Refined DNase-seq protocol and data analysis reveals intrinsic bias in transcription factor footprint identification
Open accessAbstract
Sequencing of DNase I hypersensitive sites (DNase-seq) is a powerful technique for identifying cis-regulatory elements across the genome. We studied the key experimental parameters to optimize performance of DNase-seq. Sequencing short fragments of 50-100 base pairs (bp) that accumulate in long internucleosome linker regions was more efficient for identifying transcription factor binding sites compared to sequencing longer fragments. We also assessed the potential of DNase-seq to predict transcription factor occupancy via generation of nucleotide-resolution transcription factor footprints. In modeling the sequence-specific DNase I cutting bias, we found a strong effect that varied over more than two orders of magnitude. This indicates that the nucleotide-resolution cleavage patterns at many transcription factor binding sites are derived from intrinsic DNase I cleavage bias rather than from specific protein-DNA interactions. In contrast, quantitative comparison of DNase I hypersensitivity between states can predict transcription factor occupancy associated with particular biological perturbations.
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?
Adding a methyl group to cytosine can affect local DNA shape, as shown by altered DNase I digestion rate and patterns.
“Adding a methyl group to the cytosine could affect the local DNA shape, as evidenced by the altered DNase I digestion rate and patterns70,71.”
From Transcription factors as readers and effectors of DNA methylation (2016) · cites this paper as [70]
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
Model-based Analysis of ChIP-Seq (MACS)
Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C., Myers, R. M., Brown, M., Li, W., et al. (2008) · Genome Biology · doi:10.1186/gb-2008-9-9-r137 · Cited by 18,386 · see citing works
Self-citationAn 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
Systematic Localization of Common Disease-Associated Variation in Regulatory DNA
Maurano, M. T., Humbert, R., Rynes, E., Thurman, R. E., Haugen, E., Wang, H., Reynolds, A. P., Sandstrom, R., Qu, H., Brody, J., et al. (2012) · Science · doi:10.1126/science.1222794 · Cited by 3,716 · 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
TRANSFAC(R) and its module TRANSCompel(R): transcriptional gene regulation in eukaryotes
Matys, V. (2005) · Nucleic Acids Research · doi:10.1093/nar/gkj143 · Cited by 2,142 · see citing works
DNAase footprinting a simple method for the detection of protein-DNA binding specificity
Galas, D. J., & Schmitz, A. (1978) · Nucleic Acids Research · doi:10.1093/nar/5.9.3157 · Cited by 2,109 · see citing works
Chromatin accessibility pre-determines glucocorticoid receptor binding patterns
John, S., Sabo, P. J., Thurman, R. E., Sung, M.-H., Biddie, S. C., Johnson, T. A., Hager, G. L., & Stamatoyannopoulos, J. A. (2011) · Nature Genetics · doi:10.1038/ng.759 · Cited by 954 · see citing works
An expansive human regulatory lexicon encoded in transcription factor footprints
Neph, S. J., Vierstra, J. D., Stergachis, A. B., Reynolds, A. P., Haugen, E., Vernot, B., Thurman, R. E., John, S., Sandstrom, R. S., Johnson, A., et al. (2012) · Nature · doi:10.1038/nature11212 · Cited by 746 · see citing works
New insights into nucleosome and chromatin structure: an ordered state or a disordered affair?
Luger, K., Dechassa, M. L., & Tremethick, D. J. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3382 · Cited by 738 · see citing works
DNase I sensitivity QTLs are a major determinant of human expression variation
Degner, J. F., Pai, A. A., Piqué-Regi, R., Veyrieras, J., Gaffney, D. J., Pickrell, J. K., Leon, S. D., Michelini, K., Lewellen, N., Crawford, G. E., et al. (2012) · Nature · doi:10.1038/nature10808 · Cited by 633 · see citing works
Song, L., Zhang, Z., Grasfeder, L. L., Boyle, A. P., Giresi, P. G., Lee, B.-K., Sheffield, N. C., Gräf, S., Huss, M., Keefe, D., et al. (2011) · Genome Research · doi:10.1101/gr.121541.111 · Cited by 500 · see citing works
Nucleosome dynamics define transcriptional enhancers
He, H. H., Meyer, C. A., Shin, H., Bailey, S. T., Wei, G., Wang, Q., Zhang, Y., Xu, K., Ni, M., Lupien, M., et al. (2010) · Nature Genetics · doi:10.1038/ng.545 · Cited by 476 · see citing works
Self-citationVoss, T. C., Schiltz, R. L., Sung, M.-H., Yen, P. M., Stamatoyannopoulos, J. A., Biddie, S. C., Johnson, T. A., Miranda, T. B., John, S., & Hager, G. L. (2011) · Cell · doi:10.1016/j.cell.2011.07.006 · Cited by 307 · see citing works
High-resolution genome-wide in vivo footprinting of diverse transcription factors in human cellsPreprint
Boyle, A. P., Song, L., Lee, B., London, D., Keefe, D., Birney, E., Iyer, V. R., Crawford, G. E., & Furey, T. S. (2010) · Genome Research · doi:10.1101/gr.112656.110 · Cited by 305 · see citing works
Controls of Nucleosome Positioning in the Human Genome
Gaffney, D. J., McVicker, G., Pai, A. A., Fondufe‐Mittendorf, Y. N., Lewellen, N., Michelini, K., Widom, J., Gilad, Y., & Pritchard, J. K. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003036 · Cited by 296 · see citing works
Differential DNase I hypersensitivity reveals factor-dependent chromatin dynamicsPreprint
He, H.-S. H., Meyer, C. A., Chen, M., Jordan, V. C., Brown, M. A., & Liu, X. S. (2012) · Genome Research · doi:10.1101/gr.133280.111 · Cited by 191 · see citing works
Self-citationCampbell, V. W., & Jackson, D. A. (1980) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)85765-4 · Cited by 168 · see citing works
Probing DNA shape and methylation state on a genomic scale with DNase I
Lazarovici, A., Zhou, T., Shafer, A., Dantas Machado, A. C., Riley, T. R., Sandstrom, R., Sabo, P. J., Lu, Y., Rohs, R., Stamatoyannopoulos, J. A., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1216822110 · Cited by 162 · see citing works
Identifying Positioned Nucleosomes with Epigenetic Marks in Human from ChIP-Seq
Zhang, Y., Shin, H., Song, J. S., Lei, Y., & Liu, X. S. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-537 · Cited by 138 · see citing works
Self-citationLing, G., Sugathan, A., Mazor, T., Fraenkel, E., & Waxman, D. J. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00601-10 · Cited by 105 · see citing works
Tewari, A. K., Yardımcı, G. G., Shibata, Y., Sheffield, N. C., Song, L., Taylor, B. S., Georgiev, S. G., Coetzee, G. A., Ohler, U., Furey, T. S., et al. (2012) · Genome biology · doi:10.1186/gb-2012-13-10-r88 · Cited by 76 · see citing works
Rapid genome-scale mapping of chromatin accessibility in tissue
Grøntved, L., Bandle, R., John, S., Baek, S., Chung, H., Liu, Y., Aguilera, G., Oberholtzer, J. C., Hager, G. L., & Levens, D. (2012) · Epigenetics & Chromatin · doi:10.1186/1756-8935-5-10 · Cited by 31 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Chromatin accessibility and the regulatory epigenome
Klemm, S. L., Shipony, Z., & Greenleaf, W. J. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-018-0089-8 · Cited by 1,793 · see citing works
Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads
Jiang, H., Lei, R., Ding, S., & Zhu, S. (2014) · BMC Bioinformatics · doi:10.1186/1471-2105-15-182 · Cited by 1,525 · see citing works
ArchR is a scalable software package for integrative single-cell chromatin accessibility analysis
Granja, J. M., Corces, M. R., Pierce, S. E., Bagdatli, S. T., Choudhry, H., Chang, H. Y., & Greenleaf, W. J. (2021) · Nature Genetics · doi:10.1038/s41588-021-00790-6 · Cited by 1,392 · see citing works
The chromatin accessibility landscape of primary human cancers
Corces, M. R., Granja, J. M., Shams, S., Louie, B. H., Seoane, J. A., Zhou, W., Silva, T. C., Groeneveld, C., Wong, C. K., Cho, S. W., et al. (2018) · Science · doi:10.1126/science.aav1898 · Cited by 1,230 · see citing works
Self-citationCistrome Data Browser: expanded datasets and new tools for gene regulatory analysis
Zheng, R., Wan, C., Mei, S., Qin, Q., Wu, Q., Sun, H., Chen, C.-H., Brown, M. A., Zhang, X., Meyer, C. A., et al. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky1094 · Cited by 909 · see citing works
Self-citationTranscription factors as readers and effectors of DNA methylation
Zhu, H., Wang, G., & Qian, J. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.83 · Cited by 649 · see citing works
Chromatin accessibility profiling by ATAC-seq
Grandi, F. C., Modi, H., Kampman, L., & Corces, M. R. (2022) · Nature Protocols · doi:10.1038/s41596-022-00692-9 · Cited by 557 · see citing works
Identification of transcription factor binding sites using ATAC-seq
Li, Z., Schulz, M. H., Look, T., Begemann, M., Zenke, M., & Costa, I. G. (2019) · Genome biology · doi:10.1186/s13059-019-1642-2 · Cited by 436 · see citing works
Chromatin accessibility: a window into the genome
Tsompana, M., & Buck, M. J. (2014) · Epigenetics & Chromatin · doi:10.1186/1756-8935-7-33 · Cited by 437 · see citing works
Sherwood, R. I., Hashimoto, T., O'Donnell, C. W., Lewis, S., Barkal, A. A., van Hoff, J. P., Karun, V., Jaakkola, T., & Gifford, D. K. (2014) · Nature Biotechnology · doi:10.1038/nbt.2798 · Cited by 416 · see citing works
Transcription factor–DNA binding: beyond binding site motifs
Inukai, S., Kock, K. H., & Bulyk, M. L. (2017) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2017.02.007 · Cited by 387 · see citing works
Nitta, K. R., Jolma, A., Yin, Y., Morgunova, E. Y., Kivioja, T., Akhtar, J., Hens, K., Toivonen, J., Deplancke, B., Furlong, E. E. M., et al. (2015) · eLife · doi:10.7554/elife.04837 · Cited by 358 · see citing works
Identifying and mitigating bias in next-generation sequencing methods for chromatin biology
Meyer, C. A., & Liu, X. S. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3788 · Cited by 329 · see citing works
Self-citation3D Chromatin Architecture of Large Plant Genomes Determined by Local A/B Compartments
Dong, P., Tu, X., Chu, P.-Y., Lü, P., Zhu, N., Grierson, D. S., Du, B., Li, P., & Zhong, S. (2017) · Molecular Plant · doi:10.1016/j.molp.2017.11.005 · Cited by 315 · see citing works
Combining ATAC-seq with nuclei sorting for discovery of cis-regulatory regions in plant genomes
Lu, Z., Hofmeister, B. T., Vollmers, C., DuBois, R. M., & Schmitz, R. J. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1179 · Cited by 319 · see citing works
Steroid Receptors Reprogram FoxA1 Occupancy through Dynamic Chromatin Transitions
Swinstead, E. E., Miranda, T. B., Paakinaho, V., Baek, S., Goldstein, I., Hawkins, M., Karpova, T. S., Ball, D., Mazza, D., Lavis, L. D., et al. (2016) · Cell · doi:10.1016/j.cell.2016.02.067 · Cited by 312 · see citing works
GTRD: a database on gene transcription regulation—2019 update
Yevshin, I., Sharipov, R., Kolmykov, S. K., Kondrakhin, Y. V., & Kolpakov, F. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky1128 · Cited by 257 · see citing works
Conservation of trans-acting circuitry during mammalian regulatory evolution
Stergachis, A. B., Neph, S., Sandstrom, R., Haugen, E., Reynolds, A. P., Zhang, M., Byron, R., Canfield, T., Stelhing-Sun, S., Lee, K., et al. (2014) · Nature · doi:10.1038/nature13972 · Cited by 212 · see citing works
Chromatin accessibility profiling methods
Minnoye, L., Marinov, G. K., Krausgruber, T., Pan, L., Marand, A. P., Secchia, S., Greenleaf, W. J., Furlong, E. E. M., Zhao, K., Schmitz, R. J., et al. (2021) · Nature Reviews Methods Primers · doi:10.1038/s43586-020-00008-9 · Cited by 206 · see citing works
Single-cell sequencing to multi-omics: technologies and applications
Wu, X., Yang, X., Dai, Y., Zhao, Z., Zhu, J., Guo, H., & Yang, R. (2024) · Biomarker Research · doi:10.1186/s40364-024-00643-4 · Cited by 195 · see citing works
Wang, K., & Chang, H. Y. (2018) · Circulation Research · doi:10.1161/circresaha.118.310998 · Cited by 173 · see citing works
DNase Footprint Signatures Are Dictated by Factor Dynamics and DNA Sequence
Sung, M., Guertin, M. J., Baek, S., & Hager, G. L. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.08.016 · Cited by 158 · see citing works
Epigenomic landscapes of retinal rods and cones
Mo, A., Luo, C., Davis, F. P., Mukamel, E. A., Henry, G. L., Nery, J. R., Urich, M. A., Picard, S., Lister, R., Eddy, S. R., et al. (2016) · eLife · doi:10.7554/elife.11613 · Cited by 158 · see citing works
Analysis of computational footprinting methods for DNase sequencing experiments
Gusmao, E. G., Allhoff, M., Zenke, M., & Costa, I. G. (2016) · Nature Methods · doi:10.1038/nmeth.3772 · Cited by 152 · see citing works
Beytebiere, J. R., Trott, A. J., Greenwell, B. J., Osborne, C. A., Vitet, H., Spence, J., Yoo, S. H., Chen, Z., Takahashi, J. S., Ghaffari, N., et al. (2019) · Genes & Development · doi:10.1101/gad.322198.118 · Cited by 151 · see citing works
Plant Enhancers: A Call for Discovery
Weber, B., Zicola, J., Oka, R., & Stam, M. E. (2016) · Trends in Plant Science · doi:10.1016/j.tplants.2016.07.013 · Cited by 140 · see citing works
3D Genome of macaque fetal brain reveals evolutionary innovations during primate corticogenesis
Luo, X., Liu, Y., Dang, D., Hu, T., Hou, Y., Meng, X., Zhang, F., Li, T., Wang, C., Li, M., et al. (2021) · Cell · doi:10.1016/j.cell.2021.01.001 · Cited by 137 · see citing works
Self-citationPampari, A., Shcherbina, A., Kvon, E. Z., Kosicki, M., Nair, S., Kundu, S., Kathiria, A. S., Risca, V. I., Kuningas, K., Alasoo, K., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.12.25.630221 · Cited by 161 · see citing works
Recent advances in ChIP-seq analysis: from quality management to whole-genome annotation
Nakato, R., & Shirahige, K. (2016) · Briefings in Bioinformatics · doi:10.1093/bib/bbw023 · Cited by 141 · see citing works
Grøntved, L., Waterfall, J. J., Kim, D. W., Baek, S., Sung, M., Zhao, L., Park, J. W., Nielsen, R., Walker, R. L., Zhu, Y. J., et al. (2015) · Nature Communications · doi:10.1038/ncomms8048 · Cited by 137 · see citing works
Sijacic, P., Bajic, M., McKinney, E. C., Meagher, R. B., & Deal, R. B. (2018) · The Plant Journal · doi:10.1111/tpj.13882 · Cited by 137 · see citing works
High-resolution digital profiling of the epigenome
Zentner, G. E., & Henikoff, S. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3798 · Cited by 125 · see citing works
Schmidt, F., Gasparoni, N., Gasparoni, G., Gianmoena, K., Cadenas, C., Polansky, J. K., Ebert, P., Nordström, K. J. V., Barann, M., Sinha, A. N., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1061 · Cited by 118 · see citing works
Evolving insights on how cytosine methylation affects protein-DNA binding
Dantas Machado, A. C., Zhou, T., Rao, S., Goel, P., Rastogi, C., Lazarovici, A., Bussemaker, H. J., & Rohs, R. (2015) · Briefings in Functional Genomics · doi:10.1093/bfgp/elu040 · Cited by 124 · see citing works
Mapping 3D genome architecture through in situ DNase Hi-C
Ramani, V., Cusanovich, D. A., Hause, R. J., Ma, W., Qiu, R., Deng, X., Blau, C. A., Distèche, C. M., Noble, W. S., Shendure, J., et al. (2016) · Nature Protocols · doi:10.1038/nprot.2016.126 · Cited by 112 · see citing works
Oyserman, B. O., Noguera, D. R., del Rio, T. G., Tringe, S. G., & McMahon, K. D. (2015) · The ISME Journal · doi:10.1038/ismej.2015.155 · Cited by 117 · see citing works
Bivariate Genomic Footprinting Detects Changes in Transcription Factor Activity
Baek, S., Goldstein, I., & Hager, G. L. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.05.003 · Cited by 105 · see citing works
Genomic methods in profiling DNA accessibility and factor localization
Klein, D. C., & Hainer, S. J. (2019) · Chromosome Research · doi:10.1007/s10577-019-09619-9 · Cited by 100 · see citing works
HMMRATAC: a Hidden Markov ModeleR for ATAC-seq
Tarbell, E., & Liu, T. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz533 · Cited by 102 · see citing works
Palmisano, I., Danzi, M., Hutson, T., Zhou, L.-M., Mclachlan, E., Serger, E., Shkura, K., Srivastava, P., Hervera, A., Neill, N. O., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0490-4 · Cited by 91 · see citing works
Imputation for transcription factor binding predictions based on deep learning
Qin, Q., & Feng, J. (2017) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005403 · Cited by 96 · see citing works
Calviello, A. K., Hirsekorn, A., Wurmus, R., Yusuf, D., & Ohler, U. (2019) · Genome biology · doi:10.1186/s13059-019-1654-y · Cited by 96 · see citing works
Transcriptional regulatory logic of the diurnal cycle in the mouse liver
Sobel, J., Krier, I., Andersin, T., Raghav, S. K., Canella, D., Gilardi, F., Kalantzi, A., Rey, G., Weger, B. D., Gachon, F., et al. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2001069 · Cited by 91 · see citing works
Vierstra, J. D., & Stamatoyannopoulos, J. A. (2016) · Nature Methods · doi:10.1038/nmeth.3768 · Cited by 93 · see citing works
Genome-wide epigenomic profiling for biomarker discovery
Dirks, R. A. M., Stunnenberg, H. G., & Marks, H. (2016) · Clinical Epigenetics · doi:10.1186/s13148-016-0284-4 · Cited by 90 · see citing works
Herdman, C., Mars, J.-C., Stefanovsky, V. Y., Tremblay, M. G., Sabourin‐Félix, M., Lindsay, H. A., Robinson, M. D., & Moss, T. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006899 · Cited by 89 · see citing works
Modeling cis-regulation with a compendium of genome-wide histone H3K27ac profilesPreprint
Wang, S., Zang, C., Xiao, T., Fan, J., Mei, S., Qin, Q., Wu, Q., Li, X., Xu, K., He, H. H., et al. (2016) · Genome Research · doi:10.1101/gr.201574.115 · Cited by 81 · see citing works
Self-citationChaitankar, V., Karakülah, G., Ratnapriya, R., Giuste, F., Brooks, M. J., & Swaroop, A. (2016) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2016.06.001 · Cited by 79 · see citing works
Dynamic chromatin technologies: from individual molecules to epigenomic regulation in cells
Cuvier, O., & Fierz, B. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.28 · Cited by 75 · see citing works
Genome-wide footprinting: ready for prime time?
Sung, M., Baek, S., & Hager, G. L. (2016) · Nature Methods · doi:10.1038/nmeth.3766 · Cited by 69 · see citing works
Molecular Architecture of Transcription Factor Hotspots in Early Adipogenesis
Siersbæk, R., Baek, S., Rabiee, A., Nielsen, R., Traynor, S., Clark, N., Sandelin, A., Jensen, O. N., Sung, M., Hager, G. L., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.04.043 · Cited by 65 · see citing works
miR-93 regulates Msk2-mediated chromatin remodelling in diabetic nephropathy
Badal, S. S., Wang, Y., Long, J., Corcoran, D. L., Chang, B. H., Truong, L. D., Kanwar, Y. S., Overbeek, P. A., & Danesh, F. R. (2016) · Nature Communications · doi:10.1038/ncomms12076 · Cited by 67 · see citing works
Mechanisms of X Chromosome Dosage Compensation
Ercan, S. (2014) · Journal of Genomics · doi:10.7150/jgen.10404 · Cited by 64 · see citing works
Multiscale footprints reveal the organization of cis-regulatory elements
Yan, H., Horlbeck, M. A., Zhang, R., Ma, S., Shrestha, R., Kartha, V. K., Duarte, F. M., Hock, C., Savage, R. E., Labade, A. S., et al. (2025) · Nature · doi:10.1038/s41586-024-08443-4 · Cited by 80 · see citing works
Yardımcı, G. G., Frank, C. L., Crawford, G. E., & Ohler, U. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku810 · Cited by 63 · see citing works
Gentsch, G. E., Spruce, T., Owens, N. D. L., & Smith, J. C. (2019) · Nature Communications · doi:10.1038/s41467-019-12263-w · Cited by 57 · see citing works
Srivastava, D., & Mahony, S. (2019) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2019.194443 · Cited by 52 · see citing works
Single cell transcriptomics: moving towards multi-omics
Song, Y., Xu, X., Wang, W., Tian, T., Zhu, Z., & Yang, C. J. (2019) · The Analyst · doi:10.1039/c8an01852a · Cited by 56 · see citing works
TGFβ promotes widespread enhancer chromatin opening and operates on genomic regulatory domains
Guerrero-Martinez, J. A., Ceballos-Chávez, M., Koehler, F., Peiró, S., & Reyes, J. C. (2020) · Nature Communications · doi:10.1038/s41467-020-19877-5 · Cited by 52 · see citing works
Decoding neural transcriptomes and epigenomes via high-throughput sequencing
Shin, J., Ming, G., & Song, H. (2014) · Nature Neuroscience · doi:10.1038/nn.3814 · Cited by 52 · see citing works
Martins, A. L., Walavalkar, N. M., Anderson, W. D., Zang, C., & Guertin, M. J. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx1053 · Cited by 53 · see citing works
Self-citationGenome-Wide Transcription Factor Binding in Leaves from C 3 and C 4 Grasses
Burgess, S., Reyna‐Llorens, I., Stevenson, S. R., Singh, P., Jaeger, K. E., & Hibberd, J. M. (2019) · The Plant Cell · doi:10.1105/tpc.19.00078 · Cited by 53 · see citing works
Identification of Transcription Factor Binding Sites using ATAC-seqPreprint
Li, Z., Schulz, M. H., Zenke, M., & Costa, I. G. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/362863 · Cited by 53 · see citing works
Kähärä, J., & Lähdesmäki, H. J. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv294 · Cited by 52 · see citing works
Tracing the Origin of Cell-Free DNA Molecules through Tissue-Specific Epigenetic Signatures
Oberhofer, A., Bronkhorst, A. J., Uhlig, C., Ungerer, V., & Holdenrieder, S. (2022) · Diagnostics · doi:10.3390/diagnostics12081834 · Cited by 45 · see citing works
Cooper, J., Ding, Y., Song, J., & Zhao, K. (2017) · Nature Protocols · doi:10.1038/nprot.2017.099 · Cited by 47 · see citing works
Protein–DNA binding in high-resolution
Mahony, S., & Pugh, B. F. (2015) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2015.1051505 · Cited by 46 · see citing works
Kim, M., Lu, F., & Zhang, Y. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.09.003 · Cited by 46 · see citing works
The role of chromatin dynamics in immune cell development
Winter, D. R., & Amit, I. (2014) · Immunological Reviews · doi:10.1111/imr.12200 · Cited by 43 · see citing works
An autoregulatory enhancer controls mammary-specific STAT5 functions
Metser, G., Shin, H. Y., Wang, C., Yoo, K. H., Oh, S., Villarino, A. V., O’Shea, J. J., Kang, K., & Hennighausen, L. G. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv999 · Cited by 45 · see citing works
Sequencing artifacts derived from a library preparation method using enzymatic fragmentation
Tanaka, N., Takahara, A., Hagio, T., Nishiko, R., Kanayama, J., Gotoh, O., & Mori, S. (2020) · PLoS ONE · doi:10.1371/journal.pone.0227427 · Cited by 45 · see citing works
Piper, J., Assi, S. A., Cauchy, P., Ladroue, C., Cockerill, P. N., Bonifer, C., & Ott, S. (2015) · BMC Genomics · doi:10.1186/s12864-015-2081-4 · Cited by 43 · see citing works
Pittol, J. M. R., Oruba, A., Mittler, G., Saccani, S., & van Essen, D. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2004526 · Cited by 43 · see citing works
Detecting Differential Transcription Factor Activity from ATAC-Seq Data
Tripodi, I. J., Allen, M. A., & Dowell, R. D. (2018) · Molecules · doi:10.3390/molecules23051136 · Cited by 37 · see citing works
Mocap: large-scale inference of transcription factor binding sites from chromatin accessibility
Chen, X. X., Yu, B., Carriero, N. J., Silva, C. T., & Bonneau, R. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx174 · Cited by 39 · see citing works
Unique and assay specific features of NOMe-, ATAC- and DNase I-seq data
Nordström, K. J. V., Schmidt, F., Gasparoni, N., Salhab, A., Gasparoni, G., Kattler, K., Müller, F., Ebert, P., Costa, I. G., Pfeifer, N., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz799 · Cited by 38 · see citing works
Identification of breast cancer associated variants that modulate transcription factor binding
Liu, Y., Walavalkar, N. M., Dozmorov, M. G., Rich, S. S., Civelek, M., & Guertin, M. J. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006761 · Cited by 40 · see citing works
Self-citationIntegrated epigenomic analysis stratifies chromatin remodellers into distinct functional groups
Giles, K. A., Gould, C. M., Du, Q., Skvortsova, K., Song, J. Z., Maddugoda, M. P., Achinger-Kawecka, J., Stirzaker, C., Clark, S. J., & Taberlay, P. C. (2019) · Epigenetics & Chromatin · doi:10.1186/s13072-019-0258-9 · Cited by 40 · see citing works
Single molecule and single cell epigenomics
Hyun, B., McElwee, J. L., & Soloway, P. D. (2014) · Methods · doi:10.1016/j.ymeth.2014.08.015 · Cited by 38 · see citing works
Quach, B. C., & Furey, T. S. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btw740 · Cited by 38 · see citing works
Multi-omics approaches to improve malaria therapy
Zhou, M., Varol, A., & Efferth, T. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105570 · Cited by 38 · see citing works
Chromatin information content landscapes inform transcription factor and DNA interactions
Albanus, R. D., Kyono, Y., Hensley, J., Varshney, A., Orchard, P., Kitzman, J. O., & Parker, S. C. J. (2021) · Nature Communications · doi:10.1038/s41467-021-21534-4 · Cited by 36 · see citing works
Raj, A., Shim, H., Gilad, Y., Pritchard, J. K., & Stephens, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0138030 · Cited by 36 · see citing works
Schwessinger, R., Suciu, M. C., McGowan, S. J., Telenius, J., Taylor, S., Higgs, D. R., & Hughes, J. R. (2017) · Genome Research · doi:10.1101/gr.220202.117 · Cited by 35 · see citing works
Recent trends and advances in identification and functional characterization of plant miRNAs
Zhou, X., Khare, T. R., & Kumar, V. (2020) · Acta Physiologiae Plantarum · doi:10.1007/s11738-020-3013-8 · Cited by 34 · see citing works
Bone Marrow Stroma-Induced Transcriptome and Regulome Signatures of Multiple Myeloma
Dziadowicz, S. A., Wang, L., Akhter, H., Aesoph, D., Sharma, T., Adjeroh, D., Hazlehurst, L., & Hu, G. (2022) · Cancers · doi:10.3390/cancers14040927 · Cited by 33 · see citing works
The Many Faces of Gene Regulation in Cancer: A Computational Oncogenomics Outlook
Lemus, E. H., Reyes-Gopar, H., Enríquez, J. E., & Ochoa, S. (2019) · Genes · doi:10.3390/genes10110865 · Cited by 33 · see citing works
Blumberg, A., Danko, C. G., Kundaje, A. B., & Mishmar, D. (2018) · Genome Research · doi:10.1101/gr.230409.117 · Cited by 33 · see citing works
Synthetic Promoters in Gene Therapy: Design Approaches, Features and Applications
Artemyev, V., Gubaeva, A., Paremskaia, A. I., Dzhioeva, A. A., Deviatkin, A. A., Feoktistova, S. G., Mityaeva, O. N., & Volchkov, P. (2024) · Cells · doi:10.3390/cells13231963 · Cited by 33 · see citing works
Genomic approaches to studying human-specific developmental traits
Franchini, L. F., & Pollard, K. S. (2015) · Development · doi:10.1242/dev.120048 · Cited by 29 · see citing works
Accurate annotation of accessible chromatin in mouse and human primordial germ cells
Li, J., Shen, S., Chen, J., Liu, W., Li, X., Zhu, Q., Wang, B., Chen, X., Wu, L., Wang, M., et al. (2018) · Cell Research · doi:10.1038/s41422-018-0096-5 · Cited by 28 · see citing works
Reactivation of super-enhancers by KLF4 in human Head and Neck Squamous Cell Carcinoma
Tsompana, M., Gluck, C. B., Sethi, I., Joshi, I., Bard, J., Nowak, N. J., Sinha, S., & Buck, M. J. (2019) · Oncogene · doi:10.1038/s41388-019-0990-4 · Cited by 30 · see citing works
ATAC-pipe: general analysis of genome-wide chromatin accessibility
Zuo, Z.-Q., Jin, Y., Zhang, W., Lu, Y., Li, B., & Qu, K. (2018) · Briefings in Bioinformatics · doi:10.1093/bib/bby056 · Cited by 30 · see citing works
Considerations in the analysis of plant chromatin accessibility data
Bubb, K. L., & Deal, R. B. (2020) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2020.01.003 · Cited by 30 · see citing works
Interrogating the Accessible Chromatin Landscape of Eukaryote Genomes Using ATAC-seq
Marinov, G. K., & Shipony, Z. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1103-6_10 · Cited by 30 · see citing works
Arthur, R. K., An, N., Khan, S. S., & McNerney, M. E. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx218 · Cited by 29 · see citing works
DMS-Seq for In Vivo Genome-wide Mapping of Protein-DNA Interactions and Nucleosome Centers
Umeyama, T., & Ito, T. (2017) · Current Protocols in Molecular Biology · doi:10.1002/cpmb.60 · Cited by 29 · see citing works
Pioneer Factors in Animals and Plants—Colonizing Chromatin for Gene Regulation
Lai, X., Verhage, L., Hugouvieux, V., & Zubieta, C. (2018) · Molecules · doi:10.3390/molecules23081914 · Cited by 28 · see citing works
Enhancer Dysfunction in 3D Genome and Disease
Xia, J., & Wei, G. (2019) · Cells · doi:10.3390/cells8101281 · Cited by 26 · see citing works
Raman Imaging: An Impending Approach Towards Cancer Diagnosis
Ramya, A. N., Arya, J. S., Murali, M., Shamjith, S., Vidyalekshmi, M. S., & Maiti, K. K. (2021) · Chemistry - An Asian Journal · doi:10.1002/asia.202001340 · Cited by 29 · see citing works
- Authors
- He, H. H., Meyer, C. A., Hu, S. S., Chen, M.-W., Zang, C., Liu, Y., Rao, P. K., Fei, T., Xu, H., Long, H., Liu, X. S., & Brown, M.
- Affiliations
- University Health Network (CA)
- Harvard University (US)
- Dana-Farber Cancer Institute (US)
- Tongji University (CN)
- Corresponding author
- Long, Henry
- Liu, X Shirley
- Brown, Myles
- ORCID
- Venue
- Nature Methods
- Published
- 2013-12-08
- Volume
- 11
- Issue
- 1
- Pages
- 73-78
- ISSN
- 1548-7091 (ISSN-L)
- 1548-7105
- PMC
- PMC4018771
- OpenAlex
- W2009853003
- Cited by
- 218
- References
- 22
- Citations by year
- 2026: 8 · 2025: 4 · 2024: 14 · 2023: 6 · 2022: 10 · 2021: 17 · 2020: 13 · 2019: 30 · 2018: 28 · 2017: 24 · 2016: 26 · 2015: 18 · 2014: 18 · 2013: 1
- FWCI
- 9.41
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Methods (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Funders
- National Human Genome Research Institute (U41HG007000)
- National Cancer Institute (K99CA172948, P50CA090381)
- National Institute of General Medical Sciences (R01GM099409)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK074967)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- DNase-seq, DNase I hypersensitive sites, transcription factor footprints, cis-regulatory elements, transcription factor binding sites, DNase I hypersensitivity, transcription factor occupancy, protocol optimization
- MeSH terms
- Binding Sites, Chromatin, Deoxyribonuclease I, Female, Gene Expression Regulation, Humans, Male, Nucleosomes, Nucleotides, Receptors, Androgen, Transcription Factors, Tumor Suppressor Protein p53, Sequence Analysis, DNA, K562 Cells, Amino Acid Motifs, Cell Line, Tumor, Gene Regulatory Networks, MCF-7 Cells
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review