Long-Range Enhancer Interactions Are Prevalent in Mouse Embryonic Stem Cells and Are Reorganized upon Pluripotent State Transition
Open accessAbstract
Transcriptional enhancers, including super-enhancers (SEs), form physical interactions with promoters to regulate cell-type-specific gene expression. SEs are characterized by high transcription factor occupancy and large domains of active chromatin, and they are commonly assigned to target promoters using computational predictions. How promoter-SE interactions change upon cell state transitions, and whether transcription factors maintain SE interactions, have not been reported. Here, we used promoter-capture Hi-C to identify promoters that interact with SEs in mouse embryonic stem cells (ESCs). We found that SEs form complex, spatial networks in which individual SEs contact multiple promoters, and a rewiring of promoter-SE interactions occurs between pluripotent states. We also show that long-range promoter-SE interactions are more prevalent in ESCs than in epiblast stem cells (EpiSCs) or Nanog-deficient ESCs. We conclude that SEs form cell-type-specific interaction networks that are partly dependent on core transcription factors, thereby providing insights into the gene regulatory organization of pluripotent cells.
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3C-derived methods have detected multitudes of enhancer-promoter loops in many human and mouse cell types.
“These enrichment methods have detected multitudes of enhancer–promoter loops in many human and mouse cell types [243, 286–291].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [288]
The Results section ('SEs Are Highly Interactive Hubs in ESCs'; page unavailable) reports that the authors used a 3C-based method to detect numerous enhancer–promoter interactions in mouse embryonic stem cells. This supports the mouse-cell example, but this paper does not establish the claim across many human and mouse cell types. (LLM, conf=0.85)
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Cites
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Skeletal muscle enhancer interactions identify genes controlling whole-body metabolism
Williams, K., Ingerslev, L. R., Bork‐Jensen, J., Wohlwend, M., Hansen, A. N., Small, L., Ribel‐Madsen, R., Astrup, A. V., Pedersen, O. B., Auwerx, J. H., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16537-6 · Cited by 39 · see citing works
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“However, since SEs can trigger long-distance interactions (9,10), the underlying influence of SEs accompanying HPV integration is still underestimated.”
BackgroundJMJD3 acts in tandem with KLF4 to facilitate reprogramming to pluripotency
Huang, Y., Zhang, H., Wang, L., Tang, C., Qin, X., Wu, X., Pan, M., Tang, Y., Yang, Z., Babarinde, I. A., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18900-z · Cited by 44 · see citing works
LncRNA Platr22 promotes super-enhancer activity and stem cell pluripotency
Yan, P., Lu, J. Y., Niu, J., Gao, J. T., Zhang, M. Q., Yin, Y., & Shen, X. (2020) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjaa056 · Cited by 31 · see citing works
“Moreover, chromatin interaction maps generated by both paired-end tagging (ChIA-PET) of RNA Pol II and promoter capture Hi-C suggested that the SE locus interacts with the promoter region of ZFP281 (Zhang et al., 2013; Novo et al., 2018).”
BackgroundSuper-enhancers complexes zoom in transcription in cancer
Wang, M., Chen, Q., Wang, S., Xie, H., Liu, J., Huang, R., Xiang, Y., Jiang, Y., Tian, D., & Bian, E. (2023) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-023-02763-5 · Cited by 49 · see citing works
“(2) When a SE span is short, core sites or clear, and because abnormal SE function is caused by factors such as mutation, SE function can be investigated by reconstructing the local epigenetic marks [15].”
BackgroundDynamic 3D Chromatin Reorganization during Establishment and Maintenance of Pluripotency
Pelham‐Webb, B., Murphy, D., & Apostolou, E. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.10.012 · Cited by 43 · see citing works
“Another interesting direction would be to capture the dynamic formation of other PSC-characteristic structures, such as the reported extremely long-range chromatin contacts (Joshi et al., 2015; Novo et al., 2018) and the clustering of PRC-mediated bivalent genes (Denholtz et al.”
BackgroundBell, E., Curry, E. W., Megchelenbrink, W., Jouneau, L., Brochard, V., Tomaz, R. A., Mau, K. H. T., Atlasi, Y., de Souza, R. A., Marks, H., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-14916-7 · Cited by 49 · see citing works
Deep learning at base-resolution reveals motif syntax of the cis-regulatory codePreprint
Avsec, Ž., Weilert, M., Shrikumar, A., Alexandari, A. M., Krueger, S., Dalal, K., Fropf, R., McAnany, C. E., Gagneur, J., Kundaje, A., et al. (2019) · bioRxiv · doi:10.1101/737981 · Cited by 36 · see citing works
“At individual enhancers such as those associated with Lefty1 (56), Zfp281 (57), and Sall1 (58, 59) genes (Figure 1D and Figure S1C), the predicted and observed ChIP-nexus profiles were noticeably similar with highly concordant summits of footprints.”
Chovanec, P., Collier, A. J., Krueger, C., Várnai, C., Semprich, C. I., Schoenfelder, S., Corcoran, A. E., & Rugg‐Gunn, P. J. (2021) · Nature Communications · doi:10.1038/s41467-021-22201-4 · Cited by 48 · see citing works
Self-citationDetecting chromosomal interactions in Capture Hi-C data with CHiCAGO and companion tools
Freire-Pritchett, P., Ray-Jones, H., Rosa, M. D., Eijsbouts, C., Orchard, W. R., Wingett, S., Wallace, C., Cairns, J. M., Spivakov, M., & Malysheva, V. (2021) · Nature Protocols · doi:10.1038/s41596-021-00567-5 · Cited by 34 · see citing works
Self-citationNavigating the crowd: visualizing coordination between genome dynamics, structure, and transcription
Shaban, H. A., Barth, R., & Bystricky, K. (2020) · Genome biology · doi:10.1186/s13059-020-02185-y · Cited by 28 · see citing works
“3 (B)), in particular, at super-enhancers [124, 125].”
CRUP: a comprehensive framework to predict condition-specific regulatory units
Ramisch, A., Heinrich, V., Glaser, L. V., Fuchs, A., Yang, X., Benner, P., Schöpflin, R., Li, N., Kinkley, S., Römer-Hillmann, A., et al. (2019) · Genome biology · doi:10.1186/s13059-019-1860-7 · Cited by 27 · see citing works
Song, W., Sharan, R., & Ovcharenko, I. (2019) · Genome Biology · doi:10.1186/s13059-019-1808-y · Cited by 28 · see citing works
Du, Z., Wen, X., Wang, Y., Jia, L., Zhang, S., Liu, Y., Zhou, L., Li, H. Z., Wang, Y., Wang, C., et al. (2021) · Genome biology · doi:10.1186/s13059-021-02444-6 · Cited by 28 · see citing works
“These intrachromosomal interactions have been demonstrated by several technologies, including 3C, Hi-C, and ChIA-PET [28].”
MethodChromatin regulation and dynamics in stem cells
Klein, D. C., & Hainer, S. J. (2019) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2019.11.002 · Cited by 39 · see citing works
“Super-enhancers are prevalent in ES cells, and are reorganized upon exit from a pluripotent state to facilitate cellular differentiation and specification, as shown through promoter capture experiments (Novo et al., 2018).”
BackgroundEpigenetic Regulation of Transition Among Different Pluripotent States: Concise Review
Geng, T., Zhang, D.-H., & Jiang, W. (2019) · Stem Cells · doi:10.1002/stem.3064 · Cited by 26 · see citing works
3D genome organization links non-coding disease-associated variants to genes
Orozco, G., Schoenfelder, S., Walker, N. J., Eyre, S., & Fraser, P. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.995388 · Cited by 25 · see citing works
“Promoter-Capture Hi-C (PCHi-C) specifically enriches promoter-containing ligation products from Hi-C libraries, allowing capture of promoter interacting regions for all (>22 K) promoters across the mouse genome (Schoenfelder et al., 2015a; Sahlén et al., 2015; Wilson et al., 2016; Siersbæk et al., 2017; Comoglio et al…”
BackgroundSelf-citationGiusti‐Rodríguez, P., & Sullivan, P. F. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/406330 · Cited by 72 · see citing works
SOX2 transcription factor binding and function
Hagey, D. W., Bergsland, M., & Muhr, J. (2022) · Development · doi:10.1242/dev.200547 · Cited by 28 · see citing works
Laverré, A., Tannier, E., & Necsulea, A. (2021) · bioRxiv · doi:10.1101/2021.02.26.432473 · Cited by 24
Kaneko, S., Takasawa, K., Asada, K., Shiraishi, K., Ikawa, N., Machino, H., Shinkai, N., Matsuda, M., Masuda, M., Adachi, S., et al. (2024) · Molecular Cancer · doi:10.1186/s12943-024-02035-6 · Cited by 25 · see citing works
“However, it remains unclear whether these phenomena are genuinely attributable to epigenetic abnormalities or result from genomic alterations [10, 14].”
BackgroundA genome-wide relay of signalling-responsive enhancers drives hematopoietic specification
Edginton-White, B., Maytum, A., Kellaway, S., Goode, D., Keane, P., Pagnuco, I., Assi, S. A., Ames, L., Clarke, M., Cockerill, P., et al. (2022) · bioRxiv · doi:10.1038/s41467-023-35910-9 · Cited by 22 · see citing works
Auxin-degron system identifies immediate mechanisms of OCT4
Bates, L. E., Alves, M. R. P., & Silva, J. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.05.016 · Cited by 28 · see citing works
Genetic, epigenetic and genomic effects on variation of gene expression among grape varieties.
Magris, G., Gaspero, G. D., Marroni, F., Zenoni, S., Tornielli, G. B., Celii, M., Paoli, E. D., Pezzotti, M., Conte, F., Paci, P., et al. (2019) · The Plant Journal · doi:10.1111/tpj.14370 · Cited by 21
Fine mapping chromatin contacts in capture Hi-C data
Eijsbouts, C., Burren, O., Newcombe, P., & Wallace, C. (2018) · BMC Genomics · doi:10.1186/s12864-018-5314-5 · Cited by 21 · see citing works
“Conversely, the same enhancer region can appear to interact with promoters of multiple genes [9, 10], while it remains unclear whether this reflects coregulation of these genes [11].”
BackgroundSuper enhancers as master gene regulators in the pathogenesis of hematologic malignancies
Debek, S. M., & Juszczyński, P. (2022) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2022.188697 · Cited by 21 · see citing works
Khaminets, A., Ronnen-Oron, T., Baldauf, M., Meier, E., & Jasper, H. (2020) · eLife · doi:10.7554/elife.48160 · Cited by 22 · see citing works
“These functions are dependent on recruitment of specific transcription factors and execution of particular transcriptional programs (Schaaf et al., 2013; Merkenschlager and Nora, 2016; Novo et al., 2018).”
BackgroundTranscription-coupled changes in genomic region proximities during transcriptional bursting
Ohishi, H., Shinkai, S., Owada, H., Fujii, T., Hosoda, K., Onami, S., Yamamoto, T., Ohkawa, Y., & Ochiai, H. (2024) · Science Advances · doi:10.1126/sciadv.adn0020 · Cited by 21 · see citing works
Chromatin architecture is a flexible foundation for gene expression
Misteli, T., & Finn, E. H. (2021) · Nature Genetics · doi:10.1038/s41588-021-00813-2 · Cited by 18
Kim, H. J., Osteil, P., Humphrey, S. J., Cinghu, S., Oldfield, A., Patrick, E., Wilkie, E. E., Peng, G., Suo, S., Jothi, R., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz1179 · Cited by 17 · see citing works
“Importantly, the rewiring of long-range interactions has been found to be a hallmark in pluripotent state transition in ESCs (62).”
BackgroundThe SWI/SNF ATP-dependent chromatin remodeling complex in cell lineage priming and early development
Saha, D., Animireddy, S., & Bartholomew, B. (2024) · Biochemical Society Transactions · doi:10.1042/bst20230416 · Cited by 27 · see citing works
Khan, A. H., Bagley, J. R., LaPierre, N., Gonzalez‐Figueroa, C., Spencer, T. C., Choudhury, M., Xiao, X. G., Eskin, E., Jentsch, J. D., & Smith, D. J. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112856 · Cited by 12 · see citing works
“The distance between the cis eQTLs and their corresponding genes was 0.63Mb ± 0.005 Mb, averaged across brain regions and infusates, consistent with the known linkage disequilibrium structure of the HMDP (Figures 4B and S6D).”
InfluentialArrastia, M. V., Jachowicz, J. W., Ollikainen, N., Curtis, M. S., Lai, C., Quinodoz, S. A., Selck, D. A., Guttman, M., & Ismagilov, R. F. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.11.242081 · Cited by 15 · see citing works
GOPHER: Generator Of Probes for capture Hi-C Experiments at high Resolution
Hansen, P., Ali, S., Blau, H., Danis, D., Hecht, J., Kornak, U., Lupiáñez, D. G., Mundlos, S., Steinhaus, R., & Robinson, P. (2019) · BMC Genomics · doi:10.1186/s12864-018-5376-4 · Cited by 15 · see citing works
Enhancer-Promoter Communication: It’s Not Just About Contact
Wurmser, A., & Basu, S. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.867303 · Cited by 17 · see citing works
“Such compartments could facilitate establishment of the multi-way regulatory networks between promoters and cis-regulatory elements observed during development (Sanyal et al., 2012; Schoenfelder et al., 2015; Freire-Pritchett et al., 2017; Stevens et al., 2017; Novo et al., 2018; Madsen et al., 2020; Chovanec et al.,…”
BackgroundDistinct transcription kinetics of pluripotent cell states
Shao, R., Kumar, B., Lidschreiber, K., Lidschreiber, M., Cramer, P., & Elsässer, S. (2022) · Molecular Systems Biology · doi:10.15252/msb.202110407 · Cited by 13 · see citing works
Molecular Basis of the Function of Transcriptional Enhancers
Ibragimov, A. N., Bylino, O. V., & Shidlovskii, Y. V. (2020) · Cells · doi:10.3390/cells9071620 · Cited by 14 · see citing works
Visualising three-dimensional genome organisation in two dimensions
Ing‐Simmons, E., & Vaquerizas, J. M. (2019) · Development · doi:10.1242/dev.177162 · Cited by 12 · see citing works
“These typically represent looping interactions such as those derived from ChIA-PET or HiChIP data, significant interactions from capture Hi-C or 4C-seq, or CTCF-CTCF loops (Fullwood et al., 2009; Lopes Novo et al., 2018), but could also represent significant changes between two datasets.”
BackgroundHigh‐resolution three‐dimensional chromatin profiling of the Chinese hamster ovary cell genome
Bevan, S., Schoenfelder, S., Young, R. J., Zhang, L., Andrews, S. R., Fraser, P., & O'Callaghan, P. M. (2020) · Biotechnology and Bioengineering · doi:10.1002/bit.27607 · Cited by 9 · see citing works
“, 2016), and uncover the importance of long‐range enhancer contacts in mouse embryonic stem cell pluripotency (Novo et al., 2018).”
BackgroundSelf-citationGarate, X., Gómez-García, P. A., Fernández, M., Angles, M. C., Zhu, C., Castells-García, Á., Ed-daoui, I., Martin, L., Ochiai, H., Neguembor, M. V., et al. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae476 · Cited by 6 · see citing works
“For example, long-range interactions be-tween super-enhancers and promoters are rewired ( 3 ), there is a shift between regions located in A / B compartments and their replication timing ( 64 ) and several epigenetic modifications are reprogrammed ( 51 ).”
BackgroundByers, C., Spruce, C., Fortin, H. J., Hartig, E. I., Czechanski, A., Munger, S. C., Reinholdt, L., Skelly, D. A., & Baker, C. L. (2021) · EMBO Journal · doi:10.15252/embj.2021109445 · Cited by 7 · see citing works
“Reconfiguration of chromatin accompanies, and often precedes (Bernstein et al , 2006; Bonifer & Cockerill, 2017), transcriptomic changes during cell state transitions (Chen & Dent, 2014; Factor et al , 2014; Novo et al , 2018; Pe z kowska et al , 2018; Yadav et al , 2018).”
A Tale of Two States: Pluripotency Regulation of Telomeres
Novo, C. L. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.703466 · Cited by 7 · see citing works
Self-citationRegulation of Chromatin Organization in Cell Stemness: The Emerging Role of Long Non-coding RNAs
Dehghani, H. (2021) · Stem Cell Reviews and Reports · doi:10.1007/s12015-021-10209-8 · Cited by 6 · see citing works
Manipulating the Mediator complex to induce naïve pluripotency
Lynch, C. J., Bernad, R., Calvo, I., & Serrano, M. (2020) · Experimental Cell Research · doi:10.1016/j.yexcr.2020.112215 · Cited by 8 · see citing works
“Indeed, there is evidence that nascent germ layer programs rely on relatively weak enhancers which are not yet fully established [70,82,114,115], while the”
BackgroundHockings, C., Poudel, C., Feeney, K. A., Novo, C. L., Hamouda, M., Mela, I., Fernandez-Antoran, D., Vallejo-Ramirez, P. P., Rugg-Gunn, P., Chalut, K., et al. (2020) · bioRxiv · doi:10.1101/2020.05.02.073536 · Cited by 6
“Therefore, this decompacted chromatin state may be part of the same formative period (57) whereby naïve ES cells must first decompact to reach a transition state where chromatin is accessible to a gene regulatory switch to gain competence for lineage commitment (14, 21, 32, 62).”
BackgroundSelf-citationPerspectives on the use of super-enhancers as a defining feature of cell/tissue-identity genes
Dubois‐Chevalier, J., Dubois, V., Staels, B., Lefèbvre, P., & Eeckhoute, J. (2020) · Epigenomics · doi:10.2217/epi-2019-0290 · Cited by 5 · see citing works
Camerino, M. J., Chang, W. K., & Cvekl, A. (2024) · Epigenetics & Chromatin · doi:10.1186/s13072-024-00533-x · Cited by 6 · see citing works
“This is consistent with previous studies, showing that these interactions are reorganized after individual cell-fate specific differentiation programs [69–71].”
ResultPandey, N., Chandra, O., Mishra, S., & Kumar, V. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.738194 · Cited by 4 · see citing works
“Previously Novo et al. (2018) highlighted the significant role of long-range interactions ( > 800 kbp) among promoters and super-enhancers in poising and activation of embryonic stem cells (ESCs).”
BackgroundInfluentialLiu, X., Zhao, B., Shaw, T. I., Fridley, B., Duckett, D., Tan, A., & Teng, M. (2021) · bioRxiv · doi:10.1093/nar/gkac141 · Cited by 4 · see citing works
“Recent studies further showed that, beyond the elevated activity, the inside mechanics of SEs are also critical in defining their prominent roles in gene regulation, known as multi-promoter targeting and long-range interactions(5-8).”
BackgroundRazin, S., Ulianov, S., & Gavrilov, A. (2019) · Molecular Biology · doi:10.1134/s0026893319060153 · Cited by 4 · see citing works
Giammartino, D. C. D., Liu, Y.-Y., Kloetgen, A., Polyzos, A., Kim, D., Stadtfeld, M., Tsirigos, A., & Apostolou, E. (2018) · bioRxiv · doi:10.1101/382473 · Cited by 3 · see citing works
Qi, M., Wang, B.-W., Liao, H., Xu, Y., Dong, L., Xu, L., Xia, Y., Jiang, X.-C., Ling, S.-Z., & Qin, J.-Z. (2025) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2025.108501 · Cited by 3
“…studies have shown that EpiSCs show substantially higher levels of Sox3 compared with those in ESCs, while Sox2 mRNA levels in EpiSCs are lower than in ESCs (29, 39, 42 – 44), indicating that the balance between Sox2 and Sox3 dictates the maintenance and transition among these pluripotent states.”
Nanoscale dynamics of enhancer–promoter interactions during exit from pluripotency
Stumberger, G., Hörl, D., Tsouraki, D., Steinek, C., Oudelaar, A. M., Leonhardt, H., & Harz, H. (2025) · bioRxiv · doi:10.1093/nar/gkaf1255 · Cited by 3 · see citing works
“This developmental transition is known to involve extensive epigenetic reprogramming and conformational changes at regulatory elements [ 43–46 ].”
Klingberg, T., Wachter, I., Pancholi, A., Gohar, Y., Kumar, P., Sobucki, M., Kämmer, E., Eroğlu-Kayıkçı, S., Erhardt, S., Ferrai, C., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.04.547621 · Cited by 4 · see citing works
“Additionally, super-enhancers underlying long-range contacts as well as gene expression changes are partially deactivated upon exit from pluripotency and activated upon induction of new cell types, supporting a model where transcriptional hubs would be formed and subsequently dispersed via the activation and deactivat…”
BackgroundCarey, G., Vega-Sendino, M., Tillo, D., Hoelscher, S. C., Khan, A., Taukulis, I., Olbrich, T., Saykali, B., Tran, A. D., Soni, B., et al. (2026) · EMBO Journal · doi:10.1038/s44318-026-00853-6 · Cited by 2 · see citing works
“In fact, this transition is characterized by an extensive 3D chromatin remodeling that could contribute to imposing a totipotent-like conversion barrier (Novo et al, 2018; Battle et al, 2019; Joshi et al, 2015).”
Shanel, G., Hsieh, T.-H. S., Cattoglio, C., Haham, H. A., Chou, H.-J., Li, J. Z., Shamir, R., Darzacq, X., & Elkon, R. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkaf607 · Cited by 2
“Many studies explored changes in 3D genome organization between different tissues or during differentiation, which involves massive reprogramming of cellular transcriptional programs [ 34–37 ].”
Byers, C., Spruce, C., Fortin, H. J., Czechanski, A., Munger, S. C., Reinholdt, L., Skelly, D. A., & Baker, C. L. (2021) · bioRxiv · doi:10.1101/2021.01.15.426861 · Cited by 2
van de Grift, Y. V. D., Heijmans, N., & van Amerongen, R. (2020) · bioRxiv · doi:10.1007/s10911-020-09474-z · Cited by 2 · see citing works
“While it is common 179 to do so, linear proximity alone is not an accurate measure for functional interaction 180 between an enhancer and its putative target gene [24,25].”
BackgroundEndless forms – how genome organization underlies evolution and development
Edwards, A. N., & Finn, E. H. (2026) · Journal of Cell Science · doi:10.1242/jcs.264059 · Cited by 1 · see citing works
Sun, L., McCauley, B. S., Liu, H., Chen, X., & Dang, W.-W. (2025) · Research Square · doi:10.21203/rs.3.rs-6531164/v1 · Cited by 1
“Our use of Hi-C to identify the targets of enhancers and SEs is more robust than traditional, proximity-based methods 32,66,67 , providing a direct link between changes in enhancers and differential gene expression in aging.”
InfluentialEidelman, Y., & Andreev, S. G. (2023) · Russian Journal of Genetics · doi:10.1134/s1022795423060030 · Cited by 1 · see citing works
“The data on the SE position in the genome were taken from [13].”
Properties of cancer stem cells
Wojcierowski, J., Olszewska-Bożek, K., Kolobius, E., Wojcierowska-Litwin, M., & Zmorzyński, S. (2022) · Diagnostyka Laboratoryjna · doi:10.5604/01.3001.0016.1866 · Cited by 1 · see citing works
Application of the 3C Method to Study the Developmental Genes in Drosophila Larvae
Bylino, O. V., Ibragimov, A. N., Digilio, F. A., Giordano, E., & Shidlovskii, Y. V. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.734208 · Cited by 1 · see citing works
Zhao, Y., Ding, Y., He, L., Li, Y.-Y., Chen, X., Sun, H., & Wang, H.-T. (2021) · bioRxiv · doi:10.1101/2021.12.20.473464 · Cited by 1
Transcription factors make the right contacts
Rugg-Gunn, P. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0399-x · Cited by 1 · see citing works
Self-citationMehra, P., & Kalani, A. (2018) · Life Sciences · doi:10.1016/j.lfs.2018.09.021 · Cited by 2 · see citing works
The Rules of Successful Speed Dating Are Complex, Even for Super-Enhancers.
Poot, R. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.03.001 · Cited by 1
Yeh, C. D., van de Venn, L., Kreutzer, S., Zheng, X., Cantos, N. C., Bechter, L. V., Mailänder, D., Schröder, M. S., Hofmann, R., Gerbaldo, F. E., et al. (2026) · Cell Reports · doi:10.1016/j.celrep.2026.117864
Klingberg, T., Wachter, I., Pancholi, A., Akyel, M., Gohar, Y., Kumar, P., Fernandes, A. M., Bao, Y., Schmidt-Heydt, A., Piepers, M., et al. (2026) · Advanced Science · doi:10.1002/advs.75924
LYL1 is critical for adult hematopoietic stem cell-derived B and T lymphopoiesis
Chiu, S. K., The, J., Saw, J., Boyle, J. A., Curtis, D. J., & Tremblay, C. S. (2026) · Scientific Reports · doi:10.1038/s41598-026-53398-3
Modeling nascent transcription from chromatin landscape and structure with CLASTER
Avelli, M. P., Sigurdsson, A. I., Ollé-López, J., Narita, T., Krietenstein, N., Choudhary, C., & Rasmussen, S. (2026) · Genome biology · doi:10.1186/s13059-026-03992-5
“Promoter-Capture HiC maps were obtained for mESCs from publicly available data deposited in GSM2753060 by [32].”
InfluentialSARE: an optimized method for detection functional regulatory elements in genome
Hosseinpoor, M. (2025) · Egyptian Journal of Medical Human Genetics · doi:10.1186/s43042-025-00695-7
“Medical scientists have usually been faced with troubles together with prediction, diagnosis, survival, and relapse of the illnesses [1].”
Sequential-GAM constructs the single-cell geometric 3D genome structure
Li, Y.-G., Wang, K., Shi, M.-L., Zhang, M. Q., & Gao, J. (2024) · bioRxiv · doi:10.1093/nar/gkag794
“Thus, OSN co-binding sites identified by ChIP-seq can be considered as cell-type-specific genes in mES cells [ 32 ].”
Eidelman, Y., & Andreev, S. G. (2023) · Genetika · doi:10.31857/s0016675823060036
Subramanian, S., Thoms, J., Huang, Y., Cornejo, P., Koch, F. C., Jacquelin, S., Shen, S., Song, E., Joshi, S. M., Brownlee, C., et al. (2023) · bioRxiv · doi:10.1101/2023.04.18.537282
“…leukemic haematopoiesis (Cai et al., 2000; Curtis et al., 2012; Hahn et al., 2011; Li et al., 2015; Mangan and Speck, 2011; Marcucci et al., 2005; Oram et al., 2010; Pimanda et al., 2007; Thoms et al., 2011; Vicente et al., 2012), bind combinatorially in bulk CD34+ hematopoietic stem and…”
BackgroundK-mer Content Changes with Node Degree in Promoter–Enhancer Network of Mouse ES Cells
Szyman, K., Wilczyński, B., & Dąbrowski, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158067
“From such studies, it has become apparent that in the mouse embryonic stem (ES) cells, the majority of enhancers interact over relatively short distance with just one promoter, while promoters typically interact with several enhancers, and also there are many enhancers, in particular super-enhancers that interact with…”
BackgroundA Multi-Object Simulated Annealing Approach to Identify Likely Functional Genomic PairsPreprint
Hosseinpoor, M., & Parvin, H. (2021) · Preprints.org · doi:10.20944/preprints202107.0358.v1
“Figure 7 shows the percentage of overlapping and non-overlapping of the new interacting pairs detected by the suggested method with significant enhancer-promoter regions identified in Stefan et al. This proves the ability of our proposed method in detection and extraction of the interacting pairs.”
BackgroundMethodInfluentialNewly synthesized RNA Sequencing Characterizes Transcription Dynamics in Three Pluripotent StatesPreprint
Shao, R., Kumar, B., Lidschreiber, K., Lidschreiber, M., Cramer, P., & Elsässer, S. (2021) · bioRxiv · doi:10.1101/2021.06.11.448016
“…is in line with recent studies demonstrating that rewiring of promoter-enhancer interactions, thus changes in transcriptional activity, explains changes in RNA-seq abundance between SL and 2i states for many differentially regulated genes (Atlasi et al, 2019; Joshi et al, 2015; Novo et al, 2018).”
BackgroundDynamics of Super-Enhancers Throughout Myogenesis
Abdelkarim, B. (2020) · uO Research (University of Ottawa) · doi:10.20381/ruor-24271
Characterising the reprogramming dynamics between human pluripotent states
Collier, A. (2019) · doi:10.17863/cam.35268
“Further reports indicate that enhancer rewiring is a widespread phenomenon that occurs during this pluripotent state transition (Buecker et al., 2014; Factor et al., 2014; Novo et al., 2018), and is therefore a useful”
BackgroundEnhancer Prediction Based on Epigenomic Data
Ramisch, A. (2019) · Refubium (Universitätsbibliothek der Freien Universität Berlin) · doi:10.17169/refubium-2696
- Authors
- Novo, C. L., Javierre, B.-M., Cairns, J., Segonds-Pichon, A., Wingett, S. W., Freire-Pritchett, P., Furlan-Magaril, M., Schoenfelder, S., Fraser, P., & Rugg-Gunn, P. J.
- Affiliations
- Babraham Institute (GB)
- Florida State University (US)
- ORCID
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2018-03
- Volume
- 22
- Issue
- 10
- Pages
- 2615-2627
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC5863031
- OpenAlex
- W2793769859
- Cited by
- 119
- References
- 65
- Citations by year
- 2026: 11 · 2025: 6 · 2024: 10 · 2023: 10 · 2022: 9 · 2021: 22 · 2020: 19 · 2019: 19 · 2018: 12
- FWCI
- 6.40
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Spiral (Imperial College London) (submittedVersion, cc-by)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- Apollo (cc-by)
- Funders
- Medical Research Council (MR/L007150/1, MC_UP_1302/1, MC_UP_1302/5, BB/J004480/1, MC_UP_1302/3)
- Wellcome Trust (WT093736)
- Biotechnology and Biological Sciences Research Council (BB/P013406/1, BB/M022285/1)
- 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
- super-enhancers, long-range enhancer-promoter interactions, mouse embryonic stem cells, pluripotency, epiblast stem cells, Nanog, promoter capture Hi-C, transcription factor occupancy, gene regulatory networks, cell state transitions, chromatin organization
- MeSH terms
- Mouse Embryonic Stem Cells, Nanog Homeobox Protein, Animals, Cell Differentiation, Enhancer Elements, Genetic, Germ Layers, Promoter Regions, Genetic, Protein Binding, Pluripotent Stem Cells, Mice, Gene Regulatory Networks
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