The transcription factor Grainy head primes epithelial enhancers for spatiotemporal activation by displacing nucleosomes
Open accessAbstract
Transcriptional enhancers function as docking platforms for combinations of transcription factors (TFs) to control gene expression. How enhancer sequences determine nucleosome occupancy, TF recruitment and transcriptional activation in vivo remains unclear. Using ATAC-seq across a panel of Drosophila inbred strains, we found that SNPs affecting binding sites of the TF Grainy head (Grh) causally determine the accessibility of epithelial enhancers. We show that deletion and ectopic expression of Grh cause loss and gain of DNA accessibility, respectively. However, although Grh binding is necessary for enhancer accessibility, it is insufficient to activate enhancers. Finally, we show that human Grh homologs-GRHL1, GRHL2 and GRHL3-function similarly. We conclude that Grh binding is necessary and sufficient for the opening of epithelial enhancers but not for their activation. Our data support a model positing that complex spatiotemporal expression patterns are controlled by regulatory hierarchies in which pioneer factors, such as Grh, establish tissue-specific accessible chromatin landscapes upon which other factors can act.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
A potentially large fraction of accessible regions captured by scATAC-seq may not represent functional enhancers.
“Thus, a potentially large fraction of accessible regions, as captured by scATAC-seq, may not represent functional enhancers.”
From Enhancer grammar of liver cell types and hepatocyte zonation states (2022) · cites this paper as [9]
In Results, “Grainyhead regulates enhancer accessibility but not activity” (page unavailable), 15 of 21 tested Grh-target regions showed reporter activity in the eye-antennal disc, and single-cell ATAC-seq accessibility did not establish activity. This supports the caution that accessibility alone does not establish enhancer function, but the paper does not estimate a potentially large nonfunctional fraction across scATAC-seq accessible regions; regions inactive in that disc could function elsewhere. (LLM, conf=0.84)
Experimental — accuracy not yet measuredAt least some pioneer factors, such as FOXA, OCT4 and SOX2/SOX11, initiate chromatin opening by direct displacement of histones.
“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 [41]
The introductory passage (labelled Abstract in our copy; page unavailable) describes pioneer factors as transcription factors that can displace nucleosomes and names FOXA1 and SOX2 as examples. The Results section, “Functional Grainyhead motifs are embedded in a specific DNA context” (page unavailable), also associates pioneer-factor binding with nucleosome displacement. But the paper does not establish direct histone displacement for each named factor: it mentions OCT4 as a possible additional factor needed for SOX2-dependent enhancer activation and does not mention SOX11. (LLM, conf=0.84)
Experimental — accuracy not yet measuredChromatin accessibility is not necessarily always associated with enhancer activity.
“However, chromatin accessibility is not necessarily always associated with enhancer activity35.”
From Single-cell spatial multi-omics and deep learning dissect enhancer-driven gene regulatory networks in liver zonation (2024) · cites this paper as [35]
Chromatin accessibility is necessary but not sufficient for enhancer activity.
“chromatin accessibility is necessary but not sufficient for activity9.”
From Enhancer grammar of liver cell types and hepatocyte zonation states (2022) · cites this paper as [9]
Chromatin accessibility is not necessarily always associated with enhancer activity.
“chromatin accessibility is not necessarily always associated with enhancer activity9.”
From Enhancer grammar of liver cell types and hepatocyte zonation states (2022) · cites this paper as [9]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
Scikit-learn: Machine Learning in Python
Pedregosa, F., Varoquaux, G., Gramfort, A., Michel, V., Thirion, B., Grisel, O., Blondel, M., Müller, A., Nothman, J., Louppe, G., et al. (2012) · arXiv · doi:10.48550/arxiv.1201.0490 · Cited by 71,016 · see citing works
The Sequence Alignment/Map format and SAMtools
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp352 · Cited by 62,041 · see citing works
Fast gapped-read alignment with Bowtie 2
Langmead, B., & Salzberg, S. L. (2012) · Nature Methods · doi:10.1038/nmeth.1923 · Cited by 56,400 · see citing works
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625 · see citing works
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
Liao, Y., Smyth, G. K., & Shi, W. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btt656 · Cited by 27,219 · see citing works
Model-based Analysis of ChIP-Seq (MACS)
Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C., Myers, R. M., Brown, M., Li, W., et al. (2008) · Genome Biology · doi:10.1186/gb-2008-9-9-r137 · Cited by 18,386 · see citing works
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
The variant call format and VCFtools
Danecek, P., Auton, A., Abecasis, G. R., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G. A., Marth, G., Sherry, S. T., et al. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr330 · Cited by 16,008 · see citing works
pROC: an open-source package for R and S+ to analyze and compare ROC curves
Robin, X., Turck, N., Hainard, A., Tiberti, N., Lisacek, F., Sanchez, J.-C., & Müller, M. (2011) · BMC Bioinformatics · doi:10.1186/1471-2105-12-77 · Cited by 13,697 · 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
EMBOSS: the European molecular biology open software suite.
Rice, P., Longden, I., & Bleasby, A. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(00)02024-2 · Cited by 9,466 · see citing works
The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity
Barretina, J., Caponigro, G., Stransky, N., Venkatesan, K., Margolin, A. A., Kim, S., Wilson, C. J., Lehár, J., Kryukov, G. V., Sonkin, D., et al. (2012) · Nature · doi:10.1038/nature11003 · Cited by 7,950 · see citing works
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y., & Greenleaf, W. J. (2013) · Nature Methods · doi:10.1038/nmeth.2688 · Cited by 6,422 · see citing works
Core Transcriptional Regulatory Circuitry in Human Embryonic Stem Cells
Boyer, L. A., Lee, T. I., Cole, M. F., Johnstone, S. E., Levine, S. S., Zucker, J. P., Guenther, M. G., Kumar, R. M., Murray, H. L., Jenner, R. G., et al. (2005) · Cell · doi:10.1016/j.cell.2005.08.020 · Cited by 4,505 · see citing works
Using RepeatMasker to Identify Repetitive Elements in Genomic Sequences
Tarailo‐Graovac, M., & Chen, N. (2009) · Current Protocols in Bioinformatics · doi:10.1002/0471250953.bi0410s25 · Cited by 3,429 · see citing works
An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues
Corces, M. R., Trevino, A. E., Hamilton, E. G., Greenside, P. G., Sinnott-Armstrong, N. A., Vesuna, S., Satpathy, A. T., Rubin, A. J., Montine, K. S., Wu, B., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4396 · Cited by 2,496 · see citing works
The ENCODE (ENCyclopedia Of DNA Elements) Project
(2004) · Science · doi:10.1126/science.1105136 · Cited by 2,390 · see citing works
Single-cell chromatin accessibility reveals principles of regulatory variation
Buenrostro, J. D., Wu, B., Litzenburger, U. M., Ruff, D., Gonzales, M. L., Snyder, M. P., Chang, H. Y., & Greenleaf, W. J. (2015) · Nature · doi:10.1038/nature14590 · Cited by 2,308 · see citing works
BEDTools: The Swiss‐Army Tool for Genome Feature Analysis
Quinlan, A. R. (2014) · Current Protocols in Bioinformatics · doi:10.1002/0471250953.bi1112s47 · Cited by 2,286 · see citing works
Transcription factors: from enhancer binding to developmental control
Spitz, F., & Furlong, E. E. M. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3207 · Cited by 2,227 · see citing works
The NIH Roadmap Epigenomics Mapping Consortium
Bernstein, B. E., Stamatoyannopoulos, J. A., Costello, J. F., Ren, B., Milosavljevic, A., Meissner, A., Kellis, M., Marra, M. A., Beaudet, A. L., Ecker, J. R., et al. (2010) · Nature Biotechnology · doi:10.1038/nbt1010-1045 · Cited by 1,892 · see citing works
A comparative encyclopedia of DNA elements in the mouse genome
Yue, F., Cheng, Y., Breschi, A., Vierstra, J., Wu, W., Ryba, T., Sandstrom, R., Ma, Z., Davis, C., Pope, B. D., et al. (2014) · Nature · doi:10.1038/nature13992 · Cited by 1,781 · see citing works
The Drosophila melanogaster Genetic Reference Panel
Mackay, T., Richards, S., Stone, E. A., Barbadilla, A., Ayroles, J., Zhu, D., Casillas, S., Han, Y., Magwire, M., Cridland, J., et al. (2012) · Nature · doi:10.1038/nature10811 · Cited by 1,686 · see citing works
chromVAR: inferring transcription-factor-associated accessibility from single-cell epigenomic data
Schep, A. N., Wu, B., Buenrostro, J. D., & Greenleaf, W. J. (2017) · Nature Methods · doi:10.1038/nmeth.4401 · Cited by 1,680 · see citing works
Pioneer transcription factors: establishing competence for gene expression
Zaret, K. S., & Carroll, J. S. (2011) · Genes & Development · doi:10.1101/gad.176826.111 · Cited by 1,589 · see citing works
Mutations affecting the pattern of the larval cuticle inDrosophila melanogaster
N�sslein-Volhard, C., Wieschaus, E. F., & Kluding, H. (1984) · Development Genes and Evolution · doi:10.1007/bf00848156 · Cited by 1,550 · see citing works
Robertson, G., Hirst, M., Bainbridge, M., Bilenky, M., Zhao, Y., Zeng, T., Euskirchen, G., Bernier, B., Varhol, R., Delaney, A., et al. (2007) · Nature Methods · doi:10.1038/nmeth1068 · Cited by 1,454 · see citing works
Transcriptional enhancers: from properties to genome-wide predictions
Shlyueva, D., Stampfel, G., & Stark, A. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3682 · Cited by 1,356 · see citing works
The DNA-encoded nucleosome organization of a eukaryotic genome
Kaplan, N., Moore, I. K., Fondufe-Mittendorf, Y., Gossett, A., Tillo, D., Field, Y., Leproust, E., Hughes, T., Lieb, J., Widom, J., et al. (2008) · Nature · doi:10.1038/nature07667 · Cited by 1,296 · see citing works
The Logic of Inductive Inference
Fisher, R. A. (1935) · Journal Of The Royal Statistical Society · doi:10.2307/2342435 · Cited by 1,292 · see citing works
Identification of Functional Elements and Regulatory Circuits by Drosophila modENCODE
Roy, S., Ernst, J., Kharchenko, P. V., Kheradpour, P., Negre, N. N., Eaton, M. L., Landolin, J. M., Bristow, C. A., Ma, L., Lin, M. F., et al. (2010) · Science · doi:10.1126/science.1198374 · Cited by 1,223 · see citing works
Genome-Wide Quantitative Enhancer Activity Maps Identified by STARR-seq
Arnold, C. D., Gerlach, D., Stelzer, C., Boryń, Ł. M., Rath, M., & Stark, A. (2013) · Science · doi:10.1126/science.1232542 · Cited by 1,125 · see citing works
Luo, L.-Q., Liao, Y.-J., Jan, L., & Jan, Y. (1994) · Genes & Development · doi:10.1101/gad.8.15.1787 · Cited by 1,036 · see citing works
Tools for neuroanatomy and neurogenetics in Drosophila
Pfeiffer, B. D., Jenett, A., Hammonds, A. S., Ngo, T.-T. B., Misra, S., Murphy, C., Scully, A. L., Carlson, J. W., Wan, K. H., Laverty, T., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803697105 · Cited by 974 · see citing works
124: The Logic of Inductive Inference.
Fisher, R. A. (1935) · Adelaide Research & Scholarship (AR&S) (University of Adelaide) · Cited by 872 · see citing works
Pioneer Transcription Factors Target Partial DNA Motifs on Nucleosomes to Initiate Reprogramming
Soufi, A., Garcia, M. F., Jaroszewicz, A., Osman, N., Pellegrini, M., & Zaret, K. S. (2015) · Cell · doi:10.1016/j.cell.2015.03.017 · Cited by 780 · see citing works
Visualization of a Correlation Matrix [R package corrplot version 0.84]
Wei, T., & Šimko, V. (2017) · Cited by 737 · see citing works
Melnikov, A., Murugan, A., Zhang, X., Tesileanu, T., Wang, L., Rogov, P., Feizi, S., Gnirke, A., Callan, C. G., Kinney, J. B., et al. (2012) · Nature Biotechnology · doi:10.1038/nbt.2137 · Cited by 711 · see citing works
Determinants of nucleosome positioning
Struhl, K., & Segal, E. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2506 · Cited by 685 · see citing works
DNase I sensitivity QTLs are a major determinant of human expression variation
Degner, J. F., Pai, A. A., Piqué-Regi, R., Veyrieras, J., Gaffney, D. J., Pickrell, J. K., Leon, S. D., Michelini, K., Lewellen, N., Crawford, G. E., et al. (2012) · Nature · doi:10.1038/nature10808 · Cited by 633 · see citing works
Song, L., & Crawford, G. E. (2010) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot5384 · Cited by 625 · see citing works
Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures
Stark, A., Lin, M. F., Kheradpour, P., Pedersen, J. S., Parts, L., Carlson, J. W., Crosby, M. A., Rasmussen, M. D., Roy, S., Deoras, A. N., et al. (2007) · Nature · doi:10.1038/nature06340 · Cited by 624 · see citing works
Self-citationPioneer transcription factors in cell reprogrammingPreprint
Iwafuchi, M., & Zaret, K. S. (2014) · Genes & Development · doi:10.1101/gad.253443.114 · Cited by 590 · see citing works
Emerging properties of animal gene regulatory networks
Davidson, E. H. (2010) · Nature · doi:10.1038/nature09645 · Cited by 579 · see citing works
Huang, W., Massouras, A., Inoue, Y., Peiffer, J., Ràmia, M., Tarone, A. M., Turlapati, L., Zichner, T., Zhu, D., Lyman, R. F., et al. (2014) · Genome Research · doi:10.1101/gr.171546.113 · Cited by 578 · see citing works
Massively parallel functional dissection of mammalian enhancers in vivo
Patwardhan, R. P., Hiatt, J. B., Witten, D. M., Kim, M. J., Smith, R. P., May, D., Lee, C., Andrie, J. M., Lee, S.-I., Cooper, G. M., et al. (2012) · Nature Biotechnology · doi:10.1038/nbt.2136 · Cited by 536 · see citing works
FlyBase at 25: looking to the future
Gramates, L. S., Marygold, S. J., dos Santos, G., Urbano, J.-M., Antonazzo, G., Matthews, B. B., Rey, A. J., Tabone, C. J., Crosby, M. A., Emmert, D. B., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1016 · Cited by 535 · see citing works
ChIPmentation: fast, robust, low-input ChIP-seq for histones and transcription factors
Schmidl, C., Rendeiro, A. F., Sheffield, N. C., & Bock, C. (2015) · Nature Methods · doi:10.1038/nmeth.3542 · Cited by 509 · see citing works
Transcription Factors Bind Thousands of Active and Inactive Regions in the Drosophila Blastoderm
Li, X., MacArthur, S., Bourgon, R., Nix, D. A., Pollard, D. A., Iyer, V. N., Hechmer, A., Simirenko, L., Stapleton, M., Hendriks, C. L. L., et al. (2008) · eScholarship (California Digital Library) · doi:10.1371/journal.pbio.0060027 · Cited by 479 · see citing works
The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila
Liang, H.-L., Nien, C.-Y., Liu, H.-Y., Metzstein, M. M., Kirov, N., & Rushlow, C. (2008) · Nature · doi:10.1038/nature07388 · Cited by 478 · see citing works
STAMP: a web tool for exploring DNA-binding motif similarities
Mahony, S., & Benos, P. V. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm272 · Cited by 469 · see citing works
Genome-scale functional characterization of Drosophila developmental enhancers in vivo
Kvon, E. Z., Kazmar, T., Stampfel, G., Yáñez-Cuna, J. O., Pagani, M., Schernhuber, K., Dickson, B. J., & Stark, A. (2014) · Nature · doi:10.1038/nature13395 · Cited by 436 · see citing works
seqMINER: an integrated ChIP-seq data interpretation platform
Ye, T., Krebs, A. R., Choukrallah, M.-A., Keime, C., Plewniak, F., Davidson, I., & Tora, L. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1287 · Cited by 410 · see citing works
Sox2, a key factor in the regulation of pluripotency and neural differentiation
Zhang, S. (2014) · World Journal of Stem Cells · doi:10.4252/wjsc.v6.i3.305 · Cited by 399 · see citing works
Evaluation of methods for modeling transcription factor sequence specificity
DREAM5 Consortium, Weirauch, M. T., Cote, A., Norel, R., Annala, M., Zhao, Y., Riley, T. R., Saez-Rodriguez, J., Cokelaer, T., Vedenko, A., et al. (2013) · Nature Biotechnology · doi:10.1038/nbt.2486 · Cited by 381 · see citing works
FlyMine: an integrated database for Drosophila and Anopheles genomics
Lyne, R., Smith, R. N., Rutherford, K., Wakeling, M. N., Varley, A., Guillier, F., Janssens, H., Ji, W., Mclaren, P., North, P., et al. (2007) · Genome biology · doi:10.1186/gb-2007-8-7-r129 · Cited by 376 · see citing works
Combinatorial function of transcription factors and cofactors
Reiter, F., Wienerroither, S., & Stark, A. (2017) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.12.007 · Cited by 354 · see citing works
DNA Methylation Detection: Bisulfite Genomic Sequencing Analysis
Li, Y., & Tollefsbol, T. O. (2011) · Methods in Molecular Biology · doi:10.1007/978-1-61779-316-5_2 · Cited by 352 · see citing works
Cluster-Buster: finding dense clusters of motifs in DNA sequences
Frith, M. C. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg540 · Cited by 326 · see citing works
Transcriptional enhancers: Intelligent enhanceosomes or flexible billboards?
Arnosti, D. N., & Kulkarni, M. M. (2005) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20352 · Cited by 309 · see citing works
High-resolution genome-wide in vivo footprinting of diverse transcription factors in human cellsPreprint
Boyle, A. P., Song, L., Lee, B., London, D., Keefe, D., Birney, E., Iyer, V. R., Crawford, G. E., & Furey, T. S. (2010) · Genome Research · doi:10.1101/gr.112656.110 · Cited by 305 · see citing works
Fine-mapping cellular QTLs with RASQUAL and ATAC-seq
Kumasaka, N., Knights, A. J., & Gaffney, D. J. (2015) · Nature Genetics · doi:10.1038/ng.3467 · Cited by 259 · see citing works
An Epidermal Barrier Wound Repair Pathway in Drosophila Is Mediated by grainy head
Mace, K. A., Pearson, J. C., & McGinnis, W. J. (2005) · Science · doi:10.1126/science.1107573 · Cited by 241 · see citing works
RSAT peak-motifs: motif analysis in full-size ChIP-seq datasets
Thomas‐Chollier, M., Herrmann, C., Defrance, M., Sand, O., Thieffry, D., & van Helden, J. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1104 · Cited by 239 · see citing works
Propeller-Twisting of Base-pairs and the Conformational Mobility of Dinucleotide Steps in DNA
Hassan, M. A. E., & Calladine, C. R. (1996) · Journal of Molecular Biology · doi:10.1006/jmbi.1996.0304 · Cited by 236 · see citing works
Cirillo, L. A., & Zaret, K. S. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80225-7 · Cited by 235 · see citing works
Detection of cis -element clusters in higher eukaryotic DNA
Frith, M. C., Hansen, U. M., & Weng, Z. (2001) · Bioinformatics · doi:10.1093/bioinformatics/17.10.878 · Cited by 235 · see citing works
Barozzi, I., Simonatto, M., Bonifacio, S., Yang, L., Rohs, R., Ghisletti, S., & Natoli, G. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.04.006 · Cited by 209 · see citing works
i-cisTarget 2015 update: generalized cis-regulatory enrichment analysis in human, mouse and fly
Imrichová, H., Hulselmans, G., Kalender Atak, Z., Potier, D., & Aerts, S. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv395 · Cited by 202 · see citing works
Self-citationHerrmann, C., de Sande, B. V., Potier, D., & Aerts, S. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks543 · Cited by 202 · see citing works
Self-citationDavie, K., Jacobs, J., Atkins, M., Potier, D., Christiaens, V., Halder, G. A., & Aerts, S. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1004994 · Cited by 160 · see citing works
Self-citationWilanowski, T., Tuckfield, A., Cerruti, L., O’Connell, S., Saint, R. B., Parekh, V., Tao, J., Cunningham, J. M., & Jane, S. M. (2002) · Mechanisms of Development · doi:10.1016/s0925-4773(02)00046-1 · Cited by 154 · see citing works
Chung, V. Y., Tan, T. Z., Tan, M., Wong, M. K., Kuay, K. T., Yang, Z., Ye, J., Müller, J., Koh, C. M., Guccione, E., et al. (2016) · Scientific Reports · doi:10.1038/srep19943 · Cited by 148 · see citing works
Zelda Potentiates Morphogen Activity by Increasing Chromatin Accessibility
Foo, S. M., Sun, Y., Lim, B., Ziukaite, R., O’Brien, K. M., Nien, C.-Y., Kirov, N., Shvartsman, S. Y., & Rushlow, C. A. (2014) · Current Biology · doi:10.1016/j.cub.2014.04.032 · Cited by 129 · see citing works
Castro-Mondragon, J. A., Jaeger, S., Thieffry, D., Thomas‐Chollier, M., & van Helden, J. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx314 · Cited by 126 · see citing works
Different combinations of gap repressors for common stripes in Anopheles and Drosophila embryos
Goltsev, Y., Hsiong, W., Lanzaro, G. C., & Levine, M. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.08.021 · Cited by 112 · see citing works
Genome-wide identification of direct targets of the Drosophila retinal determination protein EyelessPreprint
Ostrin, E. J., Li, Y., Hoffman, K. L., Liu, J., Wang, K., Zhang, L., Mardon, G., & Chen, R. (2006) · Genome Research · doi:10.1101/gr.4673006 · Cited by 105 · see citing works
Venkatesan, K. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg644 · Cited by 94 · see citing works
Aerts, S., Quan, X., Claeys, A., Naval-Sánchez, M., Tate, P., Yan, J., & Hassan, B. A. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000435 · Cited by 92 · see citing works
Self-citationGenome-wide identification of neuronal activity-regulated genes in Drosophila
Chen, X., Rahman, R., Guo, F., & Rosbash, M. (2016) · eLife · doi:10.7554/elife.19942 · Cited by 91 · see citing works
Grainyhead and Zelda compete for binding to the promoters of the earliest-expressed Drosophila genes
Harrison, M. M., Botchan, M. R., & Cline, T. W. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.06.026 · Cited by 88 · see citing works
Gao, X., Vockley, C. M., Pauli, F., Newberry, K. M., Xue, Y., Randell, S. H., Reddy, T. E., & Hogan, B. L. M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1307589110 · Cited by 86 · see citing works
The tyrosine kinase Stitcher activates Grainy head and epidermal wound healing in Drosophila
Wang, S., Tsarouhas, V., Xylourgidis, N., Sabri, N., Tiklová, K., Nautiyal, N., Gallio, M., & Samakovlis, C. (2009) · Nature Cell Biology · doi:10.1038/ncb1898 · Cited by 86 · see citing works
Multiplex enhancer-reporter assays uncover unsophisticated TP53 enhancer logic
Verfaillie, A., Svetlichnyy, D., Imrichova, H., Davie, K., Fiers, M., Kalender Atak, Z., Hulselmans, G., Christiaens, V., & Aerts, S. (2016) · Genome Research · doi:10.1101/gr.204149.116 · Cited by 82 · see citing works
Self-citationRoles of Grainyhead-like transcription factors in cancer
Frisch, S. M., Farris, J. C., & Pifer, P. M. (2017) · Oncogene · doi:10.1038/onc.2017.178 · Cited by 81 · see citing works
Varma, S., Cao, Y., Tagne, J.-B., Lakshminarayanan, M., Li, J., Friedman, T. B., Morell, R. J., Warburton, D., Kotton, D. N., & Ramirez, M. I. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.408401 · Cited by 79 · see citing works
Grainy head promotes expression of septate junction proteins and influences epithelial morphogenesis
Narasimha, M., Uv, A., Krejčı́, A., Brown, N. H., & Bray, S. J. (2008) · Journal of Cell Science · doi:10.1242/jcs.019422 · Cited by 77 · see citing works
Potier, D., Davie, K., Hulselmans, G. J., Naval-Sánchez, M., Haagen, L., Huynh‐Thu, V. A., Koldere, D., Çelik, A., Geurts, P., Christiaens, V., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.11.038 · Cited by 74 · see citing works
Self-citationp53 regulates enhancer accessibility and activity in response to DNA damage
Younger, S. T., & Rinn, J. L. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx577 · Cited by 71 · see citing works
GBshape: a genome browser database for DNA shape annotations
Chiu, T.-P., Yang, L., Zhou, T., Main, B. J., Parker, S. C. J., Nuzhdin, S. V., Tullius, T. D., & Rohs, R. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku977 · Cited by 61 · see citing works
Paré, A. C., Kim, M.-J., Juarez, M. T., Brody, S., & McGinnis, W. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036254 · Cited by 57 · see citing works
Nevil, M., Bondra, E. R., Schulz, K. N., Kaplan, T., & Harrison, M. M. (2016) · Genetics · doi:10.1534/genetics.116.195685 · Cited by 53 · see citing works
Structural basis of gene regulation by the Grainyhead/CP2 transcription factor family
Ming, Q., Roske, Y., Schuetz, A., Walentin, K., Ibraimi, I., Schmidt-Ott, K. M., & Heinemann, U. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx1299 · Cited by 50 · see citing works
van Bergeijk, P., Heimiller, J., Uyetake, L., & Su, T. T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036539 · Cited by 33 · see citing works
Grainyhead-like Transcription Factors in Craniofacial Development
Carpinelli, M. R., de Vries, M. E., Jane, S. M., & Dworkin, S. (2017) · Journal of Dental Research · doi:10.1177/0022034517719264 · Cited by 24 · see citing works
Svetlichnyy, D., Imrichová, H., Fiers, M. W. E. J., Atak, Z. K., & Aerts, S. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004590 · Cited by 22 · see citing works
Self-citationVarma, S., Mahavadi, P., Sasikumar, S., Cushing, L., Hyland, T., Rosser, A., Riccardi, D., Lü, J., Kalin, T. V., Kalinichenko, V. V., et al. (2013) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00143.2013 · Cited by 20 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Pioneer Transcription Factors Initiating Gene Network Changes
Zaret, K. S. (2020) · Annual Review of Genetics · doi:10.1146/annurev-genet-030220-015007 · Cited by 398 · see citing works
Ulz, P., Perakis, S. O., Zhou, Q. X., Moser, T., Belic, J., Lazzeri, I., Wölfler, A., Zebisch, A., Gerger, A., Pristauz, G., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12714-4 · Cited by 265 · see citing works
Pioneer factors as master regulators of the epigenome and cell fate
Balsalobre, A., & Drouin, J. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00464-z · Cited by 251 · see citing works
Chromatin accessibility profiling methods
Minnoye, L., Marinov, G. K., Krausgruber, T., Pan, L., Marand, A. P., Secchia, S., Greenleaf, W. J., Furlong, E. E. M., Zhao, K., Schmitz, R. J., et al. (2021) · Nature Reviews Methods Primers · doi:10.1038/s43586-020-00008-9 · Cited by 206 · see citing works
Self-citationHypoxia, partial EMT and collective migration: Emerging culprits in metastasis
Saxena, K., Jolly, M. K., & Balamurugan, K. (2020) · Translational Oncology · doi:10.1016/j.tranon.2020.100845 · Cited by 198 · see citing works
Cell-type-directed design of synthetic enhancers
Taskiran, I. I., Spanier, K. I., Dickmänken, H., Kempynck, N., Pančíková, A., Ekşi, E. C., Hulselmans, G., Ismail, J. N., Theunis, K., Vandepoel, R., et al. (2024) · Nature · doi:10.1038/s41586-023-06936-2 · Cited by 175 · see citing works
Self-citationDecoding gene regulation in the fly brain
Janssens, J., Aibar, S., Taskiran, I. I., Ismail, J. N., Spanier, K. I., Bravo González-Blas, C., Quan, X. J., Papasokrati, D., Hulselmans, G., Makhzami, S., et al. (2021) · doi:10.1101/2021.08.11.454937 · Cited by 170 · see citing works
Self-citationDecoding gene regulation in the fly brain
Janssens, J., Aibar, S., Taskiran, I. I., Ismail, J. N., Gomez, A. E., Aughey, G., Spanier, K. I., De Rop, F. V., González-Blas, C. B., Dionne, M., et al. (2022) · Nature · doi:10.1038/s41586-021-04262-z · Cited by 170 · see citing works
Self-citationPioneer and nonpioneer factor cooperation drives lineage specific chromatin opening
Mayran, A., Sochodolsky, K., Khetchoumian, K., Harris, J., Gauthier, Y., Bemmo, A., Balsalobre, A., & Drouin, J. (2019) · Nature Communications · doi:10.1038/s41467-019-11791-9 · Cited by 137 · see citing works
Pioneer factors: roles and their regulation in development
Barral, A., & Zaret, K. S. (2023) · Trends in Genetics · doi:10.1016/j.tig.2023.10.007 · Cited by 126 · see citing works
Loubiere, V., Papadopoulos, G. L., Szabo, Q., Martinez, A.-M., & Cavalli, G. (2020) · Science Advances · doi:10.1126/sciadv.aax4001 · Cited by 126 · see citing works
Liao, T., & Yang, M. (2020) · Cells · doi:10.3390/cells9030623 · Cited by 128 · see citing works
Cross-species analysis of enhancer logic using deep learning
Minnoye, L., Taskiran, I. I., Mauduit, D., Fazio, M., Van Aerschot, L., Hulselmans, G., Christiaens, V., Makhzami, S., Seltenhammer, M., Karras, P., et al. (2020) · Genome Research · doi:10.1101/gr.260844.120 · Cited by 116 · see citing works
Self-citationSeven myths of how transcription factors read the cis-regulatory code
Zeitlinger, J. (2020) · Current Opinion in Systems Biology · doi:10.1016/j.coisb.2020.08.002 · Cited by 101 · see citing works
Friman, E. T., Deluz, C., Meireles-Filho, A. C. A., Govindan, S., Gardeux, V., Deplancke, B., & Suter, D. M. (2019) · eLife · doi:10.7554/elife.50087 · Cited by 92 · see citing works
Chung, V. Y., Tan, T. Z., Ye, J., Huang, R., Lai, H., Kappei, D., Wollmann, H., Guccione, E., & Huang, R. Y. (2019) · Communications Biology · doi:10.1038/s42003-019-0506-3 · Cited by 91 · see citing works
Bravo González‐Blas, C., Quan, X., Duran‐Romaña, R., Taskiran, I. I., Koldere, D., Davie, K., Christiaens, V., Makhzami, S., Hulselmans, G., de Waegeneer, M., et al. (2020) · Molecular Systems Biology · doi:10.15252/msb.20209438 · Cited by 88 · see citing works
Self-citationTargeted design of synthetic enhancers for selected tissues in the Drosophila embryo
de Almeida, B. P., Schaub, C., Pagani, M., Secchia, S., Furlong, E. E. M., & Stark, A. (2024) · Nature · doi:10.1038/s41586-023-06905-9 · Cited by 87 · see citing works
Bravo González-Blas, C., Matetovici, I., Hillen, H., Taskiran, I. I., Vandepoel, R., Christiaens, V., Sansores-García, L., Verboven, E., Hulselmans, G., Poovathingal, S., et al. (2024) · Nature Cell Biology · doi:10.1038/s41556-023-01316-4 · Cited by 85 · see citing works
“However, chromatin accessibility is not necessarily always associated with enhancer activity 35 .”
Self-citationDeterminants of transcription factor regulatory range
Chen, C.-H., Zheng, R., Tokheim, C., Dong, X., Fan, J., Wan, C., Tang, Q., Brown, M., Liu, J. S., Meyer, C. A., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16106-x · Cited by 85 · see citing works
Actors with Multiple Roles: Pleiotropic Enhancers and the Paradigm of Enhancer Modularity
Sabarís, G., Laiker, I., Preger-Ben Noon, E., & Frankel, N. (2019) · Trends in Genetics · doi:10.1016/j.tig.2019.03.006 · Cited by 84 · see citing works
Transcriptional enhancers and their communication with gene promoters
Ray-Jones, H., & Spivakov, M. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03903-w · Cited by 81 · see citing works
Brennan, K., Weilert, M., Krueger, S., Pampari, A., Liu, H., Yang, A. W. H., Morrison, J. A., Hughes, T. R., Rushlow, C. A., Kundaje, A. B., et al. (2023) · Developmental Cell · doi:10.1016/j.devcel.2023.07.007 · Cited by 76 · see citing works
Liao, Y., Zhang, X., Chakraborty, M., & Emerson, J. J. (2021) · Genome Research · doi:10.1101/gr.266130.120 · Cited by 71 · see citing works
Androgen-regulated transcription of ESRP2 drives alternative splicing patterns in prostate cancer
Munkley, J., Li, L., Krishnan, S. R. G., Hysenaj, G., Scott, E., Dalgliesh, C., Oo, H. Z., Maia, T. M., Cheung, K., Ehrmann, I. E., et al. (2019) · eLife · doi:10.7554/elife.47678 · Cited by 73 · see citing works
Pioneering the developmental frontier
Larson, E. D., Marsh, A. J., & Harrison, M. M. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.02.020 · Cited by 64 · see citing works
Core transcription regulatory circuitry orchestrates corneal epithelial homeostasis
Li, M., Huang, H., Li, L., He, C., Zhu, L., Guo, H., Wang, L., Liu, J., Wu, S., Liu, J., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20713-z · Cited by 61 · see citing works
Collapse of the hepatic gene regulatory network in the absence of FoxA factors
Reizel, Y., Morgan, A., Gao, L., Lan, Y., Manduchi, E., Waite, E. L., Wang, A. W., Wells, A., & Kaestner, K. H. (2020) · Genes & Development · doi:10.1101/gad.337691.120 · Cited by 60 · see citing works
Inherency of Form and Function in Animal Development and Evolution
Newman, S. A. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00702 · Cited by 55 · see citing works
Gentsch, G. E., Spruce, T., Owens, N. D. L., & Smith, J. C. (2019) · Nature Communications · doi:10.1038/s41467-019-12263-w · Cited by 57 · see citing works
Galupa, R., Álvarez-Canales, G., Borst, N. O., Fuqua, T., Gándara, L., Misunou, N., Richter, K., Alves, M. R. P., Karumbi, E., Perkins, M. L., et al. (2022) · Developmental Cell · doi:10.1016/j.devcel.2022.12.003 · Cited by 51 · see citing works
Cell-type-specific Hox regulatory strategies orchestrate tissue identity
Loker, R., Sanner, J. E., & Mann, R. S. (2021) · Current Biology · doi:10.1016/j.cub.2021.07.030 · Cited by 48 · see citing works
Interpretation of allele-specific chromatin accessibility using cell state–aware deep learning
Atak, Z. K., Taskiran, I. I., Demeulemeester, J., Flerin, C., Mauduit, D., Minnoye, L., Hulselmans, G., Christiaens, V., Ghanem, G.-E., Wouters, J., et al. (2021) · Genome Research · doi:10.1101/gr.260851.120 · Cited by 48 · see citing works
Self-citationChromatin accessibility and histone acetylation in the regulation of competence in early development
Esmaeili, M., Blythe, S. A., Tobias, J. W., Zhang, K., Yang, J., & Klein, P. S. (2020) · Developmental Biology · doi:10.1016/j.ydbio.2020.02.013 · Cited by 46 · see citing works
Transcription Control of Liver Development
Tachmatzidi, E. C., Galanopoulou, O., & Talianidis, I. (2021) · Cells · doi:10.3390/cells10082026 · Cited by 45 · see citing works
Peñalosa-Ruiz, G., Bright, A. R., Mulder, K. W., & Veenstra, G. J. C. (2019) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2019.194407 · Cited by 41 · see citing works
Cell differentiation: What have we learned in 50 years?
Newman, S. A. (2019) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2019.110031 · Cited by 40 · see citing works
Fischer, F., Grigolon, G., Benner, C., & Ristow, M. (2022) · Physiological Reviews · doi:10.1152/physrev.00017.2021 · Cited by 41 · see citing works
Grainyhead-like Protein 2: The Emerging Role in Hormone-Dependent Cancers and Epigenetics
Reese, R., Harrison, M. M., & Alarid, E. T. (2019) · Endocrinology · doi:10.1210/en.2019-00213 · Cited by 38 · see citing works
Bridoux, L., Zarrineh, P., Mallen, J., Phuycharoen, M., Latorre, V., Ladam, F., Losa, M., Baker, S. M., Sagerström, C. G., Mace, K. A., et al. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1009162 · Cited by 37 · see citing works
Loker, R., & Mann, R. S. (2022) · Current Biology · doi:10.1016/j.cub.2022.06.069 · Cited by 35 · see citing works
Helzer, K. T., Ozers, M. S., Meyer, M. B., Benkusky, N. A., Solodin, N. M., Reese, R., Warren, C. L., Pike, J. W., & Alarid, E. T. (2018) · Molecular and Cellular Biology · doi:10.1128/mcb.00417-18 · Cited by 34 · see citing works
Loss of FOXC1 contributes to the corneal epithelial fate switch and pathogenesis
Li, M., Zhu, L., Liu, J., Huang, H., Guo, H., Wang, L., Li, L., Gu, S., Tan, J., Zhong, J., et al. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00378-2 · Cited by 36 · see citing works
Grainyhead-like (Grhl) Target Genes in Development and Cancer
Gasperoni, J. G., Fuller, J. N., Darido, C., Wilanowski, T., & Dworkin, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052735 · Cited by 35 · see citing works
Perry, B. W., Gopalan, S. S., Pasquesi, G. I. M., Schield, D. R., Westfall, A. K., Smith, C. F., Koludarov, I., Chippindale, P. T., Pellegrino, M. W., Chuong, E. B., et al. (2022) · Genome Research · doi:10.1101/gr.276251.121 · Cited by 35 · see citing works
Grainyhead-like-2 confers NK-sensitivity through interactions with epigenetic modifiers
MacFawn, I., Wilson, H. E., Selth, L. A., Leighton, I. A., Serebriiskii, I. G., Bleackley, R. C., Elzamzamy, O. M., Farris, J. C., Pifer, P. M., Richer, J. K., et al. (2018) · Molecular Immunology · doi:10.1016/j.molimm.2018.11.006 · Cited by 34 · see citing works
Kashgari, G. Y., Venkatesh, S., Refuerzo, S., Pham, B., Bayat, A., Klein, R. H., Ramos, R., TA, A., Plikus, M. V., Wang, P. H., et al. (2021) · JCI Insight · doi:10.1172/jci.insight.142577 · Cited by 34 · see citing works
Gibson, T. J., Larson, E. D., & Harrison, M. M. (2024) · Nature Structural & Molecular Biology · doi:10.1038/s41594-024-01231-8 · Cited by 30 · see citing works
Developmental Transcriptional Enhancers: A Subtle Interplay between Accessibility and Activity
Bozek, M., & Gompel, N. (2020) · BioEssays · doi:10.1002/bies.201900188 · Cited by 31 · see citing works
Serebreni, L., & Stark, A. (2020) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2020.11.009 · Cited by 31 · see citing works
Szigety, K. M., Liu, F., Yuan, C. Y., Moran, D., Horrell, J., Gochnauer, H. R., Cohen, R., Katz, J. P., Kaestner, K. H., Seykora, J. T., et al. (2020) · Genes & Development · doi:10.1101/gad.333674.119 · Cited by 31 · see citing works
Pioneer Factors in Animals and Plants—Colonizing Chromatin for Gene Regulation
Lai, X., Verhage, L., Hugouvieux, V., & Zubieta, C. (2018) · Molecules · doi:10.3390/molecules23081914 · Cited by 28 · see citing works
Epigenetic feedback and stochastic partitioning during cell division can drive resistance to EMT
Jia, W., Tripathi, S., Chakraborty, P., Chedere, A., Rangarajan, A., Levine, H., & Jolly, M. K. (2020) · Oncotarget · doi:10.18632/oncotarget.27651 · Cited by 29 · see citing works
Sundararajan, V., Pang, Q. Y., Choolani, M. A., & Huang, R. Y. (2020) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2020.00213 · Cited by 29 · see citing works
Shared enhancer gene regulatory networks between wound and oncogenic programs
Floc'hlay, S., Balaji, R., Stanković, D., Christiaens, V. M., Bravo González-Blas, C., De Winter, S., Hulselmans, G. J., De Waegeneer, M., Quan, X., Koldere, D., et al. (2023) · eLife · doi:10.7554/elife.81173 · Cited by 27 · see citing works
Self-citationKuang, Y., Golan, O., Preuße, K., Cain, B., Christensen, C. J., Salomone, J. R., Campbell, I., Okwubido-Williams, F. V., Hass, M. R., Yuan, Z., et al. (2020) · eLife · doi:10.7554/elife.53659 · Cited by 24 · see citing works
Pioneer Factors and Architectural Proteins Mediating Embryonic Expression Signatures in Cancer
Dobersch, S., Rubio, K., & Barreto, G. (2019) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2019.01.008 · Cited by 26 · see citing works
Grainyhead-like 2 as a double-edged sword in development and cancer.
He, J., Feng, C., Zhu, H., Wu, S., Jin, P., & Xu, T. (2020) · PubMed Central · Cited by 27 · see citing works
Domsch, K., Carnesecchi, J., Disela, V., Friedrich, J., Trost, N., Ermakova, O. V., Polychronidou, M., & Lohmann, I. (2019) · eLife · doi:10.7554/elife.42675 · Cited by 26 · see citing works
Resistance to mesenchymal reprogramming sustains clonal propagation in metastatic breast cancer
Saini, M., Schmidleitner, L., Moreno, H. D., Donato, E., Falcone, M., Bartsch, J. M., Klein, C., Vogel, V., Würth, R., Pfarr, N., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112533 · Cited by 25 · see citing works
Nevil, M., Gibson, T. J., Bartolutti, C., Iyengar, A., & Harrison, M. M. (2020) · Development · doi:10.1242/dev.185009 · Cited by 24 · see citing works
Genomic and epigenomic integrative subtypes of renal cell carcinoma in a Japanese cohort
Fukagawa, A., Hama, N., Totoki, Y., Nakamura, H. K., Arai, Y., Saito-Adachi, M., Maeshima, A. M., Matsui, Y., Yachida, S., Ushiku, T., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-44159-1 · Cited by 19 · see citing works
Xin, Y., Poul, Y. L., Ling, L., Museridze, M., Mühling, B., Jaenichen, R., Osipova, E., & Gompel, N. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2004003117 · Cited by 21 · see citing works
Grigolon, G., Araldi, E., Erni, R., Wu, J. Y., Thomas, C., Fortezza, M. L., Laube, B., Pöhlmann, D., Stoffel, M., Zarse, K., et al. (2022) · Nature Communications · doi:10.1038/s41467-021-27732-4 · Cited by 21 · see citing works
Jacobs, J., Pagani, M., Wenzl, C., & Stark, A. (2023) · Science · doi:10.1126/science.adf6149 · Cited by 19 · see citing works
Self-citationSNAI1-Driven Sequential EMT Changes Attributed by Selective Chromatin Enrichment of RAD21 and GRHL2
Sundararajan, V., Tan, M., Tan, T. Z., Pang, Q. Y., Ye, J., Chung, V. Y., & Huang, R. Y. (2020) · Cancers · doi:10.3390/cancers12051140 · Cited by 19 · see citing works
He, Y., Gan, M., Wang, Y., Huang, T., Wang, J., Han, T., & Yu, B. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-03721-9 · Cited by 18 · see citing works
Pioneer factors: nature or nurture?
Stoeber, S. D., Godin, H., Xu, C., & Bai, L. (2024) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2024.2355885 · Cited by 18 · see citing works
Huang, H., Liu, J., Li, M., Guo, H., Zhu, J., Zhu, L., Wu, S., Mo, K., Huang, Y., Tan, J., et al. (2022) · Science Advances · doi:10.1126/sciadv.abo5668 · Cited by 17 · see citing works
Grainyhead‐like transcription factors: guardians of the skin barrier
Deng, Z., Cangkrama, M., Butt, T., Jane, S. M., & Carpinelli, M. R. (2021) · Veterinary Dermatology · doi:10.1111/vde.12956 · Cited by 16 · see citing works
Recurrent FOXK1 :: GRHL and GPS2 :: GRHL fusions in trichogerminoma
Kervarrec, T., Pissaloux, D., Poilane, J., Tirode, F., Tallet, A., Collin, C., Tallegas, M., Berthon, P., Gaboriaud, P., Sohier, P., et al. (2022) · The Journal of Pathology · doi:10.1002/path.5872 · Cited by 16 · see citing works
Eichelberger, L., Saini, M., Moreno, H. D., Klein, C., Bartsch, J. M., Falcone, M., Reitberger, M., Espinet, E., Vogel, V., Graf, E., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.03.19.998823 · Cited by 16 · see citing works
Nardini, L., Holm, I., Pain, A., Bischoff, E., Gohl, D. M., Zongo, S., Guelbeogo, M. W., Sagnon, N., Vernick, K. D., & Riehle, M. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-51730-8 · Cited by 15 · see citing works
Cross-species analysis of melanoma enhancer logic using deep learningPreprint
Minnoye, L., Taskiran, I. I., Mauduit, D., Fazio, M., Aerschot, L. V., Hulsemans, G., Christiaens, V., Makhzami, S., Seltenhammer, M. H., Karras, P., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2019.12.21.885715 · Cited by 15 · see citing works
Self-citationIncreased chromatin accessibility promotes the evolution of a transcriptional silencer in Drosophila
Ling, L., Mühling, B., Jaenichen, R., & Gompel, N. (2023) · Science Advances · doi:10.1126/sciadv.ade6529 · Cited by 13 · see citing works
Bojanowski, K., Swindell, W. R., Cantor, S., & Chaudhuri, R. K. (2020) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2020.09.029 · Cited by 14 · see citing works
Reese, R., Helzer, K. T., Allen, K. O., Zheng, C., Solodin, N. M., & Alarid, E. T. (2022) · Molecular and Cellular Biology · doi:10.1128/mcb.00191-22 · Cited by 14 · see citing works
Grigolon, G., Araldi, E., Erni, R., Wu, J. Y., Thomas, C., Fortezza, M. L., Laube, B., Pöhlmann, D., Stoffel, M., Zarse, K., et al. (2022) · RePEc: Research Papers in Economics · doi:10.3929/ethz-b-000524798 · Cited by 12 · see citing works
Hox function and specificity – A tissue centric view
Pinto, P. B., Domsch, K., & Lohmann, I. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.11.011 · Cited by 12 · see citing works
GRHL2 and AP2a coordinate early surface ectoderm lineage commitment during development
Collier, A., Piekos, S. N., Liu, A., Pattison, J. M., Felix, F., Bailetti, A. A., Sedov, E., Gaddam, S., Zhen, H. H., & Oro, A. E. (2023) · iScience · doi:10.1016/j.isci.2023.106125 · Cited by 12 · see citing works
Dissecting the regulatory logic of specification and differentiation during vertebrate embryogenesisPreprint
Liu, J., Castillo-Hair, S. M., Du, L. Y., Wang, Y., Carte, A. N., Colomer-Rosell, M., Yin, C., Seelig, G., & Schier, A. F. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.08.27.609971 · Cited by 13 · see citing works
Sun, J., Zhang, C., Gao, F., & Stathopoulos, A. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113289 · Cited by 10 · see citing works
Mesenchymal-to-Epithelial Transitions in Development and Cancer
Ng-Blichfeldt, J.-P., & Röper, K. (2020) · Methods in molecular biology · doi:10.1007/978-1-0716-0779-4_7 · Cited by 9 · see citing works
Epigenetic Mechanisms Influencing Therapeutic Response in Breast Cancer
Arruabarrena-Aristorena, A., & Toska, E. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.924808 · Cited by 10 · see citing works
Exploring the reciprocity between pioneer factors and development
Freund, M. M., Harrison, M. M., & Torres‐Zelada, E. F. (2024) · Development · doi:10.1242/dev.201921 · Cited by 8 · see citing works
Holm, I., Nardini, L., Pain, A., Bischoff, E., Anderson, C. E., Zongo, S., Guelbeogo, M. W., Sagnon, N., Gohl, D. M., Nowling, R. J., et al. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2021.785934 · Cited by 9 · see citing works
Genetic variation in chromatin state across multiple tissues in Drosophila melanogaster
Huynh, K., Smith, B. R., Macdonald, S. J., & Long, A. D. (2023) · PLoS Genetics · doi:10.1371/journal.pgen.1010439 · Cited by 9 · see citing works
Legrand, M., Louveau, B., Macagno, N., Mancini, M., Kazakov, D. V., Pissaloux, D., Tirode, F., Tallet, A., Mourah, S., Lepiller, Q., et al. (2024) · Histopathology · doi:10.1111/his.15361 · Cited by 8 · see citing works
Loh, L. S., Hanly, J. J., Carter, A., Chatterjee, M., Tsimba, M., Shodja, D. N., Livraghi, L., Day, C. R., Reed, R. D., McMillan, W. O., et al. (2025) · PLoS Biology · doi:10.1371/journal.pbio.3003233 · Cited by 8 · see citing works
Khan, S. U., & Khan, M. U. (2021) · Journal of Chemistry and Nutritional Biochemistry · doi:10.48185/jcnb.v2i2.378 · Cited by 8 · see citing works
Functional roles of Grainyhead-like transcription factors in renal development and disease
Boivin, F. J., & Schmidt-Ott, K. M. (2018) · Pediatric Nephrology · doi:10.1007/s00467-018-4171-4 · Cited by 8 · see citing works
Regulatory genome annotation of 33 insect speciesPreprint
Asma, H., Tieke, E., Deem, K. D., Rahmat, J., Dong, T., Huang, X., Tomoyasu, Y., & Halfon, M. S. (2024) · eLife · doi:10.7554/elife.96738 · Cited by 8 · see citing works
GCparagon: evaluating and correcting GC biases in cell-free DNA at the fragment level
Spiegl, B., Kapidzic, F., Röner, S., Kircher, M., & Speicher, M. R. (2023) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqad102 · Cited by 7 · see citing works
Ulz, P., Perakis, S., Zhou, Q., Moser, T., Belic, J., Lazzeri, I., Wölfler, A., Zebisch, A., Gerger, A., Pristauz, G., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/456681 · Cited by 7 · see citing works
The transcription factor optomotor-blind restricts apterous expression through TrxG and PcG genes
Chen, M., Gao, E., Lin, G., Shen, J., & Wang, D. (2023) · Developmental Biology · doi:10.1016/j.ydbio.2023.03.002 · Cited by 6 · see citing works
What can genetic association panels tell us about evolutionary processes in insects?
Robin, C., Battlay, P., & Fournier‐Level, A. (2018) · Current Opinion in Insect Science · doi:10.1016/j.cois.2018.12.004 · Cited by 6 · see citing works
The role of maternal pioneer factors in predefining first zygotic responses to inductive signalsPreprint
Gentsch, G. E., Spruce, T., Owens, N. D. L., & Smith, J. C. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/306803 · Cited by 6 · see citing works
Enhancer architecture and chromatin accessibility constrain phenotypic space during developmentPreprint
Galupa, R., Álvarez-Canales, G., Borst, N. O., Fuqua, T., Gándara, L., Misunou, N., Richter, K., Alves, M. R. P., Karumbi, E., Perkins, M. L., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.02.494376 · Cited by 6 · see citing works
Enhancer grammar of liver cell types and hepatocyte zonation states
González-Blas, C. B., Matetovici, I., Hillen, H., Taskiran, I. I., Vandepoel, R., Christiaens, V., Sansores-García, L., Verboven, E., Hulselmans, G., Poovathingal, S., et al. (2022) · doi:10.1101/2022.12.08.519575 · Cited by 5 · see citing works
Self-citationFreund, M. M., deHaro-Arbona, F. J., Baloul, S., Torhorst, A., Roussos, C. S., Ruffridge, A. J., Rashoff, A. Q., Hazzard, R., Lewis, P. W., Bray, S. J., et al. (2026) · Science Advances · doi:10.1126/sciadv.aef2244 · Cited by 5 · see citing works
- Authors
- Jacobs, J., Atkins, M., Davie, K., Imrichova, H., Romanelli, L., Christiaens, V., Hulselmans, G., Potier, D., Wouters, J., Taskiran, I. I., Paciello, G., González-Blas, C. B., Koldere, D., Aibar, S., Halder, G., & Aerts, S.
- Affiliations
- VIB-KU Leuven Center for Brain & Disease Research (BE)
- VIB-KU Leuven Center for Cancer Biology (BE)
- Boğaziçi University (TR)
- Politecnico di Torino (IT)
- Corresponding author
- Aerts, Stein
- ORCID
- Venue
- Nature Genetics
- Published
- 2018-06-04
- Volume
- 50
- Issue
- 7
- Pages
- 1011-1020
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC6031307
- OpenAlex
- W2806844404
- Cited by
- 155
- References
- 98
- Citations by year
- 2026: 13 · 2025: 12 · 2024: 22 · 2023: 15 · 2022: 23 · 2021: 17 · 2020: 28 · 2019: 16 · 2018: 8
- FWCI
- 6.14
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion)
- Lirias (submittedVersion, other-oa)
- Funders
- National Institutes of Health (P40OD018537)
- 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
- transcription factors, enhancer accessibility, nucleosome displacement, pioneer factors, chromatin accessibility, GRHL1, GRHL2, GRHL3, Drosophila, transcriptional activation, regulatory hierarchy, tissue-specific gene expression, single nucleotide polymorphisms
- MeSH terms
- Animals, Binding Sites, Chromatin, DNA-Binding Proteins, Drosophila melanogaster, Enhancer Elements, Genetic, Epithelial Cells, Humans, Nucleosomes, Transcription Factors, Transcriptional Activation, Gene Expression Regulation, Developmental, Polymorphism, Single Nucleotide, Drosophila Proteins, Animals, Genetically Modified, Cell Line, Tumor, MCF-7 Cells
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 ›
Are you an author, or do you see a problem with this page? Request a review
