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Regulation of nucleosome landscape and transcription factor targeting at tissue-specific enhancers by BRG1
Open accessAbstract
Enhancers of transcription activate transcription via binding of sequence-specific transcription factors to their target sites in chromatin. In this report, we identify GATA1-bound distal sites genome-wide and find a global reorganization of the nucleosomes at these potential enhancers during differentiation of hematopoietic stem cells (HSCs) to erythrocytes. We show that the catalytic subunit BRG1 of BAF complexes localizes to these distal sites during differentiation and generates a longer nucleosome linker region surrounding the GATA1 sites by shifting the flanking nucleosomes away. Intriguingly, we find that the nucleosome shifting specifically facilitates binding of TAL1 but not GATA1 and is linked to subsequent transcriptional regulation of target genes.
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“The mechanisms of pioneer factor action are still being established [37], but at least some of them (such as FOXA, OCT4 and SOX2/SOX11) have been shown to initiate chromatin opening by direct displacement of histones [38–41], whilst many others recruit chromatin remodelers [42–50].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [48]
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Boyle, A. P., Hong, E. L., Hariharan, M., Cheng, Y., Schaub, M. A., Kasowski, M., Karczewski, K. J., Park, J., Hitz, B. C., Weng, S., et al. (2012) · Genome Research · doi:10.1101/gr.137323.112 · Cited by 2,722
“Inaddition, we have included transcriptionfactor ChIP-seq data availablefrom the NCBI Sequence Read Archive (Hollenhorst et al. 2009; Jolma et al. 2010; Verzi et al. 2010; Wei et al. 2010; Hu et al. 2011; Lo et al. 2011; Novershtern et al. 2011; Palii et al. 2011; Yu et al. 2011).”
MethodLatent Enhancers Activated by Stimulation in Differentiated Cells
Ostuni, R., Piccolo, V., Barozzi, I., Polletti, S., Termanini, A., Bonifacio, S., Curina, A., Prosperini, E., Ghisletti, S., & Natoli, G. (2013) · Cell · doi:10.1016/j.cell.2012.12.018 · Cited by 867
“…cis-regulatory landscape entails multiple TF activities, including recruitment of chromatin modifiers, nucleosome remodelers, and histone chaperons (Hu et al., 2011; Ram et al., 2011), eventually resulting in the demarcation of short DNA stretches that contain accessible TF binding sites (TFBS)…”
The SWI/SNF chromatin remodelling complex is required for maintenance of lineage specific enhancers
Alver, B. H., Kim, K. H., Lu, P., Wang, X., Manchester, H. E., Wang, W., Haswell, J. R., Park, P. J., & Roberts, C. W. M. (2017) · Nature Communications · doi:10.1038/ncomms14648 · Cited by 427
DANPOS: Dynamic analysis of nucleosome position and occupancy by sequencingPreprint
Chen, K.-F., Xi, Y., Pan, X.-W., Li, Z.-Y., Kaestner, K., Tyler, J. K., Dent, S., He, X.-W., & Li, W. (2013) · Genome Research · doi:10.1101/gr.142067.112 · Cited by 415
“To demonstrate the broad utility of DANPOS, we analyzed dynamic nucleosomes during differentiation of human hematopoietic stem cells (HSCs) to CD36+ erythrocytes (Hu et al. 2011).”
BackgroundMethodInfluentialHu, G., Cui, K., Northrup, D. L., Liu, C., Wang, C., Tang, Q., Ge, K., Levens, D., Crane‐Robinson, C., & Zhao, K. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.11.003 · Cited by 345
“Consistent with the previous reports (Hu et al., 2011; Tillo et al., 2010), in control ESs, enhancers are associated with increased nucleosome occupancy relative to neighboring regions (Figure 3A, black line), and H2A.”
Self-citationVulnerabilities of Mutant SWI/SNF Complexes in Cancer
Helming, K., Wang, X., & Roberts, C. W. M. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.07.018 · Cited by 308
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“Alternatively, it has been proposed that ATP-dependent chromatin remodellers may be required to assist pioneer transcription factors in establishing accessible chromatin (Hu et al., 2011; Marathe et al., 2013; Ceballos-Chávez et al., 2015; Swinstead et al., 2016).”
BackgroundInfluentialGenome-wide nucleosome positioning during embryonic stem cell development
Teif, V. B., Vainshtein, Y., Caudron‐Herger, M., Mallm, J., Marth, C., Höfer, T., & Rippe, K. (2012) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2419 · Cited by 263
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“AnH3K27Demethylase-Independent Function of UTX in Enhancer Regulation Shaping the enhancer landscape for chromatin opening to allow transcriptional activation entails multiple transcription (co)factor activities that include recruitment of chromatin modulators, nucleosome remodelers, and histone chaperones (Hu et al.,…”
Chromatin Remodeling BAF (SWI/SNF) Complexes in Neural Development and Disorders
Sokpor, G., Xie, Y., Rosenbusch, J., & Tuoc, T. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00243 · Cited by 230
“This process relaxes condensed chromatin (heterochromatin) to increase accessibility of transcription factor binding to activate gene expression (Hara and Sancar, 2002; Gong et al., 2006; Ho et al., 2009a; Hu et al., 2011; Tolstorukov et al., 2013).”
BackgroundDifferential DNase I hypersensitivity reveals factor-dependent chromatin dynamicsPreprint
He, H.-S. H., Meyer, C. A., Chen, M., Jordan, V. C., Brown, M. A., & Liu, X. S. (2012) · Genome Research · doi:10.1101/gr.133280.111 · Cited by 191
“2010) and with GATA1 in hematopoiesis (Hu et al. 2011).”
BackgroundTolstorukov, M. Y., Sansam, C. G., Lu, P., Koellhoffer, E. C., Helming, K. C., Alver, B. H., Tillman, E. J., Evans, J. A., Wilson, B. G., Park, P. J., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1302209110 · Cited by 190
“Previous studies have shown that ATP-dependent chromatin remodelers can modulate the spacing between individual nucleosomes and that even subtle changes in linker lengths can substantially affect transcription factor binding (38).”
BackgroundMethodBresnick, E. H., Katsumura, K. R., Lee, H., Johnson, K. D., & Perkins, A. S. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks281 · Cited by 189
Ubiquitous heterogeneity and asymmetry of the chromatin environment at regulatory elements
Kundaje, A., Kyriazopoulou-Panagiotopoulou, S., Libbrecht, M., Smith, C. L., Raha, D., Winters, E. E., Johnson, S. M., Snyder, M., Batzoglou, S., & Sidow, A. (2012) · Genome Research · doi:10.1101/gr.136366.111 · Cited by 178
“These context-specific co-binding events, and the influence of other genomic features such as proximity to promoters, will often exhibit diverse chromatin modification and nucleosome positioning landscapes (Hu et al. 2011).”
BackgroundProfiling of Pluripotency Factors in Single Cells and Early Embryos
Hainer, S. J., Bošković, A., McCannell, K. N., Rando, O. J., & Fazzio, T. G. (2019) · Cell · doi:10.1016/j.cell.2019.03.014 · Cited by 203
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“BRG1 binds extensively over the melanoma cell genome often at active H3K27ac-marked enhancers consistent with previous reports (Hu et al., 2011).”
BackgroundResultInfluentialMammalian SWI/SNF continuously restores local accessibility to chromatin
Iurlaro, M., Stadler, M. B., Masoni, F., Jagani, Z., Galli, G. G., & Schübeler, D. (2021) · Nature Genetics · doi:10.1038/s41588-020-00768-w · Cited by 190
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“In mouse CD36 cells, knocking down Brg1 alone also only modestly affected the nucleosome positioning at GATA1 sites without affecting GATA1 genomic binding [14].”
BackgroundTakaku, 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
“BRG1 is also known to function with the other GATA family proteins such as GATA1 and GATA4 [23, 50, 51] and is characterized by its ability to evict nucleosomes [52–54].”
BackgroundPrinciples of nucleosome organization revealed by single-cell micrococcal nuclease sequencing
Lai, B., Gao, W., Cui, K., Xie, W., Tang, Q., Jin, W., Hu, G., Ni, B., & Zhao, K. (2018) · Nature · doi:10.1038/s41586-018-0567-3 · Cited by 164
Self-citationTranscriptional enhancers in development and disease
Sakabe, N. J., Savic, D., & Nóbrega, M. A. (2012) · Genome biology · doi:10.1186/gb-2012-13-1-238 · Cited by 143
“Similarly to FOXA1, early binding of the TFs GATA1 [9] and CEBPA [35] has been observed in sites that became functional only upon differentiation.”
BackgroundMechanisms by which SMARCB1 loss drives rhabdoid tumor growth
Kim, K. H., & Roberts, C. W. M. (2014) · Cancer Genetics · doi:10.1016/j.cancergen.2014.04.004 · Cited by 159
Bayona‐Feliú, A., Barroso, S. I., Muñoz, S., & Aguilera, A. (2021) · Nature Genetics · doi:10.1038/s41588-021-00867-2 · Cited by 177
Large-Scale Quality Analysis of Published ChIP-seq Data
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“Our findings are consistent with previous studies showing BRG1 loss affects nucleosome positioning during differentiation of hematopoietic stem cells and in mouse fibroblasts (45, 50).”
ResultGenome accessibility is widely preserved and locally modulated during mitosisPreprint
Hsiung, C. C. ‐., Morrissey, C. S., Udugama, M., Frank, C. L., Keller, C. A., Baek, S., Giardine, B. M., Crawford, G. E., Sung, M., Hardison, R. C., et al. (2014) · Genome Research · doi:10.1101/gr.180646.114 · Cited by 118
“This result is also consistent with the ability of GATA1tobindregionswithrelativelyhighnucleosomeoccupancy (Hu et al. 2011).”
Ciernia, A. V., & Wood, M. A. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.10.002 · Cited by 108
“Similarly, Brg1 knockdown with shRNA alters nucleosome positioning at specific enhancer elements indicating that BAF complexes may act to shift flanking nucleosomes away from these sites to allow access to the underlying DNA during cellular differentiation (Hu et al., 2011).”
Integration of Hi-C and ChIP-seq data reveals distinct types of chromatin linkages
Lan, X., Witt, H. N., Katsumura, K. R., Ye, Z., Wang, Q., Bresnick, E. H., Farnham, P., & Jin, V. X. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks501 · Cited by 115
“Finally, BRG1 is reported as a cofactor of GATA1 (46,47).”
BackgroundInfluentialXue, Y., Meehan, B., Macdonald, E. A., Venneti, S., Wang, X. Q. D., Witkowski, L., Jelinic, P., Kong, T., Martínez, D., Morin, G., et al. (2019) · Nature Communications · doi:10.1038/s41467-018-06958-9 · Cited by 119
Self-citationBarutcu, A. R., Lajoie, B. R., Fritz, A. J., McCord, R. P., Nickerson, J. A., van Wijnen, A. J., Lian, J. B., Stein, J. L., Dekker, J., Stein, G. S., et al. (2016) · Genome Research · doi:10.1101/gr.201624.115 · Cited by 113
Canonical nucleosome organization at promoters forms during genome activationPreprint
Zhang, Y., Vastenhouw, N. L., Feng, J., Fu, K., Wang, C., Ge, Y., Pauli, A., Hummelen, P. V., Schier, A., & Liu, X. (2014) · Genome Research · doi:10.1101/gr.157750.113 · Cited by 104
A High-Resolution Map of Human Enhancer RNA Loci Characterizes Super-enhancer Activities in Cancer
Chen, H., & Liang, H. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.08.020 · Cited by 125
Brg1 modulates enhancer activation in mesoderm lineage commitment
Alexander, J. M., Hota, S. K., He, D. X., Thomas, S., Ho, L., Pennacchio, L. A., & Bruneau, B. G. (2015) · Development · doi:10.1242/dev.109496 · Cited by 101
“BAF and the related yeast SWI-SNF complexes mediate TF recruitment (Hu et al., 2011; Kwon et al., 1994; Takeuchi and Bruneau, 2009), but the functional interplay between SWI-SNF family complexes and histone acetyltransferases is less clear (Agalioti et al.”
InfluentialSwinstead, E. E., Paakinaho, V., Presman, D. M., & Hager, G. L. (2016) · BioEssays · doi:10.1002/bies.201600137 · Cited by 100
“potential enhancers during differentiation of hematopoietic stem cells to erythrocytes [76].”
BackgroundRole of Ldb1 in the transition from chromatin looping to transcription activation
Krivega, I., Dale, R. K., & Dean, A. (2013) · Epigenetics & Chromatin · doi:10.1186/1756-8935-6-s1-p41 · Cited by 99
“Moreover, it is known that GATA1 chromatin occupancy is not dependent on BRG1 on a genome-wide scale (Hu et al. 2011).”
Chromatin signatures of active enhancers
Spicuglia, S., & Vanhille, L. (2012) · Nucleus · doi:10.4161/nucl.19232 · Cited by 127
“Interestingly, distal BRG1 binding is well correlated with the regulation of gene expression and represent a useful marker for identifying distal cis-regulatory regions.(22,49) For instance, during erythroid differentiation, binding of TAL1 to enhancers is facilitated by GATA1 recruitment of BRG1 and”
BackgroundWest, J. A., Cook, A., Alver, B., Stadtfeld, M., Deaton, A., Hochedlinger, K., Park, P. J., Tolstorukov, M., & Kingston, R. (2014) · Nature Communications · doi:10.1038/ncomms5719 · Cited by 95
The histone variant H2A.Z is an important regulator of enhancer activity
Brunelle, M., Nordell-Markovits, A., Rodrigue, S., Lupien, M., Jacques, P., & Gévry, N. Y. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv825 · Cited by 90
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“Studies using chromatin immunoprecipitation with massively parallel sequencing (ChIP-seq) have in turn revealed that -251 A/T disrupts a binding site for several sequence specific DNA-binding transcriptor factors (62, 63).”
Miller, E. L., Hargreaves, D. C., Kadoch, C., Chang, C.-Y., Calarco, J. P., Hodges, H. C., Buenrostro, J. D., Cui, K., Greenleaf, W. J., Zhao, K., et al. (2017) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3384 · Cited by 89
Self-citationINO80 governs superenhancer-mediated oncogenic transcription and tumor growth in melanomaPreprint
Zhou, B., Wang, L., Zhang, S., Bennett, B. D., He, F., Zhang, Y., Xiong, C., Han, L., Diao, L., Li, P., et al. (2016) · Genes & Development · doi:10.1101/gad.277178.115 · Cited by 92
Self-citationMechanisms by which transcription factors gain access to target sequence elements in chromatin
Guertin, M. J., & Lis, J. T. (2012) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2012.11.008 · Cited by 85
“This observation is consistent with the role of TFs in recruiting coactivator complexes that are capable of modifying histone tails and remodeling nucleosomes [24,36–43].”
The Chromatin Fingerprint of Gene Enhancer Elements
Zentner, G. E., & Scacheri, P. C. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.r111.296491 · Cited by 92
The mechanistic basis for chromatin regulation by pioneer transcription factors
Iwafuchi‐Doi, M. (2019) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1427 · Cited by 82
“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).”
BackgroundTranscriptional 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
Trotter, K. W., King, H. A., & Archer, T. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.00230-15 · Cited by 79
“These include BRD7 (51), CBX5 (52), SMARCC1 and SMARCC2 (53), SSXT (54), TAL1 (55, 56), and TMF1 (57).”
A polymorphism in human MR1 is associated with mRNA expression and susceptibility to tuberculosis
Seshadri, C., Thuong, N. T. T., Mai, N. T. H., Bang, N. D., Chau, T. T. H., Lewinsohn, D. M., Thwaites, G. E., Dunstan, S. J., & Hawn, T. R. (2016) · Genes and Immunity · doi:10.1038/gene.2016.41 · Cited by 75
“This further is supported by ChIP-Seq data showing binding with the transcription factor BRG1 28 .”
Wu, W.-S., Morrissey, C. S., Keller, C. A., Mishra, T., Pimkin, M., Blobel, G. A., Weiss, M. J., & Hardison, R. C. (2014) · Genome Research · doi:10.1101/gr.164830.113 · Cited by 84
MACE: model based analysis of ChIP-exo
Wang, L., Chen, J., Wang, C., Uusküla-Reimand, L., Chen, K., Medina-Rivera, A., Young, E. J., Zimmermann, M. T., Yan, H., Sun, Z., et al. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku846 · Cited by 74
“We first aligned peak pairs by the midpoint, then extended by 2 kb upstream and downstream, and measured the nucleosome occupancy level using published MNase-seq data (17).”
MethodInfluentialThe LEAFY floral regulator displays pioneer transcription factor properties
Lai, X., Blanc-Mathieu, R., Grandvuillemin, L., Huang, Y., Stigliani, A., Lucas, J., Thévénon, E., Loue-Manifel, J., Turchi, L., Daher, H., et al. (2021) · bioRxiv · doi:10.1101/2021.01.07.425699 · Cited by 71
Ramachandran, S., & Henikoff, S. (2015) · Science Advances · doi:10.1126/sciadv.1500587 · Cited by 78
“Similarly, enhancers feature high nucleosome remodeler activity (36) and transcription (1), which is also reflected by high nucleosome turnover”
BackgroundPolycomb repressive complex 1 shapes the nucleosome landscape but not accessibility at target genesPreprint
King, H. W., Fursova, N. A., Blackledge, N. P., & Klose, R. J. (2018) · Genome Research · doi:10.1101/gr.237180.118 · Cited by 69
Shapira, S. N., Lim, H., Rajakumari, S., Sakers, A. P., Ishibashi, J., Harms, M. J., Won, K., & Seale, P. (2017) · Genes & Development · doi:10.1101/gad.294405.116 · Cited by 79
“Many lineage-instructive transcription factors, including EBF1, MYOD, and GATA1, recruit the BAF complex to tissue-specific promoters and enhancers (de la Serna et al. 2005; Gao et al. 2009; Hu et al. 2011).”
Tissue-specific SMARCA4 binding at active and repressed regulatory elements during embryogenesisPreprint
Attanasio, C., Nord, A. S., Zhu, Y., Blow, M. J., Biddie, S. C., Mendenhall, E. M., Dixon, J. R., Wright, C., Hosseini, R., Akiyama, J. A., et al. (2014) · Genome Research · doi:10.1101/gr.168930.113 · Cited by 63
“Recent in vitro observations indicate that SMARCA4 binding occurs at distal regulatory elements, including at enhancers (De et al. 2011; Hu et al. 2011; Rada-Iglesias et al. 2011).”
BackgroundNucleosome positioning: resources and tools online
Teif, V. B. (2015) · Briefings Bioinform. · doi:10.1093/bib/bbv086 · Cited by 66
“GSE35586 CD36+ cells with and without BRG1 knockdown [68].”
BackgroundSWI/SNF Complex Mutations in Gynecologic Cancers: Molecular Mechanisms and Models
Wang, Y., Hoang, L. N., Ji, J. X. Y., & Huntsman, D. D. (2020) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-012418-012917 · Cited by 78
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Wakabayashi, A., Ulirsch, J. C., Ludwig, L. S., Fiorini, C., Yasuda, M., Choudhuri, A., McDonel, P. E., Zon, L. I., & Sankaran, V. G. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1521754113 · Cited by 59
Accurate Prediction of Inducible Transcription Factor Binding Intensities In Vivo
Guertin, M. J., Martins, A. L., Siepel, A., & Lis, J. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002610 · Cited by 63
“For instance, both GR and GATA1 interact with the nucleosome remodeling complex Swi/Snf [32,33].”
BackgroundAndrades, Á., Peinado, P., Álvarez-Pérez, J. C., Sanjuán‐Hidalgo, J., García, D. J., Arenas, A. M., Matia‐González, A. M., & Medina, P. P. (2023) · Molecular Cancer · doi:10.1186/s12943-023-01736-8 · Cited by 81
Chen, W., Liu, Y., Zhu, S., Green, C. D., Wei, G., & Han, J. J. (2014) · Nature Communications · doi:10.1038/ncomms5909 · Cited by 74
Patel, B., Kang, Y., Cui, K., Litt, M. D., Riberio, M. S. J., Deng, C., Salz, T., Casada, S., Fu, X., Qiu, Y., et al. (2013) · Leukemia · doi:10.1038/leu.2013.158 · Cited by 65
Self-citationSen, M., Wang, X., Hamdan, F. H., Rapp, J., Eggert, J., Kosinsky, R. L., Wegwitz, F., Kutschat, A. P., Younesi, F. S., Gaedcke, J., et al. (2019) · Clinical Epigenetics · doi:10.1186/s13148-019-0690-5 · Cited by 61
Păun, O., Tan, Y. X., Patel, H., Strohbuecker, S., Ghanate, A. D., Gigli, C. C., Sopeña, M. L., Gerontogianni, L., Goldstone, R. J., Ang, S., et al. (2023) · Genes & Development · doi:10.1101/gad.350269.122 · Cited by 62
“…of pioneer factors to open chromatin, including physical eviction of nucleosomes by the pioneer factor – DNA interaction (Cirillo et al. 2002; Michael et al. 2020) and/or interaction with other transcription factors and proteins with chromatin remodeling capacity (Hu et al. 2011; Theodorouetal.”
BackgroundInfluentialDynamic regulation of epigenomic landscapes during hematopoiesis
Abraham, B. J., Cui, K., Tang, Q., & Zhao, K. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-193 · Cited by 59
“We calculated RPKM values for all RefSeq transcripts not on the Y chromosome using a previously described method [8].”
BackgroundMethodResultInfluentialSelf-citationUlirsch, J. C., Lacy, J. N., An, X., Mohandas, N., Mikkelsen, T. S., & Sankaran, V. G. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004890 · Cited by 49
“For each species, we compiled chromatin immunoprecipitation high-throughput sequencing (ChIP-seq) data sets of histone modifications (H3K4me1, H3K4me2, H3K4me3, H3K9ac, H3K27me3, H3K36me3) and master TFs of erythropoiesis (GATA1, TAL1, KLF1, NFE2) at the ProE stage of erythroid differentiation (S1 and S2 Table) [15–25…”
MethodLei, I., West, J. A., Yan, Z., Gao, X., Fang, P., Dennis, J., Gnatovskiy, L., Wang, W., Kingston, R., & Wang, Z. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.637389 · Cited by 50
“Consistent with previous reports (25, 26), nucleosomes were well positioned at the binding sites of CTCF and the REST repressor protein in both WT and BAF250a KO ES cells (Fig.”
ResultThe SWI/SNF tumor suppressor complex
Lu, P., & Roberts, C. W. M. (2013) · Nucleus · doi:10.4161/nucl.26654 · Cited by 52
“As we evaluated cells in a uniform condition, our experiments would not detect such changes, although Hu and colleagues performed such an evaluation and identified changes in transcription factor binding at enhancers upon BRG1 mutation.(30) Collectively, while our experiments implicate the SWI/SNF complex in establish…”
ResultATP-Dependent Chromatin Remodeling During Cortical Neurogenesis
Sokpor, G., Castro-Hernández, R., Rosenbusch, J., Staiger, J. F., & Tuoc, T. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00226 · Cited by 64
“…dimers and eventually the expulsion of the complete histone octamer, resulting in nucleosome disassembly (Engeholm et al., 2009) and creating euchromatin state that supports gene expression (Hara and Sancar, 2002; Gong et al., 2006; Ho et al., 2009a; Hu et al., 2011; Tolstorukov et al., 2013).”
BackgroundLi, Y., Schulz, V., Deng, C., Li, G., Shen, Y., Tusi, B. K., Ma, G., Stees, J. R., Qiu, Y., Steiner, L. A., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw327 · Cited by 45
“To understand how USF1, SETD1A and NURF interact to regulate erythroid chromatin dynamics and gene transcription, we performed ChIP (chromatin immunoprecipitation)-seq in human primary erythroid cells and compared these results to MNase (micrococcal nuclease)-seq data (24).”
InfluentialSelf-citationMechanism governing a stem cell-generating cis -regulatory element
Sanalkumar, R., Johnson, K. D., Gao, X., Boyer, M. E., Chang, Y., Hewitt, K. J., Zhang, J., & Bresnick, E. H. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400065111 · Cited by 46
Kult, S., Olender, T., Osterwalder, M., Markman, S., Leshkowitz, D., Krief, S., Blecher-Gonen, R., Ben-Moshe, S., Farack, L., Keren-Shaul, H., et al. (2020) · bioRxiv · doi:10.1101/2020.01.29.924654 · Cited by 47
“It is clear that we cannot exclude the possibility that an active mechanism, such as the SWI/SNF remodeling complexes, opens the chromatin structure in bi-fated cells to allow attachment cell dual behavior [42].”
BackgroundBET-ting on chromatin-based therapeutics for heart failure
Haldar, S. M., & McKinsey, T. A. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2014.05.002 · Cited by 51
“Genome-wide studies detailing BRG1 enrichment in the heart during pathological stress and BRG1-dependent gene expression will be informative, particularly to assess nucleosome remodeling at critical enhancer loci [32].”
BackgroundFunctional Genomics of the 9p21.3 Locus for Atherosclerosis: Clarity or Confusion?
Chen, H.-H., Almontashiri, N. A. M., Antoine, D., & Stewart, A. F. R. (2014) · Current Cardiology Reports · doi:10.1007/s11886-014-0502-7 · Cited by 45
INO80 is required for oncogenic transcription and tumor growth in non-small cell lung cancer
Zhang, S., Zhou, B., Wang, L., Li, P., Bennett, B. D., Snyder, R., Garantziotis, S., Fargo, D. C., Cox, A. D., Chen, L., et al. (2016) · Oncogene · doi:10.1038/onc.2016.311 · Cited by 52
Self-citationThe role of chromatin dynamics in immune cell development
Winter, D. R., & Amit, I. (2014) · Immunological Reviews · doi:10.1111/imr.12200 · Cited by 44
“In many regions, the nucleosomes may merely be shifted upon activation (8, 32), but in certain cases entire nucleosomes may be evicted by pioneer factors or CRs.”
BackgroundInfluentialOrlando, K. A., Nguyen, V. Q., Raab, J. R., Walhart, T. A., & Weissman, B. E. (2019) · Expert Review of Anticancer Therapy · doi:10.1080/14737140.2019.1605905 · Cited by 55
Xu, J., Li, J., Zhang, T., Jiang, H., Ramakrishnan, A., Fritzsch, B., Shen, L., & Xu, P. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2025196118 · Cited by 52
SWI/SNF chromatin remodeling controls Notch-responsive enhancer accessibility
Pillidge, Z., & Bray, S. (2018) · bioRxiv · doi:10.15252/embr.201846944 · Cited by 41
“Similarly, SWI/SNF remodelers establish accessible enhancers in fibroblasts following their recruitment by lineage-specific transcription factors and FOS/JUN [17] and function to shift nucleosomes away from GATA1 sites in hematopoietic stem cells allowing TAL1-dependent transcription [18].”
InfluentialSmall-molecule and CRISPR screening converge to reveal RTK dependencies in pediatric rhabdoid tumors
Oberlick, E. M., Rees, M., Seashore-Ludlow, B., Vazquez, F., Nelson, G. M., Dharia, N., Weir, B., Tsherniak, A., Ghandi, M., Krill-Burger, J., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.07.021 · Cited by 40
Chromatin Remodeler Mutations in Human Cancers: Epigenetic Implications
Giles, K. A., Phan, L., Clark, S. J., & Taberlay, P. C. (2014) · Epigenomics · doi:10.2217/epi.14.37 · Cited by 40
Towards an understanding of cell-specific functions of signal-dependent transcription factors
Zhang, D. X., & Glass, C. K. (2013) · Journal of Molecular Endocrinology · doi:10.1530/jme-13-0216 · Cited by 46
“For example, during hematopoietic stem cell differentiation, nucleosome remodeling by the ATP-dependent, switch/sucrose nonfermentable (SWI/SNF) chromatin-remodeling complex allows for transcription factor binding at erythroid LDTF binding sites (Hu et al. 2011).”
BackgroundKim, D. S., Burt, A., Ranchalis, J., Jarvik, E. R., Rosenthal, E. A., Hatsukami, T. S., Furlong, C. E., & Jarvik, G. P. (2013) · Journal of Lipid Research · doi:10.1194/jlr.p035238 · Cited by 37
Domain-adaptive neural networks improve cross-species prediction of transcription factor bindingPreprint
Cochran, K., Srivastava, D., Shrikumar, A., Balsubramani, A., Hardison, R. C., Kundaje, A. B., & Mahony, S. (2022) · Genome Research · doi:10.1101/gr.275394.121 · Cited by 42
“…literature for ChIP-seq data targeting orthologous TFs in erythroid progenitor, megakaryocyte, macrophage, and hematopoietic progenitor cell types (Hu et al. 2011; Tijssen et al. 2011; Pham et al. 2012; Beck et al. 2013; Kaikkonen et al. 2013; Pencovich et al. 2013; Yue et al. 2014; Goode et al.…”
Shi, X., Wang, Q., Gu, J., Xuan, Z., & Wu, J. I. (2016) · Oncogene · doi:10.1038/onc.2016.108 · Cited by 50
Transcriptional and Epigenetic Control of Mammalian Olfactory Epithelium Development
Sokpor, G., Abbas, E., Rosenbusch, J., Staiger, J. F., & Tuoc, T. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-0987-y · Cited by 41
“maintenance of the transcriptomic landscape [140, 141].”
SWI/SNF (BAF) Complexes: Guardians of the Epigenome
Mathur, R., & Roberts, C. (2018) · Annual Review of Cancer Biology · doi:10.1146/annurev-cancerbio-030617-050151 · Cited by 36
“SWI/SNF complexes have now been identified at enhancers in several developmental contexts, including in erythrocyte (Hu et al. 2011) and oligodendrocyte differentiation (Yu et al. 2013), mesoderm lineage commitment (Alexander et al. 2015), and B cell fate specification (Bossen et al. 2015).”
BackgroundGATA Factor-Mediated Gene Regulation in Human Erythropoiesis
Romano, O., Petiti, L., Félix, T., Meneghini, V., Portafax, M., Antoniani, C., Amendola, M., Bicciato, S., Peano, C., & Miccio, A. (2020) · iScience · doi:10.1016/j.isci.2020.101018 · Cited by 40
Emerging Themes in Mechanisms of Tumorigenesis by SWI/SNF Subunit Mutation
Jones, C. A., Tansey, W. P., & Weissmiller, A. M. (2022) · Epigenetics Insights · doi:10.1177/25168657221115656 · Cited by 39
Acute depletion of BRG1 reveals its primary function as an activator of transcription
Ren, G., Ku, W. L., Ge, G.-Z., Hoffman, J. A., Kang, J. Y., Tang, Q.-S., Cui, K.-R., He, Y., Guan, Y., Gao, B., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-48911-z · Cited by 32
Self-citationGATA factor transcriptional activity: Insights from genome‐wide binding profiles
Romano, O., & Miccio, A. (2019) · IUBMB Life · doi:10.1002/iub.2169 · Cited by 38
“…al. 2016 Erythrocyte precursors 8 15 Canver et al. 2017; Pinello et al. 2014; Su et al. 2013; Kang et al. 2012; Xu et al. 2012; Trompouki et al. 2011; Hu et al. 2011 Megakaryocytes 1 1 Tijssen et al. 2011 Erythroleukemia cell lines 5 12 Huang et al. 2018; Trompouki et al. 2011; Pencovich et al.…”
BackgroundInfluentialRen, J.-K., Finney, R., Ni, K., Cam, M., & Muegge, K. (2019) · Epigenetics · doi:10.1080/15592294.2019.1582275 · Cited by 32
“SNF2 homologs that remodel nucleosomes, have been shown to enhance chromatin access and facilitate transcription factor binding, such as Tal1, Stat3 and glucocorticoid receptor [55,63,64].”
BackgroundPulivarthy, S., Lion, M., Kuzu, G., Matthews, A., Borowsky, M. L., Morris, J. W., Kingston, R., Dennis, J., Tolstorukov, M., & Oettinger, M. (2016) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1605543113 · Cited by 32
Brg1 coordinates multiple processes during retinogenesis and is a tumor suppressor in retinoblastoma
Aldiri, I., Ajioka, I., Xu, B., Zhang, J., Chen, X. '., Benavente, C. A., Finkelstein, D., Johnson, D. A., Akiyama, J. A., Pennacchio, L. A., et al. (2015) · Development · doi:10.1242/dev.124800 · Cited by 35
“It has been shown previously that Brg1 can play a role in nucleosome positioning at promoters (Alexander et al., 2015; Hu et al., 2011) and this may alter gene expression.”
BackgroundDNase-seq predicts regions of rotational nucleosome stability across diverse human cell typesPreprint
Winter, D., Song, L.-Y., Mukherjee, S., Furey, T., & Crawford, G. E. (2013) · Genome Research · doi:10.1101/gr.150482.112 · Cited by 31
“Nucleosomes that are crucial in regulating gene expression may shift at this period to maintain orientation as they allow TF access in response to cell conditions (Hu et al. 2011).”
BackgroundBozhilov, Y. K., Downes, D., Telenius, J., Oudelaar, A. M., Olivier, E. N., Mountford, J., Hughes, J., Gibbons, R., & Higgs, D. (2021) · Nature Communications · doi:10.1038/s41467-021-23980-6 · Cited by 29
Orlando, K. A., Douglas, A. K., Abudu, A., Wang, Y., Tessier‐Cloutier, B., Su, W., Peters, A., Sherman, L. S., Moore, R., Nguyen, V. Q., et al. (2020) · eLife · doi:10.7554/elife.59073 · Cited by 53
The Hematopoietic Stem and Progenitor Cell Cistrome
Hewitt, K. J., Johnson, K. D., Gao, X., Keleş, S., & Bresnick, E. H. (2016) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2016.01.002 · Cited by 29
Iglesias-Platas, I., Court, F., Camprubí, C., Sparago, A., Guillaumet-Adkins, A., Martín-Trujillo, Á., Riccio, A., Moore, G., & Monk, D. (2013) · Nucleic Acids Research · doi:10.1093/nar/gks1355 · Cited by 28
“Using two published data sets (29,30), we identified two regions of strong CTCF binding, one 5 kb downstream of the PLAGL1-DMR and between this and the non-imprinted P2 promoter, and the other within the last exon of PLAGL1.”
Background
Metadata
- Authors
- Hu, G., Schones, D. E., Cui, K., Ybarra, R., Northrup, D., Tang, Q., Gattinoni, L., Restifo, N. P., Huang, S., & Zhao, K.
- Affiliations
- National Institutes of Health (US)
- University of Florida Health (US)
- ORCID
- Venue
- Genome Research
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2011-07-27
- Volume
- 21
- Issue
- 10
- Pages
- 1650-1658
- ISSN
- 1088-9051 (ISSN-L)
- PMC
- PMC3202282
- OpenAlex
- W2119037385
- Cited by
- 186
- References
- 0
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 6 · 2023: 4 · 2022: 10 · 2021: 19 · 2020: 12 · 2019: 14 · 2018: 15 · 2017: 11 · 2016: 18 · 2015: 11 · 2014: 25 · 2013: 15 · 2012: 16
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genome Research (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- National Institutes of Health
- National Heart, Lung, and Blood Institute (R01HL091929, K22HL101950, R01HL090589)
- NHLBI Division of Intramural Research
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- SMARCA4, BAF chromatin remodeling complex, nucleosome positioning, enhancers, GATA-1, TAL1, hematopoietic stem cell differentiation, erythropoiesis, transcription factor binding, chromatin regulation
- MeSH terms
- T-Cell Acute Lymphocytic Leukemia Protein 1, CCCTC-Binding Factor, Binding Sites, Cell Differentiation, Cells, Cultured, DNA Helicases, Enhancer Elements, Genetic, Gene Expression Regulation, Hematopoiesis, Hematopoietic Stem Cells, Humans, Nuclear Proteins, Nucleosomes, Organ Specificity, Proto-Oncogene Proteins, Repressor Proteins, Transcription Factors, Transcription, Genetic, Chromatin Assembly and Disassembly, Chromatin Immunoprecipitation, GATA1 Transcription Factor, Basic Helix-Loop-Helix Proteins, Primary Cell Culture
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