The mechanistic basis for chromatin regulation by pioneer transcription factors
Open accessAbstract
Pioneer transcription factors play a primary role in establishing competence for gene expression and initiating cellular programming and reprogramming, and their dysregulation causes severe effects on human health, such as promoting tumorigenesis. Although more than 200 transcription factors are expressed in each cell type, only a small number of transcription factors are necessary to elicit dramatic cell‐fate changes in embryonic development and cell‐fate conversion. Among these key transcription factors, a subset called “pioneer transcription factors” have a remarkable ability to target nucleosomal DNA, or closed chromatin, early in development, often leading to the local opening of chromatin, thereby establishing competence for gene expression. Although more key transcription factors have been identified as pioneer transcription factors, the molecular mechanisms behind their special properties are only beginning to be revealed. Understanding the pioneering mechanisms will enhance our ability to precisely control cell fate at will for research and therapeutic purposes. This article is categorized under: Biological Mechanisms > Cell Fates Biological Mechanisms > Regulatory Biology Developmental Biology > Lineages
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Pioneer TFs have the unique ability to engage their target sites in closed chromatin, render them accessible and allow other factors to bind.
“Pioneer TFs have the unique ability to engage their target sites in closed chromatin, render them accessible and allow other factors to bind (68).”
From SOX9 reprograms endothelial cells by altering the chromatin landscape (2022) · cites this paper as [68]
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Takahashi, K., & Yamanaka, S. (2006) · Cell · doi:10.1016/j.cell.2006.07.024 · Cited by 26,673 · see citing works
Kastenhuber, E. R., & Lowe, S. W. (2017) · Cell · doi:10.1016/j.cell.2017.08.028 · Cited by 1,906 · see citing works
Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5
Clark, K., Halay, E. D., Lai, E., & Burley, S. K. (1993) · Nature · doi:10.1038/364412a0 · Cited by 1,275 · see citing works
Opening of Compacted Chromatin by Early Developmental Transcription Factors HNF3 (FoxA) and GATA-4
Cirillo, L. A., Lin, F. R., Cuesta, I., Friedman, D., Jarník, M., & Zaret, K. S. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00459-8 · Cited by 1,188 · see citing works
FoxA1 Translates Epigenetic Signatures into Enhancer-Driven Lineage-Specific Transcription
Lupien, M., Eeckhoute, J., Meyer, C. A., Wang, Q., Zhang, Y., Li, W., Carroll, J. S., Liu, X. S., & Brown, M. (2008) · Cell · doi:10.1016/j.cell.2008.01.018 · Cited by 983 · see citing works
Soufi, A., Donahue, G., & Zaret, K. S. (2012) · Cell · doi:10.1016/j.cell.2012.09.045 · Cited by 887 · see citing works
FOXA1 is a key determinant of estrogen receptor function and endocrine response
Hurtado, A., Holmes, K. A., Ross-Innes, C. S., Schmidt, D., & Carroll, J. S. (2010) · Nature Genetics · doi:10.1038/ng.730 · Cited by 847 · see citing works
Pioneer Transcription Factors Target Partial DNA Motifs on Nucleosomes to Initiate Reprogramming
Soufi, A., Garcia, M. F., Jaroszewicz, A., Osman, N., Pellegrini, M., & Zaret, K. S. (2015) · Cell · doi:10.1016/j.cell.2015.03.017 · Cited by 780 · cited 1× · see citing works
“In contrast to the full DNA motif recognition of FoxA, the reprogramming factors (Sox2, Oct3/4, and Klf4) recognize one face of DNA on nucleosome by targeting a partial DNA sequence of their canonical binding motifs exposed on nucleosomes (Soufi et al., 2015).”
BackgroundCrystal structure of globular domain of histone H5 and its implications for nucleosome binding
Ramakrishnan, V., Finch, J. T., Graziano, V., Lee, P. L., & Sweet, R. M. (1993) · Nature · doi:10.1038/362219a0 · Cited by 736 · see citing works
Single-Molecule Dynamics of Enhanceosome Assembly in Embryonic Stem Cells
Chen, J., Zhang, Z., Li, L., Chen, B.-C., Revyakin, A., Hajj, B., Legant, W., Dahan, M., Lionnet, T., Betzig, E., et al. (2014) · Cell · doi:10.1016/j.cell.2014.01.062 · Cited by 602 · see citing works
Pioneer transcription factors in cell reprogrammingPreprint
Iwafuchi, M., & Zaret, K. S. (2014) · Genes & Development · doi:10.1101/gad.253443.114 · Cited by 590 · see citing works
An Oct4-Centered Protein Interaction Network in Embryonic Stem Cells
van den Berg, D. L. C., Snoek, T., Mullin, N. P., Yates, A., Bezstarosti, K., Demmers, J., Chambers, I., & Poot, R. A. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.02.014 · Cited by 542 · see citing works
Fundamentally Different Logic of Gene Regulation in Eukaryotes and Prokaryotes
Struhl, K. (1999) · Cell · doi:10.1016/s0092-8674(00)80599-1 · Cited by 486 · see citing works
AP-1 Transcription Factors and the BAF Complex Mediate Signal-Dependent Enhancer Selection
Vierbuchen, T., Ling, E., Cowley, C. J., Couch, C. H., Wang, X., Harmin, D. A., Roberts, C. W. M., & Greenberg, M. E. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.11.026 · Cited by 455 · see citing works
Espinosa, J. M., & Emerson, B. M. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00283-0 · Cited by 440 · see citing works
Iwafuchi-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
Binding of the winged‐helix transcription factor HNF3 to a linker histone site on the nucleosome
Cirillo, L. A., McPherson, C. E., Bossard, P., Stevens, K., Cherian, S., Shim, E. Y., Clark, K., Burley, S. K., & Zaret, K. S. (1998) · The EMBO Journal · doi:10.1093/emboj/17.1.244 · Cited by 381 · see citing works
An Expanded Oct4 Interaction Network: Implications for Stem Cell Biology, Development, and Disease
Pardo, M., Lang, B., Yu, L., Prosser, H., Bradley, A., Babu, M. M., & Choudhary, J. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.03.004 · Cited by 379 · see citing works
Transcription factor binding dynamics during human ES cell differentiation
Tsankov, A. M., Gu, H., Akopian, V., Ziller, M. J., Donaghey, J., Amit, I., Gnirke, A., & Meissner, A. (2015) · Nature · doi:10.1038/nature14233 · Cited by 349 · 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
King, H. W., & Klose, R. J. (2017) · eLife · doi:10.7554/elife.22631 · Cited by 270 · see citing works
Pioneer factors in hormone-dependent cancers
Jozwik, K. M., & Carroll, J. S. (2012) · Nature reviews. Cancer · doi:10.1038/nrc3263 · Cited by 265 · see citing works
Wang, A., Yue, F., Li, Y., Xie, R., Harper, T. C., Patel, N. A., Muth, K., Palmer, J., Qiu, Y., Wang, J., et al. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.02.013 · Cited by 263 · see citing works
Sox2 cooperates with Chd7 to regulate genes that are mutated in human syndromes
Engelen, E., Akinci, U., Bryne, J. C., Hou, J., Gontan, C., Moen, M., Szumska, D., Kockx, C., van IJcken, W., Dekkers, D. H. W., et al. (2011) · Nature Genetics · doi:10.1038/ng.825 · Cited by 255 · see citing works
Tissue-Specific Mitotic Bookmarking by Hematopoietic Transcription Factor GATA1
Kadauke, S., Udugama, M., Pawlicki, J. M., Achtman, J. C., Jain, D., Cheng, Y., Hardison, R. C., & Blobel, G. A. (2012) · Cell · doi:10.1016/j.cell.2012.06.038 · Cited by 232 · see citing works
Epigenetic switch involved in activation of pioneer factor FOXA1-dependent enhancersPreprint
Sérandour, A. A., Avner, S., Percevault, F., Demay, F., Bizot, M., Lucchetti-Miganeh, C., Barloy-Hubler, F., Brown, M. A., Lupien, M., Métivier, R., et al. (2011) · Genome Research · doi:10.1101/gr.111534.110 · Cited by 228 · see citing works
Sekiya, T., Muthurajan, U. M., Luger, K., Tulin, A. V., & Zaret, K. S. (2009) · Genes & Development · doi:10.1101/gad.1775509 · Cited by 221 · see citing works
Bookmarking by specific and nonspecific binding of FoxA1 pioneer factor to mitotic chromosomesPreprint
Caravaca, J. M., Donahue, G., Becker, J. S., He, X., Charles, V., & Zaret, K. S. (2013) · Genes & Development · doi:10.1101/gad.206458.112 · Cited by 218 · see citing works
Epigenetics, cellular memory and gene regulation
Henikoff, S., & Greally, J. M. (2016) · Current Biology · doi:10.1016/j.cub.2016.06.011 · Cited by 215 · see citing works
Ptashne, M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305399110 · Cited by 208 · see citing works
Hu, G., Schones, D. E., Cui, K., Ybarra, R., Northrup, D., Tang, Q., Gattinoni, L., Restifo, N. P., Huang, S., & Zhao, K. (2011) · Genome Research · doi:10.1101/gr.121145.111 · Cited by 186 · cited 1× · see citing works
“More pioneer factors, such as Sox2, p63, Gata, and AP-1, have also been reported to recruit chromatin remodelers to their target sites (Bao et al., 2015; Engelen et al., 2011; Hu et al., 2011; Takaku et al., 2016; Vierbuchen et al., 2017).”
BackgroundMaster 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
Pioneer 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
High Nucleosome Occupancy Is Encoded at Human Regulatory Sequences
Tillo, D., Kaplan, N., Moore, I. K., Fondufe‐Mittendorf, Y. N., Gossett, A. J., Field, Y., Lieb, J. D., Widom, J., Segal, E., & Hughes, T. R. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009129 · Cited by 169 · see citing works
Genetic 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
FOXA1 Directs H3K4 Monomethylation at Enhancers via Recruitment of the Methyltransferase MLL3
Jozwik, K. M., Chernukhin, I. V., Sérandour, A. A., Nagarajan, S., & Carroll, J. S. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.11.028 · Cited by 164 · see citing works
Bao, X., Rubin, A. J., Qu, K., Zhang, J., Giresi, P. G., Chang, H. Y., & Khavari, P. A. (2015) · Genome Biology · doi:10.1186/s13059-015-0840-9 · Cited by 164 · see citing works
Oct4 links multiple epigenetic pathways to the pluripotency network
Ding, J., Xu, H., Faiola, F., Ma'ayan, A., & Wang, J. (2012) · Cell Research · doi:10.1038/cr.2011.179 · Cited by 162 · see citing works
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 · see citing works
Takaku, M., Grimm, S. A., Shimbo, T., Perera, L., Menafra, R., Stunnenberg, H. G., Archer, T. K., Machida, S., Kurumizaka, H., & Wade, P. A. (2016) · Genome Biology · doi:10.1186/s13059-016-0897-0 · Cited by 151 · see citing works
Identification of two DNA‐binding sites on the globular domain of histone H5.
Goytisolo, F. A., Gerchman, S. E., Yu, X., Rees, C., Graziano, V., Ramakrishnan, V., & Thomas, J. O. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00708.x · Cited by 151 · see citing works
Widespread mitotic bookmarking by histone marks and transcription factors in pluripotent stem cells
Liu, Y.-Y., Pelham-Webb, B., Giammartino, D. C. D., Li, J.-X., Kim, D., Kita, K., Saiz, N., Garg, V., Doane, A., Giannakakou, P., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.04.067 · Cited by 142 · see citing works
Boller, S., Ramamoorthy, S., Akbas, D., Nechanitzky, R., Burger, L., Murr, R., Schübeler, D., & Grosschedl, R. (2016) · Immunity · doi:10.1016/j.immuni.2016.02.021 · Cited by 133 · see citing works
Sammons, M. A., Zhu, J., Drake, A. M., & Berger, S. L. (2014) · Genome Research · doi:10.1101/gr.181883.114 · Cited by 114 · see citing works
Liu, Z., & Kraus, W. L. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.01.017 · Cited by 113 · see citing works
Laptenko, O., Beckerman, R., Freulich, E., & Prives, C. L. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105680108 · Cited by 99 · see citing works
p53 binds preferentially to genomic regions with high DNA-encoded nucleosome occupancyPreprint
Nili, E. L., Field, Y., Lubling, Y., Widom, J., Oren, M., & Segal, E. (2010) · Genome Research · doi:10.1101/gr.103945.109 · Cited by 90 · see citing works
Nucleation of DNA repair factors by FOXA1 links DNA demethylation to transcriptional pioneering
Zhang, Y., Zhang, D., Li, Q., Liang, J., Sun, L., Yi, X., Chen, Z., Yan, R., Xie, G., Li, W., et al. (2016) · Nature Genetics · doi:10.1038/ng.3635 · Cited by 73 · see citing works
Chromatin scanning by dynamic binding of pioneer factors
Zaret, K. S., Lerner, J., & Iwafuchi-Doi, M. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.05.024 · Cited by 68 · see citing works
Pluripotency factors functionally premark cell-type-restricted enhancers in ES cells
Kim, H. S., Tan, Y., Ma, W., Merkurjev, D., Destici, E., Ma, Q., Suter, T., Ohgi, K. A., Friedman, M. J., Skowronska‐Krawczyk, D., et al. (2018) · Nature · doi:10.1038/s41586-018-0048-8 · Cited by 49 · see citing works
p53 Binding to Nucleosomal DNA Depends on the Rotational Positioning of DNA Response Element
Sahu, G., Wang, D., Chen, C. B., Zhurkin, V. B., Harrington, R. E., Appella, E., Hager, G. L., & Nagaich, A. K. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.081182 · Cited by 48 · see citing works
Cui, F., & Zhurkin, V. B. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt943 · Cited by 43 · see citing works
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Joshi, K., Liu, S., Breslin, P., & Zhang, J. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04396-x · Cited by 172 · see citing works
Transcription Factors and DNA Play Hide and Seek
Suter, D. M. (2020) · Trends in Cell Biology · doi:10.1016/j.tcb.2020.03.003 · Cited by 143 · see citing works
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Diacou, R., Nandigrami, P., Fiser, A., Liu, W., Ashery‐Padan, R., & Cvekl, A. (2022) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2022.101093 · Cited by 103 · see citing works
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Berasain, C., Arechederra, M., Argemí, J., Fernández-Barrena, M. G., & Avila, M. A. (2023) · Journal of Hepatology · doi:10.1016/j.jhep.2022.09.001 · Cited by 99 · see citing works
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Raccaud, M., Friman, E. T., Alber, A. B., Agarwal, H., Deluz, C., Kuhn, T., Gebhardt, J. C. M., & Suter, D. M. (2019) · Nature Communications · doi:10.1038/s41467-019-08417-5 · Cited by 98 · see citing works
The LEAFY floral regulator displays pioneer transcription factor properties
Lai, X., Blanc‐Mathieu, R., GrandVuillemin, L., Huang, Y., Stigliani, A., Lucas, J., Thévenon, E., Loue-Manifel, J., Turchi, L., Daher, H., et al. (2021) · Molecular Plant · doi:10.1016/j.molp.2021.03.004 · Cited by 89 · see citing works
Miao, L., Tang, Y., Bonneau, A. R., Chan, S. H., Kojima, M. L., Pownall, M. E., Vejnar, C. E., Gao, F., Krishnaswamy, S., Hendry, C., et al. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.01.024 · Cited by 87 · see citing works
Barragán-Rosillo, A. C., Peralta‐Álvarez, C. A., Ojeda‐Rivera, J. O., Arzate‐Mejía, R. G., Targa, F. R., & Herrera‐Estrella, L. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2107558118 · Cited by 80 · see citing works
Transcriptional enhancers and their communication with gene promoters
Ray-Jones, H., & Spivakov, M. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03903-w · Cited by 81 · see citing works
Autophagy mediates temporary reprogramming and dedifferentiation in plant somatic cells
Rodriguez, E., Chevalier, J. R., Olsen, J., Ansbøl, J., Kapousidou, V., Zuo, Z., Svenning, S., Löfke, C., Koemeda, S., Drozdowskyj, P. S., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2019103315 · Cited by 73 · see citing works
Perenthaler, E., Yousefi, S., Niggl, E., & Barakat, T. S. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00352 · Cited by 71 · see citing works
Pioneering the developmental frontier
Larson, E. D., Marsh, A. J., & Harrison, M. M. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.02.020 · Cited by 64 · see citing works
LEAFY, a Pioneer Transcription Factor in Plants: A Mini-Review
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Takaku, M., Grimm, S. A., Kumar, B. D., Bennett, B. D., & Wade, P. A. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa179 · Cited by 58 · see citing works
Vanzan, L., Soldati, H., Ythier, V., Anand, S. K., Braun, S. M. G., Francis, N. J., & Murr, R. (2021) · Nature Communications · doi:10.1038/s41467-021-23630-x · Cited by 52 · see citing works
Galupa, R., Álvarez-Canales, G., Borst, N. O., Fuqua, T., Gándara, L., Misunou, N., Richter, K., Alves, M. R. P., Karumbi, E., Perkins, M. L., et al. (2022) · Developmental Cell · doi:10.1016/j.devcel.2022.12.003 · Cited by 51 · see citing works
Redirecting the pioneering function of FOXA1 with covalent small molecules
Won, S. J., Zhang, Y., Reinhardt, C. J., Hargis, L. M., MacRae, N. S., DeMeester, K. E., Njomen, E., Remsberg, J. R., Melillo, B. N., Cravatt, B. F., et al. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.09.024 · Cited by 45 · see citing works
Larson, E. D., Komori, H., Gibson, T. J., Ostgaard, C. M., Hamm, D. C., Schnell, J., Lee, C., & Harrison, M. M. (2021) · Nature Communications · doi:10.1038/s41467-021-27506-y · Cited by 45 · see citing works
Khan, A. A., Huat, T. J., Mutery, A. A., El-Serafi, A. T., Kacem, H. H., Abdallah, S. H., Reza, M. F., Abdullah, J. M., & Jaafar, H. (2020) · Cell & Bioscience · doi:10.1186/s13578-020-00487-z · Cited by 39 · see citing works
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Chen, R., Cao, Y., Liu, Y., Zhao, D., Li, J., Cheng, Z., Bi, C., & Zhang, X. (2023) · Nature Communications · doi:10.1038/s41467-023-35919-0 · Cited by 31 · see citing works
Identification of mammalian transcription factors that bind to inaccessible chromatin
Pop, R. T., Pisante, A., Nagy, D., Martin, P. C. N., Mikheeva, L. A., Hayat, A., Ficz, G., & Zabet, N. R. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad614 · Cited by 28 · see citing works
Grosse, L., & Bulavin, D. V. (2020) · Aging · doi:10.18632/aging.103492 · Cited by 27 · see citing works
Nair, V. D., Vasoya, M., Nair, V., Smith, G. R., Pinças, H., Ge, Y., Douglas, C. M., Esser, K. A., & Sealfon, S. C. (2021) · Genomics · doi:10.1016/j.ygeno.2021.09.013 · Cited by 25 · see citing works
Nevil, M., Gibson, T. J., Bartolutti, C., Iyengar, A., & Harrison, M. M. (2020) · Development · doi:10.1242/dev.185009 · Cited by 24 · see citing works
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Stephens, G. S., Fu, C.-H., Romain, C. P. S., Zheng, Y., Botterill, J. J., Scharfman, H. E., Liu, Y., & Chin, J. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00472 · Cited by 22 · see citing works
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Andrysík, Z., & Espinosa, J. M. (2025) · Transcription · doi:10.1080/21541264.2025.2452711 · Cited by 18 · see citing works
Stephens, G. S., Park, J. K., Eagle, A. L., You, J. C., Silva‐Pérez, M., Fu, C.-H., Choi, S., Romain, C. P. S., Sugimoto, C., Buffington, S. A., et al. (2024) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2024.102612 · Cited by 15 · see citing works
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Takada, S., Brandani, G. B., & Tan, C. (2020) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2019.11.013 · Cited by 15 · see citing works
Saotome, M., Poduval, D. B., Grimm, S. A., Nagornyuk, A., Gunarathna, S., Shimbo, T., Wade, P. A., & Takaku, M. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae025 · Cited by 15 · see citing works
Ruffo, P., Traynor, B. J., & Conforti, F. L. (2025) · Genes & Diseases · doi:10.1016/j.gendis.2025.101652 · Cited by 14 · see citing works
How Pioneer Transcription Factors Search for Target Sites on Nucleosomal DNA
Felipe, C., Shin, J., & Kolomeisky, A. B. (2022) · The Journal of Physical Chemistry B · doi:10.1021/acs.jpcb.2c01931 · Cited by 14 · see citing works
Detection of new pioneer transcription factors as cell-type-specific nucleosome binders
Peng, Y., Song, W., Teif, V. B., Ovcharenko, I., Landsman, D., & Panchenko, A. R. (2023) · eLife · doi:10.7554/elife.88936 · Cited by 14 · see citing works
Harnessing targeted DNA methylation and demethylation using dCas9
Pflueger, C., Swain, T., & Lister, R. (2019) · Essays in Biochemistry · doi:10.1042/ebc20190029 · Cited by 14 · see citing works
Mitotic chromosome binding predicts transcription factor properties in interphasePreprint
Raccaud, M., Alber, A. B., Friman, E. T., Agarwal, H., Deluz, C., Kuhn, T., Gebhardt, J. C. M., & Suter, D. M. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/404723 · Cited by 13 · see citing works
The non-coding genome in genetic brain disorders: new targets for therapy?
Salsench, E. M., Karkala, F., Lanko, K., & Barakat, T. S. (2021) · Essays in Biochemistry · doi:10.1042/ebc20200121 · Cited by 11 · see citing works
Picking a nucleosome lock: Sequence- and structure-specific recognition of the nucleosome
Makowski, M. M., Gaullier, G., & Luger, K. (2020) · Journal of Biosciences · doi:10.1007/s12038-019-9970-7 · Cited by 11 · see citing works
Dyer, M., Lin, Q. X. X., Shapoval, S., Thieffry, D., & Benoukraf, T. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad894 · Cited by 11 · see citing works
Tsukanov, A. V., Mironova, V., & Levitsky, V. G. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.938545 · Cited by 10 · see citing works
MAF functions as a pioneer transcription factor that initiates and sustains myelomagenesis
Katsarou, A., Trasanidis, N., Ponnusamy, K., Kostopoulos, I. V., Alvarez-Benayas, J., Papaleonidopoulou, F., Keren, K., Sabbattini, P. M. R., Feldhahn, N., Papaioannou, M., et al. (2023) · Blood Advances · doi:10.1182/bloodadvances.2023009772 · Cited by 10 · see citing works
Miao, L., Tang, Y., Bonneau, A. R., Chan, S. H., Kojima, M. L., Pownall, M. E., Vejnar, C. E., & Giráldez, A. J. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.09.01.278796 · Cited by 9 · see citing works
Giannopoulou, A.-I., Kanakoglou, D. S., Papavassiliou, A. G., & Piperi, C. (2022) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2022.188801 · Cited by 9 · see citing works
Sheng, J., Li, C., Dong, M., & Jiang, K. (2020) · Cancer Management and Research · doi:10.2147/cmar.s262017 · Cited by 9 · see citing works
Steggall, J., Rajeeve, V., Alsubaie, N. M., Naeem, A., Ikram, A., Naeem, A., & Hayat, A. (2025) · British Journal of Cancer · doi:10.1038/s41416-025-03174-3 · Cited by 6 · see citing works
Tsukanov, A. V., Levitsky, V. G., & Merkulova, T. I. (2021) · Vavilov Journal of Genetics and Breeding · doi:10.18699/vj21.002 · Cited by 6 · see citing works
Enhancer architecture and chromatin accessibility constrain phenotypic space during developmentPreprint
Galupa, R., Álvarez-Canales, G., Borst, N. O., Fuqua, T., Gándara, L., Misunou, N., Richter, K., Alves, M. R. P., Karumbi, E., Perkins, M. L., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.02.494376 · Cited by 6 · see citing works
Thang, N. X., Yoo, S., La, H., Lee, H., Park, C., Park, K. S., & Hong, K. (2022) · Biomedicines · doi:10.3390/biomedicines10040748 · Cited by 5 · see citing works
Grigoryan, E. N., & Markitantova, Y. V. (2025) · Biomedicines · doi:10.3390/biomedicines13071552 · Cited by 4 · see citing works
Salaün, C., Thévenin, J., Edoura‐Gaena, A., Qiu, Y., Burguet, J., Miquel, M., Lepiniec, L., & Dubreucq, B. (2025) · The Plant Journal · doi:10.1111/tpj.70380 · Cited by 4 · see citing works
Chen, M., Zhou, Y., Fu, Z., & Wu, C. (2024) · Acta Biochimica et Biophysica Sinica · doi:10.3724/abbs.2024237 · Cited by 2 · see citing works
Enhancers, development, and evolution
Kuroiwa, A. (2020) · Development Growth & Differentiation · doi:10.1111/dgd.12683 · Cited by 2 · see citing works
Fuglerud, B. M., Drissler, S., Lotto, J., Stephan, T. L., Thakur, A., Cullum, R. L., & Hoodless, P. A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.09.11.293993 · Cited by 2 · see citing works
The pioneer transcription factor ELF2 remodels the nucleosome near transcription start sitesPreprint
Xiao, T., Crowe-McAuliffe, C., Ochmann, M., Du, Y., Hou, T., Chen, Y., Zhu, F., Seyednasrollah, F., Osmala, M., Vanharanta, S., et al. (2025) · bioRxiv · doi:10.1101/2024.05.24.595749 · Cited by 2 · see citing works
Recognition of diverse GATA motifs necessitates multimodal GATA3-DNA binding
Gharui, S., Puntambekar, S. S., Sarkar, R. R., Narlikar, L., & Sengupta, D. (2026) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2026.153718 · Cited by 1 · see citing works
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) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.10.540098 · Cited by 1 · see citing works
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 · see citing works
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 · see citing works
GATA3 mutation disrupts a functional network governed by estrogen receptor, FOXA1 and GATA3Preprint
Takaku, M., Grimm, S. A., Kumar, B. D., Bennett, B. D., & Wade, P. A. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/654871
Ogunshola, F. J., Smidt, W., Naidoo, A., Nkosi, T., Ngubane, T., Khaba, T., Baiyegunhi, O. O., Rasehlo, S., Jajbhay, I., Dong, K. L., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.17.208470
Bergo, V., & Trompouki, E. (2021) · Briefings in Functional Genomics · doi:10.1093/bfgp/elab001
Mefford, H. C. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.736437709.793571951
Transcriptional Regulatory Activity as the Default State for DNA in Animal DevelopmentPreprint
Galupa, R., Álvarez-Canales, G., Borst, N. O., Fuqua, T., Gándara, L., Misunou, N., Richter, K., Alves, M. R. P., Karumbi, E., Perkins, M. L., et al. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4186258
Saotome, M., Poduval, D. B., Grimm, S. A., Nagornyuk, A., Gunarathna, S., Shimbo, T., Wade, P. A., & Takaku, M. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.02.530867
Takaku, M., Saotome, M., Poduval, D. B., Grimm, S. A., Nagornyuk, A., Gunarathna, S., Shimbo, T., & Wade, P. A. (2023) · Research Square · doi:10.21203/rs.3.rs-2587918/v1
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.88936.3
Peng, Y., Song, W., Teif, V. B., Ovcharenko, I., Landsman, D., & Panchenko, A. R. (2023) · eLife · doi:10.7554/elife.88936.3.sa4
Wang, J., Jin, Y., Zhu, Q., Liu, X., Xie, Z., Wu, J. S., Xing, Z., Mu, M., & Zhu, F. (2025) · SSRN Electronic Journal · doi:10.2139/ssrn.5111178
Khan, A. A., Huat, T. J., Al Mutery, A., El-Serafi, A. T., Kacem, H. H., Abdallah, S. H., Reza, M. F., Abdullah, J. M., & Jaafar, H. (2020) · Figshare · doi:10.6084/m9.figshare.13161651
Khan, A. A., Huat, T. J., Al Mutery, A., El-Serafi, A. T., Kacem, H. H., Abdallah, S. H., Reza, M. F., Abdullah, J. M., & Jaafar, H. (2020) · Figshare · doi:10.6084/m9.figshare.13161648
Oleynik, V., Kadangodan, A. E., Gahramanov, V., Das, S. R., Levi, B., Yaglom, J. A., Аношкин, К. И., Kumar, S., Steinberg, B. G., Reizel, Y., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.20.707073
Somatic embryogenesis in plants: unraveling the genetic and epigenetic factors
Ahmadabadi, M., & Dehghanian, Z. (2026) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-026-03523-x
Oriented binding of transcription factors to nucleosomes remodels chromatin at human promoters.
Xiao, T., Crowe-McAuliffe, C., Ochmann, M., Warrier, T., Du, Y., Hou, T., Zou, S.-W., Chen, Y., Zhu, F., Zhang, D., et al. (2026) · Molecules and Cells · doi:10.1016/j.molcel.2026.08.005
- Authors
- Iwafuchi‐Doi, M.
- Affiliations
- Division of Developmental Biology, Center for Stem Cell & Organoid Medicine (CuSTOM), Cincinnati Children's Hospital Medical Center University of Cincinnati College of Medicine Cincinnati Ohio
- Venue
- WIREs Systems Biology and Medicine
- Publisher
- Wiley
- Published
- 2018-06-27
- Volume
- 11
- Issue
- 1
- Pages
- e1427-e1427
- ISSN
- 1939-005X (ISSN-L)
- 1939-5094
- PMC
- PMC6585746
- OpenAlex
- W2810449531
- Cited by
- 82
- References
- 52
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 6 · 2023: 15 · 2022: 13 · 2021: 12 · 2020: 20 · 2019: 5 · 2018: 1
- FWCI
- 0.93
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- WIREs Systems Biology and Medicine (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- pioneer transcription factors, chromatin regulation, closed chromatin, chromatin opening, cell fate conversion, cellular reprogramming, embryonic development, carcinogenesis
- MeSH terms
- Animals, Cell Differentiation, Humans, Models, Biological, Neoplasm Proteins, Nucleosomes, Transcription Factors, Chromatin Assembly and Disassembly, Carcinogenesis
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