An ultra high-throughput method for single-cell joint analysis of open chromatin and transcriptome
Open accessAbstract
Simultaneous profiling of transcriptome and chromatin accessibility within single cells is a powerful approach to dissect gene regulatory programs in complex tissues. However, current tools are limited by modest throughput. We now describe an ultra high-throughput method, Paired-seq, for parallel analysis of transcriptome and accessible chromatin in millions of single cells. We demonstrate the utility of Paired-seq for analyzing the dynamic and cell-type-specific gene regulatory programs in complex tissues by applying it to mouse adult cerebral cortex and fetal forebrain. The joint profiles of a large number of single cells allowed us to deconvolute the transcriptome and open chromatin landscapes in the major cell types within these brain tissues, infer putative target genes of candidate enhancers, and reconstruct the trajectory of cellular lineages within the developing forebrain.
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?
Compared to prior single-cell multiomics sequencing methods for joint RNA and epigenome analyses, Paired-Damage-seq displayed similar sensitivity in RNA detection.
“Compared to prior single-cell multiomics sequencing methods for joint RNA and epigenome analyses27,39–41, Paired-Damage-seq displayed similar sensitivity in RNA detection, despite different DNA modalities being measured”
From Single-cell parallel analysis of DNA damage and transcriptome reveals selective genome vulnerability (2025) · cites this paper as [39]
Milo may also be useful for single-cell assays beyond scRNA-seq, including multi-omic assays.
“Milo may also be applicable to single-cell assays other than scRNA-seq, including multi-omic assays [35–39].”
From Differential abundance testing on single-cell data using k-nearest neighbor graphs (2022) · cites this paper as [38]
Joint snRNA-seq and snATAC-seq on more than 15,000 fetal and adult mouse cortical cells showed dynamic, cell-type-specific changes in promoter accessibility during development.
“Paired snRNA-seq and snATAC-seq of over 15,000 cells in fetal and adult mouse cortex revealed cell type-specific dynamic regulation of promoter accessibility during brain development (Chen et al., 2019b; Zhu et al., 2019).”
From Single-Cell Sequencing of Brain Cell Transcriptomes and Epigenomes (2021) · cites this paper as Zhu et al., 2019
In mouse cerebral cortex, high-throughput multi-omics detected only 9-22 cell types, whereas scRNA-seq detected more than 100.
“As a result, high-throughput multi-omics studies in mouse cerebral cortex identified 9–22 cell types (Chen et al., 2019b; Zhu et al., 2019), compared with over 100 cell types found using scRNA-seq (Tasic et al., 2018; Yao et al., 2020a, 2020b).”
From Single-Cell Sequencing of Brain Cell Transcriptomes and Epigenomes (2021) · cites this paper as Zhu et al., 2019
Paired-seq used three rounds of ligation-based combinatorial indexing to process 1 million nuclei in a single experiment for parallel transcriptome and chromatin accessibility analyses.
“This strategy was implemented shortly after by Paired-seq, which used three rounds of ligation-based combinatorial indexing to process 1 million nuclei in a single experiment for parallel transcriptome and chromatin accessibility analyses59.”
From The technological landscape and applications of single-cell multi-omics (2023) · cites this paper as [59]
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
Fast gapped-read alignment with Bowtie 2
Langmead, B., & Salzberg, S. L. (2012) · Nature Methods · doi:10.1038/nmeth.1923 · Cited by 56,400 · 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
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
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
Integrating single-cell transcriptomic data across different conditions, technologies, and species
Butler, A., Hoffman, P., Smibert, P., Papalexi, E., & Satija, R. (2018) · Nature Biotechnology · doi:10.1038/nbt.4096 · Cited by 13,174 · see citing works
Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets.
Macosko, E. Z., Basu, A., Satija, R., Nemesh, J., Shekhar, K., Goldman, M., Tirosh, I., Bialas, A. R., Kamitaki, N., Martersteck, E. M., et al. (2015) · Cell · doi:10.1016/j.cell.2015.05.002 · Cited by 7,110 · 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
McCarthy, D. J., Chen, Y., & Smyth, G. K. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks042 · Cited by 5,195 · see citing works
deepTools: a flexible platform for exploring deep-sequencing data
Ramírez, F., Dündar, F., Diehl, S., Grüning, B. A., & Manke, T. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku365 · Cited by 3,738 · see citing works
Droplet barcoding for single-cell transcriptomics applied to embryonic stem cells
Klein, A. M., Mazutis, L., Akartuna, I., Tallapragada, N., Veres, A., Li, V., Peshkin, L., Weitz, D. A., & Kirschner, M. W. (2015) · Cell · doi:10.1016/j.cell.2015.04.044 · Cited by 3,356 · see citing works
Simultaneous epitope and transcriptome measurement in single cells
Stoeckius, M., Hafemeister, C., Stephenson, W., Houck-Loomis, B., Chattopadhyay, P. K., Swerdlow, H., Satija, R., & Smibert, P. (2017) · Nature Methods · doi:10.1038/nmeth.4380 · Cited by 3,098 · see citing works
Genome-Wide Mapping of in Vivo Protein-DNA Interactions
Johnson, D. S., Mortazavi, A., Myers, R. M., & Wold, B. (2007) · Science · doi:10.1126/science.1141319 · Cited by 2,927 · 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
CUT&Tag for efficient epigenomic profiling of small samples and single cells
Kaya-Okur, H. S., Wu, S. J., Codomo, C. A., Pledger, E. S., Bryson, T. D., Henikoff, J. G., Ahmad, K., & Henikoff, S. (2019) · Nature Communications · doi:10.1038/s41467-019-09982-5 · Cited by 2,187 · 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
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
Single-cell Hi-C reveals cell-to-cell variability in chromosome structure
Nagano, T., Lubling, Y., Stevens, T. J., Schoenfelder, S., Yaffe, E., Dean, W., Laue, E. D., Tanay, A., & Fraser, P. (2013) · Nature · doi:10.1038/nature12593 · Cited by 1,589 · see citing works
Khan, A., Fornés, O., Stigliani, A., Gheorghe, M., Castro-Mondragon, J. A., van der Lee, R., Bessy, A., Chèneby, J., Kulkarni, S. R., Tan, G., et al. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx1126 · Cited by 1,436 · 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
Cao, J., Packer, J. S., Ramani, V., Cusanovich, D. A., Huynh, C., Daza, R., Qiu, X., Lee, C., Furlan, S. N., Steemers, F. J., et al. (2017) · doi:10.1101/104844 · Cited by 1,402 · see citing works
Diffusion pseudotime robustly reconstructs lineage branching
Haghverdi, L., Büttner, M., Wolf, F. A., Buettner, F., & Theis, F. J. (2016) · Nature Methods · doi:10.1038/nmeth.3971 · Cited by 1,385 · see citing works
Mapping RNA‐seq Reads with STAR
Dobin, A., & Gingeras, T. (2015) · Current Protocols in Bioinformatics · doi:10.1002/0471250953.bi1114s51 · Cited by 1,265 · see citing works
Multiplex 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
Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity
Smallwood, S. A., Lee, H. J., Angermueller, C., Krueger, F., Saadeh, H., Peat, J., Andrews, S. R., Stegle, O., Reik, W., & Kelsey, G. (2014) · Nature Methods · doi:10.1038/nmeth.3035 · Cited by 1,125 · 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
Joint profiling of chromatin accessibility and gene expression in thousands of single cells
Cao, J., Cusanovich, D. A., Ramani, V., Aghamirzaie, D., Pliner, H. A., Hill, A. J., Daza, R. M., McFaline-Figueroa, J. L., Packer, J. S., Christiansen, L., et al. (2018) · Science · doi:10.1126/science.aau0730 · Cited by 938 · see citing works
Single-cell ChIP-seq reveals cell subpopulations defined by chromatin state
Rotem, A., Ram, O., Shoresh, N., Sperling, R. A., Goren, A., Weitz, D. A., & Bernstein, B. E. (2015) · Nature Biotechnology · doi:10.1038/nbt.3383 · Cited by 854 · see citing works
Multiplexed quantification of proteins and transcripts in single cells
Peterson, V. M., Zhang, K. X., Kumar, N., Wong, J., Li, L., Wilson, D. C., Moore, R., McClanahan, T. K., Sadekova, S., & Klappenbach, J. A. (2017) · Nature Biotechnology · doi:10.1038/nbt.3973 · Cited by 832 · see citing works
High-throughput sequencing of the transcriptome and chromatin accessibility in the same cell
Chen, S., Lake, B. B., & Zhang, K. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0290-0 · Cited by 810 · 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
G&T-seq: parallel sequencing of single-cell genomes and transcriptomes
Macaulay, I. C., Haerty, W., Kumar, P., Li, Y. I., Hu, T. X., Teng, M. J., Goolam, M., Saurat, N., Coupland, P., Shirley, L. M., et al. (2015) · Nature Methods · doi:10.1038/nmeth.3370 · Cited by 750 · see citing works
Parallel single-cell sequencing links transcriptional and epigenetic heterogeneity
Angermueller, C., Clark, S. J., Lee, H. J., Macaulay, I. C., Teng, M. J., Hu, T. X., Krueger, F., Smallwood, S. A., Ponting, C. P., Voet, T., et al. (2016) · Nature Methods · doi:10.1038/nmeth.3728 · Cited by 717 · see citing works
Clark, S. J., Argelaguet, R., Kapourani, C.-A., Stubbs, T. M., Lee, H. J., Alda-Catalinas, C., Krueger, F., Sanguinetti, G., Kelsey, G., Marioni, J. C., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03149-4 · Cited by 657 · see citing works
Hou, Y., Guo, H., Cao, C., Li, X., Hu, B., Zhu, P., Wu, X., Wen, L., Tang, F., Huang, Y., et al. (2016) · Cell Research · doi:10.1038/cr.2016.23 · Cited by 647 · see citing works
<i>destiny</i> : diffusion maps for large-scale single-cell data in R
Angerer, P., Haghverdi, L., Büttner, M., Theis, F. J., Marr, C., & Buettner, F. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btv715 · Cited by 640 · see citing works
Single-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-citationTopology of mammalian developmental enhancers and their regulatory landscapes
de Laat, W., & Duboule, D. (2013) · Nature · doi:10.1038/nature12753 · Cited by 521 · see citing works
Guo, H., Zhu, P., Wu, X., Li, X., Wen, L., & Tang, F. (2013) · Genome Research · doi:10.1101/gr.161679.113 · Cited by 518 · see citing works
Integrated genome and transcriptome sequencing of the same cell
Dey, S. S., Kester, L., Spanjaard, B., Bienko, M., & van Oudenaarden, A. (2015) · Nature Biotechnology · doi:10.1038/nbt.3129 · Cited by 502 · see citing works
Crawford, G. E., Holt, I. E., Whittle, J. R. R., Webb, B. D., Tai, D. S., Davis, S. R., Margulies, E. H., Chen, Y., Bernat, J. A., Ginsburg, D., et al. (2005) · Genome Research · doi:10.1101/gr.4074106 · Cited by 487 · see citing works
High-throughput single-cell ChIP-seq identifies heterogeneity of chromatin states in breast cancer
Grosselin, K., Durand, A., Marsolier, J., Poitou, A., Marangoni, E., Nemati, F., Dahmani, A., Lameiras, S., Reyal, F., Frenoy, O., et al. (2019) · Nature Genetics · doi:10.1038/s41588-019-0424-9 · Cited by 466 · 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
Single-cell epigenomics: Recording the past and predicting the future
Kelsey, G., Stegle, O., & Reik, W. (2017) · Science · doi:10.1126/science.aan6826 · Cited by 415 · see citing works
Single-cell multi-omics sequencing of mouse early embryos and embryonic stem cells
Guo, F., Li, L., Li, J., Wu, X., Hu, B., Zhu, P., Wen, L., & Tang, F. (2017) · Cell Research · doi:10.1038/cr.2017.82 · Cited by 374 · see citing works
The Three-Dimensional Organization of Mammalian Genomes
Yu, M., & Ren, B. (2017) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100616-060531 · Cited by 366 · see citing works
Self-citationSOX9 Is an Astrocyte-Specific Nuclear Marker in the Adult Brain Outside the Neurogenic Regions
Sun, W., Cornwell, A., Li, J., Peng, S., Osorio, M. J., Aalling, N., Wang, S., Benraiss, A., Lou, N., Goldman, S. A., et al. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.3199-16.2017 · Cited by 357 · see citing works
Mapping of long-range chromatin interactions by proximity ligation-assisted ChIP-seq
Fang, R., Yu, M., Li, G., Chee, S., Liu, T., Schmitt, A. D., & Ren, B. (2016) · Cell Research · doi:10.1038/cr.2016.137 · Cited by 344 · see citing works
Self-citationSimultaneous profiling of 3D genome structure and DNA methylation in single human cells
Lee, D.-S., Luo, C., Zhou, J., Chandran, S., Rivkin, A., Bartlett, A., Nery, J. R., Fitzpatrick, C., O’Connor, C., Dixon, J. R., et al. (2019) · Nature Methods · doi:10.1038/s41592-019-0547-z · Cited by 340 · see citing works
Genome-wide detection of DNase I hypersensitive sites in single cells and FFPE tissue samples
Jin, W., Tang, Q., Wan, M., Cui, K., Zhang, Y., Ren, G., Ni, B., Sklar, J., Przytycka, T. M., Childs, R., et al. (2015) · Nature · doi:10.1038/nature15740 · Cited by 332 · 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-citationSOX5 Controls the Sequential Generation of Distinct Corticofugal Neuron Subtypes
Lai, T. S., Jabaudon, D., Molyneaux, B. J., Azim, E., Arlotta, P., Menezes, J. R. L., & Macklis, J. D. (2008) · Neuron · doi:10.1016/j.neuron.2007.12.023 · Cited by 300 · see citing works
Simultaneous profiling of transcriptome and DNA methylome from a single cell
Hu, Y., Huang, K., An, Q., Du, G., Hu, G., Xue, J., Zhu, X., Wang, C.-Y., Xue, Z., & Fan, G. (2016) · Genome Biology · doi:10.1186/s13059-016-0950-z · Cited by 300 · see citing works
Mapping of long-range chromatin interactions by proximity ligation-assisted ChIP-seqPreprint
Fang, R.-X., Yu, M., Li, G., Chee, S., Liu, T., Schmitt, A., & Ren, B. (2016) · Cell Research · doi:10.1101/074294 · Cited by 298 · see citing works
Self-citationDeconvolution of single-cell multi-omics layers reveals regulatory heterogeneity
Liu, L., Liu, C., Quintero, A., Wu, L., Yuan, Y., Wang, M., Cheng, M., Leng, L., Xu, L., Dong, G., et al. (2019) · Nature Communications · doi:10.1038/s41467-018-08205-7 · Cited by 243 · see citing works
Pott, S. (2017) · eLife · doi:10.7554/elife.23203 · Cited by 230 · see citing works
Joint profiling of DNA methylation and chromatin architecture in single cells
Li, G., Liu, Y., Zhang, Y., Kubo, N., Yu, M., Fang, R., Kellis, M., & Ren, B. (2019) · Nature Methods · doi:10.1038/s41592-019-0502-z · Cited by 218 · see citing works
Self-citationŠubelj, L., & Bajec, M. (2011) · Physical Review E · doi:10.1103/physreve.83.036103 · Cited by 194 · see citing works
Molecular Control of Neurogenesis: A View from the Mammalian Cerebral CortexPreprint
Martynoga, B., Drechsel, D., & Guillemot, F. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008359 · Cited by 187 · see citing works
Profiling of pluripotency factors in single cells and early embryos
Hainer, S. J., Boskovic, A., McCannell, K. N., Rando, O. J., & Fazzio, T. (2019) · Cell · doi:10.1016/j.cell.2019.03.014 · Cited by 171 · see citing works
Mooijman, D., Dey, S. S., Boisset, J.-C., Crosetto, N., & van Oudenaarden, A. (2016) · Nature Biotechnology · doi:10.1038/nbt.3598 · Cited by 165 · see citing works
Zhu, C., Gao, Y., Guo, H., Xia, B., Song, J., Wu, X., Zeng, H., Kee, K., Tang, F., & Yi, C. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.02.013 · Cited by 159 · see citing works
Self-citationA chromatin integration labelling method enables epigenomic profiling with lower input
Harada, A., Maehara, K., Handa, T., Arimura, Y., Nogami, J., Hayashi‐Takanaka, Y., Shirahige, K., Kurumizaka, H., Kimurâ, H., & Ohkawa, Y. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0248-3 · Cited by 155 · see citing works
Integrative single-cell analysis by transcriptional and epigenetic states in human adult brainPreprint
Lake, B. B., Chen, S., Sos, B. C., et al. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/128520 · Cited by 122 · see citing works
MAPS: Model-based analysis of long-range chromatin interactions from PLAC-seq and HiChIP experiments
Juric, I., Yu, M., Abnousi, A., Raviram, R., Fang, R., Zhao, Y., Zhang, Y., Qiu, Y., Yang, Y., Li, Y., et al. (2019) · PLOS Computational Biology · doi:10.1371/journal.pcbi.1006982 · Cited by 121 · see citing works
Self-citationSimultaneous mapping of active DNA demethylation and sister chromatid exchange in single cellsPreprint
Wu, X., Inoue, A., Suzuki, T., & Zhang, Y. (2017) · Genes & Development · doi:10.1101/gad.294843.116 · Cited by 49 · see citing works
TELP, a sensitive and versatile library construction method for next-generation sequencing
Xu, P., Wu, J., Brunmeir, R., Kim, S.-Y., Zhang, Q., Ding, C., Han, W., Xie, W., & Xu, F. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku818 · Cited by 45 · see citing works
SnapATAC: A Comprehensive Analysis Package for Single Cell ATAC-seqPreprint
Fang, R.-X., Preissl, S., Li, Y., Hou, X.-M., Lucero, J., Wang, X.-X., Motamedi, A., Shiau, A., Zhou, X.-Z., Xie, F.-M., et al. (2019) · bioRxiv · doi:10.1101/615179 · Cited by 44 · see citing works
Self-citationDeconvolution of single-cell multi-omics layers reveals regulatory heterogeneityPreprint
Liu, L., Liu, C., Quintero, A., Wu, L. L., Yuan, Y., Wang, M., Cheng, M., Leng, L., Xu, L., Dong, G., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/316208 · Cited by 37 · see citing works
MAPS: model-based analysis of long-range chromatin interactions from PLAC-seq and HiChIP experimentsPreprint
Jurić, I., Yu, M., Abnousi, A., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/411835 · Cited by 20 · see citing works
Self-citationImproved single-cell ATAC-seq reveals chromatin dynamics of in vitro corticogenesisPreprint
Mulqueen, R. M., DeRosa, B. A., Thornton, C. A., Sayar, Z., Torkenczy, K. A., Fields, A. J., Wright, K. M., Nan, X., Ramji, R., Steemers, F. J., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/637256 · Cited by 12 · see citing works
Flagged first, then by citations
Research works printed but not linked: 4
- [37]Lee D-S Single-cell multi-omic profiling of chromatin conformation and DNA methylome. bioRxiv, 503235 (2018).
- [41]Chen S, Lake BB & Zhang K Linking transcriptome and chromatin accessibility in nanoliter droplets for single-cell sequencing. bioRxiv, 692608 (2019).
- [46]Fang R Fast and Accurate Clustering of Single Cell Epigenomes Reveals <em>Cis</em>-Regulatory Elements in Rare Cell Types. bioRxiv, 615179 (2019).
- [52]Gorkin DU An atlas of dynamic chromatin landscapes in the developing mouse fetus. Nature (In Press).
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
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
Methods and applications for single-cell and spatial multi-omics
Vandereyken, K., Sifrim, A., Thienpont, B., & Voet, T. (2023) · Nature Reviews Genetics · doi:10.1038/s41576-023-00580-2 · Cited by 1,244 · see citing works
The technological landscape and applications of single-cell multi-omics
Baysoy, A., Bai, Z., Satija, R., & Fan, R. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00615-w · Cited by 1,037 · see citing works
Differential abundance testing on single-cell data using k-nearest neighbor graphs
Dann, E., Henderson, N. C., Teichmann, S. A., Morgan, M. D., & Marioni, J. C. (2022) · Nature Biotechnology · doi:10.1038/s41587-021-01033-z · Cited by 938 · see citing works
Mimitou, E. P., Lareau, C. A., Chen, K. Y., Zorzetto-Fernandes, A. L., Hao, Y., Takeshima, Y., Luo, W., Huang, T.-S., Yeung, B. Z., Papalexi, E., et al. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-00927-2 · Cited by 529 · see citing works
Single-cell multiomics: technologies and data analysis methods
Lee, J., Hyeon, D. Y., & Hwang, D. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-0420-2 · Cited by 524 · see citing works
Single-cell multimodal omics: the power of many
Zhu, C., Preissl, S., & Ren, B. (2020) · Nature Methods · doi:10.1038/s41592-019-0691-5 · Cited by 386 · see citing works
Self-citationJoint 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 techniques from individual to multiomics analyses
Kashima, Y., Sakamoto, Y., Kaneko, K., Seki, M., Suzuki, Y., & Suzuki, A. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-00499-2 · Cited by 270 · see citing works
Single-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
Automated methods for cell type annotation on scRNA-seq data
Pasquini, G., Rojo Arias, J. E., Schäfer, P., & Busskamp, V. (2021) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2021.01.015 · Cited by 249 · see citing works
Decoding gene regulation in the fly brain
Janssens, J., Aibar, S., Taskiran, I. I., Ismail, J. N., Spanier, K. I., Bravo González-Blas, C., Quan, X. J., Papasokrati, D., Hulselmans, G., Makhzami, S., et al. (2021) · doi:10.1101/2021.08.11.454937 · Cited by 170 · see citing works
Decoding gene regulation in the fly brain
Janssens, J., Aibar, S., Taskiran, I. I., Ismail, J. N., Gomez, A. E., Aughey, G., Spanier, K. I., De Rop, F. V., González-Blas, C. B., Dionne, M., et al. (2022) · Nature · doi:10.1038/s41586-021-04262-z · Cited by 170 · see citing works
Cobolt: integrative analysis of multimodal single-cell sequencing data
Gong, B., Zhou, Y., & Purdom, E. (2021) · Genome Biology · doi:10.1186/s13059-021-02556-z · Cited by 168 · see citing works
Recent advances in single-cell sequencing technologies
Wen, L., & Tang, F. (2022) · Precision Clinical Medicine · doi:10.1093/pcmedi/pbac002 · Cited by 127 · see citing works
Multimodal chromatin profiling using nanobody-based single-cell CUT&Tag
Bartosovic, M., & Castelo-Branco, G. (2023) · Nature Biotechnology · doi:10.1038/s41587-022-01535-4 · Cited by 146 · see citing works
Xiong, H., Luo, Y., Wang, Q., Yu, X., & He, A. (2021) · Nature Methods · doi:10.1038/s41592-021-01129-z · Cited by 100 · see citing works
MIRA: joint regulatory modeling of multimodal expression and chromatin accessibility in single cells
Lynch, A. W., Theodoris, C. V., Long, H. W., Brown, M., Liu, X. S., & Meyer, C. A. (2022) · Nature Methods · doi:10.1038/s41592-022-01595-z · Cited by 80 · see citing works
Into the multiverse: advances in single-cell multiomic profiling
Ogbeide, S., Giannese, F., Mincarelli, L., & Macaulay, I. C. (2022) · Trends in Genetics · doi:10.1016/j.tig.2022.03.015 · Cited by 82 · see citing works
Droplet-based single-cell joint profiling of histone modifications and transcriptomes
Xie, Y., Zhu, C., Wang, Z., Tastemel, M., Chang, L., Li, Y. E., & Ren, B. (2023) · Nature Structural & Molecular Biology · doi:10.1038/s41594-023-01060-1 · Cited by 69 · see citing works
Self-citationSingle 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
Single-cell parallel analysis of DNA damage and transcriptome reveals selective genome vulnerability
Bai, D., Cao, Z., Attada, N., Song, J., & Zhu, C. (2025) · Nature Methods · doi:10.1038/s41592-025-02632-3 · Cited by 16 · see citing works
Self-citation
- Authors
- Zhu, C., Yu, M., Huang, H., Juric, I., Abnousi, A., Hu, R., Lucero, J., Behrens, M. M., Hu, M., & Ren, B.
- Affiliations
- Ludwig Cancer Research (US)
- University of California San Diego (US)
- Cleveland Clinic (US)
- Salk Institute for Biological Studies (US)
- Corresponding author
- Ren, Bing
- ORCID
- Venue
- Nature Structural & Molecular Biology
- Published
- 2019-11
- Volume
- 26
- Issue
- 11
- Pages
- 1063-1070
- ISSN
- 1545-9985 (ISSN-L)
- 1545-9993
- PMC
- PMC7231560
- OpenAlex
- W2985765936
- Cited by
- 344
- References
- 71
- Citations by year
- 2026: 30 · 2025: 47 · 2024: 56 · 2023: 66 · 2022: 56 · 2021: 56 · 2020: 31 · 2019: 1
- FWCI
- 11.91
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Structural & Molecular Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute of Mental Health (U19MH114831)
- National Human Genome Research Institute (U54HG006997)
- 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 › Chromatin Remodeling and Cancer
- Keywords
- single-cell transcriptomics, chromatin accessibility, open chromatin, enhancer target genes, gene regulatory programs, forebrain development, cerebral cortex
- MeSH terms
- Animals, Brain, Chromatin, Humans, Male, Mice, Inbred C57BL, Gene Expression Profiling, NIH 3T3 Cells, Mice, Hep G2 Cells, HEK293 Cells, Single-Cell Analysis, Transcriptome
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