Supervised enhancer prediction with epigenetic pattern recognition and targeted validation
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Abstract
Enhancers are important non-coding elements, but they have traditionally been hard to characterize experimentally. The development of massively parallel assays allows the characterization of large numbers of enhancers for the first time. Here, we developed a framework using Drosophila STARR-seq to create shape-matching filters based on meta-profiles of epigenetic features. We integrated these features with supervised machine-learning algorithms to predict enhancers. We further demonstrated that our model could be transferred to predict enhancers in mammals. We comprehensively validated the predictions using a combination of in vivo and in vitro approaches, involving transgenic assays in mice and transduction-based reporter assays in human cell lines (153 enhancers in total). The results confirmed that our model can accurately predict enhancers in different species without re-parameterization. Finally, we examined the transcription factor binding patterns at predicted enhancers versus promoters. We demonstrated that these patterns enable the construction of a secondary model that effectively distinguishes enhancers and promoters.
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Enhancer detection based on chromatin profiling may falsely detect regions without appreciable regulatory activity, as well as miss some functional elements.
“While enhancer detection based on chromatin profiling has become standard, this approach may falsely detect regions without appreciable regulatory activity, as well as miss some functional elements [146, 162].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [162]
The Online methods (Model assessment; page unavailable) describe non-STARR-seq regions with H3K27ac signal, supporting the possibility that a chromatin signal can occur without measured enhancer activity. The Introduction (page unavailable) says active enhancers are *usually* in open chromatin, but the copy does not directly establish that chromatin-based detection misses functional elements. (LLM, conf=0.79)
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Cites
Breiman, L. (2001) · Machine Learning · doi:10.1023/a:1010933404324 · Cited by 133,538 · 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
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
A Tutorial on Support Vector Machines for Pattern Recognition
Burges, C. J. C. (1998) · Data Mining and Knowledge Discovery · doi:10.1023/a:1009715923555 · Cited by 16,437 · see citing works
Ridge regression: Biased estimation for nonorthogonal problems
Hoerl, A. E., & Kennard, R. W. (1970) · Technometrics · doi:10.1080/00401706.1970.10488634 · Cited by 9,648 · see citing works
Ridge Regression: Biased Estimation for Nonorthogonal Problems
Hoerl, A. E., & Kennard, R. W. (2000) · Technometrics · doi:10.2307/1271436 · Cited by 6,553 · see citing works
Integrative analysis of 111 reference human epigenomes
Roadmap Epigenomics Consortium, Kundaje, A., Meuleman, W., Ernst, J., Bilenky, M., Yen, A., Heravi-Moussavi, A., Kheradpour, P., Zhang, Z., Wang, J., et al. (2015) · Nature · doi:10.1038/nature14248 · Cited by 6,368 · see citing works
GENCODE: The reference human genome annotation for The ENCODE Project
Harrow, J., Frankish, A., Gonzalez, J. M., Tapanari, E., Diekhans, M., Kokocinski, F., Aken, B. L., Barrell, D., Zadissa, A., Searle, S., et al. (2012) · Genome Research · doi:10.1101/gr.135350.111 · Cited by 4,585 · see citing works
Self-citationHistone H3K27ac separates active from poised enhancers and predicts developmental state
Creyghton, M. P., Cheng, A. W., Welstead, G. G., Kooistra, T., Carey, B. W., Steine, E. J., Hanna, J., Lodato, M. A., Frampton, G. M., Sharp, P. A., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016071107 · Cited by 4,302 · see citing works
Heintzman, N. D., Stuart, R. K., Hon, G., Fu, Y., Ching, C. W., Hawkins, R. D., Barrera, L. O., Van Calcar, S., Qu, C., Ching, K. A., et al. (2007) · Nature Genetics · doi:10.1038/ng1966 · Cited by 3,398 · cited 1× · see citing works
“These attributes lead to an enriched peak-trough-peak (“double peak”) signal, which has been observed in previous studies [22].”
Mapping and analysis of chromatin state dynamics in nine human cell types
Ernst, J., Kheradpour, P., Mikkelsen, T. S., Shoresh, N., Ward, L. D., Epstein, C. B., Zhang, X., Wang, L., Issner, R., Coyne, M., et al. (2011) · Nature · doi:10.1038/nature09906 · Cited by 2,898 · see citing works
The accessible chromatin landscape of the human genome
Thurman, R. E., Rynes, E., Humbert, R., Vierstra, J., Maurano, M. T., Haugen, E., Sheffield, N. C., Stergachis, A. B., Wang, H., Vernot, B., et al. (2012) · Nature · doi:10.1038/nature11232 · Cited by 2,679 · see citing works
An atlas of active enhancers across human cell types and tissues
The FANTOM Consortium, Andersson, R., Gebhard, C., Miguel-Escalada, I., Hoof, I., Bornholdt, J., Boyd, M., Chen, Y., Zhao, X., Schmidl, C., et al. (2014) · Nature · doi:10.1038/nature12787 · Cited by 2,550 · see citing works
ChromHMM: automating chromatin-state discovery and characterization
Ernst, J., & Kellis, M. (2012) · Nature Methods · doi:10.1038/nmeth.1906 · Cited by 2,489 · 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
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
Expression of a β-globin gene is enhanced by remote SV40 DNA sequences
Banerji, J., Rusconi, S., & Schaffner, W. (1981) · Cell · doi:10.1016/0092-8674(81)90413-x · Cited by 1,724 · see citing works
ChIP-seq accurately predicts tissue-specific activity of enhancers
Visel, A., Blow, M. J., Li, Z., Zhang, T., Akiyama, J. A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., Chen, F., et al. (2009) · Nature · doi:10.1038/nature07730 · Cited by 1,639 · see citing works
Self-citationThe evolutionary significance of cis-regulatory mutations
Wray, G. A. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2063 · Cited by 1,521 · 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
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
In vivo enhancer analysis of human conserved non-coding sequences
Pennacchio, L. A., Ahituv, N., Moses, A. M., Prabhakar, S., Nobrega, M. A., Shoukry, M., Minovitsky, S., Dubchak, I., Holt, A., Lewis, K. D., et al. (2006) · Nature · doi:10.1038/nature05295 · Cited by 1,165 · see citing works
Self-citationGenome-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
Highly Conserved Non-Coding Sequences Are Associated with Vertebrate Development
Woolfe, A., Goodson, M., Goode, D. K., Snell, P., McEwen, G. K., Vavouri, T., Smith, S. F., North, P., Callaway, H., Kelly, K., et al. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0030007 · Cited by 970 · see citing works
Enhancer function: new insights into the regulation of tissue-specific gene expression
Ong, C.-T., & Corces, V. G. (2011) · Nature Reviews Genetics · doi:10.1038/nrg2957 · Cited by 929 · see citing works
Enhancer Evolution across 20 Mammalian Species
Villar, D., Berthelot, C., Aldridge, S., Rayner, T. F., Lukk, M., Pignatelli, M., Park, T. J., Deaville, R., Erichsen, J. T., Jasinska, A. J., et al. (2015) · Cell · doi:10.1016/j.cell.2015.01.006 · Cited by 825 · 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
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
Enhancers: five essential questions
Pennacchio, L. A., Bickmore, W. A., Dean, A., Nóbrega, M. A., & Bejerano, G. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3458 · Cited by 584 · see citing works
Self-citationConserved epigenomic signals in mice and humans reveal immune basis of Alzheimer's disease
Gjoneska, E., Pfenning, A. R., Mathys, H., Quon, G., Kundaje, A., Tsai, L.-H., & Kellis, M. (2015) · Nature · doi:10.1038/nature14252 · Cited by 576 · see citing works
Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells
Arner, E., Daub, C. O., Vitting‐Seerup, K., Andersson, R., Lilje, B., Drabløs, F., Lennartsson, A., Rönnerblad, M., Hrydziuszko, O., Vitezic, M., et al. (2015) · Science · doi:10.1126/science.1259418 · Cited by 570 · see citing works
Unsupervised pattern discovery in human chromatin structure through genomic segmentation
Hoffman, M. M., Buske, O. J., Wang, J., Weng, Z., Bilmes, J., & Noble, W. S. (2012) · Nature Methods · doi:10.1038/nmeth.1937 · Cited by 566 · see citing works
Partitioning Heritability of Regulatory and Cell-Type-Specific Variants across 11 Common Diseases
Gusev, A., Lee, S. H., Trynka, G., Finucane, H., Vilhjálmsson, B. J., Xu, H., Zang, C., Ripke, S., Bulik-Sullivan, B., Stahl, E., et al. (2014) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2014.10.004 · Cited by 544 · see citing works
Absence of a simple code: how transcription factors read the genome
Slattery, M., Zhou, T., Yang, L., Dantas Machado, A. C., Gordân, R., & Rohs, R. (2014) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2014.07.002 · Cited by 537 · 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
Self-citationIntegrative annotation of chromatin elements from ENCODE data
Hoffman, M. M., Ernst, J., Wilder, S. P., Kundaje, A. B., Harris, R. S., Libbrecht, M., Giardine, B. M., Ellenbogen, P. M., Bilmes, J. A., Birney, E., et al. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1284 · Cited by 521 · see citing works
Enhanced Regulatory Sequence Prediction Using Gapped k-mer Features
Ghandi, M., Lee, D., Mohammad-Noori, M., & Beer, M. A. (2014) · PLoS Comput. Biol. · doi:10.1371/journal.pcbi.1003711 · Cited by 514 · see citing works
Enhancer–core-promoter specificity separates developmental and housekeeping gene regulation
Zabidi, M. A., Arnold, C. D., Schernhuber, K., Pagani, M., Rath, M., Frank, O., & Stark, A. (2015) · Nature · doi:10.1038/nature13994 · Cited by 471 · see citing works
The landscape of histone modifications across 1% of the human genome in five human cell linesPreprint
Andrews, R., Beare, D., Flicek, P., Bruce, A., Carter, N., Clelland, G., Wilcox, S., Beare, D. M., Fowler, J. C., Dovey, O., et al. (2007) · Genome Research · doi:10.1101/gr.5704207 · Cited by 441 · see citing works
Unsupervised pattern discovery in human chromatin structure through genomic segmentation
Hoffman, M. M., Buske, O. J., Wang, J., Weng, Z., Bilmes, J., & Noble, W. S. (2012) · eScholarship@UMassChan · Cited by 397 · see citing works
Towards a comprehensive catalogue of validated and target-linked human enhancers
Gasperini, M., Tome, J. M., & Shendure, J. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-019-0209-0 · Cited by 396 · see citing works
Rapid and Pervasive Changes in Genome-wide Enhancer Usage during Mammalian Development
Nord, A. S., Blow, M. J., Attanasio, C., Akiyama, J. A., Holt, A., Hosseini, R., Phouanenavong, S., Plajzer-Frick, I., Shoukry, M., Afzal, V., et al. (2013) · Cell · doi:10.1016/j.cell.2013.11.033 · Cited by 375 · see citing works
Self-citationUltraconservation identifies a small subset of extremely constrained developmental enhancers
Visel, A., Prabhakar, S., Akiyama, J. A., Shoukry, M., Lewis, K. D., Holt, A., Plajzer-Frick, I., Afzal, V., Rubin, E. M., & Pennacchio, L. A. (2008) · Nature Genetics · doi:10.1038/ng.2007.55 · Cited by 325 · see citing works
Self-citationInducible expression of an hsp68-lacZ hybrid gene in transgenic mice
Kothary, R., Clapoff, S., Darling, S. M., Perry, M. D., Moran, L. A., & Rossant, J. (1989) · Development · doi:10.1242/dev.105.4.707 · Cited by 323 · see citing works
Correlation Pattern Recognition
Kumar, B. V. K. V., Mahalanobis, A., & Juday, R. D. (2005) · Cambridge University Press eBooks · doi:10.1017/cbo9780511541087 · Cited by 322 · see citing works
Comparative analysis of the transcriptome across distant species
Gerstein, M., Rozowsky, J. S., Yan, K., Wang, D., Cheng, C., Brown, J. B., Davis, C., Hillier, L., Sisu, C., Li, J. J., et al. (2014) · Nature · doi:10.1038/nature13424 · Cited by 290 · see citing works
Self-citationUnsupervised pattern discovery in human chromatin structure through genomic segmentation
Hoffman, M. M., Buske, O. J., Wang, J., Weng, Z., Bilmes, J. A., & Noble, W. S. (2013) · ACM International Conference on Bioinformatics, Computational Biology, and Health Informatics (ACM-BCB) · doi:10.1145/2506583.2506701 · Cited by 288 · see citing works
Principles Of Regulatory Information Conservation Between Mouse And Human
Cheng, Y., Ma, Z., Kim, B.-H., Wu, W.-S., Cayting, P., Boyle, A., Sundaram, V., Xing, X., Dogan, N., Li, J.-J., et al. (2014) · Nature · doi:10.1038/nature13985 · Cited by 268 · see citing works
Self-citationEnhancer–promoter specificity mediated by DPE or TATA core promoter motifs
Butler, J. E. F., & Kadonaga, J. T. (2001) · Genes & Development · doi:10.1101/gad.924301 · Cited by 265 · see citing works
A tiling-deletion-based genetic screen for cis-regulatory element identification in mammalian cells
Diao, Y., Fang, R., Li, B., Meng, Z., Yu, J., Qiu, Y., Lin, K. C., Huang, H., Liu, T., Marina, R. J., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4264 · Cited by 259 · see citing works
Modeling gene expression using chromatin features in various cellular contexts
Dong, X., Greven, M. C., Kundaje, A. B., Djebali, S., Brown, J., Cheng, C., Gingeras, T., Gerstein, M., Guigó, R., Birney, E., et al. (2012) · Genome biology · doi:10.1186/gb-2012-13-9-r53 · Cited by 254 · see citing works
Self-citationYip, K. Y.-L., Cheng, C., Bhardwaj, N., Brown, J., Leng, J., Kundaje, A. B., Rozowsky, J. S., Birney, E., Bickel, P. J., Snyder, M. P., et al. (2012) · Genome biology · doi:10.1186/gb-2012-13-9-r48 · Cited by 244 · see citing works
Self-citationEnhancer variants: evaluating functions in common disease
Corradin, O., & Scacheri, P. C. (2014) · Genome Medicine · doi:10.1186/s13073-014-0085-3 · Cited by 241 · see citing works
Different core promoters possess distinct regulatory activities in the Drosophila embryoPreprint
Ohtsuki, S., Levine, M., & Cai, H. N. (1998) · Genes & Development · doi:10.1101/gad.12.4.547 · Cited by 231 · see citing works
High-throughput functional testing of ENCODE segmentation predictions
Kwasnieski, J. C., Fiore, C., Chaudhari, H. G., & Cohen, B. A. (2014) · Genome Research · doi:10.1101/gr.173518.114 · Cited by 224 · see citing works
RFECS: A Random-Forest Based Algorithm for Enhancer Identification from Chromatin State
Rajagopal, N., Xie, W., Li, Y., Wagner, U., Wang, W., Stamatoyannopoulos, J. A., Ernst, J., Kellis, M., & Ren, B. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002968 · Cited by 221 · see citing works
The Evolution of Lineage-Specific Regulatory Activities in the Human Embryonic Limb
Cotney, J. L., Leng, J., Yin, J., Reilly, S. K., DeMare, L. E., Emera, D., Ayoub, A. E., RAKIC, P. T., & Noonan, J. P. (2013) · Cell · doi:10.1016/j.cell.2013.05.056 · Cited by 208 · see citing works
Resolving systematic errors in widely used enhancer activity assays in human cells
Muerdter, F., Boryń, Ł. M., Woodfin, A. R., Neumayr, C., Rath, M., Zabidi, M. A., Pagani, M., Haberle, V., Kazmar, T., Catarino, R. R., et al. (2018) · Nature Methods · doi:10.1038/nmeth.4534 · Cited by 208 · see citing works
Comparative analysis of regulatory information and circuits across distant species
Boyle, A. P., Araya, C. L., Brdlik, C. M., Cayting, P. D., Cheng, C., Cheng, Y., Gardner, K. E., Hillier, L., Janette, J., Jiang, L., et al. (2014) · Nature · doi:10.1038/nature13668 · Cited by 201 · see citing works
Self-citationComparative Epigenomic Annotation of Regulatory DNA
Shu Dong, X. I. A. O., Xie, D., Cao, X., Yu, P., Xing, X., Chen, C.-C., Musselman, M., Xie, M., West, F. D., Lewin, H. A., et al. (2012) · Cell · doi:10.1016/j.cell.2012.04.029 · Cited by 199 · see citing works
ZNF143 provides sequence specificity to secure chromatin interactions at gene promoters
Bailey, S. D., Zhang, X., Desai, K., Aid, M., Corradin, O., Cowper-Sal·lari, R., Akhtar-Zaidi, B., Scacheri, P. C., Haibe-Kains, B., & Lupien, M. (2015) · Nature Communications · doi:10.1038/ncomms7186 · Cited by 194 · see citing works
Ubiquitous heterogeneity and asymmetry of the chromatin environment at regulatory elements
Kundaje, A., Kyriazopoulou-Panagiotopoulou, S., Libbrecht, M., Smith, C. L., Raha, D., Winters, E. E., Johnson, S. M., Snyder, M., Batzoglou, S., & Sidow, A. (2012) · Genome Research · doi:10.1101/gr.136366.111 · Cited by 178 · see citing works
Statistical performance of support vector machines
Blanchard, G., Bousquet, O., & Massart, P. (2008) · The Annals of Statistics · doi:10.1214/009053607000000839 · Cited by 168 · see citing works
Discover regulatory DNA elements using chromatin signatures and artificial neural network
Firpi, H. A., Ucar, D., & Tan, K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq248 · Cited by 159 · see citing works
Integrating Diverse Datasets Improves Developmental Enhancer Prediction
Erwin, G. D., Oksenberg, N., Truty, R., Kostka, D., Murphy, K. K., Ahituv, N., Pollard, K. S., & Capra, J. A. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003677 · Cited by 154 · see citing works
Yáñez-Cuna, J. O., Arnold, C. D., Stampfel, G., Boryń, Ł. M., Gerlach, D., Rath, M., & Stark, A. (2014) · Genome Research · doi:10.1101/gr.169243.113 · Cited by 145 · see citing works
Unraveling determinants of transcription factor binding outside the core binding sitePreprint
Levo, M., Zalckvar, E., Sharon, E., Machado, A. C. D., Kalma, Y., Lotan‐Pompan, M., Weinberger, A., Zohar Yakhini, B., Rohs, R., & Segal, E. (2015) · Genome Research · doi:10.1101/gr.185033.114 · Cited by 144 · see citing works
Functional assessment of human enhancer activities using whole-genome STARR-sequencing
Liu, Y., Yu, S., Dhiman, V. K., Brunetti, T., Eckart, H., & White, K. P. (2017) · Genome Biology · doi:10.1186/s13059-017-1345-5 · Cited by 136 · see citing works
DEEP: a general computational framework for predicting enhancers
Kleftogiannis, D., Kalnis, P., & Bajic, V. B. (2015) · Nucleic Acids Research · doi:10.1093/nar/gku1058 · Cited by 125 · see citing works
Cotney, J. L., Leng, J., Oh, S., DeMare, L. E., Reilly, S. K., Gerstein, M., & Noonan, J. P. (2012) · Genome Research · doi:10.1101/gr.129817.111 · Cited by 124 · see citing works
Self-citationCheng, C., & Gerstein, M. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr752 · Cited by 121 · see citing works
Self-citationFernández, M., & Miranda‐Saavedra, D. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks149 · Cited by 121 · see citing works
Shibata, Y., Sheffield, N. C., Fedrigo, O. D., Babbitt, C. C., Wortham, M., Tewari, A. K., London, D., Song, L., Lee, B., Iyer, V. R., et al. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002789 · Cited by 121 · see citing works
Genome-wide discovery of human heart enhancersPreprint
Narlikar, L., Sakabe, N. J., Blanski, A. A., Arimura, F. E., Westlund, J. M., Nóbrega, M. A., & Ovcharenko, I. (2010) · Genome Research · doi:10.1101/gr.098657.109 · Cited by 117 · see citing works
Genome-wide prediction of transcription factor binding sites using an integrated model
Won, K.-J., Ren, B., & Wang, W. (2010) · Genome Biology · doi:10.1186/gb-2010-11-1-r7 · Cited by 116 · see citing works
Promoter specificity mediates the independent regulation of neighboring genes.
Merli, C., Bergstrom, D. E., Cygan, J. A., & Blackman, R. K. (1996) · Genes & Development · doi:10.1101/gad.10.10.1260 · Cited by 115 · see citing works
Li, X., & Noll, M. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06274.x · Cited by 105 · see citing works
Murtha, M., Tokcaer-Keskin, Z., Tang, Z., Strino, F., Chen, X., Wang, Y., Xi, X., Basilico, C., Brown, S. M., Bonneau, R., et al. (2014) · Nature Methods · doi:10.1038/nmeth.2885 · Cited by 102 · see citing works
Characterization of Enhancer Function from Genome-Wide Analyses
Maston, G. A., Landt, S. G., Snyder, M. P., & Green, M. R. (2012) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-090711-163723 · Cited by 97 · see citing works
Function-based identification of mammalian enhancers using site-specific integration
Dickel, D. E., Zhu, Y., Nord, A. S., Wylie, J. N., Akiyama, J. A., Afzal, V., Plajzer-Frick, I., Kirkpatrick, A. M., Göttgens, B., Bruneau, B. G., et al. (2014) · Nature Methods · doi:10.1038/nmeth.2886 · Cited by 81 · see citing works
Self-citationImproved regulatory element prediction based on tissue-specific local epigenomic signatures
He, Y., Gorkin, D. U., Dickel, D. E., Nery, J. R., Castanon, R., Lee, A. Y., Shen, Y., Visel, A., Pennacchio, L. A., Ren, B., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1618353114 · Cited by 70 · see citing works
Self-citationHighly parallel assays of tissue-specific enhancers in whole Drosophila embryos
Gisselbrecht, S. S., Barrera, L. A., Porsch, M., Aboukhalil, A., Estep, P. W., Vedenko, A., Palagi, A., Kim, Y., Zhu, X., Busser, B. W., et al. (2013) · Nature Methods · doi:10.1038/nmeth.2558 · Cited by 62 · see citing works
Lu, Y., Qu, W., Shan, G., & Zhang, C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0130622 · Cited by 51 · see citing works
Xenobiotic metabolizing enzymes of rat liver nonparenchymal cells
Lafranconi, W. M., Glatt, H. R., & Oesch, F. (1986) · Toxicology and Applied Pharmacology · doi:10.1016/0041-008x(86)90255-3 · Cited by 25 · see citing works
Anomalous Attachment of Mitral Valve Causing Subaortic Atresia
Jue, K. L., & Edwards, J. E. (1967) · Circulation · doi:10.1161/01.cir.35.5.928 · Cited by 21 · see citing works
Seventh Dame Rosalind Paget Memorial Lecture: "Caring for tomorrow".
Poole, A. A. (1987) · PubMed · Cited by 9 · see citing works
Flagged first, then by citations
3 of the 89 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- [56]Ernst J. and Kellis M, ChromHMM: automating chromatin-state discovery and characterization. Nature Methods, 2012. 9(3): p. 215– 216. 22373907 PMC3577932
Cited by
Sorted by citations
Expanded encyclopaedias of DNA elements in the human and mouse genomes
The ENCODE Project Consortium, Abascal, F., Acosta, R., Addleman, N. J., Adrian, J., Afzal, V., Ai, R., Aken, B., Akiyama, J. A., Jammal, O. A., et al. (2020) · Nature · doi:10.1038/s41586-020-2493-4 · Cited by 2,378 · see citing works
Self-citationAn atlas of dynamic chromatin landscapes in mouse fetal development
Gorkin, D. U., Barozzi, I., Zhao, Y., Zhang, Y., Huang, H., Lee, A. Y., Li, B., Chiou, J., Wildberg, A., Ding, B., et al. (2020) · Nature · doi:10.1038/s41586-020-2093-3 · Cited by 364 · see citing works
Self-citationAn integrative ENCODE resource for cancer genomics
Zhang, J., Lee, D., Dhiman, V., Jiang, P., Xu, J., McGillivray, P., Yang, H., Liu, J., Meyerson, W., Clarke, D., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-14743-w · Cited by 172 · see citing works
Self-citationKNN Classification with One-step Computation
Zhang, S., & Li, J. (2021) · IEEE Transactions on Knowledge and Data Engineering · doi:10.1109/tkde.2021.3119140 · Cited by 118 · see citing works
Recycling of modified H2A-H2B provides short-term memory of chromatin states
Flury, V., Reverón-Gómez, N., Alcaraz, N., Stewart-Morgan, K. R., Wenger, A., Klose, R. J., & Groth, A. (2023) · Cell · doi:10.1016/j.cell.2023.01.007 · Cited by 97 · 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
Single-cell omics: experimental workflow, data analyses and applications
Sun, F., Li, H., Sun, D., Fu, S., Gu, L., Shao, X., Wang, Q., Dong, X., Duan, B., Xing, F., et al. (2024) · Science China Life Sciences · doi:10.1007/s11427-023-2561-0 · Cited by 81 · see citing works
The EN-TEx resource of multi-tissue personal epigenomes & variant-impact models
Rozowsky, J. S., Gao, J., Borsari, B., Yang, Y., Galeev, T. R., Gürsoy, G., Epstein, C. B., Xiong, K., Xu, J., Li, T., et al. (2023) · Cell · doi:10.1016/j.cell.2023.02.018 · Cited by 77 · see citing works
Self-citationZhang, L., Zhang, J., & Nie, Q. H. (2022) · Science Advances · doi:10.1126/sciadv.abl7393 · Cited by 74 · see citing works
Centers for Mendelian Genomics: A decade of facilitating gene discovery
Baxter, S. M., Posey, J. E., Lake, N. J., Sobreira, N. L. D. M., Chong, J. X., Buyske, S. G., Blue, E., Chadwick, L. H., Coban‐Akdemir, Z., Doheny, K. F., et al. (2022) · Genetics in Medicine · doi:10.1016/j.gim.2021.12.005 · Cited by 72 · see citing works
Self-citationSTARRPeaker: uniform processing and accurate identification of STARR-seq active regions
Lee, D., Shi, M., Moran, J. R., Wall, M., Zhang, J., Liu, J. J., Fitzgerald, D., Kyono, Y., Ma, L., White, K. P., et al. (2020) · Genome biology · doi:10.1186/s13059-020-02194-x · Cited by 59 · see citing works
Self-citationTHRONE: A New Approach for Accurate Prediction of Human RNA N7-Methylguanosine Sites
Shoombuatong, W., Basith, S., Pitti, T., Lee, G., & Manavalan, B. (2022) · Journal of Molecular Biology · doi:10.1016/j.jmb.2022.167549 · Cited by 58 · see citing works
Machine Learning in Epigenomics: Insights into Cancer Biology and Medicine
Arslan, E., Schulz, J., & Rai, K. (2021) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2021.188588 · Cited by 47 · see citing works
Extrusion fountains are hallmarks of chromosome organization emerging upon zygotic genome activation
Galitsyna, A. A., Ulianov, S. V., Bazarevich, M., Bykov, N. S., Veil, M., Gao, M., Perevoschikova, K., Gelfand, M. S., Razin, S. V., Mirny, L. A., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-69105-9 · Cited by 40 · see citing works
Predicting transfer RNA gene activity from sequence and genome contextPreprint
Thornlow, B. P., Armstrong, J. C., Holmes, A., Howard, J. M., Corbett-Detig, R. B., & Lowe, T. M. (2019) · Genome Research · doi:10.1101/gr.256164.119 · Cited by 40 · see citing works
Zhang, Z., Feng, F., Qiu, Y., & Liu, J. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad436 · Cited by 37 · see citing works
Synthetic reversed sequences reveal default genomic states
Camellato, B. R., Brosh, R., Ashe, H. J., Maurano, M. T., & Boeke, J. D. (2024) · Nature · doi:10.1038/s41586-024-07128-2 · Cited by 35 · see citing works
An overview of artificial intelligence in the field of genomics
Maqsood, K., Hagras, H., & Zabet, N. R. (2024) · Discover Artificial Intelligence · doi:10.1007/s44163-024-00103-w · Cited by 34 · see citing works
Complex regulatory networks influence pluripotent cell state transitions in human iPSCs
Arthur, T. D., Nguyen, J., D’Antonio‐Chronowska, A., Matsui, H., da Silva, N. S., Joshua, I. N., Aguiar, L. R., Arias, A. D., Benaglio, P., Berggren, W. T., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-45506-6 · Cited by 30 · see citing works
Chromatin remodeller CHD7 is required for GABAergic neuron development by promoting PAQR3 expression
Jamadagni, P., Breuer, M., Schmeißer, K., Cardinal, T., Kassa, B., Parker, J. A., Pilon, N., Samarut, É., & Patten, S. A. (2021) · EMBO Reports · doi:10.15252/embr.202050958 · Cited by 29 · see citing works
Information content differentiates enhancers from silencers in mouse photoreceptors
Friedman, R. Z., Granas, D. M., Myers, C. A., Corbo, J. C., Cohen, B. A., & White, M. A. (2021) · eLife · doi:10.7554/elife.67403 · Cited by 28 · see citing works
Wolfe, J. C., Mikheeva, L. A., Hagras, H., & Zabet, N. R. (2021) · Genome biology · doi:10.1186/s13059-021-02532-7 · Cited by 27 · see citing works
Functional maps of a genomic locus reveal confinement of an enhancer by its target gene
Eder, M., Moene, C. J. I., Dauban, L., Magnitov, M. D., Drayton, J. A., de Haas, M., Leemans, C., Verkuilen, M., de Wit, E., Hansen, A. S., et al. (2025) · Science · doi:10.1126/science.ads6552 · Cited by 27 · see citing works
Aging and pathological aging signatures of the brain: through the focusing lens of SIRT6
Stein, D., Mizrahi, A., Golova, A., Saretzky, A., García-Venzor, A., Slobodnik, Z., Kaluski, S., Einav, M., Khrameeva, E. E., & Toiber, D. (2021) · Aging · doi:10.18632/aging.202755 · Cited by 24 · see citing works
ZBTB12 is a molecular barrier to dedifferentiation in human pluripotent stem cells
Han, D., Liu, G., Oh, Y., Oh, S., Yang, S., Mandjikian, L., Rani, N., Almeida, M. C., Kosik, K. S., & Jang, J. (2023) · Nature Communications · doi:10.1038/s41467-023-36178-9 · Cited by 21 · see citing works
RicENN: Prediction of Rice Enhancers with Neural Network Based on DNA Sequences
Gao, Y., Chen, Y., Feng, H., Zhang, Y., & Yue, Z. (2022) · Interdisciplinary Sciences Computational Life Sciences · doi:10.1007/s12539-022-00503-5 · Cited by 21 · see citing works
Molecular basis of FAAH-OUT -associated human pain insensitivity
Mikaeili, H., Habib, A. M., Yeung, C., Santana‐Varela, S., Luiz, A. P., Panteleeva, K., Zuberi, S. R., Athanasiou‐Fragkouli, A., Houlden, H., Wood, J. N., et al. (2023) · Brain · doi:10.1093/brain/awad098 · Cited by 20 · see citing works
Review and Evaluate the Bioinformatics Analysis Strategies of ATAC-seq and CUT&Tag Data
Cheng, S., Miao, B., Li, T., Zhao, G., & Zhang, B. (2024) · Genomics Proteomics & Bioinformatics · doi:10.1093/gpbjnl/qzae054 · Cited by 20 · see citing works
Ni, P., Moe, J., & Su, Z. (2022) · BMC Biology · doi:10.1186/s12915-022-01426-9 · Cited by 17 · see citing works
Emerging insights into enhancer biology and function
Arnold, M., & Stengel, K. R. (2023) · Transcription · doi:10.1080/21541264.2023.2222032 · Cited by 18 · see citing works
Zhang, T., Flores, M. A., & Huang, Y. (2021) · Analytical Biochemistry · doi:10.1016/j.ab.2021.114120 · Cited by 18 · see citing works
Uncovering the mesendoderm gene regulatory network through multi-omic data integration
Jansen, C. S., Paraiso, K. D., Zhou, J. J., Blitz, I. L., Fish, M. B., Charney, R. M., Cho, J. S., Yasuoka, Y., Sudou, N., Bright, A. R., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110364 · Cited by 18 · see citing works
Self-supervised Learning for DNA sequences with circular dilated convolutional networks
Cheng, L., Yu, T., Khalitov, R., & Yang, Z. (2024) · Neural Networks · doi:10.1016/j.neunet.2023.12.002 · Cited by 12 · see citing works
Chen, Z., Zhang, J., Liu, J. J., Dai, Y. Q., Lee, D., Min, M. R., Xu, M., & Gerstein, M. (2021) · Bioinformatics · doi:10.1093/bioinformatics/btab283 · Cited by 12 · see citing works
Self-citationReFeaFi: Genome-wide prediction of regulatory elements driving transcription initiation
Umarov, R., Li, Y., Arakawa, T., Takizawa, S., Gao, X., & Arner, E. (2021) · bioRxiv · doi:10.1371/journal.pcbi.1009376 · Cited by 9 · see citing works
The homeodomain of Oct4 is a dimeric binder of methylated CpG elements
Tan, D. S., Cheung, S. L., Gao, Y., Weinbuch, M., Hu, H., Shi, L., Ti, S.-C., Hutchins, A. P., Cojocaru, V., & Jauch, R. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac1262 · Cited by 11 · see citing works
STARRPeaker: Uniform processing and accurate identification of STARR-seq active regionsPreprint
Lee, D., Shi, M., Moran, J., Wall, M., Zhang, J., Liu, J. J., Fitzgerald, D., Kyono, Y., Ma, L., White, K. P., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/694869 · Cited by 11 · see citing works
Self-citationDEK–nucleosome structure shows DEK modulates H3K27me3 and stem cell fate
Shen, Y., Liu, Y., Guo, M., Mao, S., Chen, R., Wang, M., Li, Z., Li, Y., Chen, W., Chen, F., et al. (2025) · Nature Structural & Molecular Biology · doi:10.1038/s41594-025-01559-9 · Cited by 10 · see citing works
Identification and prediction of developmental enhancers in sea urchin embryos
Arenas‐Mena, C., Miljovska, S., Rice, E. J., Gurges, J., Shashikant, T., Wang, Z., Ercan, S., & Danko, C. G. (2021) · BMC Genomics · doi:10.1186/s12864-021-07936-0 · Cited by 10 · see citing works
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 6 · see citing works
Towards Highly-Efficient k-Nearest Neighbor Algorithm for Big Data Classification
Abdalla, H. I., & Amer, A. A. (2022) · International Conference on Networking, Information Systems & Security (NISS) · doi:10.1109/niss55057.2022.10085013 · Cited by 9 · see citing works
Recapitulation of patient-specific 3D chromatin conformation using machine learning
Xu, D., Forbes, A. N., Cohen, S. M., Palladino, A. C., Karadimitriou, T., & Khurana, E. (2023) · Cell Reports Methods · doi:10.1016/j.crmeth.2023.100578 · Cited by 11 · see citing works
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 · see citing works
Identification, Design, and Application of Noncoding Cis-Regulatory Elements
Xu, L., & Liu, Y. (2024) · Biomolecules · doi:10.3390/biom14080945 · Cited by 9 · see citing works
Super-enhancer landscape rewiring in cancer: The epigenetic control at distal sites
Giorgio, E. D., Benetti, R., Kerschbamer, E., Xodo, L. E., & Brancolini, C. (2023) · International review of cytology · doi:10.1016/bs.ircmb.2023.03.013 · Cited by 8 · see citing works
Ali, M. M., Itoh, Y., Badji, A. M. P., Gallant, S., Tsirigoti, C., Bai, Y., Filipek‐Górniok, B., Miyazawa, K., Heldin, C., & Moustakas, A. (2026) · Cell Death and Disease · doi:10.1038/s41419-026-08435-4 · Cited by 7 · see citing works
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 7 · see citing works
YAP controls cell migration and invasion through a Rho-GTPase switchPreprint
Shah, S. R., Ren, C., Tippens, N. D., Park, J., Mohyeldin, A., Wang, S., Vela, G., Martínez-Gutiérrez, J. C., Margolis, S. S., Schmidt, S., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/602052 · Cited by 7 · see citing works
Abnizova, I., Stapel, C., Boekhorst, R. T., Lee, J. T. H., & Hemberg, M. (2024) · BMC Biology · doi:10.1186/s12915-024-01869-2 · Cited by 6 · see citing works
Self-distillation improves self-supervised learning for DNA sequence inference
Yu, T., Cheng, L., Khalitov, R., Olsson, E. B., & Yang, Z. (2024) · Neural Networks · doi:10.1016/j.neunet.2024.106978 · Cited by 6 · see citing works
Patel, Z. M., & Hughes, T. (2021) · Genome Biology · doi:10.1186/s13059-021-02503-y · Cited by 6 · see citing works
Cis-regulatory atlas of primary human CD4+ T cells
Stefan, K., & Barski, A. (2023) · BMC Genomics · doi:10.1186/s12864-023-09288-3 · Cited by 6 · see citing works
ChIP-GSM: Inferring active transcription factor modules to predict functional regulatory elements
Chen, X., Neuwald, A. F., Hilakivi-Clarke, L. A., Clarke, R. C., & Xuan, J. (2021) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1009203 · Cited by 6 · see citing works
AthEDL: Identifying Enhancers in Arabidopsis thaliana Using an Attention-based Deep Learning Method
Chen, Y., Gao, Y., Zhou, H., Zuo, Y., Zhang, Y., & Yue, Z. (2021) · Current Bioinformatics · doi:10.2174/1574893616666211123094301 · Cited by 5 · see citing works
Resolving a Systematic Error in STARR-seq for Quantitative Enhancer Activity MappingPreprint
Niu, L., Wan, J., Sun, J., Huang, Y., He, N., Li, L., & Hou, C. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.20.346908 · Cited by 3 · see citing works
Pig-eRNAdb: a comprehensive enhancer and eRNA dataset of pigs
Wang, Y., Jin, W., Pan, X., Liao, W., Shen, Q., Cai, J., Gong, W., Tian, Y., Xu, D., Li, Y., et al. (2024) · Scientific Data · doi:10.1038/s41597-024-02960-7 · Cited by 4 · see citing works
A map of enhancer regions in primary human neural progenitor cells using capture STARR-seqPreprint
Gaynor-Gillett, S. C., Cheng, L., Shi, M., Liu, J. J., Wang, G., Spector, M., Guo, Q., Qi, L., Flaherty, M., Wall, M., et al. (2025) · Genome Research · doi:10.1101/gr.279584.124 · Cited by 4 · see citing works
Self-citationMinimizing far-extending chromatin perturbation in genome editing preserves stem cell identity
Zhu, M., Yuan, J., Meng, Q., Yu, J., Xu, X., Xu, M., Ren, X., Hu, Y., Wei, G., Jia, Z., et al. (2026) · Cell stem cell · doi:10.1016/j.stem.2026.01.015 · Cited by 3 · see citing works
Transcriptional competence defines the heterochromatin nucleating potential of isolated MSR units
Lo, Y.-H., Shukeir, N., Erikson, G. A., Edupuganti, R. R., Ching, R. W., Puri, D., Jerabek, L., Shiekhattar, R., & Jenuwein, T. (2026) · Nature Communications · doi:10.1038/s41467-026-70991-2 · Cited by 3 · see citing works
Yang, D., Zhang, T., Yang, Y., Zhang, D., Zhou, Z., Wang, N., Fan, J., Xu, C., Fang, Y., Kang, L., et al. (2025) · Interdisciplinary medicine · doi:10.1002/inmd.70053 · Cited by 3 · see citing works
Weinstock, L. D., Schambach, J., Lara, A., Kunstadt, C., Lee, D. E., Koning, E. R., Morrell, W., Mays, W., Davis, W., IV, & Krishnakumar, R. (2026) · iScience · doi:10.1016/j.isci.2026.117280 · Cited by 3 · see citing works
Computational methods for identifying enhancer‐promoter interactions
Gong, H., Chen, Z., Tang, Y.-X., Li, M.-H., Zhang, S., Zhang, X.-T., & Chen, Y. (2023) · Quant. Biol. · doi:10.15302/j-qb-022-0322 · Cited by 3 · see citing works
Yong, F., Yan, M., Zhang, L., Ji, W., Zhao, S., & Gao, Y. (2023) · Veterinary Sciences · doi:10.3390/vetsci10070452 · Cited by 3 · see citing works
The Impact of Data Normalization on KNN Rendering
Abdalla, H. I., & Altaf, A. (2023) · Lecture notes on data engineering and communications technologies · doi:10.1007/978-3-031-43247-7_16 · Cited by 3 · see citing works
Identification and Validation of eRNA as a Prognostic Indicator for Cervical Cancer
Huang, L., Zhang, J., Songyang, Z., & Xiong, Y. (2024) · Biology · doi:10.3390/biology13040227 · Cited by 3 · see citing works
Dincer, T. U., & Ernst, J. (2025) · Genome biology · doi:10.1186/s13059-025-03579-6 · Cited by 3 · see citing works
Xu, D., Forbes, A. N., Cohen, S. M., Palladino, A. C., Karadimitriou, T., & Khurana, E. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.16.468857 · Cited by 3 · see citing works
PorcineAI-Enhancer: Prediction of Pig Enhancer Sequences Using Convolutional Neural Networks
Wang, J., Zhang, H., Chen, N., Zeng, T., Ai, X., & Wu, K. (2023) · Animals · doi:10.3390/ani13182935 · Cited by 2 · see citing works
Harmanci, A. O., Harmanci, A. O., Swaminathan, J., & Gopalakrishnan, V. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz702 · Cited by 2 · see citing works
Functional characteristics and computational model of abundant hyperactive loci in the human genomePreprint
Hudaiberdiev, S., & Ovcharenko, I. (2024) · eLife · doi:10.7554/elife.95170 · Cited by 2 · see citing works
Yuan, S., Ni, P., & Su, Z. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.07.592879 · Cited by 2 · see citing works
Mancheno-Ferris, A., Immarigeon, C., Rivero, A., Depierre, D., Schickele, N., Fosseprez, O., Chanard, N., Aughey, G., Lhoumaud, P., Anglade, J., et al. (2023) · iScience · doi:10.1016/j.isci.2023.108624 · Cited by 1 · see citing works
Liu, X., Gillis, N., Jiang, C., McCofie, A., Shaw, T. I., Tan, A. C., Zhao, B., Wan, L., Duckett, D. R., & Teng, M. (2024) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1011873 · Cited by 1 · see citing works
Paul, N. B., Wolber, J. C., Sahrhage, M., Beißbarth, T., & Haubrock, M. (2025) · Bioinformatics · doi:10.1093/bioinformatics/btaf033 · Cited by 1 · see citing works
Functional Validation of Noncoding Variants Associated With Nonsyndromic Orofacial Cleft
Zhu, S.-Y., Tao, H., Cornell, R. A., & Liu, H. (2025) · Human Mutation · doi:10.1155/humu/6824122 · Cited by 1 · see citing works
Le, D. J., Hafner, A., Venkatesh, A. R., Udomlumleart, T., Gaddam, S., Novačić, A., Wang, K., & Boettiger, A. N. (2026) · Cell Genomics · doi:10.1016/j.xgen.2026.101331 · Cited by 1 · see citing works
Predictive design of tissue-specific mammalian enhancers that function in the mouse embryo
Chen, S., Loubière, V., Hollingsworth, E. W., Ken, M., Mandlburger, N., Jacinto, S. H., Dizehchi, A., Schreiber, J. M., Kvon, E. Z., & Stark, A. (2026) · Nature Genetics · doi:10.1038/s41588-026-02729-1 · Cited by 2 · see citing works
A sparse and wide neural network model for DNA sequences
Yu, T., Cheng, L., Khalitov, R., & Yang, Z. (2024) · Neural Networks · doi:10.1016/j.neunet.2024.107040 · Cited by 1 · see citing works
Functional characteristics and computational model of abundant hyperactive loci in the human genome
Hudaiberdiev, S., & Ovcharenko, I. (2024) · eLife · doi:10.7554/elife.95170.3 · Cited by 1 · see citing works
Induce Pluripotency via Specific distal enhancer-promoter associationsPreprint
Zhu, X., Huang, L., Li, D., Luo, J., Huang, Q., Wang, X., & Zhang, Y. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.06.09.447809 · Cited by 1 · see citing works
Validation of Enhancer Regions in Primary Human Neural Progenitor Cells using Capture STARR-seqPreprint
Gaynor-Gillett, S. C., Cheng, L., Shi, M., Liu, J. J., Wang, G., Spector, M., Flaherty, M., Wall, M., Hwang, A., Gu, M., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.14.585066 · Cited by 1 · see citing works
Self-citationFunctional characteristics and computational model of abundant hyperactive loci in the human genomePreprint
Hudaiberdiev, S., & Ovcharenko, I. (2024) · eLife · doi:10.7554/elife.95170.2 · Cited by 1 · see citing works
Inhibition of cytosolic DNA sensing and transposon activity safeguards pluripotencyPreprint
Garcia-Llagostera, F., Putman, A. L. K., Choromidis, A., Leeke, B. J., Stanik, K., Ramos, A., Moyon, B., Gil, J., Barr, A. R., & Percharde, M. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.26.645264 · Cited by 1 · see citing works
Effects of CTCF on the regulatory landscape of the mouse Sox2 locusPreprint
Eder, M., Moene, C. J. I., Kaagman, M., Braccioli, L., de Wit, E., & van Steensel, B. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.16.711995 · Cited by 1 · see citing works
Mancheno-Ferris, A., Immarigeon, C., Rivero, A., Depierre, D., Chanard, N., Fosseprez, O., Aughey, G., Lhoumaud, P., Anglade, J., Southall, T. D., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.03.522588
Prediction accuracy of regulatory elements from sequence varies by functional sequencing technique
Nowling, R. J., Njoya, K., Peters, J. G., & Riehle, M. M. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1182567
Identification of Cancer-specific Constituent Elements inside Super-enhancers (cSEAdb) v1Preprint
Liu, X., Gillis, N., Jiang, C., McCofie, A., Shaw, T. I., Tan, A.-C., Zhao, B., Wan, L., Duckett, D. R., & Teng, M. (2024) · doi:10.17504/protocols.io.kxygx38wzg8j/v1
Sequence characteristics and an accurate model of abundant hyperactive loci in the human genomePreprint
Hudaiberdiev, S., & Ovcharenko, I. (2024) · eLife · doi:10.7554/elife.95170.1
Self-Distillation Improves DNA Sequence InferencePreprint
Yu, T., Cheng, L., Khalitov, R., Olsson, E. B., & Yang, Z. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4862343
A Type-2 Fuzzy Logic-Based Explainable Artificial Intelligence for the Prediction of Enhancers
Maqsood, K., Hagras, H., & Zabet, N. R. (2024) · IEEE International Conference on Fuzzy Systems (FUZZ-IEEE) · doi:10.1109/fuzz-ieee60900.2024.10611999
Functional interrogation of candidate cis -regulatory elements at the LDLR locusPreprint
Leix, K., Serrano-Zayas, C., Graham, S. E., & Emmer, B. T. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.20.644385
scPPF: Predicting Promoter Fragments in scATAC-seq Based on Transcription Factor Motifs
Li, J., Li, H., Wang, F., Yuan, L., & Zhao, Y. (2025) · Current Bioinformatics · doi:10.2174/0115748936385361250710042542
Patel, Z. M., & Hughes, T. R. (2021) · Figshare · doi:10.6084/m9.figshare.16767622
Additional file 3 of Identification and prediction of developmental enhancers in sea urchin embryos
Arenas‐Mena, C., Miljovska, S., Rice, E. J., Gurges, J., Shashikant, T., Wang, Z., Ercan, S., & Danko, C. G. (2021) · Figshare · doi:10.6084/m9.figshare.16835059
Additional file 1 of Identification and prediction of developmental enhancers in sea urchin embryos
Arenas‐Mena, C., Miljovska, S., Rice, E. J., Gurges, J., Shashikant, T., Wang, Z., Ercan, S., & Danko, C. G. (2021) · Figshare · doi:10.6084/m9.figshare.16835053
Additional file 4 of Cis-regulatory atlas of primary human CD4+ T cells
Stefan, K., & Barski, A. (2024) · Figshare · doi:10.6084/m9.figshare.26588769
Additional file 5 of Cis-regulatory atlas of primary human CD4+ T cells
Stefan, K., & Barski, A. (2024) · Figshare · doi:10.6084/m9.figshare.26588772
Additional file 5 of Identification and prediction of developmental enhancers in sea urchin embryos
Arenas‐Mena, C., Miljovska, S., Rice, E. J., Gurges, J., Shashikant, T., Wang, Z., Ercan, S., & Danko, C. G. (2021) · Figshare · doi:10.6084/m9.figshare.16835065
Additional file 6 of Identification and prediction of developmental enhancers in sea urchin embryos
Arenas‐Mena, C., Miljovska, S., Rice, E. J., Gurges, J., Shashikant, T., Wang, Z., Ercan, S., & Danko, C. G. (2021) · Figshare · doi:10.6084/m9.figshare.16835068
Patel, Z. M., & Hughes, T. R. (2021) · Figshare · doi:10.6084/m9.figshare.16767610
- Authors
- Sethi, A., Gu, M., Gumusgoz, E., Chan, L., Yan, K.-K., Rozowsky, J., Barozzi, I., Afzal, V., Akiyama, J. A., Plajzer-Frick, I., Yan, C., Novak, C. S., Kato, M., Garvin, T. H., Pham, Q., Harrington, A., Mannion, B. J., Lee, E. A., Fukuda-Yuzawa, Y., Visel, A., Dickel, D. E., Yip, K. Y., Sutton, R., Pennacchio, L. A., & Gerstein, M.
- Affiliations
- Yale University (US)
- Chinese University of Hong Kong (HK)
- Lawrence Berkeley National Laboratory (US)
- Corresponding author
- Gerstein, Mark
- ORCID
- Sethi, Anurag
- Gu, Mengting
- Gumusgoz, Emrah
- Chan, Landon
- Yan, Koon-Kiu
- Rozowsky, Joel
- Barozzi, Iros
- Afzal, Veena
- Akiyama, Jennifer A.
- Yan, Chengfei
- Kato, Momoe
- Garvin, Tyler H.
- Harrington, Anne
- Mannion, Brandon J.
- Lee, Elizabeth A.
- Visel, Axel
- Dickel, Diane E.
- Yip, Kevin Y.
- Sutton, Richard
- Pennacchio, Len A.
- Gerstein, Mark
- Venue
- Nature Methods
- Published
- 2020-07-29
- Volume
- 17
- Issue
- 8
- Pages
- 807-814
- ISSN
- 1548-7091 (ISSN-L)
- 1548-7105
- PMC
- PMC8073243
- OpenAlex
- W3046699218
- Cited by
- 109
- References
- 89
- Citations by year
- 2026: 14 · 2025: 11 · 2024: 23 · 2023: 18 · 2022: 10 · 2021: 24 · 2020: 6 · 2019: 3
- FWCI
- 4.65
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- Nature Methods (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- U.S. Department of Health & Human Services | National Institutes of Health (HG009446-01)
- U.S. Department of Health & Human Services | NIH | National Heart, Lung, and Blood Institute (R24HL123879)
- U.S. Department of Health & Human Services | NIH | National Human Genome Research Institute (R01HG003988, U54HG006997, UM1HG009421)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- enhancer prediction, STARR-seq, epigenetic features, supervised learning, interspecies transmission, transcription factor binding, promoter identification, Drosophila, non-coding elements
- MeSH terms
- Animals, Cell Line, Drosophila, Histones, Humans, Mice, Transgenic, Pattern Recognition, Automated, Reproducibility of Results, Epigenesis, Genetic, Mice
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