Remodeling of the enhancer landscape during macrophage activation is coupled to enhancer transcription
Open accessAbstract
Recent studies suggest a hierarchical model in which lineage-determining factors act in a collaborative manner to select and prime cell-specific enhancers, thereby enabling signal-dependent transcription factors to bind and function in a cell-type-specific manner. Consistent with this model, TLR4 signaling primarily regulates macrophage gene expression through a pre-existing enhancer landscape. However, TLR4 signaling also induces priming of ∼3,000 enhancer-like regions de novo, enabling visualization of intermediates in enhancer selection and activation. Unexpectedly, we find that enhancer transcription precedes local mono- and dimethylation of histone H3 lysine 4 (H3K4me1/2). H3K4 methylation at de novo enhancers is primarily dependent on the histone methyltransferases Mll1, Mll2/4, and Mll3 and is significantly reduced by inhibition of RNA polymerase II elongation. Collectively, these findings suggest an essential role of enhancer transcription in H3K4me1/2 deposition at de novo enhancers that is independent of potential functions of the resulting eRNA transcripts.
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The level of eRNA transcription correlates with enhancer activity.
“Several studies have shown that the level of eRNA transcription correlates with enhancer activity [60,61].”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [60]
In untreated macrophages, H3K27ac was enriched both at the promoter region of Tet2 and a region lying 40kb upstream, constituting a putative distal enhancer element.
“In untreated macrophages, H3K27ac was enriched both at the promoter region of Tet2 and a region lying 40kb upstream, thus constituting a putative distal enhancer element (Figure 2A).”
From TET2 Regulates the Neuroinflammatory Response in Microglia (2019) · cites this paper as Kaikkonen et al., 2013
The Introduction and Results discuss enhancer marks and transcription in macrophages, but the passages found do not describe H3K27ac at the Tet2 promoter or a site 40 kb upstream in untreated macrophages. Searches for Tet2 and the 40-kb upstream region found no passage addressing that locus-specific claim; page numbers were not available in our copy. (LLM, conf=0.75)
Experimental — accuracy not yet measuredImmune memory in microglia and macrophages is shaped by epigenetically mediated alterations in the enhancer repertoire of targeted genes.
“Immune memory in microglia and macrophages are shaped by epigenetically mediated alterations in the enhancer repertoire of targeted genes [11, 32].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [32]
Within cell-specific enhancers, DNA sequences provide information about the identities of key lineage-determining transcription factors and the activity states of signaling pathways that control the functions of signal-dependent transcription factors.
“Within cell-specific enhancers, DNA sequences provide information about the identities of key LDTFs and the activity states of signaling pathways that control the functions of SDTFs (31, 33–35).”
From An environment-dependent transcriptional network specifies human microglia identity (2017) · cites this paper as [33]
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An integrated encyclopedia of DNA elements in the human genome
The ENCODE Project Consortium (2012) · Nature · doi:10.1038/nature11247 · Cited by 18,072 · see citing works
Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H., & Glass, C. K. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.05.004 · Cited by 13,382 · see citing works
Histone H3K27ac separates active from poised enhancers and predicts developmental state
Creyghton, M. P., Cheng, A. W., Welstead, G. G., Kooistra, T., Carey, B. W., Steine, E. J., Hanna, J., Lodato, M. A., Frampton, G. M., Sharp, P. A., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016071107 · Cited by 4,302 · see citing works
Genome-Wide Analysis in Vivo of Translation with Nucleotide Resolution Using Ribosome Profiling
Ingolia, N. T., Ghaemmaghami, S., Newman, J. R. S., & Weissman, J. S. (2009) · Science · doi:10.1126/science.1168978 · Cited by 3,853 · see citing works
Role of Histone H3 Lysine 27 Methylation in Polycomb-Group Silencing
Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., Jones, R. S., & Zhang, Y. (2002) · Science · doi:10.1126/science.1076997 · Cited by 3,775 · see citing works
Heintzman, N. D., Stuart, R. K., Hon, G., Fu, Y., Ching, C. W., Hawkins, R. D., Barrera, L. O., Van Calcar, S., Qu, C., Ching, K. A., et al. (2007) · Nature Genetics · doi:10.1038/ng1966 · Cited by 3,398 · cited 3× · see citing works
“, high enrichment of histone H3 lysine 4 mono- and dimethylation (H3K4me1 and H3K4me2, respectively) and low enrichment of H3K4me3 compared to promoters (Heintzman et al., 2007).”
BackgroundThe accessible chromatin landscape of the human genome
Thurman, R. E., Rynes, E., Humbert, R., Vierstra, J., Maurano, M. T., Haugen, E., Sheffield, N. C., Stergachis, A. B., Wang, H., Vernot, B., et al. (2012) · Nature · doi:10.1038/nature11232 · Cited by 2,679 · see citing works
Histone modifications at human enhancers reflect global cell-type-specific gene expression
Heintzman, N. D., Hon, G. C., Hawkins, R. D., Kheradpour, P., Stark, A., Harp, L. F., Ye, Z., Lee, L. K., Stuart, R. K., Ching, C. W., et al. (2009) · Nature · doi:10.1038/nature07829 · Cited by 2,533 · see citing works
Widespread transcription at neuronal activity-regulated enhancers
Kim, T.-K., Hemberg, M., Gray, J. M., Costa, A. M., Bear, D. M., Wu, J., Harmin, D. A., Laptewicz, M., Barbara-Haley, K., Kuersten, S., et al. (2010) · Nature · doi:10.1038/nature09033 · Cited by 2,450 · see citing works
A unique chromatin signature uncovers early developmental enhancers in humans
Rada-Iglesias, A., Bajpai, R., Swigut, T., Brugmann, S. A., Flynn, R. A., & Wysocka, J. (2011) · Nature · doi:10.1038/nature09692 · Cited by 2,233 · see citing works
Nascent RNA Sequencing Reveals Widespread Pausing and Divergent Initiation at Human Promoters
Core, L. J., Waterfall, J. J., & Lis, J. T. (2008) · Science · doi:10.1126/science.1162228 · Cited by 1,986 · see citing works
ChIP-seq accurately predicts tissue-specific activity of enhancers
Visel, A., Blow, M. J., Li, Z., Zhang, T., Akiyama, J. A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., Chen, F., et al. (2009) · Nature · doi:10.1038/nature07730 · Cited by 1,639 · see citing works
Suppression of inflammation by a synthetic histone mimic
Nicodeme, E., Jeffrey, K. L., Schaefer, U., Beinke, S., Dewell, S., Chung, C.-W., Chandwani, R., Marazzi, I., Wilson, P., Coste, H., et al. (2010) · Nature · doi:10.1038/nature09589 · Cited by 1,563 · see citing works
Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia
Dawson, M. A., Prinjha, R. K., Dittmann, A., Giotopoulos, G., Bantscheff, M., Chan, W.-I., Robson, S. C., Chung, C., Hopf, C., Savitski, M. M., et al. (2011) · Nature · doi:10.1038/nature10509 · Cited by 1,512 · see citing works
Bennett, C. F., & Swayze, E. E. (2010) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.010909.105654 · Cited by 1,381 · see citing works
Genome-wide analysis of estrogen receptor binding sites
Carroll, J. S., Meyer, C. A., Song, J. S., Li, W., Geistlinger, T., Eeckhoute, J., Brodsky, A. S., Keeton, E. K., Fertuck, K. C., Hall, G., et al. (2006) · Nature Genetics · doi:10.1038/ng1901 · Cited by 1,368 · see citing works
Jang, M. K., Mochizuki, K., Zhou, M., Jeong, H., Brady, J. N., & Ozato, K. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.06.027 · Cited by 1,301 · see citing works
In vivo enhancer analysis of human conserved non-coding sequences
Pennacchio, L. A., Ahituv, N., Moses, A. M., Prabhakar, S., Nobrega, M. A., Shoukry, M., Minovitsky, S., Dubchak, I., Holt, A., Lewis, K. D., et al. (2006) · Nature · doi:10.1038/nature05295 · Cited by 1,165 · see citing works
Recruitment of P-TEFb for Stimulation of Transcriptional Elongation by the Bromodomain Protein Brd4
Yang, Z., Yik, J. H. N., Chen, R., He, N., Jang, M. K., Ozato, K., & Zhou, Q. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.06.029 · Cited by 1,141 · see citing works
Ng, H., Robert, F., Young, R. A., & Struhl, K. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00092-3 · Cited by 1,097 · see citing works
Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation
Li, W., Notani, D., Ma, Q., Tanasa, B., Nunez, E., Chen, A. Y., Merkurjev, D., Zhang, J., Ohgi, K., Song, X., et al. (2013) · Nature · doi:10.1038/nature12210 · Cited by 1,049 · see citing works
Transcriptional control of the inflammatory response
Medzhitov, R., & Horng, T. (2009) · Nature Reviews Immunology · doi:10.1038/nri2634 · Cited by 1,035 · see citing works
Highly Conserved Non-Coding Sequences Are Associated with Vertebrate Development
Woolfe, A., Goodson, M., Goode, D. K., Snell, P., McEwen, G. K., Vavouri, T., Smith, S. F., North, P., Callaway, H., Kelly, K., et al. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0030007 · Cited by 970 · see citing works
Chromatin accessibility pre-determines glucocorticoid receptor binding patterns
John, S., Sabo, P. J., Thurman, R. E., Sung, M.-H., Biddie, S. C., Johnson, T. A., Hager, G. L., & Stamatoyannopoulos, J. A. (2011) · Nature Genetics · doi:10.1038/ng.759 · Cited by 954 · see citing works
A Large Fraction of Extragenic RNA Pol II Transcription Sites Overlap Enhancers
De Santa, F., Barozzi, I., Mietton, F., Ghisletti, S., Polletti, S., Tusi, B. K., Muller, H., Ragoussis, J., Wei, C.-L., & Natoli, G. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000384 · Cited by 934 · see citing works
Latent 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 · see citing works
Activating RNAs associate with Mediator to enhance chromatin architecture and transcription
Lai, F., Ørom, U. A., Cesaroni, M., Beringer, M., Taatjes, D. J., Blobel, G. A., & Shiekhattar, R. (2013) · Nature · doi:10.1038/nature11884 · Cited by 857 · see citing works
Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA
Wang, D., García-Bassets, I., Benner, C. W., Li, W., Su, X. B., Zhou, Y., Qiu, J., Liu, W., Kaikkonen, M. U., Ohgi, K. A., et al. (2011) · Nature · doi:10.1038/nature10006 · Cited by 820 · see citing works
Krogan, N. J., Kim, M., Tong, A. H. Y., Golshani, A., Cagney, G., Canadien, V., Richards, D. P., Beattie, B. K., Emili, A., Boone, C. M., et al. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.12.4207-4218.2003 · Cited by 680 · see citing works
Ghisletti, S., Barozzi, I., Mietton, F., Polletti, S., De Santa, F., Venturini, E., Gregory, L., Lonie, L., Chew, A., Wei, C.-L., et al. (2010) · Immunity · doi:10.1016/j.immuni.2010.02.008 · Cited by 666 · see citing works
Control of RNA Polymerase II Elongation Potential by a Novel Carboxyl-terminal Domain Kinase
Marshall, N. F., Peng, J., Xie, Z., & Price, D. H. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.43.27176 · Cited by 662 · see citing works
Control of Inducible Gene Expression by Signal-Dependent Transcriptional Elongation
Hargreaves, D. C., Horng, T., & Medzhitov, R. M. (2009) · Cell · doi:10.1016/j.cell.2009.05.047 · Cited by 649 · see citing works
Menin Associates with a Trithorax Family Histone Methyltransferase Complex and with the Hoxc8 Locus
Hughes, C. M., Rozenblatt–Rosen, O., Milne, T. A., Copeland, T. D., Levine, S. S., Lee, J. C., Hayes, D. N., Shanmugam, K. S., Bhattacharjee, A., Biondi, C., et al. (2004) · Molecular Cell · doi:10.1016/s1097-2765(04)00081-4 · Cited by 645 · see citing works
Flavopiridol Inactivates P-TEFb and Blocks Most RNA Polymerase II Transcription in Vivo
Chao, S., & Price, D. H. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m102306200 · Cited by 623 · see citing works
Enhancer decommissioning by LSD1 during embryonic stem cell differentiation
Whyte, W. A., Bilodeau, S., Orlando, D. A., Hoke, H. A., Frampton, G. M., Foster, C. T., Cowley, S. M., & Young, R. A. (2012) · Nature · doi:10.1038/nature10805 · Cited by 602 · see citing works
Master Transcription Factors Determine Cell-Type-Specific Responses to TGF-β Signaling
Mullen, A. C., Orlando, D. A., Newman, J. J., Lovén, J., Kumar, R., Bilodeau, S., Reddy, J., Guenther, M. G., DeKoter, R. P., & Young, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.08.050 · Cited by 563 · see citing works
Inhibition of RNA synthesis by actinomycin D: Characteristic dose‐response of different RNA species
Perry, R. P., & Kelley, D. E. (1970) · Journal of Cellular Physiology · doi:10.1002/jcp.1040760202 · Cited by 559 · see citing works
Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription
Lam, M. T. Y., Cho, H., Lesch, H. P., Gosselin, D., Heinz, S., Tanaka-Oishi, Y., Benner, C., Kaikkonen, M. U., Kim, A. S., Kosaka, M., et al. (2013) · Nature · doi:10.1038/nature12209 · Cited by 548 · see citing works
eRNAs Are Required for p53-Dependent Enhancer Activity and Gene Transcription
Melo, C. A., Drost, J., Wijchers, P. J., van de Werken, H., de Wit, E., Vrielink, J. A. F. O., Elkon, R., Melo, S. A., Léveillé, N., Kalluri, R., et al. (2013) · Molecular Cell · doi:10.1016/j.molcel.2012.11.021 · Cited by 544 · see citing works
Nielsen, R., Pedersen, T. Å., Hagenbeek, D., Moulos, P., Siersbæk, R., Megens, E., Denissov, S., Børgesen, M., Françoijs, K., Mandrup, S., et al. (2008) · Genes & Development · doi:10.1101/gad.501108 · Cited by 520 · see citing works
XPB, a subunit of TFIIH, is a target of the natural product triptolide
Titov, D. V., Gilman, B. W., He, Q., Bhat, S., Low, W., Dang, Y., Smeaton, M. B., Demain, A. L., Miller, P. S., Kugel, J. F., et al. (2011) · Nature Chemical Biology · doi:10.1038/nchembio.522 · Cited by 513 · see citing works
Transcription Factor AP1 Potentiates Chromatin Accessibility and Glucocorticoid Receptor Binding
Biddie, S. C., John, S., Sabo, P. J., Thurman, R. E., Johnson, T. A., Schiltz, R. L., Miranda, T. B., Sung, M.-H., Trump, S., Lightman, S. L., et al. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.06.016 · Cited by 503 · see citing works
Bonn, S., Zinzen, R. P., Girardot, C., Gustafson, E. H., Perez-Gonzalez, A., Delhomme, N., Ghavi-Helm, Y., Wilczyński, B., Riddell, A., & Furlong, E. E. M. (2012) · Nature Genetics · doi:10.1038/ng.1064 · Cited by 502 · see citing works
Hah, N., Danko, C. G., Core, L. J., Waterfall, J. J., Siepel, A. C., Lis, J. T., & Kraus, W. L. (2011) · Cell · doi:10.1016/j.cell.2011.03.042 · Cited by 488 · see citing works
Bhatt, D. M., Pandya‐Jones, A., Tong, A.-J., Barozzi, I., Lissner, M. M., Natoli, G., Black, D. L., & Smale, S. T. (2012) · Cell · doi:10.1016/j.cell.2012.05.043 · Cited by 442 · see citing works
Schiltz, R. L., Mizzen, C. A., Vassilev, A. P., Cook, R. G., Allis, C. D., & Nakatani, Y. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.3.1189 · Cited by 416 · see citing works
Wood, A., Schneider, J., Dover, J., Johnston, M., & Shilatifard, A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.c300269200 · Cited by 396 · see citing works
Herz, H.-M., Mohan, M., Garruss, A. S., Liang, K., Takahashi, Y.-H., Mickey, K., Voets, O., Verrijzer, C. P., & Shilatifard, A. (2012) · Genes & Development · doi:10.1101/gad.201327.112 · Cited by 388 · see citing works
Trompouki, E., Bowman, T. V., Lawton, L. N., Fan, Z. P., Wu, D.-C., DiBiase, A., Martin, C., Cech, J. N., Sessa, A. K., LeBlanc, J., et al. (2011) · Cell · doi:10.1016/j.cell.2011.09.044 · Cited by 303 · see citing works
Brueckner, F., & Cramer, P. (2008) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1458 · Cited by 263 · see citing works
Walsh, J. C., DeKoter, R. P., Lee, H.-J., Smith, E. D., Lancki, D. W., Gurish, M. F., Friend, D. S., Stevens, R. L., Anastasi, J., & Singh, H. (2002) · Immunity · doi:10.1016/s1074-7613(02)00452-1 · Cited by 262 · see citing works
Bcl-6 and NF-κB cistromes mediate opposing regulation of the innate immune responsePreprint
Barish, G. D., Yu, R. T., Karunasiri, M. S., Ocampo, C. B., Dixon, J. R., Benner, C. W., Dent, A. L., Tangirala, R. K., & Evans, R. M. (2010) · Genes & Development · doi:10.1101/gad.1998010 · Cited by 256 · see citing works
Wedelolactone suppresses LPS-induced caspase-11 expression by directly inhibiting the IKK Complex
Kobori, M., Yang, Z., Gong, D., Heissmeyer, V., Zhu, H., Jung, Y.-K., Gakidis, M. A. M., Rao, A., Sekine, T., Ikegami, F., et al. (2003) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401325 · Cited by 249 · see citing works
MLL associates specifically with a subset of transcriptionally active target genes
Milne, T. A., Dou, Y., Martin, M. E., Brock, H. W., Roeder, R. G., & Hess, J. L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503630102 · Cited by 230 · see citing works
Valledor, A. F., Hsu, L.-C., Ogawa, S., Sawka‐Verhelle, D., Karin, M., & Glass, C. K. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407749101 · Cited by 223 · see citing works
Kdo2-Lipid A of Escherichia coli, a defined endotoxin that activates macrophages via TLR-4
Raetz, C. R. H., Garrett, T. A., Reynolds, C. M., Shaw, W. A., Moore, J. D., Smith, D. C., Ribeiro, A. A., Murphy, R. C., Ulevitch, R. J., Fearns, C., et al. (2006) · Journal of Lipid Research · doi:10.1194/jlr.m600027-jlr200 · Cited by 222 · see citing works
Lefterova, M. I., Steger, D. J., Zhuo, D. X., Qatanani, M., Mullican, S. E., Tuteja, G., Manduchi, E., Grant, G. R., & Lazar, M. A. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.01651-09 · Cited by 208 · see citing works
A Highly Purified RNA Polymerase II Elongation Control System
Renner, D. B., Yamaguchi, Y., Wada, T., Handa, H., & Price, D. H. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104967200 · Cited by 193 · see citing works
Mechanisms Establishing TLR4-Responsive Activation States of Inflammatory Response Genes
Escoubet‐Lozach, L., Benner, C. W., Kaikkonen, M. U., Lozach, J., Heinz, S., Spann, N. J., Crotti, A., Stender, J. D., Ghisletti, S., Reichart, D. R., et al. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002401 · Cited by 161 · see citing works
Transcriptional regulation in the innate immune system
Smale, S. T. (2012) · Current Opinion in Immunology · doi:10.1016/j.coi.2011.12.008 · Cited by 95 · see citing works
Rana, R., Surapureddi, S., Kam, W., Ferguson, S., & Goldstein, J. A. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00847-10 · Cited by 67 · see citing works
Activator-dependent p300 Acetylation of Chromatin in Vitro
Szerlong, H. J., Prenni, J. E., Nyborg, J. K., & Hansen, J. C. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.148718 · Cited by 65 · see citing works
Phosphorylation of the Menin Tumor Suppressor Protein on Serine 543 and Serine 583
MacConaill, L. E., Hughes, C. M., Rozenblatt–Rosen, O., Nannepaga, S., & Meyerson, M. M. (2006) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-06-0123 · Cited by 27 · see citing works
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Trained immunity: A program of innate immune memory in health and– disease
Netea, M. G., Joosten, L. A. B., Latz, E., Mills, K. H. G., Natoli, G., Stunnenberg, H. G., O’Neill, L. A. J., & Xavier, R. J. (2016) · Science · doi:10.1126/science.aaf1098 · Cited by 2,768 · see citing works
Gosselin, D., Link, V. M., Romanoski, C. E., Fonseca, G. J., Eichenfield, D. Z., Spann, N. J., Stender, J. D., Chun, H. B., Garner, H., Geissmann, F., et al. (2014) · Cell · doi:10.1016/j.cell.2014.11.023 · Cited by 1,307 · see citing works
An environment-dependent transcriptional network specifies human microglia identity
Gosselin, D., Skola, D., Coufal, N. G., Holtman, I. R., Schlachetzki, J. C. M., Sajti, E., Jaeger, B. N., O’Connor, C., Fitzpatrick, C., Pasillas, M. P., et al. (2017) · Science · doi:10.1126/science.aal3222 · Cited by 1,220 · see citing works
Innate immune memory in the brain shapes neurological disease hallmarks
Wendeln, A.-C., Degenhardt, K., Kaurani, L., Gertig, M., Ulas, T., Jain, G., Wagner, J., Häsler, L. M., Wild, K., Skodras, A., et al. (2018) · Nature · doi:10.1038/s41586-018-0023-4 · Cited by 956 · see citing works
The selection and function of cell type-specific enhancers
Heinz, S., Romanoski, C. E., Benner, C., & Glass, C. K. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3949 · Cited by 1,010 · see citing works
Self-citationThe multidimensional mechanisms of long noncoding RNA function
Marchese, F. P., Raimondi, I., & Huarte, M. (2017) · Genome biology · doi:10.1186/s13059-017-1348-2 · Cited by 966 · see citing works
Chromatin state dynamics during blood formation
Lara-Astiaso, D., Weiner, A., Lorenzo-Vivas, E., Zaretsky, I., Jaitin, D. A., David, E., Keren-Shaul, H., Mildner, A., Winter, D., Jung, S., et al. (2014) · Science · doi:10.1126/science.1256271 · Cited by 776 · see citing works
Enhancers as non-coding RNA transcription units: recent insights and future perspectives
Li, W., Notani, D., & Rosenfeld, M. G. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.4 · Cited by 710 · see citing works
Macrophages and cancer: from mechanisms to therapeutic implications
Ostuni, R., Kratochvill, F., Murray, P. J., & Natoli, G. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.02.004 · Cited by 685 · see citing works
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Rao, R., & Dou, Y. (2015) · Nature Reviews. Cancer · doi:10.1038/nrc3929 · Cited by 558 · see citing works
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Brown, J. D., Lin, C. Y., Duan, Q., Griffin, G., Federation, A. J., Paranal, R. M., Bair, S., Newton, G., Lichtman, A. H., Kung, A. L., et al. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.08.024 · Cited by 614 · see citing works
Innate and Adaptive Immune Memory: an Evolutionary Continuum in the Host’s Response to Pathogens
Netea, M. G., Schlitzer, A., Placek, K., Joosten, L. A. B., & Schultze, J. L. (2019) · Cell Host & Microbe · doi:10.1016/j.chom.2018.12.006 · Cited by 602 · see citing works
The Energetics and Physiological Impact of Cohesin Extrusion
Vian, L., Pękowska, A., Rao, S. S. P., Kieffer-Kwon, K.-R., Jung, S., Baranello, L., Huang, S.-C., El Khattabi, L., Dose, M., Pruett, N., et al. (2018) · Cell · doi:10.1016/j.cell.2018.03.072 · Cited by 581 · see citing works
The interplay of epigenetic marks during stem cell differentiation and development
Atlasi, Y., & Stunnenberg, H. G. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.57 · Cited by 569 · see citing works
Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells
Arner, E., Daub, C. O., Vitting‐Seerup, K., Andersson, R., Lilje, B., Drabløs, F., Lennartsson, A., Rönnerblad, M., Hrydziuszko, O., Vitezic, M., et al. (2015) · Science · doi:10.1126/science.1259418 · Cited by 570 · see citing works
Molecular control of activation and priming in macrophages
Glass, C. K., & Natoli, G. (2015) · Nature Immunology · doi:10.1038/ni.3306 · Cited by 522 · see citing works
Enhancer RNAs and regulated transcriptional programs
Lam, M. T. Y., Li, W., Rosenfeld, M. G., & Glass, C. K. (2014) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2014.02.007 · Cited by 502 · see citing works
Lee, J.-E., Wang, C., Xu, S., Cho, Y.-W., Wang, L., Feng, X., Baldridge, A., Sartorelli, V., Zhuang, L., Peng, W., et al. (2013) · eLife · doi:10.7554/elife.01503 · Cited by 522 · see citing works
Transcription factor trapping by RNA in gene regulatory elements
Sigova, A. A., Abraham, B. J., Ji, X., Molinie, B., Hannett, N. M., Guo, Y. E., Jangi, M., Giallourakis, C. C., Sharp, P. A., & Young, R. A. (2015) · Science · doi:10.1126/science.aad3346 · Cited by 492 · see citing works
Disruption of KMT2D perturbs germinal center B cell development and promotes lymphomagenesis
Zhang, J., Dominguez-Sola, D., Hussein, S., Lee, J., Holmes, A. B., Bansal, M., Vlasevska, S., Mo, T., Tang, H., Basso, K., et al. (2015) · Nature Medicine · doi:10.1038/nm.3940 · Cited by 463 · see citing works
Riggi, N., Knoechel, B., Gillespie, S. M., Rheinbay, E., Boulay, G., Suvà, M. L., Rossetti, N. E., Boonseng, W. E., Oksuz, O., Cook, E., et al. (2014) · Cancer Cell · doi:10.1016/j.ccell.2014.10.004 · Cited by 447 · see citing works
Briggs, J., Wolvetang, E. J., Mattick, J. S., Rinn, J. L., & Barry, G. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.045 · Cited by 443 · see citing works
RNA Binding to CBP Stimulates Histone Acetylation and Transcription
Bose, D. A., Donahue, G., Reinberg, D., Shiekhattar, R., Bonasio, R., & Berger, S. L. (2017) · Cell · doi:10.1016/j.cell.2016.12.020 · Cited by 426 · see citing works
Long non-coding RNAs in the regulation of the immune response
Heward, J. A., & Lindsay, M. A. (2014) · Trends in Immunology · doi:10.1016/j.it.2014.07.005 · Cited by 418 · see citing works
Different Neuronal Activity Patterns Induce Different Gene Expression Programs
Tyssowski, K. M., DeStefino, N. R., Cho, J.-H., Dunn, C. J., Poston, R. G., Carty, C. E., Jones, R. D., Chang, S. M., Romeo, P., Wurzelmann, M. K., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.04.001 · Cited by 390 · see citing works
Epigenetic regulation of the innate immune response to infection
Zhang, Q., & Cao, X. (2019) · Nature Reviews Immunology · doi:10.1038/s41577-019-0151-6 · Cited by 366 · see citing works
Enhancer RNAs are an important regulatory layer of the epigenome
Sartorelli, V., & Lauberth, S. M. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-0446-0 · Cited by 367 · see citing works
Phase separation of ligand-activated enhancers licenses cooperative chromosomal enhancer assembly
Nair, S. J., Lu, Y., Meluzzi, D., Oh, S., Yang, F., Friedman, M. J., Wang, S. S., Suter, T., Alshareedah, I., Gamliel, A., et al. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0190-5 · Cited by 366 · see citing works
Long noncoding RNAs: fresh perspectives into the RNA world
Yang, L., Froberg, J. E., & Lee, J. T. (2013) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2013.10.002 · Cited by 356 · see citing works
Oishi, Y., Spann, N. J., Link, V. M., Muse, E. D., Strid, T., Edillor, C., Kolar, M. J., Matsuzaka, T., Hayakawa, S., Tao, J., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2016.11.009 · Cited by 342 · see citing works
Architectural and Functional Commonalities between Enhancers and Promoters
Kim, T.-K., & Shiekhattar, R. (2015) · Cell · doi:10.1016/j.cell.2015.08.008 · Cited by 331 · see citing works
Transcription of the non-coding RNA upperhand controls Hand2 expression and heart development
Anderson, K. M., Anderson, D. M., McAnally, J., Shelton, J. M., Bassel‐Duby, R., & Olson, E. N. (2016) · Nature · doi:10.1038/nature20128 · Cited by 334 · see citing works
Rubin, A. J., Parker, K. R., Satpathy, A. T., Qi, Y., Wu, B., Ong, A. J., Mumbach, M. R., Ji, A. L., Kim, D. S., Cho, S. W., et al. (2019) · Cell · doi:10.1016/j.cell.2018.11.022 · Cited by 314 · see citing works
Epigenetic control of myeloid cell differentiation, identity and function
Álvarez‐Errico, D., Vento‐Tormo, R., Sieweke, M. H., & Ballestar, E. (2014) · Nature reviews. Immunology · doi:10.1038/nri3777 · Cited by 328 · see citing works
Molecular and epigenetic basis of macrophage polarized activation
Porta, C., Riboldi, E., Ippolito, A., & Sica, A. (2015) · Seminars in Immunology · doi:10.1016/j.smim.2015.10.003 · Cited by 319 · see citing works
Epigenetic regulation of macrophages: from homeostasis maintenance to host defense
Chen, S., Yang, J., Wei, Y., & Wei, X. (2019) · Cellular and Molecular Immunology · doi:10.1038/s41423-019-0315-0 · Cited by 317 · see citing works
Enhancer biology and enhanceropathies
Smith, E. R., & Shilatifard, A. (2014) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2784 · Cited by 310 · see citing works
The Many Alternative Faces of Macrophage Activation
Hume, D. A. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00370 · Cited by 303 · see citing works
Effect of natural genetic variation on enhancer selection and function
Heinz, S., Romanoski, C. E., Benner, C., Allison, K. A., Kaikkonen, M. U., Orozco, L. D., & Glass, C. K. (2013) · Nature · doi:10.1038/nature12615 · Cited by 298 · see citing works
Ilott, N. E., Heward, J. A., Roux, B. T., Tsitsiou, E., Fenwick, P. S., Lenzi, L., Goodhead, I., Hertz‐Fowler, C., Heger, A., Hall, N., et al. (2014) · Nature Communications · doi:10.1038/ncomms4979 · Cited by 294 · see citing works
Metabolic and Epigenetic Coordination of T Cell and Macrophage Immunity
Phan, A. T., Goldrath, A. W., & Glass, C. K. (2017) · Immunity · doi:10.1016/j.immuni.2017.04.016 · Cited by 291 · see citing works
Dealing with Pervasive Transcription
Jensen, T. H., Jacquier, A., & Libri, D. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.10.032 · Cited by 284 · see citing works
Innate immune memory: An evolutionary perspective
Gourbal, B., Pinaud, S., Beckers, G. J. M., van der Meer, J. W. M., Conrath, U., & Netea, M. G. (2018) · Immunological Reviews · doi:10.1111/imr.12647 · Cited by 283 · see citing works
Epigenetics and Trained Immunity
van der Heijden, C. D. C. C., Noz, M. P., Joosten, L. A. B., Netea, M. G., Riksen, N. P., & Keating, S. T. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7310 · Cited by 284 · see citing works
Mikhaylichenko, O., Bondarenko, V., Harnett, D., Schor, I. E., Males, M., Viales, R. R., & Furlong, E. E. M. (2018) · Genes & Development · doi:10.1101/gad.308619.117 · Cited by 293 · see citing works
Stimulus-specific combinatorial functionality of neuronal c-fos enhancers
Joo, J.-Y., Schaukowitch, K., Farbiak, L., Kilaru, G., & Kim, T.-K. (2016) · Nature Neuroscience · doi:10.1038/nn.4170 · Cited by 271 · see citing works
AP-1 imprints a reversible transcriptional programme of senescent cells.
Martínez-Zamudio, R. I., Roux, P.-F., de Freitas, J. A. N. L. F., Robinson, L., Doré, G., Sun, B., Belenki, D., Milanovic, M., Herbig, U., Schmitt, C. A., et al. (2020) · Nature Cell Biology · doi:10.1038/s41556-020-0529-5 · Cited by 236 · see citing works
Priming Microglia for Innate Immune Memory in the Brain
Neher, J. J., & Cunningham, C. M. (2019) · Trends in Immunology · doi:10.1016/j.it.2019.02.001 · Cited by 255 · see citing works
Diversity and Emerging Roles of Enhancer RNA in Regulation of Gene Expression and Cell Fate
Arnold, P. R., Wells, A. D., & Li, X. C. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00377 · Cited by 247 · see citing works
Nascent RNA analyses: tracking transcription and its regulation
Wissink, E. M., Vihervaara, A., Tippens, N. D., & Lis, J. T. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-019-0159-6 · Cited by 247 · see citing works
Functional Long Non-coding RNAs Evolve from Junk Transcripts
Palazzo, A. F., & Koonin, E. V. (2020) · Cell · doi:10.1016/j.cell.2020.09.047 · Cited by 240 · see citing works
Enhancer priming by H3K4 methyltransferase MLL4 controls cell fate transition
Wang, C., Lee, J.-E., Lai, B., Macfarlan, T. S., Xu, S., Zhuang, L., Liu, C., Peng, W., & Ge, K. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1606857113 · Cited by 242 · see citing works
Regulatory Networks Involving STATs, IRFs, and NFκB in Inflammation
Platanitis, E., & Decker, T. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02542 · Cited by 251 · see citing works
Park, S. H., Kang, K., Γιαννοπούλου, Ε., Qiao, Y., Kang, K., Kim, G., Park‐Min, K., & Ivashkiv, L. B. (2017) · Nature Immunology · doi:10.1038/ni.3818 · Cited by 237 · see citing works
Bacterial infection remodels the DNA methylation landscape of human dendritic cellsPreprint
Pacis, A., Tailleux, L., Morin, A. M., Lambourne, J. J., MacIsaac, J. L., Yotova, V., Dumaine, A., Danckaert, A., Luca, F., Grenier, J., et al. (2015) · Genome Research · doi:10.1101/gr.192005.115 · Cited by 230 · see citing works
Untangling Genetic Risk for Alzheimer’s Disease
Pimenova, A. A., Raj, T., & Goate, A. M. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.05.014 · Cited by 223 · see citing works
Scruggs, B. S., Gilchrist, D. A., Nechaev, S., Muse, G. W., Burkholder, A., Fargo, D. C., & Adelman, K. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.04.006 · Cited by 218 · see citing works
Evaluating Enhancer Function and Transcription
Field, A. R., & Adelman, K. (2020) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-011420-095916 · Cited by 218 · see citing works
High-Resolution Sequencing and Modeling Identifies Distinct Dynamic RNA Regulatory Strategies
Rabani, M., Raychowdhury, R., Jovanovic, M., Rooney, M., Stumpo, D. J., Pauli, A., Hacohen, N., Schier, A. F., Blackshear, P. J., Friedman, N., et al. (2014) · Cell · doi:10.1016/j.cell.2014.11.015 · Cited by 226 · see citing works
Cuartero, S., Weiss, F. D., Dharmalingam, G., Guo, Y., Ing-Simmons, E., Masella, S., Robles-Rebollo, I., Xiao, X., Wang, Y.-F., Barozzi, I., et al. (2018) · Nature Immunology · doi:10.1038/s41590-018-0184-1 · Cited by 210 · see citing works
Matsuda, T., Irie, T., Katsurabayashi, S., Hayashi, Y., Nagai, T., Hamazaki, N., Adefuin, A. M. D., Miura, F., Ito, T., Kimurâ, H., et al. (2019) · Neuron · doi:10.1016/j.neuron.2018.12.010 · Cited by 220 · see citing works
Transcriptional control of microglia phenotypes in health and disease
Holtman, I. R., Skola, D., & Glass, C. K. (2017) · Journal of Clinical Investigation · doi:10.1172/jci90604 · Cited by 218 · see citing works
Self-citationA unified architecture of transcriptional regulatory elements
Andersson, R., Sandelin, A., & Danko, C. G. (2015) · Trends in Genetics · doi:10.1016/j.tig.2015.05.007 · Cited by 211 · see citing works
Opposing macrophage polarization programs show extensive epigenomic and transcriptional cross-talk
Piccolo, V., Curina, A., Genua, M., Ghisletti, S., Simonatto, M., Sabò, A., Amati, B. B., Ostuni, R., & Natoli, G. (2017) · Nature Immunology · doi:10.1038/ni.3710 · Cited by 209 · see citing works
Link, V. M., Duttke, S. H., Chun, H. B., Holtman, I. R., Westin, E., Hoeksema, M. A., Abe, Y., Skola, D., Romanoski, C. E., Tao, J., et al. (2018) · Cell · doi:10.1016/j.cell.2018.04.018 · Cited by 182 · see citing works
Self-citationCatarino, R. R., & Stark, A. (2018) · Genes & Development · doi:10.1101/gad.310367.117 · Cited by 205 · see citing works
Kang, K., Park, S. H., Chen, J., Qiao, Y., Giannopoulou, E., Berg, K., Hanidu, A., Li, J., Nabozny, G., Kang, K., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.07.017 · Cited by 196 · see citing works
CDK9: a signaling hub for transcriptional control
Bacon, C. W., & D’Orso, I. (2018) · Transcription · doi:10.1080/21541264.2018.1523668 · Cited by 201 · see citing works
Functional Hallmarks of Healthy Macrophage Responses: Their Regulatory Basis and Disease Relevance
Sheu, K. M., & Hoffmann, A. (2022) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101320-031555 · Cited by 209 · see citing works
Epigenetics of Atherosclerosis: Emerging Mechanisms and Methods
Khyzha, N., Alizada, A., Wilson, M. D., & Fish, J. E. (2017) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2017.02.004 · Cited by 193 · see citing works
Inflammation-sensitive super enhancers form domains of coordinately regulated enhancer RNAs
Hah, N., Benner, C. W., Chong, L.-W., Yu, R. T., Downes, M., & Evans, R. M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1424028112 · Cited by 189 · see citing works
Zawistowski, J. S., Bevill, S. M., Goulet, D. R., Stuhlmiller, T. J., Beltran, A. S., Olivares-Quintero, J. F., Singh, D., Sciaky, N., Parker, J. S., Rashid, N. U., et al. (2017) · Cancer Discovery · doi:10.1158/2159-8290.cd-16-0653 · Cited by 180 · see citing works
Adaptation and memory in immune responses
Natoli, G., & Ostuni, R. (2019) · Nature Immunology · doi:10.1038/s41590-019-0399-9 · Cited by 186 · see citing works
Identification and dynamic quantification of regulatory elements using total RNAPreprint
Duttke, S. H. C., Chang, M. W., Heinz, S., & Benner, C. W. (2019) · Genome Research · doi:10.1101/gr.253492.119 · Cited by 172 · see citing works
A Muscle-Specific Enhancer RNA Mediates Cohesin Recruitment and Regulates Transcription In trans
Tsai, P.-F., Dell’Orso, S., Rodriguez, J., Vivanco, K. O., Ko, K.-D., Jiang, K., Juan, A. H., Sarshad, A. A., Vian, L., Tran, M. D., et al. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.06.008 · Cited by 178 · see citing works
Dániel, B., Nagy, G., Czimmerer, Z., Horváth, A., Hammers, D. W., Cuaranta‐Monroy, I., Póliska, S., Tzerpos, P., Kolostyák, Z., Hays, T. T., et al. (2018) · Immunity · doi:10.1016/j.immuni.2018.09.005 · Cited by 180 · see citing works
NF-κB dynamics determine the stimulus specificity of epigenomic reprogramming in macrophages
Cheng, Q. J., Ohta, S., Sheu, K. M., Spreafico, R., Adelaja, A., Taylor, B. E., & Hoffmann, A. (2021) · Science · doi:10.1126/science.abc0269 · Cited by 164 · see citing works
Enhancer Logic and Mechanics in Development and Disease
Rickels, R. A., & Shilatifard, A. (2018) · Trends in Cell Biology · doi:10.1016/j.tcb.2018.04.003 · Cited by 165 · see citing works
NF-κB Regulates PD-1 Expression in Macrophages
Bally, A. P. R., Lu, P., Tang, Y., Austin, J. W., Scharer, C. D., Ahmed, R., & Boss, J. M. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402550 · Cited by 164 · see citing works
MLL3/MLL4/COMPASS Family on Epigenetic Regulation of Enhancer Function and Cancer
Sze, C. C., & Shilatifard, A. (2016) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a026427 · Cited by 164 · see citing works
Thomas, G. D., Hanna, R. N., Vasudevan, N. T., Hamers, A. A. J., Romanoski, C. E., McArdle, S., Ross, K. D., Blatchley, A., Yoakum, D., Hamilton, B. A., et al. (2016) · Immunity · doi:10.1016/j.immuni.2016.10.011 · Cited by 163 · see citing works
Epigenetic drug discovery: breaking through the immune barrier
Tough, D. F., Tak, P. P., Tarakhovsky, A., & Prinjha, R. K. (2016) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2016.185 · Cited by 160 · see citing works
BET Family Protein BRD4: An Emerging Actor in NFκB Signaling in Inflammation and Cancer
Hajmirza, A., Emadali, A., Gauthier, A., Casasnovas, O., Gressin, R., & Callanan, M. B. (2018) · Biomedicines · doi:10.3390/biomedicines6010016 · Cited by 159 · see citing works
Decque, A., Joffre, O. P., Magalhaes, J. G., Cossec, J., Blecher‐Gonen, R., Lapaquette, P., Silvin, A., Manel, N., Joubert, P.-E., Seeler, J.-S., et al. (2015) · Nature Immunology · doi:10.1038/ni.3342 · Cited by 157 · see citing works
Epigenetic Remodeling in Innate Immunity and Inflammation
Zhang, Q., & Cao, X. (2021) · Annual Review of Immunology · doi:10.1146/annurev-immunol-093019-123619 · Cited by 158 · see citing works
High-throughput functional comparison of promoter and enhancer activities
Nguyen, T. A., Jones, R. D., Snavely, A. R., Pfenning, A. R., Kirchner, R., Hemberg, M., & Gray, J. M. (2016) · Genome Research · doi:10.1101/gr.204834.116 · Cited by 146 · see citing works
Dichotomous engagement of HDAC3 activity governs inflammatory responses
Nguyen, H. C. B., Adlanmerini, M., Hauck, A. K., & Lazar, M. A. (2020) · Nature · doi:10.1038/s41586-020-2576-2 · Cited by 150 · see citing works
Epigenetics Control Microglia Plasticity
Cheray, M., & Joseph, B. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00243 · Cited by 151 · see citing works
Gene activation precedes DNA demethylation in response to infection in human dendritic cells
Pacis, A., Mailhot-Léonard, F., Tailleux, L., Randolph, H. E., Yotova, V., Dumaine, A., Grenier, J., & Barreiro, L. B. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1814700116 · Cited by 146 · see citing works
Ready, pause, go: regulation of RNA polymerase II pausing and release by cellular signaling pathways
Liu, X., Kraus, W. L., & Bai, X. (2015) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2015.07.003 · Cited by 152 · see citing works
LncRNA-MM2P Identified as a Modulator of Macrophage M2 Polarization
Cao, J., Dong, R., Li, J., Gong, Y., Meng, Y. G., You, J., Meng, W., Chen, Z., Zhang, N., Weng, Q., et al. (2018) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-18-0145 · Cited by 151 · see citing works
Efficient chromatin accessibility mapping in situ by nucleosome-tethered tagmentation
Henikoff, S., Henikoff, J. G., Kaya-Okur, H. S., & Ahmad, K. (2020) · eLife · doi:10.7554/elife.63274 · Cited by 153 · see citing works
The Hierarchy of Transcriptional Activation: From Enhancer to Promoter
Vernimmen, D., & Bickmore, W. A. (2015) · Trends in Genetics · doi:10.1016/j.tig.2015.10.004 · Cited by 155 · see citing works
Beating the odds: BETs in disease
Wang, C., & Filippakopoulos, P. (2015) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2015.06.002 · Cited by 148 · see citing works
Ligand-Dependent Enhancer Activation Regulated by Topoisomerase-I Activity
Puc, J., Koźbiał, P., Li, W., Tan, Y., Liu, Z., Suter, T., Ohgi, K. A., Zhang, J., Aggarwal, A. K., & Rosenfeld, M. G. (2015) · Cell · doi:10.1016/j.cell.2014.12.023 · Cited by 139 · see citing works
Super-enhancer function and its application in cancer targeted therapy
Tang, F., Yang, Z., Tan, Y., & Li, Y. (2020) · npj Precision Oncology · doi:10.1038/s41698-020-0108-z · Cited by 143 · see citing works
Emerging Roles of Non-Coding RNA Transcription
Kaikkonen, M. U., & Adelman, K. (2018) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2018.06.002 · Cited by 141 · see citing works
KMT2D regulates specific programs in heart development via histone H3 lysine 4 di-methylation
Ang, S., Uebersohn, A., Spencer, C. I., Huang, Y., Lee, J., Ge, K., & Bruneau, B. G. (2016) · Development · doi:10.1242/dev.132688 · Cited by 142 · see citing works
Valilou, S. F., Keshavarz‐Fathi, M., Silvestris, N., Argentiero, A., & Rezaei, N. (2018) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2018.01.007 · Cited by 141 · see citing works
Kang, K., Bachu, M., Park, S. H., Kang, K., Bae, S., Park‐Min, K., & Ivashkiv, L. B. (2019) · Nature Communications · doi:10.1038/s41467-019-11147-3 · Cited by 139 · see citing works
- Authors
- Kaikkonen, M. U., Spann, N. J., Heinz, S., Romanoski, C. E., Allison, K. A., Stender, J. D., Chun, H. B., Tough, D. F., Prinjha, R. K., Benner, C., & Glass, C. K.
- Affiliations
- University of Eastern Finland (FI)
- University of California San Diego (US)
- GlaxoSmithKline (United Kingdom) (GB)
- Salk Institute for Biological Studies (US)
- Corresponding author
- Glass, Christopher K.
- ORCID
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2013-08
- Volume
- 51
- Issue
- 3
- Pages
- 310-325
- ISSN
- 1097-2765 (ISSN-L)
- PMC
- PMC3779836
- OpenAlex
- W1998871958
- Cited by
- 672
- References
- 63
- Citations by year
- 2026: 26 · 2025: 36 · 2024: 43 · 2023: 35 · 2022: 52 · 2021: 56 · 2020: 50 · 2019: 46 · 2018: 69 · 2017: 73 · 2016: 61 · 2015: 66 · 2014: 48 · 2013: 11
- FWCI
- 27.79
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Fondation Leducq
- Academy of Finland
- Suomen Kulttuurirahasto
- Sydäntutkimussäätiö
- National Institutes of Health
- National Cancer Institute (R01CA173903, CA17390)
- National Institute of General Medical Sciences (T32GM008806)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK063491, DK091183, P01DK074868, P30DK063491, R01DK091183)
- 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
- enhancer remodeling, macrophage activation, enhancer transcription, TLR4 signaling, H3K4 methylation, MLL1, MLL3, RNA polymerase II elongation, enhancer RNA, histone methyltransferase
- MeSH terms
- Proto-Oncogene Protein Spi-1, Animals, Base Sequence, Cells, Cultured, DNA-Binding Proteins, Enhancer Elements, Genetic, Gene Expression Regulation, Histones, Macrophage Activation, Macrophages, Male, Mice, Inbred C57BL, Histone-Lysine N-Methyltransferase, Proto-Oncogene Proteins, RNA Polymerase II, Transcription, Genetic, Signal Transduction, Trans-Activators, Gene Expression, NF-kappa B, Sequence Analysis, DNA, DNA Methylation, CCAAT-Enhancer-Binding Proteins, Toll-Like Receptor 4, Mice, Myeloid-Lymphoid Leukemia Protein, Transcription Factor RelA
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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