose, R. J. (2017) · eLife · doi:10.7554/elife.22631 · Cited by 270 · see citing works
“DOI: 10.7554/eLife.22631 15 of 24 nucleosomal DNA (Figure 1; Soufi et al., 2012, 2015), suggesting that OCT4 may be able to dynamically sample its target sites throughout the genome.”
BackgroundInfluentialPioneer factors as master regulators of the epigenome and cell fate
Balsalobre, A., & Drouin, J. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00464-z · Cited by 251 · see citing works
AP-1 imprints a reversible transcriptional programme of senescent cells.
Martínez-Zamudio, R. I., Roux, P.-F., de Freitas, J. A. N. L. F., Robinson, L., Doré, G., Sun, B., Belenki, D., Milanovic, M., Herbig, U., Schmitt, C. A., et al. (2020) · Nature Cell Biology · doi:10.1038/s41556-020-0529-5 · Cited by 236 · see citing works
MNase titration reveals differences between nucleosome occupancy and chromatin accessibility
Mieczkowski, J., Cook, A., Bowman, S., Mueller, B., Alver, B. H., Kundu, S., Deaton, A. M., Urban, J. A., Larschan, E., Park, P. J., et al. (2016) · Nature Communications · doi:10.1038/ncomms11485 · Cited by 235 · see citing works
Chromatin Accessibility Dynamics during iPSC Reprogramming
Li, D., Liu, J., Yang, X., Zhou, C., Guo, J., Wu, C., Qin, Y., Guo, L., He, J., Yu, S., et al. (2017) · Cell Stem Cell · doi:10.1016/j.stem.2017.10.012 · Cited by 251 · see citing works
“It became apparent that, while all three of OSK can open loci and are thus acting as pioneer TFs to open chromatin (Soufi et al., 2015), S and K could open nearly twice as many loci as O alone, and only 257 O peaks were exclusively opened by O, as many of the O-specific peaks could also be opened by S or K alone (Figu…”
BackgroundInfluentialPioneer transcription factors shape the epigenetic landscape
Mayran, A., & Drouin, J. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.r117.001232 · Cited by 238 · see citing works
“For the OSK factors, their ability to target partial consensus motifs may allow their DNAbinding domains to interact directly with nucleosomes (53).”
BackgroundMechanisms of OCT4-SOX2 motif readout on nucleosomes
Michael, A. K., Grand, R. S., Isbel, L., Cavadini, S., Kozicka, Z., Kempf, G., Bunker, R. D., Schenk, A. D., Graff-Meyer, A., Pathare, G. R., et al. (2020) · Science · doi:10.1126/science.abb0074 · Cited by 237 · see citing works
Transcription Factors Drive Tet2-Mediated Enhancer Demethylation to Reprogram Cell Fate
Sardina, J. L., Collombet, S., Tian, T. V., Gómez, A., Stefano, B. D., Berenguer, C., Brumbaugh, J., Stadhouders, R., Segura-Morales, C., Gut, M., et al. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.08.016 · Cited by 230 · see citing works
“In conclusion, our data show that among the pluripotency factors Klf4, Oct4, and Sox2, described to have pioneer activity (Soufi et al., 2015), Klf4 is unique in its ability to bind transposase inaccessible chromatin that becomes demethylated and decorated with the enhancer mark H3K4me2.”
BackgroundLineage-Determining Transcription Factor TCF-1 Initiates the Epigenetic Identity of T Cells
Johnson, J. L., Georgakilas, G., Petrovic, J., Kurachi, M., Cai, S., Harly, C., Pear, W. S., Bhandoola, A., Wherry, E. J., & Vahedi, G. (2018) · Immunity · doi:10.1016/j.immuni.2018.01.012 · Cited by 226 · see citing works
“The extent to which TCF-1 bound to nucleosome-occupied regions in fibroblasts was comparable to reprogramming transcription factors such as OCT4 (85%), SOX2 (80%), and KLF4 (65%) (Soufi et al., 2015).”
BackgroundInfluentialPlant transcription factors — being in the right place with the right company
Strader, L. C., Weijers, D., & Wagner, D. (2021) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2021.102136 · Cited by 222 · see citing works
Insights into Nucleosome Organization in Mouse Embryonic Stem Cells through Chemical Mapping
Voong, L. N., Xi, L., Sebeson, A. C., Xiong, B., Wang, J., & Wang, X. (2016) · Cell · doi:10.1016/j.cell.2016.10.049 · Cited by 203 · see citing works
“Nucleosome Occupancy at Pluripotency Transcription Factor-Binding Sites in ES Cells Emerging evidence suggests that pluripotency transcription factors Oct4, Sox2, and Klf4 can function as pioneer factors to bind to their target sites on nucleosomes in vitro (Soufi et al., 2015).”
InfluentialLink, V. M., Duttke, S. H., Chun, H. B., Holtman, I. R., Westin, E., Hoeksema, M. A., Abe, Y., Skola, D., Romanoski, C. E., Tao, J., et al. (2018) · Cell · doi:10.1016/j.cell.2018.04.018 · Cited by 182 · see citing works
Catarino, R. R., & Stark, A. (2018) · Genes & Development · doi:10.1101/gad.310367.117 · Cited by 205 · see citing works
Structural Features of Transcription Factors Associating with Nucleosome Binding
García, M. F., Moore, C. D., Schulz, K. N., Alberto, O., Donague, G., Harrison, M. M., Zhu, H., & Zaret, K. S. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.06.009 · Cited by 196 · see citing works
Self-citationFunctional Hallmarks of Healthy Macrophage Responses: Their Regulatory Basis and Disease Relevance
Sheu, K. M., & Hoffmann, A. (2022) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101320-031555 · Cited by 209 · see citing works
Reprogramming roadmap reveals route to human induced trophoblast stem cells
Liu, X., Ouyang, J. F., Rossello, F. J., Tan, J. P., Davidson, K. C., Valdes, D. S., Schröder, J., Sun, Y., Chen, J., Knaupp, A. S., et al. (2020) · Nature · doi:10.1038/s41586-020-2734-6 · Cited by 198 · see citing works
Schulz, K. N., Bondra, E. R., Moshe, A., Villalta, J. E., Lieb, J. D., Kaplan, T., McKay, D. J., & Harrison, M. M. (2015) · Genome Research · doi:10.1101/gr.192682.115 · Cited by 177 · see citing works
“Furthermore, Pou5f3 and Sox2 are known to be pioneer factors instrumental in reprogramming differentiated cells to a pluripotent state (Soufi et al. 2012, 2015).”
BackgroundSoufi, A., & Dalton, S. (2016) · Development · doi:10.1242/dev.142075 · Cited by 183 · see citing works
“It has been shown that OCT4, SOX2 and KLF4 (together termed OSK) can access closed chromatin by acting as pioneer factors during iPSC reprogramming (Soufi et al., 2012, 2015).”
BackgroundSelf-citationPioneer factor pax7 deploys a stable enhancer repertoire for specification of cell fate
Mayran, A., Khetchoumian, K., Hariri, F., Pastinen, T., Gauthier, Y., Balsalobre, A., & Drouin, J. (2018) · Nature Genetics · doi:10.1038/s41588-017-0035-2 · Cited by 171 · see citing works
Master regulatory role of p63 in epidermal development and disease
Soares, E., & Zhou, H. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2701-z · Cited by 183 · see citing works
Giammartino, D. C. D., Kloetgen, A., Polyzos, A., Liu, Y., Kim, D., Murphy, D., Abuhashem, A., Cavaliere, P., Aronson, B. E., Shah, V., et al. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0390-6 · Cited by 174 · see citing works
Farr, S. E., Woods, E. J., Joseph, J. A., Garaizar, A., & Collepardo‐Guevara, R. (2021) · Nature Communications · doi:10.1038/s41467-021-23090-3 · Cited by 176 · see citing works
Molecular Co-occupancy Identifies Transcription Factor Binding Cooperativity In Vivo
Sönmezer, C., Kleinendorst, R., Imanci, D., Barzaghi, G., Villacorta, L., Schübeler, D., Benes, V., Molina, N., & Krebs, A. R. (2021) · Molecular Cell · doi:10.1016/j.molcel.2020.11.015 · Cited by 162 · see citing works
Mitotic binding of Esrrb marks key regulatory regions of the pluripotency network
Festuccia, N., Dubois, A., Vandormael-Pournin, S., Gallego Tejeda, E., Mouren, A., Bessonnard, S., Mueller, F., Proux, C., Cohen-Tannoudji, M., & Navarro, P. (2016) · Nature Cell Biology · doi:10.1038/ncb3418 · Cited by 158 · see citing works
NF-κB dynamics determine the stimulus specificity of epigenomic reprogramming in macrophages
Cheng, Q. J., Ohta, S., Sheu, K. M., Spreafico, R., Adelaja, A., Taylor, B. E., & Hoffmann, A. (2021) · Science · doi:10.1126/science.abc0269 · Cited by 164 · see citing works
“The role of temporal dynamics may thus complement the structure-function model in which distance from the nucleosome core determines accessibility to partially exposed DNA motifs (38).”
BackgroundGenetic determinants and epigenetic effects of pioneer-factor occupancy
Donaghey, J., Thakurela, S., Charlton, J., Chen, J., Smith, Z. D., Gu, H., Pop, R., Clement, K., Stamenova, E. K., Karnik, R., et al. (2018) · Nature Genetics · doi:10.1038/s41588-017-0034-3 · Cited by 169 · see citing works
“…targeting and remodeling capabilities of pioneer TFs, they also display a degree of cell type specificity 8–10 with recent work suggesting that cell-type specific co-factors 11–13 , signaling 14 , and the underlying chromatin landscape 5,6 can influence the genomic occupancy of pioneer TFs.”
Single-cell and single-molecule epigenomics to uncover genome regulation at unprecedented resolution
Shema, E., Bernstein, B., & Buenrostro, J. D. (2018) · Nature Genetics · doi:10.1038/s41588-018-0290-x · Cited by 164 · see citing works
A latent lineage potential in resident neural stem cells enables spinal cord repair
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“OLIG2 was predicted to have a DNA binding domain with possible pioneer activity based on its structure (32).”
BackgroundMechanisms that regulate the activities of TET proteins
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Sequence-dependent surface condensation of a pioneer transcription factor on DNA
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“Since mitotic chromatin consists mainly of highly compacted DNA wrapped around nucle-osomes, our results could be explained by the higher affinity of SOX2 for nonspecific sequences on nucleosomal DNA as compared with OCT4 (Soufi et al. 2015).”
Phase separation of OCT4 controls TAD reorganization to promote cell fate transitions
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Generating specificity in genome regulation through transcription factor sensitivity to chromatin
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Molecular features of cellular reprogramming and development
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Human pancreatic beta-like cells converted from fibroblasts
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Single-Molecule Nanoscopy Elucidates RNA Polymerase II Transcription at Single Genes in Live Cells
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“, 2014a) or degenerate and/or partial motif binding (Soufi et al., 2015).”
BackgroundPioneer Factor-Nucleosome Binding Events during Differentiation Are Motif Encoded
Meers, M. P., Janssens, D. H., & Henikoff, S. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.05.025 · Cited by 135 · see citing works
“, 2016), and GATA4, EOMES, and HMG box transcription factors such as Sox17 have all been similarly implicated in possessing characteristics of pioneer factors (Cirillo et al., 2002; Soufi et al., 2015; Zhu et al., 2018).”
BackgroundThe Hierarchy of Transcriptional Activation: From Enhancer to Promoter
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“Other TFs involved in reprogramming of somatic cells to pluripotency such as Oct4, Sox2, and Klf4, also function as pioneer factors utilizing unique adaptations of their DNA recognition surfaces to accommodate nucleosome structure, which likely represents a common genome interrogation mechanism of the pioneer class [1…”
BackgroundPoli, V., Fagnocchi, L., Fasciani, A., Cherubini, A., Mazzoleni, S., Ferrillo, S., Miluzio, A., Gaudioso, G., Vaira, V., Turdo, A., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03264-2 · Cited by 146 · see citing works
Transcription Factors and DNA Play Hide and Seek
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Widespread mitotic bookmarking by histone marks and transcription factors in pluripotent stem cells
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“In agreementwith these results,motif scanninganalysesusingeither the ESC or the G1E bookmarked H3K27ac enhancer peaks enriched for binding sites recognized by the master regulators of each cell type, such as OSN (OCT4-SOX2-NANOG) and ESRRB or GATA1, respectively (Figure S2E; Table S2).”
BackgroundInfluentialTwo-Parameter Mobility Assessments Discriminate Diverse Regulatory Factor Behaviors in Chromatin
Lerner, J., Gomez-Garcia, P. A., McCarthy, R. L., Liu, Z., Lakadamyali, M., & Zaret, K. S. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.05.036 · Cited by 110 · see citing works
“, 2019) show that the genomic occupancy by transcription factor is sensitive to the local chromatin context (Soufi et al., 2015).”
BackgroundSelf-citationBalakrishnan, A., Belfiore, L., Chu, T., Fleming, T., Midha, R., Biernaskie, J. A., & Schuurmans, C. J. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.608442 · Cited by 139 · see citing works
“Similarly, Olig2 is incorporated in oligodendrocyte reprogramming protocols for its function as a pioneer factor (Yu et al., 2013), as are Sox family genes (Soufi et al., 2015; Hou et al., 2017).”
BackgroundChromatin Control of Developmental Dynamics and Plasticity
Perino, M., & Veenstra, G. J. C. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.08.004 · Cited by 131 · see citing works
Rapid Chromatin Switch in the Direct Reprogramming of Fibroblasts to Neurons
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“, 2012) and DNA elements preferentially pioneered contain only parts of the canonical binding motifs (Soufi et al., 2015).”
Pioneer and nonpioneer factor cooperation drives lineage specific chromatin opening
Mayran, A., Sochodolsky, K., Khetchoumian, K., Harris, J., Gauthier, Y., Bemmo, A., Balsalobre, A., & Drouin, J. (2019) · Nature Communications · doi:10.1038/s41467-019-11791-9 · Cited by 137 · see citing works
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LEAFY is a pioneer transcription factor and licenses cell reprogramming to floral fate
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Histone Interaction Landscapes Visualized by Crosslinking Mass Spectrometry in Intact Cell Nuclei
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“Hn-RNPK can act both as transcriptional co-activator or repressor and plays a role in the transcriptional regulation of p53 after DNA damage (66, 67).”
BackgroundInfluentialPioneer factors: roles and their regulation in development
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Self-citationThe Sox2 transcription factor binds RNA
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The emerging roles of Oct4 in tumor-initiating cells
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“Purified Oct4 proteins can bind nucleosomes in vitro, and in vivo they preferentially target silent sites enriched for nucleosomes thereby acting as a pioneer transcription factor during cell reprogramming (90, 91).”
BackgroundLi, Z., Martin, M., Zhang, J., Huang, H., Bai, L., Zhang, J., Kang, J., He, M., Li, J., Maurya, M. R., et al. (2017) · Circulation · doi:10.1161/circulationaha.117.027462 · Cited by 122 · see citing works
Hormone-dependent control of developmental timing through regulation of chromatin accessibilityPreprint
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“More recently, the master transcription factors of embryonic stem cell identity — Oct4, Sox2, and Klf4 — were shown to have pio-neering activity during induction of pluripotency in induced pluripotency stem (iPS) cells (Soufi et al. 2015).”
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“, FoxA1) function as pioneer TFs for genome accessibility has been debated in the recent literature (Franco et al., 2015; Iwafuchi-Doi et al., 2016; Soufi et al., 2015; Swinstead et al., 2016; Zaret et al., 2016).”
BackgroundInfluentialMolecular basis for the genome engagement by Sox proteins
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“t early stages of iPSC generation [134,135].”
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Cooperation between bHLH transcription factors and histones for DNA access
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Mechanisms of Binding Specificity among bHLH Transcription Factors
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“[98] associated the pioneer characteristics of some transcription factors to the length of the basic helix-1 and to their ability to bind centrally degenerate motifs in the surface of the nucleosome [98].”
BackgroundResultInfluentialContinued Activity of the Pioneer Factor Zelda Is Required to Drive Zygotic Genome Activation
McDaniel, S. L., Gibson, T. J., Schulz, K. N., García, M. F., Nevil, M., Jain, S. U., Lewis, P. W., Zaret, K. S., & Harrison, M. M. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.01.014 · Cited by 107 · see citing works
“The ability to bind DNA even when it is wrapped around histones in nucleosomes likely enables Oct4 to bind closed chromatin and initiate reprogramming (Soufi et al., 2015).”
Self-citationHistone modifications regulate pioneer transcription factor cooperativity
Sinha, K. K., Bilokapić, S., Du, Y., Malik, D., & Halić, M. (2023) · Nature · doi:10.1038/s41586-023-06112-6 · Cited by 109 · see citing works
Chromatin expansion microscopy reveals nanoscale organization of transcription and chromatin
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Self-citationBeyond proneural: emerging functions and regulations of proneural proteins
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Pioneering function of Isl1 in the epigenetic control of cardiomyocyte cell fate
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“In a small percentage of the cells, the OSKM factors have the ability to bind to repressed chromatin domains and activate pluripotency gene expression (Soufi et al., 2012, 2015).”
BackgroundStefano, B. D., Collombet, S., Jakobsen, J. S., Wierer, M., Sardina, J. L., Lackner, A., Stadhouders, R., Segura-Morales, C., Francesconi, M., Limone, F., et al. (2016) · Nature Cell Biology · doi:10.1038/ncb3326 · Cited by 103 · see citing works
Chromatin remodeling in bovine embryos indicates species-specific regulation of genome activation
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Foxa2 identifies a cardiac progenitor population with ventricular differentiation potential
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Systematic Study of Nucleosome-Displacing Factors in Budding Yeast
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“For PFs, it was proposed that the pioneer activities rely on special DBD structures that allow them to bind nucleosome with high affinity (Soufi et al., 2015; Zaret and Carroll, 2011).”
Mueller, B., Mieczkowski, J., Kundu, S., Wang, P., Sadreyev, R., Tolstorukov, M. Y., & Kingston, R. E. (2017) · Genes & Development · doi:10.1101/gad.293118.116 · Cited by 100 · see citing works
“…certain TSSs, transiently destabilized nucleosomes during viral induction of gene expression, and retention of nucleosomes in enhancer regions bound by FoxA and other factors (Xi et al. 2011; Knight et al. 2014; Sexton et al. 2014; Teif et al. 2014; Soufi et al. 2015; Iwafuchi-Doi et al. 2016).”
BackgroundChromatin Fiber Invasion and Nucleosome Displacement by the Rap1 Transcription Factor
Mivelaz, M., Cao, A.-M., Kubik, S., Zencir, S., Hovius, R., Boichenko, I., Stachowicz, A. M., Kurat, C. F., Shore, D., & Fierz, B. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.10.025 · Cited by 99 · see citing works
“A common feature of DNA binding domains (DBDs) of pTFs is their ability to bind partial sequence motifs displayed on nucleosomes (Soufi et al., 2015).”
BackgroundInteraction of the pioneer transcription factor GATA3 with nucleosomes
Tanaka, H., Takizawa, Y., Takaku, M., Kato, D., Kumagawa, Y., Grimm, S. A., Wade, P. A., & Kurumizaka, H. (2020) · Nature Communications · doi:10.1038/s41467-020-17959-y · Cited by 99 · see citing works
- 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 · 2013: 1
- 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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