Comprehensive analysis of single cell ATAC-seq data with SnapATAC
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Abstract
Identification of the cis-regulatory elements controlling cell-type specific gene expression patterns is essential for understanding the origin of cellular diversity. Conventional assays to map regulatory elements via open chromatin analysis of primary tissues is hindered by sample heterogeneity. Single cell analysis of accessible chromatin (scATAC-seq) can overcome this limitation. However, the high-level noise of each single cell profile and the large volume of data pose unique computational challenges. Here, we introduce SnapATAC, a software package for analyzing scATAC-seq datasets. SnapATAC dissects cellular heterogeneity in an unbiased manner and map the trajectories of cellular states. Using the Nyström method, SnapATAC can process data from up to a million cells. Furthermore, SnapATAC incorporates existing tools into a comprehensive package for analyzing single cell ATAC-seq dataset. As demonstration of its utility, SnapATAC is applied to 55,592 single-nucleus ATAC-seq profiles from the mouse secondary motor cortex. The analysis reveals ~370,000 candidate regulatory elements in 31 distinct cell populations in this brain region and inferred candidate cell-type specific transcriptional regulators.
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Chromatin accessibility of CREs associated with a gene can be summarized into gene activity scores by summing counts within genes and a certain distance upstream of the TSS.
“This can be achieved by summing up counts within genes and a certain distance upstream of the TSS136,143,150.”
From Best practices for single-cell analysis across modalities (2023) · cites this paper as [136]
Binarization of peaks is the most common normalization strategy for scATAC-seq data.
“In scATAC-seq data, the most common normalization strategy is binarization of peaks136,140,141.”
From Best practices for single-cell analysis across modalities (2023) · cites this paper as [136]
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Cites
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
Fast unfolding of communities in large networks
Blondel, V. D., Guillaume, J.-L., Lambiotte, R., & Lefebvre, E. (2008) · Journal of Statistical Mechanics: Theory and Experiment · doi:10.1088/1742-5468/2008/10/p10008 · Cited by 21,424 · see citing works
Model-based Analysis of ChIP-Seq (MACS)
Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C., Myers, R. M., Brown, M., Li, W., et al. (2008) · Genome Biology · doi:10.1186/gb-2008-9-9-r137 · Cited by 18,386 · see citing works
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
Comprehensive Integration of Single-Cell Data
Stuart, T., Butler, A., Hoffman, P., Hafemeister, C., Papalexi, E., Mauck, W. M., Hao, Y., Stoeckius, M., Smibert, P., & Satija, R. (2019) · Cell · doi:10.1016/j.cell.2019.05.031 · Cited by 15,453 · see citing works
Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H., & Glass, C. K. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.05.004 · Cited by 13,382 · see citing works
Fast, sensitive and accurate integration of single-cell data with Harmony
Korsunsky, I., Millard, N., Fan, J., Slowikowski, K., Zhang, F., Wei, K., Baglaenko, Y., Brenner, M., Loh, P.-R., & Raychaudhuri, S. (2019) · Nature Methods · doi:10.1038/s41592-019-0619-0 · Cited by 10,488 · see citing works
A 3D Map of the Human Genome at Kilobase Resolution Reveals Principles of Chromatin Looping
Rao, S. S. P., Huntley, M. H., Durand, N. C., Stamenova, E. K., Bochkov, I. D., Robinson, J. T., Sanborn, A. L., Machol, I., Omer, A. D., Lander, E. S., et al. (2014) · Cell · doi:10.1016/j.cell.2014.11.021 · Cited by 9,212 · see citing works
Comprehensive Mapping of Long-Range Interactions Reveals Folding Principles of the Human Genome
Lieberman-Aiden, E., van Berkum, N. L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., Amit, I., Lajoie, B. R., Sabo, P. J., Dorschner, M. O., et al. (2009) · Science · doi:10.1126/science.1181369 · Cited by 8,898 · see citing works
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y., & Greenleaf, W. J. (2013) · Nature Methods · doi:10.1038/nmeth.2688 · Cited by 6,422 · see citing works
GREAT improves functional interpretation of cis-regulatory regions
McLean, C. Y., Bristor, D., Hiller, M., Clarke, S. L., Schaar, B. T., Lowe, C. B., Wenger, A. M., & Bejerano, G. (2010) · Nature Biotechnology · doi:10.1038/nbt.1630 · Cited by 4,502 · see citing works
Hafemeister, C., & Satija, R. (2019) · Genome Biology · doi:10.1186/s13059-019-1874-1 · Cited by 4,479 · cited 2× · see citing works
“Pair-end reads are converted into fragments and only those that meet the following criteria are kept: (1) properly paired (according to SMA fl ag value); (2) uniquely mapped (MAPQ >30); (3) insert distance within [50 – 1000 bp].”
BackgroundMethodSlingshot: cell lineage and pseudotime inference for single-cell transcriptomics
Street, K., Risso, D., Fletcher, R. B., Das, D., Ngai, J., Yosef, N., Purdom, E., & Dudoit, S. (2018) · BMC Genomics · doi:10.1186/s12864-018-4772-0 · Cited by 3,159 · see citing works
Mechanisms and Functional Implications of Adult Neurogenesis
Zhao, C., Deng, W., & Gage, F. H. (2008) · Cell · doi:10.1016/j.cell.2008.01.033 · Cited by 3,007 · see citing works
Molecular Architecture of the Mouse Nervous System
Zeisel, A., Hochgerner, H., Lönnerberg, P., Johnsson, A., Memic, F., van der Zwan, J., Häring, M., Braun, E., Borm, L. E., La Manno, G., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.021 · Cited by 2,995 · see citing works
Scrublet: computational identification of cell doublets in single-cell transcriptomic data
Wolock, S. L., Lopez, R., & Klein, A. M. (2018) · doi:10.1101/357368 · Cited by 2,758 · cited 5× · see citing works
“To examine this, we applied Scrublet to a single-cell ATAC-seq dataset of mixed human and mouse cells where the “ ground-truth ” doublets can be identi fi ed based on the alignment ratio to human and mouse genome.”
MethodInfluentialScrublet: computational identification of cell doublets in single-cell transcriptomic data
Wolock, S. L., Lopez, R., & Klein, A. M. (2019) · Cell Systems · doi:10.1016/j.cels.2018.11.005 · Cited by 2,758 · see citing works
Single-cell chromatin accessibility reveals principles of regulatory variation
Buenrostro, J. D., Wu, B., Litzenburger, U. M., Ruff, D., Gonzales, M. L., Snyder, M. P., Chang, H. Y., & Greenleaf, W. J. (2015) · Nature · doi:10.1038/nature14590 · Cited by 2,308 · see citing works
Global epigenomic reconfiguration during mammalian brain development
Lister, R., Mukamel, E. A., Nery, J. R., Urich, M., Puddifoot, C. A., Johnson, N. D., Lucero, J., Huang, Y., Dwork, A. J., Schultz, M. D., et al. (2013) · Science · doi:10.1126/science.1237905 · Cited by 1,830 · see citing works
Self-citationAdult mouse cortical cell taxonomy revealed by single cell transcriptomics
Tasic, B., Menon, V., Nguyen, T. N., Kim, T. K., Jarsky, T., Yao, Z., Levi, B., Gray, L. T., Sorensen, S. A., Dolbeare, T., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4216 · Cited by 1,714 · see citing works
chromVAR: inferring transcription-factor-associated accessibility from single-cell epigenomic data
Schep, A. N., Wu, B., Buenrostro, J. D., & Greenleaf, W. J. (2017) · Nature Methods · doi:10.1038/nmeth.4401 · Cited by 1,680 · see citing works
CTCF: Master Weaver of the Genome
Phillips‐Cremins, J. E., & Corces, V. G. (2009) · Cell · doi:10.1016/j.cell.2009.06.001 · Cited by 1,540 · see citing works
Single-cell profiling of the developing mouse brain and spinal cord with split-pool barcoding
Rosenberg, A. B., Roco, C. M., Muscat, R. A., Kuchina, A., Sample, P., Yao, Z., Graybuck, L. T., Peeler, D. J., Mukherjee, S., Chen, W., et al. (2018) · Science · doi:10.1126/science.aam8999 · Cited by 1,422 · see citing works
High-Resolution Mapping and Characterization of Open Chromatin across the Genome
Boyle, A. P., Davis, S., Shulha, H. P., Meltzer, P., Margulies, E. H., Weng, Z., Furey, T. S., & Crawford, G. E. (2008) · Cell · doi:10.1016/j.cell.2007.12.014 · Cited by 1,415 · see citing works
A map of the cis-regulatory sequences in the mouse genome
Shen, Y., Yue, F., McCleary, D. F., Ye, Z., Edsall, L., Kuan, S., Wagner, U., Dixon, J., Lee, L., Lobanenkov, V. V., et al. (2012) · Nature · doi:10.1038/nature11243 · Cited by 1,361 · see citing works
Self-citationMultiplex single-cell profiling of chromatin accessibility by combinatorial cellular indexing
Cusanovich, D. A., Daza, R., Adey, A., Pliner, H. A., Christiansen, L., Gunderson, K. L., Steemers, F. J., Trapnell, C., & Shendure, J. (2015) · Science · doi:10.1126/science.aab1601 · Cited by 1,248 · see citing works
VISTA Enhancer Browser—a database of tissue-specific human enhancers
Visel, A., Minovitsky, S., Dubchak, I., & Pennacchio, L. A. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkl822 · Cited by 1,080 · see citing works
Integrative single-cell analysis of transcriptional and epigenetic states in the human adult brain
Lake, B. B., Chen, S., Sos, B. C., Fan, J., Kaeser, G. E., Yung, Y. C., Duong, T. E., Gao, D., Chun, J., Kharchenko, P. V., et al. (2018) · Nature Biotechnology · doi:10.1038/nbt.4038 · Cited by 983 · see citing works
Self-citationSatpathy, A. T., Granja, J. M., Yost, K. E., Qi, Y., Meschi, F., McDermott, G. P., Olsen, B. N., Mumbach, M. R., Pierce, S. E., Corces, M. R., et al. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0206-z · Cited by 980 · see citing works
Tn5 transposase and tagmentation procedures for massively scaled sequencing projectsPreprint
Picelli, S., Björklund, Å. K., Reinius, B., Sagasser, S., Winberg, G., & Sandberg, R. (2014) · Genome Research · doi:10.1101/gr.177881.114 · Cited by 829 · see citing works
Cicero predicts cis-regulatory DNA interactions from single-cell chromatin accessibility data
Pliner, H. A., Packer, J. S., McFaline-Figueroa, J. L., Cusanovich, D. A., Daza, R. M., Aghamirzaie, D., Srivatsan, S., Qiu, X., Jackson, D., Minkina, A., et al. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.06.044 · Cited by 789 · see citing works
Innate Immune Activity Conditions the Effect of Regulatory Variants upon Monocyte Gene Expression
Fairfax, B. P., Humburg, P., Makino, S., Naranbhai, V., Wong, D., Lau, E., Jostins, L., Plant, K., Andrews, R., McGee, C., et al. (2014) · Science · doi:10.1126/science.1246949 · Cited by 764 · see citing works
A Single-Cell Atlas of In Vivo Mammalian Chromatin Accessibility
Cusanovich, D. A., Hill, A. J., Aghamirzaie, D., Daza, R. M., Pliner, H. A., Berletch, J. B., Filippova, G. N., Huang, X., Christiansen, L., DeWitt, W. S., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.052 · Cited by 759 · see citing works
The landscape of accessible chromatin in mammalian preimplantation embryos
Wu, J.-Y., Huang, B., Chen, H., Yin, Q.-Z., Liu, Y., Xiang, Y.-L., Zhang, B., Liu, B.-F., Wang, Q.-J., Xia, W., et al. (2016) · Nature · doi:10.1038/nature18606 · Cited by 669 · see citing works
Self-citationSingle-cell methylomes identify neuronal subtypes and regulatory elements in mammalian cortex
Luo, C., Keown, C. L., Kurihara, L., Zhou, J., He, Y., Li, J., Castanon, R., Lucero, J., Nery, J. R., Sandoval, J. P., et al. (2017) · Science · doi:10.1126/science.aan3351 · Cited by 545 · see citing works
Self-citationDevelopmental diversification of cortical inhibitory interneurons
Mayer, C., Hafemeister, C., Bandler, R. C., Machold, R., Batista Brito, R., Jaglin, X., Allaway, K., Butler, A., Fishell, G., & Satija, R. (2018) · Nature · doi:10.1038/nature25999 · Cited by 492 · see citing works
From reads to insight: a hitchhiker’s guide to ATAC-seq data analysis
Yan, F., Powell, D., Curtis, D. J., & Wong, N. C. (2020) · Genome biology · doi:10.1186/s13059-020-1929-3 · Cited by 467 · see citing works
cisTopic: cis-regulatory topic modeling on single-cell ATAC-seq data
Bravo González-Blas, C., Minnoye, L., Papasokrati, D., Aibar, S., Hulselmans, G., Christiaens, V., Davie, K., Wouters, J., & Aerts, S. (2019) · Nature Methods · doi:10.1038/s41592-019-0367-1 · Cited by 456 · see citing works
Droplet-based combinatorial indexing for massive-scale single-cell chromatin accessibility
Lareau, C. A., Duarte, F. M., Chew, J. G., Kartha, V. K., Burkett, Z. D., Kohlway, A. S., Pokholok, D., Aryee, M. J., Steemers, F. J., Lebofsky, R., et al. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0147-6 · Cited by 444 · see citing works
An 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-citationThe cis-regulatory dynamics of embryonic development at single-cell resolution
Cusanovich, D. A., Reddington, J. P., Garfield, D. A., Daza, R. M., Aghamirzaie, D., Marco-Ferreres, R., Pliner, H. A., Christiansen, L., Qiu, X., Steemers, F. J., et al. (2018) · Nature · doi:10.1038/nature25981 · Cited by 363 · see citing works
Preissl, S., Fang, R., Huang, H., Zhao, Y., Raviram, R., Gorkin, D. U., Zhang, Y., Sos, B. C., Afzal, V., Dickel, D. E., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0079-3 · Cited by 332 · see citing works
Self-citationAssessment of computational methods for the analysis of single-cell ATAC-seq data
Chen, H., Lareau, C., Andreani, T., Vinyard, M. E., Garcia, S. P., Clement, K., Andrade-Navarro, M. A., Buenrostro, J. D., & Pinello, L. (2019) · Genome Biology · doi:10.1186/s13059-019-1854-5 · Cited by 332 · see citing works
Rubin, A. J., Parker, K. R., Satpathy, A. T., Qi, Y., Wu, B., Ong, A. J., Mumbach, M. R., Ji, A. L., Kim, D. S., Cho, S. W., et al. (2019) · Cell · doi:10.1016/j.cell.2018.11.022 · Cited by 314 · see citing works
Ecker, J. R., Geschwind, D. H., Kriegstein, A. R., Ngai, J., Osten, P., Polioudakis, D., Regev, A., Šestan, N., Wickersham, I. R., & Zeng, H. (2017) · Neuron · doi:10.1016/j.neuron.2017.10.007 · Cited by 254 · see citing works
Self-citationHafemeister, C., & Satija, R. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/576827 · Cited by 238 · see citing works
Sampling methods for the Nyström method
Kumar, S., Mohri, M., & Talwalkar, A. (2012) · Cited by 227 · see citing works
The diversity of GABAergic neurons and neural communication elements
Huang, Z. J., & Paul, A. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0195-4 · Cited by 201 · cited 1× · see citing works
“In mammalian brain, GABAergic interneurons exhibit spectacular diversity that shapes the spatiotemporal dynamics of neural circuits underlying cognition 38 .”
BackgroundbHLH Transcription factors and mammalian neuronal differentiation
Kageyama, R., Ishibashi, M., Takebayashi, K., & Tomita, K. (1997) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(97)89968-2 · Cited by 181 · see citing works
High-throughput chromatin accessibility profiling at single-cell resolution
Mezger, A., Klemm, S. L., Mann, I. K., Brower, K. K., Mir, A. A., Bostick, M. L., Farmer, A. A., Fordyce, P. M., Linnarsson, S., & Greenleaf, W. J. (2018) · Nature Communications · doi:10.1038/s41467-018-05887-x · Cited by 149 · see citing works
Satpathy, A. T., Granja, J. M., Yost, K. E., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/610550 · Cited by 120 · see citing works
Kumar, S., Mohri, M., & Talwalkar, A. (2009) · Cited by 109 · see citing works
BROCKMAN: deciphering variance in epigenomic regulators by k-mer factorization
de Boer, C. G., & Regev, A. (2018) · BMC Bioinformatics · doi:10.1186/s12859-018-2255-6 · Cited by 48 · see citing works
Landmark diffusion maps (L-dMaps): Accelerated manifold learning out-of-sample extension
Long, A. W., & Ferguson, A. L. (2017) · Applied and Computational Harmonic Analysis · doi:10.1016/j.acha.2017.08.004 · Cited by 40 · see citing works
Systematic mapping of chromatin state landscapes during mouse developmentPreprint
Gorkin, D. U., Barozzi, I., Zhang, Y.-X., Lee, A.-Y., Li, B., Zhao, Y., Wildberg, A., Ding, B., Zhang, B., Wang, M.-C., et al. (2017) · bioRxiv · doi:10.1101/166652 · Cited by 33 · see citing works
Self-citationGraybuck (2019) · doi:10.1101/525014 · Cited by 31 · see citing works
Diffusion Maps meet NyströmPreprint
Erichson, N. B., Mathelin, L., Brunton, S. L., et al. (2018) · arXiv (Cornell University) · doi:10.48550/arxiv.1802.08762 · Cited by 1 · see citing works
Single Cell Analysis of Chromatin Accessibility
Fang, R. (2019) · eScholarship (California Digital Library) · Cited by 1 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- [51]Li, M., Kwok, J. T. & Lu, B.-L. Making large-scale Nyström approximation possible. in Proc. 27th International Conference on Machine Learning 631–638 (2010).
Cited by
Sorted by citations
Single-cell chromatin state analysis with Signac
Stuart, T., Srivastava, A., Madad, S., Lareau, C. A., & Satija, R. (2021) · Nature Methods · doi:10.1038/s41592-021-01282-5 · Cited by 1,769 · see citing works
Benchmarking atlas-level data integration in single-cell genomics
Luecken, M. D., Büttner, M., Chaichoompu, K., Danese, A., Interlandi, M., Mueller, M. F., Strobl, D. C., Zappia, L., Dugas, M., Colomé-Tatché, M., et al. (2022) · Nature Methods · doi:10.1038/s41592-021-01336-8 · Cited by 1,438 · see citing works
Chromatin Potential Identified by Shared Single-Cell Profiling of RNA and Chromatin
Ma, S., Zhang, B., LaFave, L. M., Earl, A. S., Chiang, Z., Hu, Y., Ding, J., Brack, A., Kartha, V. K., Tay, T., et al. (2020) · Cell · doi:10.1016/j.cell.2020.09.056 · Cited by 1,146 · see citing works
Best practices for single-cell analysis across modalities
Heumos, L., Schaar, A. C., Lance, C., Litinetskaya, A., Drost, F., Zappia, L., Lücken, M. D., Strobl, D. C., Henao, J., Curion, F., et al. (2023) · Nature Reviews Genetics · doi:10.1038/s41576-023-00586-w · Cited by 1,051 · see citing works
“Although advancements in experimental assays allow for the paired measurements of many modality combinations 246 , different modalities are still commonly measured independently, resulting in unpaired data 247 .”
BackgroundMethodInfluentialSCENIC+: single-cell multiomic inference of enhancers and gene regulatory networks
Bravo González-Blas, C., De Winter, S., Hulselmans, G., Hecker, N., Matetovici, I., Christiaens, V., Poovathingal, S., Wouters, J., Aibar, S., & Aerts, S. (2023) · Nature Methods · doi:10.1038/s41592-023-01938-4 · Cited by 778 · see citing works
A multimodal cell census and atlas of the mammalian primary motor cortex
BRAIN Initiative Cell Census Network (BICCN), BRAIN Initiative Cell Census Network (BICCN) Corresponding authors, Callaway, E. M., Dong, H.-W., Ecker, J. R., Hawrylycz, M. J., Huang, Z. J., Lein, E. S., Ngai, J., Osten, P., et al. (2021) · Nature · doi:10.1038/s41586-021-03950-0 · Cited by 522 · see citing works
Self-citationA transcriptomic and epigenomic cell atlas of the mouse primary motor cortex
Yao, Z., Liu, H., Xie, F., Fischer, S., Adkins, R. S., Aldridge, A. I., Ament, S. A., Bartlett, A., Behrens, M. M., Van den Berge, K., et al. (2021) · Nature · doi:10.1038/s41586-021-03500-8 · Cited by 398 · see citing works
Self-citationIntegrative Single-Cell RNA-Seq and ATAC-Seq Analysis of Human Developmental Hematopoiesis
Ranzoni, A. M., Tangherloni, A., Berest, I., Riva, S. G., Myers, B., Strzelecka, P. M., Xu, J., Panada, E., Mohorianu, I., Zaugg, J. B., et al. (2021) · Cell Stem Cell · doi:10.1016/j.stem.2020.11.015 · Cited by 331 · see citing works
Joint profiling of histone modifications and transcriptome in single cells from mouse brain
Zhu, C., Zhang, Y., Li, Y. E., Lucero, J., Behrens, M. M., & Ren, B. (2021) · Nature Methods · doi:10.1038/s41592-021-01060-3 · Cited by 301 · see citing works
Self-citationSingle-Cell Sequencing of Brain Cell Transcriptomes and Epigenomes
Armand, E. J., Li, J., Xie, F., Luo, C., & Mukamel, E. A. (2021) · Neuron · doi:10.1016/j.neuron.2020.12.010 · Cited by 241 · see citing works
Self-citationMUON: multimodal omics analysis framework
Bredikhin, D., Kats, I., & Stegle, O. (2022) · Genome Biology · doi:10.1186/s13059-021-02577-8 · Cited by 216 · see citing works
Functional enhancer elements drive subclass-selective expression from mouse to primate neocortex
Mich, J. K., Graybuck, L. T., Hess, E. E., Mahoney, J. T., Kojima, Y., Ding, Y., Somasundaram, S., Miller, J. A., Kalmbach, B. E., Radaelli, C., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108754 · Cited by 193 · see citing works
Spatially resolved epigenomic profiling of single cells in complex tissues
Lu, T., Ang, C. E., & Zhuang, X. (2022) · Cell · doi:10.1016/j.cell.2022.09.035 · Cited by 197 · see citing works
A genetic map of the mouse dorsal vagal complex and its role in obesity
Ludwig, M. Q., Cheng, W., Gordian, D., Lee, J., Paulsen, S. J., Hansen, S. N., Egerod, K. L., Barkholt, P., Rhodes, C. J., Secher, A., et al. (2021) · Nature Metabolism · doi:10.1038/s42255-021-00363-1 · Cited by 186 · see citing works
An atlas of gene regulatory elements in adult mouse cerebrum
Li, Y. E., Preissl, S., Hou, X., Zhang, Z., Zhang, K., Qiu, Y., Poirion, O. B., Li, B., Chiou, J., Liu, H., et al. (2021) · Nature · doi:10.1038/s41586-021-03604-1 · Cited by 185 · see citing works
Self-citationA comparative atlas of single-cell chromatin accessibility in the human brain
Li, Y. E., Preissl, S., Miller, M., Johnson, N. D., Wang, Z., Jiao, H., Zhu, C., Wang, Z., Xie, Y., Poirion, O., et al. (2023) · Science · doi:10.1126/science.adf7044 · Cited by 173 · see citing works
Self-citationTargeting histone acetylation dynamics and oncogenic transcription by catalytic P300/CBP inhibition
Hogg, S. J., Motorna, O., Cluse, L. A., Johanson, T. M., Coughlan, H. D., Raviram, R., Myers, R. M., Costacurta, M., Todorovski, I., Pijpers, L., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.04.015 · Cited by 170 · see citing works
Mouse models of neutropenia reveal progenitor-stage-specific defects
Muench, D. E., Olsson, A., Ferchen, K., Pham, G., Serafin, R. A., Chutipongtanate, S., Dwivedi, P., Song, B., Hay, S., Chetal, K., et al. (2020) · Nature · doi:10.1038/s41586-020-2227-7 · Cited by 115 · see citing works
SCENIC+: single-cell multiomic inference of enhancers and gene regulatory networks
González-Blas, C. B., De Winter, S., Hulselmans, G., Hecker, N., Matetovici, I., Christiaens, V., Poovathingal, S., Wouters, J., Aibar, S., & Aerts, S. (2022) · doi:10.1101/2022.08.19.504505 · Cited by 778 · see citing works
Zhang, Y., Amaral, M. L., Zhu, C., Grieco, S. F., Hou, X., Lin, L., Buchanan, J., Tong, L., Preissl, S., Xu, X., et al. (2022) · Cell Research · doi:10.1038/s41422-022-00719-6 · Cited by 89 · see citing works
Self-citationA cell-type-specific error-correction signal in the posterior parietal cortex
Green, J., Bruno, C. A., Traunmüller, L., Ding, J., Hrvatin, S., Wilson, D. E., Khodadad, T., Samuels, J., Greenberg, M. E., & Harvey, C. D. (2023) · Nature · doi:10.1038/s41586-023-06357-1 · Cited by 43 · see citing works
Single cell epigenomic atlas of the developing human brain and organoids
Ziffra, R. S., Kim, C. N., Wilfert, A., Turner, T. N., Haeussler, M., Casella, A. M., Przytycki, P. F., Kreimer, A., Pollard, K. S., Ament, S. A., et al. (2019) · doi:10.1101/2019.12.30.891549 · Cited by 33 · see citing works
Enhanced integration of single-cell multi-omics data using graph attention networks
Liao, X., Li, Y., Li, S., Wen, L., Li, X., & Yu, B. (2025) · ACS Synthetic Biology · doi:10.1021/acssynbio.4c00864 · Cited by 5 · see citing works
Self-citation
- Authors
- Fang, R., Preissl, S., Li, Y., Hou, X., Lucero, J., Wang, X., Motamedi, A., Shiau, A. K., Zhou, X., Xie, F., Mukamel, E. A., Zhang, K., Zhang, Y., Behrens, M. M., Ecker, J. R., & Ren, B.
- Affiliations
- Harvard University (US)
- University of California San Diego (US)
- Ludwig Cancer Research (US)
- Salk Institute for Biological Studies (US)
- Ludwig Cancer Research (BE)
- Corresponding author
- Ren, Bing
- ORCID
- Venue
- Nature Communications
- Published
- 2021-02-26
- Volume
- 12
- Issue
- 1
- Pages
- 1337-1337
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC7910485
- OpenAlex
- W3133082627
- Cited by
- 455
- References
- 58
- Citations by year
- 2026: 41 · 2025: 63 · 2024: 94 · 2023: 78 · 2022: 88 · 2021: 65 · 2020: 17 · 2019: 9
- FWCI
- 27.39
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- FreiDok plus (Universitätsbibliothek Freiburg) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- Howard Hughes Medical Institute
- Damon Runyon Cancer Research Foundation
- National Institutes of Health
- University of California, San Diego
- National Institute of Mental Health (U19MH114831)
- National Cancer Institute (K99CA252020, P30CA014195)
- School of Medicine, University of California, San Diego
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
- Keywords
- single-cell ATAC-seq, cis-regulatory elements, open chromatin, cellular heterogeneity, cell type-specific gene expression, single-nucleus ATAC-seq, secondary motor cortex, transcription factors, cell trajectory inference, Nyström method, software package
- MeSH terms
- Chromatin Immunoprecipitation Sequencing, Animals, Chromatin, Male, Mice, Inbred C57BL, Motor Cortex, Sequence Analysis, DNA, Computational Biology, Mice, Epigenomics, Single-Cell Analysis
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