Cited by 474Genomics and Chromatin DynamicsDevelopmental Biology and Gene RegulationChromosomal and Genetic Variations

The DOI matches its Crossref record; 7 of the 7 references it cites were found in a registry or an index.

Shadow Enhancers as a Source of Evolutionary Novelty

Open access

Hong, Joung-Woo, Hendrix, David A., Levine, Michael S.·2008·Science

DOI 10.1126/science.1160631PMC PMC4257485

Open this paper in CoChat — free account

Abstract

Some developmentally important genes can be regulated via two enhancers, one located nearby and the other, a "shadow" enhancer, 10 to 20 kilobases away.

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

Crossref · 10.1126/science.1160631

Cites

7 of 7 references verified0 citation errors · 0 not checkable

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Genome-wide analysis of clustered Dorsal binding sites identifies putative target genes in the Drosophila embryo
Markstein, M., Markstein, P., Markstein, V., & Levine, M. S. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.012591199 · Cited by 375
Self-citation
Whole-genome analysis of dorsal-ventral patterning in the Drosophila embryo.
Stathopoulos, A., Drenth, M. V., Erives, A. J., Markstein, M., & Levine, M. (2002) · Cell · doi:10.1016/s0092-8674(02)01087-5 · Cited by 310
Self-citation
The Evolution of Gene Regulation Underlies a Morphological Difference between Two Drosophila Sister Species
Jeong, S., Rebeiz, M., Andolfatto, P., Werner, T., True, J., & Carroll, S. B. (2008) · Cell · doi:10.1016/j.cell.2008.01.014 · Cited by 309
Whole-genome ChIP–chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo
Zeitlinger, J., Zinzen, R. P., Stark, A., Kellis, M., Zhang, H., Young, R. A., & Levine, M. (2007) · Genes & Development · doi:10.1101/gad.1509607 · Cited by 286
Self-citation
A functional screen for sonic hedgehog regulatory elements across a 1 Mb interval identifies long-range ventral forebrain enhancers
Jeong, Y., El-Jaick, K. B., Roessler, E., Muenke, M., & Epstein, D. J. (2006) · Development · doi:10.1242/dev.02239 · Cited by 238
Redundant and Unique Roles of Two Enhancer Elements in the TCRγ Locus in Gene Regulation and γδ T Cell Development
Xiong, N., Kang, C., & Raulet, D. H. (2002) · Immunity · doi:10.1016/s1074-7613(02)00285-6 · Cited by 65
Comprehensive identification of Drosophila dorsal–ventral patterning genes using a whole-genome tiling array
Biemar, F., Nix, D. A., Piel, J., Peterson, B., Ronshaugen, M., Sementchenko, V., Bell, I., Manak, J. R., & Levine, M. S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604484103 · Cited by 53
Self-citation

Flagged first, then by citations

Show all 7 references

Sorted by citations

Items 301–400 of 462

Sufficiency analysis of estrogen responsive enhancers using synthetic activators
Ginley-Hidinger, M., Carleton, J. B., Rodriguez, A. C., Berrett, K. C., & Gertz, J. (2019) · Life Science Alliance · doi:10.26508/lsa.201900497 · Cited by 12
The design and logic of terminal patterning in Drosophila
Smits, C. M., & Shvartsman, S. Y. (2020) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2019.11.008 · Cited by 12
Biphasic wnt8a expression is achieved through interactions of multiple regulatory inputs
Narayanan, A., & Lekven, A. C. (2012) · Developmental Dynamics · doi:10.1002/dvdy.23787 · Cited by 13
The significance of alternative transcripts for Caenorhabditis eleganstranscription factor genes, based on expression pattern analysis
Craig, H. L., Wirtz, J., Bamps, S., Dolphin, C. T., & Hope, I. A. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-249 · Cited by 12
A novel description of a syndrome consisting of 7q21.3 deletion including DYNC1I1 with preserved DLX5/6 without ectrodactyly: a case report
Ramos‐Zaldívar, H. M., Martínez-Irías, D. G., Espinoza‐Moreno, N. A., Napky-Rajo, J. S., Bueso-Aguilar, T. A., Reyes-Perdomo, K. G., Montes-Gambarelli, J. A., Euceda, I. M., Ponce-Barahona, A., Gámez-Fernández, C. A., et al. (2016) · Journal of Medical Case Reports · doi:10.1186/s13256-016-0921-8 · Cited by 12
A candidate causal variant underlying both enhanced cognitive performance and increased risk of bipolar disorderPreprint
Shen, S. Q., Kim‐Han, J. S., Cheng, L., Xu, D., Gökçümen, Ö., Hughes, A. E. O., Myers, C. A., & Corbo, J. C. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/580258 · Cited by 13
Analysis of single-cell CRISPR perturbations indicates that enhancers predominantly act multiplicatively
Zhou, J., Guruvayurappan, K., Toneyan, S., Chen, H. V., Chen, A. R., Koo, P. K., & McVicker, G. (2024) · Cell Genomics · doi:10.1016/j.xgen.2024.100672 · Cited by 11
Pax3/7 regulates neural tube closure and patterning in a non-vertebrate chordate
Kim, K., Orvis, J., & Stolfi, A. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.999511 · Cited by 11
Shadow enhancers modulate distinct transcriptional parameters that differentially effect downstream patterning events
Whitney, P. H., Shrestha, B., Xiong, J., Zhang, T., & Rushlow, C. A. (2022) · Development · doi:10.1242/dev.200940 · Cited by 12
Recently Evolved Enhancers Emerge with High Interindividual Variability and Less Frequently Associate with Disease
Castelijns, B., Baak, M. L., Geeven, G., Vermunt, M. W., Wiggers, C. R. M., Timpanaro, I. S., Kondova, I. I., de Laat, W. L., & Creyghton, M. P. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107799 · Cited by 11
Human Origins and Evolution: Cold Spring Harbor, Deja VuPreprint
White, T. D. (2009) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2009.74.016 · Cited by 11
Oncogenic Enhancers in Leukemia
Mulet‐Lazaro, R., & Delwel, R. (2024) · Blood Cancer Discovery · doi:10.1158/2643-3230.bcd-23-0211 · Cited by 11
EnhancerNet: a predictive model of cell identity dynamics through enhancer selection
Karin, O. (2024) · Development · doi:10.1242/dev.202997 · Cited by 10
Enhancers are genes that express organizational RNAs
Mattick, J. S. (2023) · Frontiers in RNA Research · doi:10.3389/frnar.2023.1194526 · Cited by 10
Microsatellite Repeat Instability Fuels Evolution of Embryonic Enhancers in Hawaiian Drosophila
Brittain, A. M., Stroebele, E., & Erives, A. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0101177 · Cited by 10
Enhancers
Cho, K. W. Y. (2012) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.53 · Cited by 10
Evidence for compensatory evolution within pleiotropic regulatory elementsPreprint
Kliesmete, Z., Orchard, P., Lee, V. Y. K., Geuder, J., Krauß, S. M., Ohnuki, M., Jocher, J., Vieth, B., Enard, W., & Hellmann, I. (2024) · Genome Research · doi:10.1101/gr.279001.124 · Cited by 11
Functional genomic assays to annotate enhancer–promoter interactions genome wide
Leung, A. K.-Y., Li, Y., & Yu, H. (2022) · Human Molecular Genetics · doi:10.1093/hmg/ddac204 · Cited by 9
In vivo mapping of mutagenesis sensitivity of human enhancers
Kosicki, M., Zhang, B., Hecht, V., Pampari, A., Cook, L. E., Slaven, N., Akiyama, J., Plajzer-frick, I., Novak, C. S., Kato, M., et al. (2025) · Nature · doi:10.1038/s41586-025-09182-w · Cited by 6
Cis -regulatory Landscape Size, Constraint, and Tissue Specificity Associate with Gene Function and Expression
Benton, M. L., Ruderfer, D. M., & Capra, J. A. (2023) · Genome Biology and Evolution · doi:10.1093/gbe/evad126 · Cited by 9
From Genotype to Phenotype: How Enhancers Control Gene Expression and Cell Identity in Hematopoiesis
Mulet‐Lazaro, R., & Delwel, R. (2023) · HemaSphere · doi:10.1097/hs9.0000000000000969 · Cited by 11
Multiple cis -regulatory elements control prox1a expression in distinct lymphatic vascular beds
Panara, V., Yu, H., Peng, D., Staxäng, K., Hodik, M., Filipek‐Górniok, B., Kazenwadel, J., Skoczylas, R., Mason, E. A., Allalou, A., et al. (2024) · Development · doi:10.1242/dev.202525 · Cited by 9
Sequential construction of a model for modular gene expression control, applied to spatial patterning of theDrosophilagenehunchback
Spirov, A. V., Марковна, М. Е., & Holloway, D. M. (2016) · Journal of Bioinformatics and Computational Biology · doi:10.1142/s0219720016410055 · Cited by 9
How to study enhancers in non-traditional insect models
Tomoyasu, Y., & Halfon, M. S. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.212241 · Cited by 9
A synthetic synthesis to explore animal evolution and development
Perkins, M. L., Gándara, L., & Crocker, J. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2020.0517 · Cited by 9
Enhancer trap infidelity inDrosophila optomotor-blind
Mayer, L., Diegelmann, S., Abassi, Y., Eichinger, F., & Pflugfelder, G. O. (2013) · Fly · doi:10.4161/fly.23657 · Cited by 9
ChIP-ping the branches of the tree: functional genomics and the evolution of eukaryotic gene regulation
Marinov, G. K., & Kundaje, A. B. (2018) · Briefings in Functional Genomics · doi:10.1093/bfgp/ely004 · Cited by 9
Synergistic activity of Nanog, Pou5f3, and Sox19b establishes chromatin accessibility and developmental competence in a context-dependent mannerPreprint
Miao, L., Tang, Y., Bonneau, A. R., Chan, S. H., Kojima, M. L., Pownall, M. E., Vejnar, C. E., & Giráldez, A. J. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.09.01.278796 · Cited by 8
Multi-layered transcriptional control of cranial neural crest development
Candido-Ferreira, I., Lukoseviciute, M., & Sauka‐Spengler, T. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.07.010 · Cited by 8
Enhancer selectivity across cell types delineates three functionally distinct enhancer-promoter regulation patterns
Wu, C., & Huang, J. (2024) · BMC Genomics · doi:10.1186/s12864-024-10408-w · Cited by 8
Gene-regulatory networks in the Ciona embryos
Kubo, A., Imai, K. S., & Satou, Y. (2009) · Briefings in Functional Genomics and Proteomics · doi:10.1093/bfgp/elp018 · Cited by 8
Promoter-enhancer looping and shadow enhancers of the mouse αA-crystallin locus
McGreal, R., Wolf, L. V., & Cvekl, A. (2018) · Biology Open · doi:10.1242/bio.036897 · Cited by 8
An in silico analysis of robust but fragile gene regulation links enhancer length to robustness
Barr, K., Reinitz, J., & Radulescu, O. (2019) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1007497 · Cited by 9
Sex‐specific evolution of a Drosophila sensory system via interacting cis‐ and trans‐ regulatory changes
Luecke, D. M., Rice, G. R., & Kopp, A. (2022) · Evolution & Development · doi:10.1111/ede.12398 · Cited by 9
Using evolutionary algorithms to study the evolution of gene regulatory networks controlling biological development
Spirov, A. V., & Holloway, D. M. (2016) · Wiley eBooks · doi:10.1002/9781119079453.ch10 · Cited by 8
Zelda potentiates transcription factor binding to zygotic enhancers by increasing local chromatin accessibility during early Drosophila melanogaster embryogenesisPreprint
Li, X., & Eisen, M. B. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/380857 · Cited by 8
Genetic and Epigenetic Dysregulation of Transcriptional Enhancers in Cancer
Botten, G. A., & Xu, J. (2024) · Annual Review of Cancer Biology · doi:10.1146/annurev-cancerbio-060324-114306 · Cited by 7
Modular organization of enhancer network provides transcriptional robustness in mammalian development
Lin, H., Ye, X., Chen, W., Hong, D., Liu, L., Chen, F., Sun, N., Ye, K., Hong, J., Zhang, Y., et al. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkae1323 · Cited by 7
Self-citation
Reporter Analyses Reveal Redundant Enhancers that Confer Robustness on Cis-Regulatory Mechanisms
Fujiwara, S., & Cañestro, C. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-7545-2_7 · Cited by 7
Comparative Evidence of an Exceptional Impact of Gene Duplication on the Developmental Evolution of Drosophila and the Higher Diptera
Bao, R., Dia, S. E., Issa, H. A. A., Alhusein, D., & Friedrich, M. (2018) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2018.00063 · Cited by 7
Analysis of the landscape of human enhancer sequences in biological databases
Mulero-Hernández, J., & Fernández‐Breis, J. T. (2022) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2022.05.045 · Cited by 9
Cross-tissue patterns of DNA hypomethylation reveal genetically distinct histories of cell development
Scott, T. J., Hansen, T. J., McArthur, E., & Hodges, E. C. (2023) · BMC Genomics · doi:10.1186/s12864-023-09622-9 · Cited by 7
Timeless noncoding DNA contains cell-type preferential enhancers important for proper Drosophila circadian regulation
Ma, D., Ojha, P., Yu, A. D., Araújo, M. D. S., Luo, W., Keefer, E., Díaz, M. M., Wu, M., Joiner, W. J., Abruzzi, K. C., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2321338121 · Cited by 6
Modularity in Biological Evolution and Evolutionary Computation
Spirov, A. V., & Eremeev, A. V. (2020) · Biology Bulletin Reviews · doi:10.1134/s2079086420040076 · Cited by 6
Exploring the Role of Enhancer-Mediated Transcriptional Regulation in Precision Biology
Wang, X., Liu, D., Luo, J., Kong, D., & Zhang, Y. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241310843 · Cited by 7
The contributions of DNA accessibility and transcription factor occupancy to enhancer activity during cellular differentiation
Long, T., Bhattacharyya, T., Repele, A., Naylor, M., Nooti, S. K., Krueger, S., & Manu (2023) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkad269 · Cited by 8
In silicoevolution of thehunchbackgene indicates redundancy in cis-regulatory organization and spatial gene expression
Zagrijchuk, E. A., Sabirov, M. A., Holloway, D. M., & Spirov, A. V. (2014) · Journal of Bioinformatics and Computational Biology · doi:10.1142/s0219720014410091 · Cited by 6
Dichotomy in redundant enhancers points to presence of initiators of gene regulation
Song, W., & Ovcharenko, I. (2018) · BMC Genomics · doi:10.1186/s12864-018-5335-0 · Cited by 6
Evolution of modular and pleiotropic enhancers
Murugesan, S. N., & Monteiro, A. (2022) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.23131 · Cited by 7
Tuning cell differentiation patterns and single cell dynamics by regulating proteins’ functionalities in a toggle switch
Dai, X., Healy, S., Yli-Harja, O. P., & Ribeiro, A. S. (2009) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2009.08.024 · Cited by 6
Entangled and non-modular enhancer sequences producing independent spatial activities
Museridze, M., Ceolin, S., Mühling, B., Ramanathan, S., Barmina, O. Y., Sekhar, P. S., & Gompel, N. (2024) · Science Advances · doi:10.1126/sciadv.adr9856 · Cited by 5
A scaffolding element rewires local 3D chromatin architecture during differentiation
Jerković, I., Stefano, M. D., Reboul, H., Szalay, M., Normanno, D., Paldi, F., Papadopoulos, G. L., Szabo, Q., Bantignies, F., & Cavalli, G. (2026) · Nature Communications · doi:10.1038/s41467-026-77603-z · Cited by 5
Repurposing of the enhancer-promoter communication underlies the compensation of Mesp2 by Mesp1
Okada, H., & Saga, Y. (2022) · PLoS Genetics · doi:10.1371/journal.pgen.1010000 · Cited by 5
Accelerated evolution in the human lineage led to gain and loss of transcriptional enhancers in theRBFOX1locus
Berasain, L., Beati, P., Trigila, A. P., Rubinstein, M., & Franchini, L. F. (2024) · Science Advances · doi:10.1126/sciadv.adl1049 · Cited by 6
Interpreting the regulatory genome: the genomics of transcription factor function in Drosophila melanogaster
Slattery, M. R. F., Nègre, N., & White, K. P. (2012) · Briefings in Functional Genomics · doi:10.1093/bfgp/els034 · Cited by 6
Transcriptional Dynamics at Brain Enhancers: from Functional Specialization to Neurodegeneration
Vermunt, M. W., & Creyghton, M. P. (2016) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-016-0689-7 · Cited by 5
Enhancer jungles establish robust tissue-specific regulatory control in the human genome
Li, S., & Ovcharenko, I. (2019) · Genomics · doi:10.1016/j.ygeno.2019.12.022 · Cited by 5
No Need to Stick Together to Be Connected: Multiple Types of Enhancers’ Networking
Vitale, E., Gugnoni, M., & Ciarrocchi, A. (2021) · Cancers · doi:10.3390/cancers13205201 · Cited by 5
Hnf1b renal expression directed by a distal enhancer responsive to Pax8
Goea, L., Buisson, I., Bello, V., Eschstruth, A., Paces-Fessy, M., Bouffant, R. L., Chesneau, A., Cereghini, S., Riou, J., & Umbhauer, M. (2022) · Scientific Reports · doi:10.1038/s41598-022-21171-x · Cited by 7
Functional dissection of the ARGONAUTE 7 promoter
Hoyer, J. S., Pruneda-Paz, J. L., Breton, G., Hassert, M., Holcomb, E. E., Fowler, H., Bauer, K. M., Mreen, J., Kay, S. A., & Carrington, J. C. (2019) · Plant Direct · doi:10.1002/pld3.102 · Cited by 6
Speed Regulation and Gradual Enhancer Switching Models as Flexible and Evolvable Patterning MechanismsPreprint
Kuhlmann, L., & El‐Sherif, E. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/261891 · Cited by 5
A Human Accelerated Region is a Leydig cell GLI2 Enhancer that Affects Male-Typical BehaviorPreprint
Norman, A. R., Ryu, A. H., Jamieson, K., Thomas, S., Shen, Y., Ahituv, N., Pollard, K. S., & Reiter, J. F. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.01.27.428524 · Cited by 5
A digital twin reproducing gene regulatory network dynamics of early Ciona embryos indicates robust buffers in the network
Tokuoka, M., & Satou, Y. (2023) · PLoS Genetics · doi:10.1371/journal.pgen.1010953 · Cited by 4
The fushi tarazu zebra element is not required for Drosophila viability or fertility
Graham, P. L., Fischer, M. D., Giri, A., & Pick, L. (2021) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkab300 · Cited by 4
The ftz upstream element drives late ftz stripes but is not required for regulation of Ftz target genes
Fischer, M. D., Graham, P. L., & Pick, L. (2023) · Developmental Biology · doi:10.1016/j.ydbio.2023.11.004 · Cited by 4
Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J., Abdalla-Wyse, A., & Goldowitz, D. (2023) · BMC Genomics · doi:10.1186/s12864-023-09368-4 · Cited by 4
Shaping the nebulous enhancer in the era of high-throughput assays and genome editing
Ho, E. Y.-K., Cao, Q., Gu, M., Chan, R. W.-L., Wu, Q., Gerstein, M., & Yip, K. Y.-L. (2019) · Briefings in Bioinformatics · doi:10.1093/bib/bbz030 · Cited by 4
The role of the epidermis enhancer element in positive and negative transcriptional regulation of ebony in Drosophila melanogaster
Akiyama, N., Sato, S., Tanaka, K. M., Sakai, T., & Takahashi, A. (2022) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkac010 · Cited by 5
Genomic signatures of the evolution of a diurnal lifestyle in Strigiformes
Espíndola‐Hernández, P., Mueller, J. C., & Kempenaers, B. (2022) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkac135 · Cited by 5
A cis-regulatory sequence of the selector gene vestigial drives the evolution of wing scaling in Drosophila species
Farfán‐Pira, K. J., Martínez-Cuevas, T. I., Evans, T. A., & Nahmad, M. (2023) · Journal of Experimental Biology · doi:10.1242/jeb.244692 · Cited by 4
Shadow enhancers mediate trade-offs between transcriptional noise and fidelity
Fletcher, A., Wunderlich, Z., & Enciso, G. (2023) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1011071 · Cited by 4
A novel cis-regulatory element drives early expression of Nkx3.2 in the gnathostome primary jaw joint
Leyhr, J., Waldmann, L., Filipek‐Górniok, B., Zhang, H., Allalou, A., & Haitina, T. (2022) · eLife · doi:10.7554/elife.75749 · Cited by 4
Many rare genetic variants have unrecognized large-effect disruptions to exon recognitionPreprint
Cheung, R., Insigne, K. D., Yao, D., Burghard, C. P., Jones, E. M., Goodman, D. B., & Kosuri, S. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/199927 · Cited by 5
An Osteoblast-Specific Enhancer and Subenhancer Cooperatively Regulate Runx2 Expression in Chondrocytes
Matsuo, Y., Qin, X., Moriishi, T., Kawata-Matsuura, V. K. S., Komori, H., Sakane, C., Yabuta, S., Jiang, Q., Kaneko, H., Ito, K., et al. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26041653 · Cited by 4
Divergent combinations of enhancers encode spatial gene expression
Hong, D., Shu, M., Liu, J., Liu, L., Cheng, H., Zhu, M., Du, Y., Xu, B., Hu, D., Liu, Z., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-60482-1 · Cited by 5
Segmentally Duplicated Regulatory Elements Undergo Human-Specific Rewiring
Weaver, S., & Lowe, C. B. (2026) · Molecular Biology and Evolution · doi:10.1093/molbev/msag140 · Cited by 3
Transcriptional activity of the short gastrulation primary enhancer in the ventral midline requires its early activity in the presumptive neurogenic ectoderm
Shin, D.-H., & Hong, J. (2016) · BMB Reports · doi:10.5483/bmbrep.2016.49.10.119 · Cited by 3
Self-citation
Identification and functional modelling of plausibly causative cis-regulatory variants in a highly-selected cohort with X-linked intellectual disability
Bengani, H., Grozeva, D., Moyon, L., Bhatia, S., Louros, S. R., Hope, J. E., Jackson, A., Prendergast, J. G. D., Owen, L. J., Naville, M., et al. (2021) · PLoS ONE · doi:10.1371/journal.pone.0256181 · Cited by 3
Midline enhancer activity of the short gastrulation shadow enhancer is characterized by three unusual features for cis-regulatory DNA
Shin, D.-H., & Hong, J. (2015) · BMB Reports · doi:10.5483/bmbrep.2015.48.10.155 · Cited by 3
Self-citation
Two Enhancers Regulate HoxB Genes Expression During Retinoic Acid-Induced Early Embryonic Stem Cells Differentiation Through Long-Range Chromatin Interactions
Zheng, J., Su, G., Wang, W., Zhao, X., Liu, M., Bi, J., Zhao, Z., Shi, J., Lu, W., & Zhang, L. (2021) · Stem Cells and Development · doi:10.1089/scd.2021.0020 · Cited by 3
Cis acting variation is common, can propagates across multiple regulatory layers, but is often buffered in developmental programsPreprint
Floc’hlay, S., Wong, E. S. W., Zhao, B., Viales, R. R., Thomas‐Chollier, M., Thieffry, D., Garfield, D. A., & Furlong, E. E. M. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.21.107961 · Cited by 3
Decoding the Epigenetics and Chromatin Loop Dynamics of Androgen Receptor-Mediated TranscriptionPreprint
Altıntaş, U. B., Seo, J.-H., Giambartolomei, C., Özturan, D., Fortunato, B. J., Nelson, G. M., Goldman, S. R., Adelman, K., Hach, F., Freedman, M. L., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.12.22.573134 · Cited by 3
Evidence for compensatory evolution within pleiotropic regulatory elementsPreprint
Kliesmete, Z., Orchard, P., Lee, V. Y. K., Geuder, J., Krauß, S. M., Ohnuki, M., Jocher, J., Vieth, B., Enard, W., & Hellmann, I. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.10.575014 · Cited by 3
Molecular co-accessibility identifies coordinated regulation between distant cis-regulatory elements
Boulanger, M., Chatsirisupachai, K., Badayeva, Y., Snajder, R., Bonder, M. J., Lapouge, K., Remans, K., & Krebs, A. R. (2026) · Molecular Cell · doi:10.1016/j.molcel.2026.07.020 · Cited by 5
Use of alternative promoters may hide genetic effects on phenotypic traits
Ruiz-Narváez, E. (2012) · Journal of Human Genetics · doi:10.1038/jhg.2012.115 · Cited by 2
Two coacting shadow enhancers regulate twin of eyeless expression during early Drosophila development
Dresch, J. M., Nourie, L., Conrad, R. D., Carlson, L. T., Tchantouridze, E. I., Tesfaye, B., Verhagen, E., Gupta, M., Borges-Rivera, D., & Drewell, R. A. (2024) · Genetics · doi:10.1093/genetics/iyae176 · Cited by 2
Enhancer‐dependent gene regulation in space, time, and malignancies
Blum, B., Dachtler, V., & Feldmann, A. (2025) · International Journal of Cancer · doi:10.1002/ijc.35350 · Cited by 2
GRHL and PGR control WNT4 expression via 3D looping of conserved and species-specific enhancers
van de Grift, Y. B. C., Aarts, M. T., Wiese, K. E., Heijmans, N., Hooijkaas, I. B., Pritchard, C. E. J., Henneman, L., Krimpenfort, P., van Boxtel, A. L., & van Amerongen, R. (2026) · Cell Reports · doi:10.1016/j.celrep.2026.117575 · Cited by 2
Gene Regulatory Elements
Ahituv, N. (2012) · Springer eBooks · doi:10.1007/978-1-4614-1683-8_1 · Cited by 2
Self-organization in the ontogeny of multicellular organisms: A computer simulation
Markov, M. A., & Markov, A. V. (2012) · Biology Bulletin Reviews · doi:10.1134/s2079086412010033 · Cited by 2
The short gastrulation shadow enhancer employs dual modes of transcriptional synergy
Shin, D.-H., & Hong, J. (2016) · The International Journal of Developmental Biology · doi:10.1387/ijdb.160165jh · Cited by 2
Self-citation
Shared cis-regulatory modules control expression of the tandem paralogs midline and H15 in the follicular epithelium
Stevens, C. A., Stott, H. L., Desai, S. V., & Yakoby, N. (2022) · Development · doi:10.1242/dev.201016 · Cited by 3
LucFlow: A method to measure Luciferase reporter expression in single cells
Nooti, S. K., Naylor, M., Long, T., Groll, B., & Manu (2023) · PLoS ONE · doi:10.1371/journal.pone.0292317 · Cited by 2
The shadow enhancer of short gastrulation also directs its expression in the ventral midline of the Drosophila embryo
Shin, D.-H., & Hong, J. (2015) · Genes & Genomics · doi:10.1007/s13258-015-0302-5 · Cited by 2
Self-citation
Identification of novel cis-regulatory elements of Eya1 in Xenopus laevis using BAC recombineering
Maharana, S. K., Pollet, N., & Schlosser, G. (2017) · Scientific Reports · doi:10.1038/s41598-017-15153-7 · Cited by 2
Two pair‐rule responsive enhancers regulate wingless transcription in the Drosophila blastoderm embryo
Bell, K., Skier, K., Chen, K. H., & Gergen, J. P. (2019) · Developmental Dynamics · doi:10.1002/dvdy.142 · Cited by 2
Enhancers, development, and evolution
Kuroiwa, A. (2020) · Development Growth & Differentiation · doi:10.1111/dgd.12683 · Cited by 3
[Hypophosphatemia in critically ill patients].
Nguyen, T., & Vincent, J. (2011) · PubMed · Cited by 2
The vestigial Quadrant Enhancer is dispensable for pattern formation and development of the Drosophila wing
Farfán‐Pira, K. J., Martínez-Cuevas, T. I., Reyes, R., Evans, T. A., & Nahmad, M. (2022) · PubMed Central · doi:10.17912/micropub.biology.000585 · Cited by 2
Prediction and analysis of cis-regulatory elements in Dorsal and Ventral patterning genes of Tribolium castaneum and its comparison with Drosophila melanogaster
Kapil, S., Sobti, R. C., & Kaur, T. (2023) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-023-04712-4 · Cited by 2

Authors: Hong, J.-W., Hendrix, D. A., & Levine, M. S.
Affiliations: University of California, Berkeley (US)
Corresponding author: Levine, Michael S.
ORCID: Hong, Joung-Woo
Hendrix, David A.
Levine, Michael S.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2008-09-05
Volume: 321
Issue: 5894
Pages: 1314-1314
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.1160631
PMC: PMC4257485
OpenAlex: W2006824094
Cited by: 474
References: 7
Citations by year: 2026: 17 · 2025: 15 · 2024: 27 · 2023: 31 · 2022: 34 · 2021: 20 · 2020: 31 · 2019: 31 · 2018: 30 · 2017: 24 · 2016: 32 · 2015: 29 · 2014: 33 · 2013: 31 · 2012: 22
FWCI: 9.04
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Science (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of General Medical Sciences (GM-46638, R01GM046638)
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 › Genetics › Chromosomal and Genetic Variations
Keywords: enhancer regulation, evolutionary innovation, developmental genes, gene expression regulation, cis-regulatory elements
MeSH terms: Animals, Binding Sites, Drosophila, Drosophila melanogaster, Enhancer Elements, Genetic, Introns, Nuclear Proteins, Phosphoproteins, Phylogeny, Transcription Factors, Gene Expression Regulation, Developmental, Evolution, Molecular, Computational Biology, Body Patterning, Oligonucleotide Array Sequence Analysis, 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

Shadow Enhancers as a Source of Evolutionary Novelty

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks