Zelda Binding in the Early Drosophila melanogaster Embryo Marks Regions Subsequently Activated at the Maternal-to-Zygotic Transition
Open accessAbstract
The earliest stages of development in most metazoans are driven by maternally deposited proteins and mRNAs, with widespread transcriptional activation of the zygotic genome occurring hours after fertilization, at a period known as the maternal-to-zygotic transition (MZT). In Drosophila, the MZT is preceded by the transcription of a small number of genes that initiate sex determination, patterning, and other early developmental processes; and the zinc-finger protein Zelda (ZLD) plays a key role in their transcriptional activation. To better understand the mechanisms of ZLD activation and the range of its targets, we used chromatin immunoprecipitation coupled with high-throughput sequencing (ChIP-Seq) to map regions bound by ZLD before (mitotic cycle 8), during (mitotic cycle 13), and after (late mitotic cycle 14) the MZT. Although only a handful of genes are transcribed prior to mitotic cycle 10, we identified thousands of regions bound by ZLD in cycle 8 embryos, most of which remain bound through mitotic cycle 14. As expected, early ZLD-bound regions include the promoters and enhancers of genes transcribed at this early stage. However, we also observed ZLD bound at cycle 8 to the promoters of roughly a thousand genes whose first transcription does not occur until the MZT and to virtually all of the thousands of known and presumed enhancers bound at cycle 14 by transcription factors that regulate patterned gene activation during the MZT. The association between early ZLD binding and MZT activity is so strong that ZLD binding alone can be used to identify active promoters and regulatory sequences with high specificity and selectivity. This strong early association of ZLD with regions not active until the MZT suggests that ZLD is not only required for the earliest wave of transcription but also plays a major role in activating the genome at the MZT.
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?
In Drosophila, Zelda is critical for lowering the nucleosome barrier at enhancers for genes driving zygotic gene activation.
“In Drosophila, the Zinc Finger Early Drosophila Activator (Zelda) is critical for lowering the nucleosome barrier at enhancers for genes driving zygotic gene activation [33–35].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [34]
The Discussion (page unavailable) says Zelda is important at promoters and enhancers and proposes that it promotes zygotic genome activation by controlling chromatin accessibility. But it does not establish that Zelda lowers a nucleosome barrier; it explicitly allows that Zelda may maintain chromatin that is already accessible rather than actively open it. (LLM, conf=0.88)
Experimental — accuracy not yet measured
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
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849 · see citing works
A bivalent chromatin structure marks key developmental genes in embryonic stem cells
Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., et al. (2006) · Cell · doi:10.1016/j.cell.2006.02.041 · Cited by 5,361 · see citing works
Fitting a mixture model by expectation maximization to discover motifs in biopolymers.
Bailey, T. L., & Elkan, C. (1994) · PubMed · Cited by 4,933 · see citing works
Genome-wide maps of chromatin state in pluripotent and lineage-committed cells
Mikkelsen, T. S., Ku, M., Jaffe, D. B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T.-K., Koche, R. P., et al. (2007) · Nature · doi:10.1038/nature06008 · Cited by 4,129 · 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
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
Opening of Compacted Chromatin by Early Developmental Transcription Factors HNF3 (FoxA) and GATA-4
Cirillo, L. A., Lin, F. R., Cuesta, I., Friedman, D., Jarník, M., & Zaret, K. S. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00459-8 · Cited by 1,188 · see citing works
The maternal-to-zygotic transition: a play in two acts
Tadros, W., & Lipshitz, H. D. (2009) · Development · doi:10.1242/dev.033183 · Cited by 1,177 · see citing works
Controlling the elongation phase of transcription with P-TEFb
Peterlin, B. M., & Price, D. H. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.06.014 · Cited by 1,144 · see citing works
Foe, V. E., & Alberts, B. (1983) · Journal of Cell Science · doi:10.1242/jcs.61.1.31 · Cited by 1,056 · see citing works
A major developmental transition in early xenopus embryos: II. control of the onset of transcription
Newport, J., & Kirschner, M. (1982) · Cell · doi:10.1016/0092-8674(82)90273-2 · Cited by 1,055 · see citing works
FlyBase: enhancing Drosophila Gene Ontology annotations
Tweedie, S., Ashburner, M., Falls, K. M., Leyland, P. C., McQuilton, P., Marygold, S. J., Millburn, G., Osumi-Sutherland, D., Schroeder, A., Seal, R. L., et al. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn788 · Cited by 702 · see citing works
Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control.Preprint
Gualdi, R., Bossard, P., Zheng, M., Hamada, Y., Coleman, J. R., & Zaret, K. S. (1996) · Genes & Development · doi:10.1101/gad.10.13.1670 · Cited by 590 · see citing works
Open chromatin in pluripotency and reprogramming
Gaspar‐Maia, A., Alajem, A., Meshorer, E., & Ramalho‐Santos, M. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3036 · Cited by 568 · see citing works
Pavesi, G., Mereghetti, P., Mauri, G., & Pesole, G. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh465 · Cited by 491 · 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
Self-citationThe 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
Ultrastructural patterns of RNA synthesis during early embryogenesis of drosophila melanogaster
McKnight, S. L., & Miller Jr., O. L. (1976) · Cell · doi:10.1016/0092-8674(76)90014-3 · Cited by 400 · see citing works
Chromatin signature of embryonic pluripotency is established during genome activation
Vastenhouw, N. L., Zhang, Y., Woods, I. G., Imam, F. B., Regev, A., Liu, X. S., Rinn, J. L., & Schier, A. F. (2010) · Nature · doi:10.1038/nature08866 · Cited by 367 · see citing works
MacArthur, S., Li, X., Li, J. J., Brown, J. B., Chu, H. C., Zeng, L., Grondona, B. P., Hechmer, A., Simirenko, L., Keränen, S. V. E., et al. (2009) · Genome biology · doi:10.1186/gb-2009-10-7-r80 · Cited by 332 · see citing works
Self-citationFunctional Anatomy of Polycomb and Trithorax Chromatin Landscapes in Drosophila Embryos
Schuettengruber, B., Ganapathi, M., Leblanc, B., Portoso, M., Jaschek, R., Tolhuis, B., van Lohuizen, M., Tanay, A., & Cavalli, G. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000013 · Cited by 331 · see citing works
Maternal BRG1 regulates zygotic genome activation in the mousePreprint
Bultman, S. J., Gebuhr, T. C., Pan, H., Svoboda, P., Schultz, R. M., & Magnuson, T. (2006) · Genes & Development · doi:10.1101/gad.1435106 · Cited by 330 · see citing works
Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loadingPreprint
MacAlpine, H. K., Gordân, R., Powell, S., Hartemink, A. J., & MacAlpine, D. M. (2009) · Genome Research · doi:10.1101/gr.097873.109 · Cited by 266 · see citing works
Unmasking Activation of the Zygotic Genome Using Chromosomal Deletions in the Drosophila Embryo
De Renzis, S., Elemento, O., Tavazoie, S., & Wieschaus, E. F. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050117 · Cited by 265 · see citing works
DNA topology, not DNA sequence, is a critical determinant for Drosophila ORC–DNA binding
Remus, D., Beall, E. L., & Botchan, M. R. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600077 · Cited by 263 · see citing works
Self-citationA Hierarchy of H3K4me3 and H3K27me3 Acquisition in Spatial Gene Regulation in Xenopus Embryos
Akkers, R. C., van Heeringen, S. J., Jacobi, U. G., Janssen‐Megens, E. M., Françoijs, K., Stunnenberg, H. G., & Veenstra, G. J. C. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.08.005 · Cited by 244 · see citing works
Structure and function of a transcriptional network activated by the MAPK Hog1
Capaldi, A. P., Kaplan, T., Liu, Y., Habib, N., Regev, A., Friedman, N., & O’Shea, E. K. (2008) · Nature Genetics · doi:10.1038/ng.235 · Cited by 233 · see citing works
Self-citationLi, X.-Y., Thomas, S., Sabo, P. J., Eisen, M. B., Stamatoyannopoulos, J. A., & Biggin, M. D. (2011) · Genome Biology · doi:10.1186/gb-2011-12-4-r34 · Cited by 217 · see citing works
Self-citationβ-Catenin/Tcf-regulated transcription prior to the midblastula transition
Yang, J., Tan, C. L., Darken, R. S., Wilson, P. A., & Klein, P. S. (2002) · Development · doi:10.1242/dev.00150 · Cited by 211 · see citing works
Lott, S. E., Villalta, J. E., Schroth, G. P., Luo, S. J., Tonkin, L. A., & Eisen, M. B. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1000590 · Cited by 204 · see citing works
Self-citationModeling dependencies in protein-DNA binding sites
Barash, Y., Elidan, G., Friedman, N., & Kaplan, T. (2003) · Research in Computational Molecular Biology · doi:10.1145/640075.640079 · Cited by 203 · see citing works
Self-citationBradley, R. K., Li, X., Trapnell, C., Davidson, S. M., Pachter, L. S., Chu, H. C., Tonkin, L. A., Biggin, M. D., & Eisen, M. B. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000343 · Cited by 190 · see citing works
Self-citationDynamic reprogramming of chromatin accessibility during Drosophilaembryo development
Thomas, S., Li, X., Sabo, P. J., Sandstrom, R. S., Thurman, R. E., Canfield, T. K., Giste, E., Fisher, W., Hammonds, A. S., Celniker, S., et al. (2011) · Genome biology · doi:10.1186/gb-2011-12-5-r43 · Cited by 176 · see citing works
Self-citationBlythe, S. A., Cha, S., Tadjuidje, E., Heasman, J., & Klein, P. S. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.07.007 · Cited by 165 · see citing works
Pritchard, D. K., & Schubiger, G. (1996) · Genes & Development · doi:10.1101/gad.10.9.1131 · Cited by 164 · see citing works
Rates of synthesis of major classes of RNA in Drosophila embryos
Anderson, K. V., & Lengyel, J. A. (1979) · Developmental Biology · doi:10.1016/0012-1606(79)90018-6 · Cited by 164 · see citing works
The TAGteam DNA motif controls the timing of <i>Drosophila</i> pre-blastoderm transcription
Bosch, J. R. T., Benavides, J. A., & Cline, T. W. (2006) · Development · doi:10.1242/dev.02373 · Cited by 161 · see citing works
Kaplan, T., Li, X., Sabo, P. J., Thomas, S., Stamatoyannopoulos, J. A., Biggin, M. D., & Eisen, M. B. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1001290 · Cited by 159 · see citing works
Self-citationGrainyhead 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
Self-citationStaudt, N. D., Fellert, S., Chung, H., Jäckle, H., & Vorbrüggen, G. (2006) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-11-1056 · Cited by 64 · see citing works
STAT Is an Essential Activator of the Zygotic Genome in the Early Drosophila Embryo
Tsurumi, A., Fan, X., Li, J., Larson, K., LaFrance, R. M., & Li, W. X. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002086 · Cited by 55 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
Modification of Enhancer Chromatin: What, How, and Why?
Calo, E., & Wysocka, J. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.01.038 · Cited by 1,457 · see citing works
Hendrickson, P. G., Dorais, J., Grow, E. J., Whiddon, J. L., Lim, J.-W., Wike, C. L., Weaver, B. D., Pflueger, C., Emery, B. R., Wilcox, A. L., et al. (2017) · Nature Genetics · doi:10.1038/ng.3844 · Cited by 710 · see citing works
Zygotic Genome Activation During the Maternal-to-Zygotic Transition
Lee, M. T., Bonneau, A. R., & Giráldez, A. J. (2014) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100913-013027 · Cited by 643 · see citing works
Pioneer transcription factors in cell reprogrammingPreprint
Iwafuchi, M., & Zaret, K. S. (2014) · Genes & Development · doi:10.1101/gad.253443.114 · Cited by 590 · see citing works
Mechanisms regulating zygotic genome activation
Schulz, K. N., & Harrison, M. M. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0087-x · Cited by 543 · see citing works
Self-citationLooping Back to Leap Forward: Transcription Enters a New Era
Levine, M., Cattoglio, C., & Tjian, R. (2014) · Cell · doi:10.1016/j.cell.2014.02.009 · Cited by 481 · see citing works
Zygotic Genome Activation in Vertebrates
Jukam, D., Shariati, S. A., & Skotheim, J. M. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.07.026 · Cited by 478 · see citing works
Chromatin Architecture Emerges during Zygotic Genome Activation Independent of Transcription
Hug, C. B., Grimaldi, A. G., Kruse, K., & Vaquerizas, J. M. (2017) · Cell · doi:10.1016/j.cell.2017.03.024 · Cited by 466 · 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
The maternal-to-zygotic transition revisited
Vastenhouw, N. L., Cao, W. X., & Lipshitz, H. D. (2019) · Development · doi:10.1242/dev.161471 · Cited by 433 · see citing works
A high-resolution mRNA expression time course of embryonic development in zebrafish
White, R. J., Collins, J. E., Sealy, I. M., Wali, N., Dooley, C. M., Digby, Z., Stemple, D. L., Murphy, D. N., Billis, K., Hourlier, T., et al. (2017) · eLife · doi:10.7554/elife.30860 · Cited by 345 · see citing works
Iterative random forests to discover predictive and stable high-order interactions
Basu, S., Kumbier, K., Brown, J. B., & Yu, B. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1711236115 · 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
Cardozo Gizzi, A. M., Cattoni, D. I., Fiche, J.-B., Espinola, S. M., Gurgo, J., Messina, O., Houbron, C., Ogiyama, Y., Papadopoulos, G. L., Cavalli, G., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.01.011 · Cited by 258 · see citing works
Polycomb-Dependent Chromatin Looping Contributes to Gene Silencing during Drosophila Development
Ogiyama, Y., Schuettengruber, B., Papadopoulos, G. L., Chang, J., & Cavalli, G. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.05.032 · Cited by 242 · see citing works
Pou5f1 Transcription Factor Controls Zygotic Gene Activation In Vertebrates
Leichsenring, M., Maes, J., Mössner, R., Driever, W., & Onichtchouk, D. (2013) · Science · doi:10.1126/science.1242527 · Cited by 228 · see citing works
Genome organization controls transcriptional dynamics during development
Batut, P. J., Bing, X., Sisco, Z., Raimundo, J., Levo, M., & Levine, M. (2022) · Science · doi:10.1126/science.abi7178 · Cited by 226 · see citing works
Disentangling the Many Layers of Eukaryotic Transcriptional Regulation
Lelli, K. M., Slattery, M. G., & Mann, R. S. (2012) · Annual Review of Genetics · doi:10.1146/annurev-genet-110711-155437 · Cited by 218 · see citing works
Establishment of regions of genomic activity during the Drosophila maternal to zygotic transition
Li, X., Harrison, M. M., Villalta, J. E., Kaplan, T., & Eisen, M. B. (2014) · eLife · doi:10.7554/elife.03737 · Cited by 208 · see citing works
Self-citationMir, M., Stadler, M. R., Ortiz, S. A., Hannon, C. E., Harrison, M. M., Darzacq, X., & Eisen, M. B. (2018) · eLife · doi:10.7554/elife.40497 · Cited by 207 · see citing works
Self-citationChromatin 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
Herrmann, C., de Sande, B. V., Potier, D., & Aerts, S. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks543 · Cited by 202 · see citing works
Zygotic Genome Activation Triggers the DNA Replication Checkpoint at the Midblastula Transition
Blythe, S. A., & Wieschaus, E. F. (2015) · Cell · doi:10.1016/j.cell.2015.01.050 · Cited by 194 · see citing works
Enhancer additivity and non-additivity are determined by enhancer strength in the Drosophila embryo
Bothma, J. P., Garcia, H. G., Ng, S., Perry, M. W., Gregor, T., & Levine, M. (2015) · eLife · doi:10.7554/elife.07956 · Cited by 192 · see citing works
Dense Bicoid hubs accentuate binding along the morphogen gradient
Mir, M., Reimer, A., Haines, J. E., Li, X.-Y., Stadler, M., Garcia, H., Eisen, M. B., & Darzacq, X. (2017) · Genes & Development · doi:10.1101/gad.305078.117 · Cited by 192 · see citing works
Self-citationTranscriptional coupling of distant regulatory genes in living embryos
Levo, M., Raimundo, J., Bing, X. Y., Sisco, Z., Batut, P. J., Ryabichko, S., Gregor, T., & Levine, M. S. (2022) · Nature · doi:10.1038/s41586-022-04680-7 · Cited by 188 · see citing works
Visualizing transcription factor dynamics in living cells
Liu, Z. J., & Tjian, R. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201710038 · Cited by 182 · see citing works
Schulz, K. N., Bondra, E. R., Moshe, A., Villalta, J. E., Lieb, J. D., Kaplan, T., McKay, D. J., & Harrison, M. M. (2015) · Genome Research · doi:10.1101/gr.192682.115 · Cited by 177 · see citing works
Self-citationEspinola, S. M., Götz, M., Bellec, M., Messina, O., Fiche, J.-B., Houbron, C., Dejean, M., Reim, I., Cardozo Gizzi, A. M., Lagha, M., et al. (2021) · Nature Genetics · doi:10.1038/s41588-021-00816-z · Cited by 174 · see citing works
From Egg to Gastrula: How the Cell Cycle Is Remodeled During the Drosophila Mid-Blastula Transition
Farrell, J. A., & O’Farrell, P. H. (2014) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133531 · Cited by 173 · see citing works
Sun, Y., Nien, C.-Y., Chen, K., Liu, H.-Y., Johnston, J. J., Zeitlinger, J., & Rushlow, C. A. (2015) · Genome Research · doi:10.1101/gr.192542.115 · Cited by 172 · see citing works
Establishment and maintenance of heritable chromatin structure during early Drosophila embryogenesis
Blythe, S. A., & Wieschaus, E. F. (2016) · eLife · doi:10.7554/elife.20148 · Cited by 168 · see citing works
Brd4 and P300 Confer Transcriptional Competency during Zygotic Genome Activation
Chan, S. H., Tang, Y., Miao, L., Darwich‐Codore, H., Vejnar, C. E., Beaudoin, J.-D., Musaev, D., Fernández, J. P., Benitez, M. D. J., Bazzini, A., et al. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.05.037 · Cited by 160 · see citing works
Independence of chromatin conformation and gene regulation during Drosophila dorsoventral patterning
Ing-Simmons, E., Vaid, R., Bing, X. Y., Levine, M., Mannervik, M., & Vaquerizas, J. M. (2021) · Nature Genetics · doi:10.1038/s41588-021-00799-x · Cited by 159 · see citing works
A global change in RNA polymerase II pausing during the Drosophila midblastula transition
Chen, K., Johnston, J. J., Shao, W., Meier, S. R., Staber, C. J., & Zeitlinger, J. (2013) · eLife · doi:10.7554/elife.00861 · Cited by 153 · see citing works
Dufourt, J., Trullo, A., Hunter, J., Fernandez, C., Lazaro, J., Dejean, M., Morales, L., Nait-Amer, S., Schulz, K. N., Harrison, M. M., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07613-z · Cited by 150 · see citing works
Self-citationKvon, E. Z., Stampfel, G., Yáñez-Cuna, J. O., Dickson, B. J., & Stark, A. (2012) · Genes & Development · doi:10.1101/gad.188052.112 · Cited by 147 · see citing works
Joseph, S. R., Pálfy, M., Hilbert, L., Kumar, M., Karschau, J., Zaburdaev, V., Shevchenko, A., & Vastenhouw, N. L. (2017) · eLife · doi:10.7554/elife.23326 · Cited by 145 · see citing works
Mechanisms of transcriptional precision in animal development
Lagha, M., Bothma, J. P., & Levine, M. (2012) · Trends in Genetics · doi:10.1016/j.tig.2012.03.006 · Cited by 145 · see citing works
Cooperativity and Rapid Evolution of Cobound Transcription Factors in Closely Related Mammals
Stefflova, K., Thybert, D., Wilson, M. D., Streeter, I., Aleksic, J., Karagianni, P., Brāzma, A., Adams, D. J., Talianidis, I., Marioni, J. C., et al. (2013) · Cell · doi:10.1016/j.cell.2013.07.007 · Cited by 145 · see citing works
Gaskill, M. M., Gibson, T. J., Larson, E. D., & Harrison, M. M. (2021) · eLife · doi:10.7554/elife.66668 · Cited by 136 · see citing works
Self-citationChromatin Control of Developmental Dynamics and Plasticity
Perino, M., & Veenstra, G. J. C. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.08.004 · Cited by 131 · 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
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
Deciphering the transcriptional cis-regulatory code
Yáñez-Cuna, J. O., Kvon, E. Z., & Stark, A. (2012) · Trends in Genetics · doi:10.1016/j.tig.2012.09.007 · Cited by 124 · see citing works
Control of Tissue Development by Morphogens
Kicheva, A., & Briscoe, J. (2023) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-020823-011522 · Cited by 120 · see citing works
New insights into the maternal to zygotic transition
Langley, A. R., Smith, J. C., Stemple, D. L., & Harvey, S. A. (2014) · Development · doi:10.1242/dev.102368 · Cited by 113 · see citing works
Uncovering cis-regulatory sequence requirements for context-specific transcription factor bindingPreprint
Yáñez-Cuna, J. O., Dinh, H. Q., Kvon, E. Z., Shlyueva, D., & Stark, A. (2012) · Genome Research · doi:10.1101/gr.132811.111 · Cited by 113 · see citing works
Continued Activity of the Pioneer Factor Zelda Is Required to Drive Zygotic Genome Activation
McDaniel, S. L., Gibson, T. J., Schulz, K. N., García, M. F., Nevil, M., Jain, S. U., Lewis, P. W., Zaret, K. S., & Harrison, M. M. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.01.014 · Cited by 107 · see citing works
Self-citationStadler, M. R., Haines, J. E., & Eisen, M. B. (2017) · eLife · doi:10.7554/elife.29550 · Cited by 104 · see citing works
Self-citationA complete workflow for the analysis of full-size ChIP-seq (and similar) data sets using peak-motifs
Thomas‐Chollier, M., Darbo, É., Herrmann, C., Defrance, M., Thieffry, D., & van Helden, J. (2012) · Nature Protocols · doi:10.1038/nprot.2012.088 · Cited by 104 · see citing works
Impact of gut microbiota on the fly’s germ line
Elgart, M., Stern, S., Salton, O., Gnainsky, Y., Heifetz, Y., & Soen, Y. (2016) · Nature Communications · doi:10.1038/ncomms11280 · Cited by 104 · see citing works
Samata, M., Alexiadis, A., Richard, G., Georgiev, P., Nuebler, J., Kulkarni, T., Renschler, G., Basilicata, M. F., Zenk, F. L., Shvedunova, M., et al. (2020) · Cell · doi:10.1016/j.cell.2020.05.026 · Cited by 97 · see citing works
The continuum of Drosophila embryonic development at single-cell resolution
Calderon, D., Blecher‐Gonen, R., Huang, X., Secchia, S., Kentro, J. A., Daza, R. M., Martin, B., Dulja, A., Schaub, C., Trapnell, C., et al. (2022) · Science · doi:10.1126/science.abn5800 · Cited by 96 · see citing works
Xu, Z., Chen, H., Jia, L., Yu, D., Struffi, P., & Small, S. (2014) · Genes & Development · doi:10.1101/gad.234534.113 · Cited by 94 · see citing works
The RNA Pol II Elongation Factor Ell3 Marks Enhancers in ES Cells and Primes Future Gene Activation
Lin, C., Garruss, A. S., Luo, Z., Guo, F., & Shilatifard, A. (2012) · Cell · doi:10.1016/j.cell.2012.12.015 · Cited by 92 · see citing works
CLAMP and Zelda function together to promote Drosophila zygotic genome activation
Duan, J. E., Rieder, L. E., Colonnetta, M. M., Huang, A., Mckenney, M., Watters, S., Deshpande, G., Jordan, W. T., Fawzi, N. L., & Larschan, E. (2021) · eLife · doi:10.7554/elife.69937 · Cited by 91 · see citing works
Paris, M., Kaplan, T., Li, X. Y., Villalta, J. E., Lott, S. E., & Eisen, M. B. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003748 · Cited by 90 · see citing works
Self-citationSaunders, A., Core, L. J., Sutcliffe, C., Lis, J. T., & Ashe, H. L. (2013) · Genes & Development · doi:10.1101/gad.215459.113 · Cited by 90 · see citing works
Yamada, S., Whitney, P. H., Huang, S.-K., Eck, E. C., Garcia, H. G., & Rushlow, C. A. (2019) · Current Biology · doi:10.1016/j.cub.2019.03.019 · Cited by 88 · see citing works
Long distance relationships: Enhancer–promoter communication and dynamic gene transcription
Marsman, J., & Horsfield, J. A. (2012) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2012.10.008 · Cited by 88 · see citing works
Genome-wide RIP-Chip analysis of translational repressor-bound mRNAs in the Plasmodium gametocyte
Guerreiro, A., Deligianni, E., Santos, J. M., Silva, P. A. G. C., Louis, C., Pain, A., Janse, C. J., Franke-Fayard, B. M. D., Carret, C., Sidén‐Kiamos, I., et al. (2014) · Genome biology · doi:10.1186/s13059-014-0493-0 · Cited by 88 · see citing works
Concentration dependent chromatin states induced by the bicoid morphogen gradient
Hannon, C. E., Blythe, S. A., & Wieschaus, E. F. (2017) · eLife · doi:10.7554/elife.28275 · Cited by 87 · see citing works
A conserved role for Snail as a potentiator of active transcriptionPreprint
Rembold, M., Ciglar, L., Yáñez-Cuna, J. O., Zinzen, R. P., Girardot, C., Jain, A., Welte, M. A., Stark, A., Leptin, M., & Furlong, E. E. M. (2014) · Genes & Development · doi:10.1101/gad.230953.113 · Cited by 87 · see citing works
Laver, J. D., Li, X., Ray, D., Cook, K. B., Hahn, N. A., Nabeel‐Shah, S., Kekis, M., Luo, H., Marsolais, A. J., Fung, K. Y., et al. (2015) · Genome biology · doi:10.1186/s13059-015-0659-4 · Cited by 85 · see citing works
Self-citationWidespread evidence of cooperative DNA binding by transcription factors in Drosophila development
Kazemian, M., Pham, H. N., Wolfe, S. A., Brodsky, M. H., & Sinha, S. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt598 · Cited by 85 · 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
Laver, J. D., Li, X., Ancevicius, K., Westwood, J. T., Smibert, C. A., Morris, Q., & Lipshitz, H. D. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt702 · Cited by 81 · see citing works
Self-citationA Comprehensive Drosophila melanogaster Transcription Factor Interactome
Shokri, L., Inukai, S., Hafner, A., Weinand, K., Hens, K., Vedenko, A., Gisselbrecht, S. S., Dainese, R., Bischof, J., Furger, E., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.03.071 · Cited by 80 · see citing works
Laver, J. D., Marsolais, A. J., Smibert, C. A., & Lipshitz, H. D. (2015) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2015.06.007 · Cited by 78 · see citing works
Transcriptional Memory in the Drosophila Embryo
Ferraro, T., Esposito, E., Mancini, L., Ng, S., Lucas, T., Coppey, M., Dostatni, N., Walczak, A. M., Levine, M., & Lagha, M. (2015) · Current Biology · doi:10.1016/j.cub.2015.11.058 · Cited by 78 · see citing works
The maternal-to-zygotic transition: reprogramming of the cytoplasm and nucleus
Kojima, M. L., Hoppe, C., & Giráldez, A. J. (2024) · Nature Reviews Genetics · doi:10.1038/s41576-024-00792-0 · Cited by 77 · 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
Veil, M., Yampolsky, L. Y., Grüning, B. A., & Onichtchouk, D. (2019) · Genome Research · doi:10.1101/gr.240572.118 · Cited by 75 · see citing works
Taf7l cooperates with Trf2 to regulate spermiogenesis
Zhou, H., Grubisic, I., Zheng, K., He, Y., Wang, P. J., Kaplan, T., & Tjian, R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1317034110 · Cited by 72 · see citing works
Self-citationKwasnieski, J. C., Orr‐Weaver, T. L., & Bartel, D. P. (2019) · Genome Research · doi:10.1101/gr.242164.118 · Cited by 72 · see citing works
Hamm, D. C., & Harrison, M. M. (2018) · Open Biology · doi:10.1098/rsob.180183 · Cited by 70 · see citing works
Self-citationThe timing of zygotic genome activation
Pálfy, M., Joseph, S. R., & Vastenhouw, N. L. (2017) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.12.001 · Cited by 69 · see citing works
Transcriptional elongation checkpoint control in development and diseasePreprint
Smith, E. R., & Shilatifard, A. (2013) · Genes & Development · doi:10.1101/gad.215137.113 · Cited by 68 · 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
Self-citationKoenecke, N., Johnston, J., Gaertner, B., Natarajan, M., & Zeitlinger, J. (2016) · Genome Biology · doi:10.1186/s13059-016-1057-2 · Cited by 65 · see citing works
Transcriptional Activation of the Zygotic Genome in Drosophila
Harrison, M. M., & Eisen, M. B. (2015) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2015.07.028 · Cited by 63 · see citing works
Self-citationCoordinating Cell Cycle Remodeling with Transcriptional Activation at the Drosophila MBT
Blythe, S. A., & Wieschaus, E. F. (2015) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2015.06.002 · Cited by 62 · see citing works
The tumor suppressor Brat controls neuronal stem cell lineages by inhibiting Deadpan and Zelda
Reichardt, I., Bonnay, F., Steinmann, V., Loedige, I., Burkard, T. R., Meister, G., & Knoblich, J. A. (2017) · EMBO Reports · doi:10.15252/embr.201744188 · Cited by 61 · see citing works
Histone concentration regulates the cell cycle and transcription in early development
Chari, S., Wilky, H., Govindan, J., & Amodeo, A. A. (2019) · Development · doi:10.1242/dev.177402 · Cited by 58 · see citing works
Cohesin facilitates zygotic genome activation in zebrafish
Meier, M., Grant, J., Dowdle, A., Thomas, A., Gerton, J. L., Collas, P., O'Sullivan, J. M., & Horsfield, J. A. (2017) · Development · doi:10.1242/dev.156521 · Cited by 58 · see citing works
The genome-wide multi-layered architecture of chromosome pairing in early Drosophila embryos
Erceg, J., Abed, J. A., Goloborodko, A. A., Lajoie, B. R., Fudenberg, G., Abdennur, N. A., Imakaev, M., McCole, R. B., Nguyen, S. C., Saylor, W., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12211-8 · Cited by 58 · see citing works
Pattern Formation by Graded and Uniform Signals in the Early Drosophila Embryo
Kanodia, J., Liang, H.-L., Kim, Y., Lim, B., Zhan, M., Lu, H., Rushlow, C. A., & Shvartsman, S. Y. (2012) · Biophysical Journal · doi:10.1016/j.bpj.2011.12.042 · Cited by 57 · see citing works
Cavalheiro, G. R., Girardot, C., Viales, R. R., Feng, S., Pollex, T., Cao, T. B. N., Lacour, P., Rabinowitz, A. H., & Furlong, E. E. M. (2023) · Science Advances · doi:10.1126/sciadv.ade1085 · Cited by 56 · see citing works
Soluri, I. V., Zumerling, L. M., Parra, O. A. P., Clark, E. G., & Blythe, S. A. (2020) · eLife · doi:10.7554/elife.53916 · Cited by 56 · see citing works
Drosophila poised enhancers are generated during tissue patterning with the help of repressionPreprint
Koenecke, N., Johnston, J. J., He, Q., Meier, S. R., & Zeitlinger, J. (2016) · Genome Research · doi:10.1101/gr.209486.116 · Cited by 56 · see citing works
6mA-DNA-binding factor Jumu controls maternal-to-zygotic transition upstream of Zelda
He, S., Zhang, G., Wang, J., Gao, Y., Sun, R., Cao, Z., Chen, Z., Zheng, X.-D., Yuan, J., Luo, Y., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-10202-3 · Cited by 54 · 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
Self-citationEck, E., Liu, J., Kazemzadeh-Atoufi, M., Ghoreishi, S., Blythe, S. A., & García, H. G. (2020) · eLife · doi:10.7554/elife.56429 · Cited by 52 · see citing works
GAGA factor: a multifunctional pioneering chromatin protein
Chetverina, D., Erokhin, M., & Schedl, P. D. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03776-z · Cited by 52 · see citing works
Galupa, R., Álvarez-Canales, G., Borst, N. O., Fuqua, T., Gándara, L., Misunou, N., Richter, K., Alves, M. R. P., Karumbi, E., Perkins, M. L., et al. (2022) · Developmental Cell · doi:10.1016/j.devcel.2022.12.003 · Cited by 51 · see citing works
Epigenetic Marking of the Zebrafish Developmental Program
Andersen, I. S., Lindeman, L. C., Reiner, A. H., Østrup, O., Aanes, H., Aleström, P., & Collas, P. (2013) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416027-9.00003-6 · Cited by 51 · see citing works
The emergence of genome architecture and zygotic genome activation
Vallot, A., & Tachibana, K.-E. K. (2020) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2020.02.002 · Cited by 50 · see citing works
Krüppel Expression Levels Are Maintained through Compensatory Evolution of Shadow Enhancers
Wunderlich, Z., Bragdon, M. D. J., Vincent, B. J., White, J. A., Estrada, J., & DePace, A. H. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.08.021 · Cited by 49 · see citing works
- Authors
- Harrison, M. M., Li, X.-Y., Kaplan, T., Botchan, M. R., & Eisen, M. B.
- Affiliations
- University of California, Berkeley (US)
- QB3 (US)
- Corresponding author
- Eisen, Michael B.
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-10-20
- Volume
- 7
- Issue
- 10
- Pages
- e1002266
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC3197655
- OpenAlex
- W2004533772
- Cited by
- 338
- References
- 41
- Citations by year
- 2026: 14 · 2025: 17 · 2024: 23 · 2023: 23 · 2022: 20 · 2021: 27 · 2020: 23 · 2019: 26 · 2018: 24 · 2017: 31 · 2016: 20 · 2015: 22 · 2014: 20 · 2013: 28 · 2012: 18
- FWCI
- 8.84
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (CA30490)
- National Human Genome Research Institute (HG002779, R01HG002779)
- National Cancer Institute (R37 CA3049, R37CA030490)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- Zelda, maternal-to-zygotic transition, Drosophila melanogaster embryo, transcriptional activation, enhancer binding, promoter binding, mitotic cycle, chromatin binding, sex determination
- MeSH terms
- Animals, Drosophila melanogaster, Female, Mitosis, Nuclear Proteins, Promoter Regions, Genetic, Protein Binding, Transcription Factors, Transcription, Genetic, Zygote, Transcriptional Activation, Genome, Gene Expression Regulation, Developmental, Body Patterning, Sex Determination Processes, Drosophila Proteins, Embryonic Development, Chromatin Immunoprecipitation
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