Chromatin Potential Identified by Shared Single-Cell Profiling of RNA and Chromatin
Open accessPublished version of a preprint
Abstract
Cell differentiation and function are regulated across multiple layers of gene regulation, including modulation of gene expression by changes in chromatin accessibility. However, differentiation is an asynchronous process precluding a temporal understanding of regulatory events leading to cell fate commitment. Here we developed simultaneous high-throughput ATAC and RNA expression with sequencing (SHARE-seq), a highly scalable approach for measurement of chromatin accessibility and gene expression in the same single cell, applicable to different tissues. Using 34,774 joint profiles from mouse skin, we develop a computational strategy to identify cis-regulatory interactions and define domains of regulatory chromatin (DORCs) that significantly overlap with super-enhancers. During lineage commitment, chromatin accessibility at DORCs precedes gene expression, suggesting that changes in chromatin accessibility may prime cells for lineage commitment. We computationally infer chromatin potential as a quantitative measure of chromatin lineage-priming and use it to predict cell fate outcomes. SHARE-seq is an extensible platform to study regulatory circuitry across diverse cells in tissues.
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?
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 [39]
SHARE-seq uses several rounds of hybridization blocking to label mRNA and chromatin fragments in single cells.
“Increasing throughput, SHARE-seq was built based on SPLiT-seq and Paired-seq and uses several rounds of hybridization blocking to label mRNA and chromatin fragments in single cells60.”
From The technological landscape and applications of single-cell multi-omics (2023) · cites this paper as [60]
Paired experimental methods are easier computationally because modalities can be tethered to a single cell or spot, but sequencing capacity of each modality decreases overall sample size.
“By contrast, paired experimental methods (10x Multiome, SHARE-seq60, DBiT-seq123, SNARE-seq57, CITE-seq68 and others) are easier to work with computationally as different modalities can be tethered to a single cell or a single spot; however, the sequencing capacity of each modality causes the overall sample size to decrease.”
From The technological landscape and applications of single-cell multi-omics (2023) · cites this paper as [60]
Computational methods can integrate data from multiple omics but cannot readily uncover mechanistic links between different omics layers.
“Although computational methods can integrate data from multiple omics10, they cannot readily uncover the mechanistic links between different omics layers.”
From Spatial epigenome–transcriptome co-profiling of mammalian tissues (2023) · cites this paper as [10]
The high accessibility but modest or low RNA expression of Pax6, Sox2 and Myt1l may indicate lineage priming of these genes in embryonic brain development.
“which may indicate lineage priming10,27 of these genes in embryonic brain development.”
From Spatial epigenome–transcriptome co-profiling of mammalian tissues (2023) · cites this paper as [10]
The elevated chromatin accessibility at earlier stages for genes such as Dcx and Tubb3 suggests lineage priming of these genes in expression.
“suggesting lineage priming of these genes in expression10,27.”
From Spatial epigenome–transcriptome co-profiling of mammalian tissues (2023) · cites this paper as [10]
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
R: A Language and Environment for Statistical Computing
R Core Team (2000) · doi:10.32614/r.manuals · Cited by 355,706 · see citing works
The Sequence Alignment/Map format and SAMtools
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp352 · Cited by 62,041 · see citing works
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
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
Liao, Y., Smyth, G. K., & Shi, W. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btt656 · Cited by 27,219 · 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
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
UMAP: Uniform Manifold Approximation and Projection
McInnes, L., Healy, J., Saul, N., & Großberger, L. (2018) · Journal of Open Source Software · doi:10.21105/joss.00861 · Cited by 9,826 · 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
Self-citationWnt/β-Catenin Signaling in Development and Disease
Clevers, H. (2006) · Cell · doi:10.1016/j.cell.2006.10.018 · Cited by 5,568 · see citing works
A bivalent chromatin structure marks key developmental genes in embryonic stem cells
Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., et al. (2006) · Cell · doi:10.1016/j.cell.2006.02.041 · Cited by 5,361 · see citing works
Master Transcription Factors and Mediator Establish Super-Enhancers at Key Cell Identity Genes
Whyte, W. A., Orlando, D. A., Hnisz, D., Abraham, B. J., Lin, C. Y., Kagey, M. H., Rahl, P. B., Lee, T. I., & Young, R. A. (2013) · Cell · doi:10.1016/j.cell.2013.03.035 · Cited by 4,143 · see citing works
La Manno, G., Soldatov, R., Zeisel, A., Braun, E., Hochgerner, H., Petukhov, V., Lidschreiber, K., Kastriti, M. E., Lönnerberg, P., Furlan, A., et al. (2018) · Nature · doi:10.1038/s41586-018-0414-6 · Cited by 4,118 · see citing works
Super-enhancers in the control of cell identity and disease
Hnisz, D., Abraham, B. J., Lee, T. I., Lau, A., Saint-André, V., Sigova, A. A., Hoke, H. A., & Young, R. A. (2013) · Cell · doi:10.1016/j.cell.2013.09.053 · Cited by 3,662 · 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
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
An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues
Corces, M. R., Trevino, A. E., Hamilton, E. G., Greenside, P. G., Sinnott-Armstrong, N. A., Vesuna, S., Satpathy, A. T., Rubin, A. J., Montine, K. S., Wu, B., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4396 · Cited by 2,496 · 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
Self-citationA unique chromatin signature uncovers early developmental enhancers in humans
Rada-Iglesias, A., Bajpai, R., Swigut, T., Brugmann, S. A., Flynn, R. A., & Wysocka, J. (2011) · Nature · doi:10.1038/nature09692 · Cited by 2,233 · 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
Smith, T. S., Heger, A., & Sudbery, I. M. (2017) · Genome Research · doi:10.1101/gr.209601.116 · Cited by 2,072 · see citing works
Similarity network fusion for aggregating data types on a genomic scale
Wang, B., Mezlini, A. M., Demir, F., Fiume, M., Tu, Z., Brudno, M., Haibe-Kains, B., & Goldenberg, A. (2014) · Nature Methods · doi:10.1038/nmeth.2810 · Cited by 2,036 · see citing works
Dixit, A., Parnas, O., Li, B., Chen, J., Fulco, C. P., Jerby-Arnon, L., Marjanovic, N. D., Dionne, D., Burks, T., Raychowdhury, R., et al. (2016) · Cell · doi:10.1016/j.cell.2016.11.038 · Cited by 1,863 · see citing works
Self-citationMolecular diversity and specializations among the cells of the adult mouse brain
Saunders, A., Macosko, E. Z., Wysoker, A., Goldman, M., Krienen, F. M., de Rivera, H., Bien, E., Baum, M., Bortolin, L., Wang, S., et al. (2018) · Cell · doi:10.1016/j.cell.2018.07.028 · Cited by 1,847 · see citing works
A Phase Separation Model for Transcriptional Control
Hnisz, D., Shrinivas, K., Young, R. A., Chakraborty, A. K., & Sharp, P. A. (2017) · Cell · doi:10.1016/j.cell.2017.02.007 · Cited by 1,753 · 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
Self-citationBlanpain, C., Lowry, W. E., Geoghegan, A., Polak, L., & Fuchs, E. (2004) · Cell · doi:10.1016/j.cell.2004.08.012 · Cited by 1,428 · 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
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 RNA-seq supports a developmental hierarchy in human oligodendroglioma
Tirosh, I., Venteicher, A. S., Hebert, C. M., Escalante, L. E., Patel, A. P., Yizhak, K., Fisher, J. M., Rodman, C., Mount, C., Filbin, M. G., et al. (2016) · Nature · doi:10.1038/nature20123 · Cited by 1,216 · see citing works
Self-citationSingle-Cell Multi-omic Integration Compares and Contrasts Features of Brain Cell Identity
Welch, J. D., Kozareva, V., Ferreira, A., Vanderburg, C., Martin, C., & Macosko, E. Z. (2019) · Cell · doi:10.1016/j.cell.2019.05.006 · Cited by 1,193 · see citing works
Long-range enhancer–promoter contacts in gene expression control
Schoenfelder, S., & Fraser, P. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-019-0128-0 · Cited by 1,102 · see citing works
Massively parallel single-nucleus RNA-seq with DroNc-seq
Habib, N., Avraham-Davidi, I., Basu, A., Burks, T., Shekhar, K., Hofree, M., Choudhury, S. R., Aguet, F., Gelfand, E., Ardlie, K., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4407 · Cited by 1,069 · see citing works
Self-citationDensely Interconnected Transcriptional Circuits Control Cell States in Human Hematopoiesis
Novershtern, N., Subramanian, A., Lawton, L. N., Mak, R. H., Haining, W. N., McConkey, M. E., Habib, N., Yosef, N., Chang, C. Y., Shay, T., et al. (2011) · Cell · doi:10.1016/j.cell.2011.01.004 · Cited by 942 · see citing works
Self-citationJoint 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
Latent Enhancers Activated by Stimulation in Differentiated Cells
Ostuni, R., Piccolo, V., Barozzi, I., Polletti, S., Termanini, A., Bonifacio, S., Curina, A., Prosperini, E., Ghisletti, S., & Natoli, G. (2013) · Cell · doi:10.1016/j.cell.2012.12.018 · Cited by 867 · see citing works
Characterization of cell fate probabilities in single-cell data with Palantir
Setty, M., Kiseliovas, V., Levine, J., Gayoso, A., Mazutis, L., & Pe’er, D. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0068-4 · Cited by 833 · 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
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
Chromatin state dynamics during blood formation
Lara-Astiaso, D., Weiner, A., Lorenzo-Vivas, E., Zaretsky, I., Jaitin, D. A., David, E., Keren-Shaul, H., Mildner, A., Winter, D., Jung, S., et al. (2014) · Science · doi:10.1126/science.1256271 · Cited by 776 · see citing works
Mouse Gli1 mutants are viable but have defects in SHH signaling in combination with a Gli2 mutation
Park, H. L., Bai, C., Platt, K. A., Matise, M. P., Beeghly, A., Hui, C., Nakashima, M., & Joyner, A. L. (2000) · Development · doi:10.1242/dev.127.8.1593 · Cited by 717 · see citing works
A Genome-wide Framework for Mapping Gene Regulation via Cellular Genetic Screens
Gasperini, M., Hill, A. J., McFaline-Figueroa, J. L., Martin, B., Kim, S., Zhang, M. D., Jackson, D., Leith, A., Schreiber, J., Noble, W. S., et al. (2019) · Cell · doi:10.1016/j.cell.2018.11.029 · Cited by 613 · see citing works
Div-Seq: Single-nucleus RNA-Seq reveals dynamics of rare adult newborn neurons
Habib, N., Li, Y., Heidenreich, M., Swiech, L., Avraham-Davidi, I., Trombetta, J. J., Hession, C., Zhang, F., & Regev, A. (2016) · Science · doi:10.1126/science.aad7038 · Cited by 601 · see citing works
Self-citationRabani, M., Levin, J. Z., Fan, L., Adiconis, X., Raychowdhury, R., Garber, M., Gnirke, A., Nusbaum, C., Hacohen, N., Friedman, N., et al. (2011) · Nature Biotechnology · doi:10.1038/nbt.1861 · Cited by 583 · see citing works
Self-citationEmerging interactions between skin stem cells and their niches
Hsu, Y., Li, L., & Fuchs, E. V. (2014) · Nature Medicine · doi:10.1038/nm.3643 · Cited by 563 · see citing works
Self-citationTcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skinPreprint
Merrill, B. J., Gat, U., DasGupta, R., & Fuchs, E. V. (2001) · Genes & Development · doi:10.1101/gad.891401 · Cited by 559 · see citing works
Hair follicle stem cells are specified and function in early skin morphogenesis
Nowak, J. A., Polak, L., Pasolli, H. A., & Fuchs, E. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.05.009 · Cited by 554 · see citing works
Genomic encoding of transcriptional burst kinetics
Larsson, A. J. M., Johnsson, P., Hagemann-Jensen, M., Hartmanis, L., Faridani, O. R., Reinius, B., Segerstolpe, Å., Rivera, C. M., Ren, B., & Sandberg, R. (2019) · Nature · doi:10.1038/s41586-018-0836-1 · Cited by 534 · see citing works
The Transcriptional Repressor ZEB1 Promotes Metastasis and Loss of Cell Polarity in Cancer
Spaderna, S., Schmalhofer, O., Wahlbuhl, M., Dimmler, A. W., Bauer, K., Sultan, A., Hlubek, F., Jung, A., Strand, D. J., Eger, A., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-5682 · Cited by 532 · see citing works
Mumbach, M. R., Satpathy, A. T., Boyle, E. A., Dai, C., Gowen, B. G., Cho, S. W., Nguyen, M. L., Rubin, A. J., Granja, J. M., Kazane, K. R., et al. (2017) · Nature Genetics · doi:10.1038/ng.3963 · Cited by 490 · see citing works
Single-cell analysis of mixed-lineage states leading to a binary cell fate choice
Olsson, A., Venkatasubramanian, M., Chaudhri, V. K., Aronow, B. J., Salomonis, N., Singh, H., & Grimes, H. L. (2016) · Nature · doi:10.1038/nature19348 · Cited by 476 · see citing works
From single-cell to cell-pool transcriptomes: Stochasticity in gene expression and RNA splicing
Marinov, G. K., Williams, B. A., McCue, K., Schroth, G. P., Gertz, J., Myers, R. M., & Wold, B. J. (2014) · Genome Research · doi:10.1101/gr.161034.113 · Cited by 468 · see citing works
Li, Q., Peterson, K. R., Fang, X., & Stamatoyannopoulos, G. (2002) · Blood · doi:10.1182/blood-2002-04-1104 · Cited by 456 · 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
Comprehensive analysis of single cell ATAC-seq data with SnapATAC
Fang, R., Preissl, S., Li, Y., Hou, X., Lucero, J., Wang, X., Motamedi, A., Shiau, A. K., Zhou, X., Xie, F., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21583-9 · Cited by 455 · 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
Self-citationJoost, S., Zeisel, A., Jacob, T., Sun, X., La Manno, G., Lönnerberg, P., Linnarsson, S., & Kasper, M. (2016) · Cell Systems · doi:10.1016/j.cels.2016.08.010 · Cited by 429 · 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
Spatial organization within a niche as a determinant of stem-cell fate
Rompolas, P., Mesa, K. R., & Greco, V. (2013) · Nature · doi:10.1038/nature12602 · Cited by 398 · see citing works
Live imaging of stem cell and progeny behaviour in physiological hair-follicle regeneration
Rompolas, P., Deschene, E. R., Zito, G., Gonzalez, D. G., Saotome, I., Haberman, A. M., & Greco, V. (2012) · Nature · doi:10.1038/nature11218 · Cited by 379 · see citing works
Pioneer factors govern super-enhancer dynamics in stem cell plasticity and lineage choice
Adam, R. C., Yang, H., Rockowitz, S., Larsen, S. B., Nikolova, M., Oristian, D., Polak, L., Kadaja, M., Asare, A., Zheng, D., et al. (2015) · Nature · doi:10.1038/nature14289 · Cited by 376 · see citing works
An ultra high-throughput method for single-cell joint analysis of open chromatin and transcriptome
Zhu, C., Yu, M., Huang, H., Juric, I., Abnousi, A., Hu, R., Lucero, J., Behrens, M. M., Hu, M., & Ren, B. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0323-x · Cited by 344 · 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
Pan, Y., Lin, M., Tian, X., Cheng, H., Gridley, T., Shen, J., & Kopan, R. (2004) · Developmental Cell · doi:10.1016/j.devcel.2004.09.014 · Cited by 326 · see citing works
Sonic hedgehog-dependent activation of Gli2 is essential for embryonic hair follicle developmentPreprint
Mill, P., Mo, R., Fu, H. E., Grachtchouk, M. A., Kim, P. C. W., Dlugosz, A. A., & Hui, C. (2003) · Genes & Development · doi:10.1101/gad.1038103 · Cited by 326 · see citing works
The Molecular Anatomy of Mouse Skin during Hair Growth and Rest
Joost, S., Annusver, K., Jacob, T., Sun, X., Dalessandri, T., Sivan, U., Sequeira, I., Sandberg, R., & Kasper, M. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.01.012 · Cited by 312 · see citing works
Sequencing thousands of single-cell genomes with combinatorial indexing
Vitak, S. A., Torkenczy, K. A., Rosenkrantz, J. L., Fields, A. J., Christiansen, L., Wong, M. H., Carbone, L., Steemers, F. J., & Adey, A. (2017) · Nature Methods · doi:10.1038/nmeth.4154 · Cited by 294 · see citing works
WNT Signaling in the Control of Hair Growth and Structure
Millar, S. E., Willert, K., Salinas, P. C., Roelink, H., Nusse, R., Sussman, D. J., & Barsh, G. S. (1999) · Developmental Biology · doi:10.1006/dbio.1998.9140 · Cited by 292 · see citing works
Hoxc13 mutant mice lack external hairPreprint
Godwin, A. R. F., & Capecchi, M. R. (1998) · Genes & Development · doi:10.1101/gad.12.1.11 · Cited by 252 · see citing works
Epithelial-Mesenchymal Micro-niches Govern Stem Cell Lineage Choices
Yang, H., Adam, R. C., Ge, Y., Hua, Z. L., & Fuchs, E. V. (2017) · Cell · doi:10.1016/j.cell.2017.03.038 · Cited by 249 · see citing works
Identity Noise and Adipogenic Traits Characterize Dermal Fibroblast Aging
Salzer, M. C., Lafzi, A., Berenguer, A., Youssif, C., Castellanos‐Martín, A., Solanas, G., Peixoto, F. O., Attolini, C. S., Prats, N., Aguilera, M., et al. (2018) · Cell · doi:10.1016/j.cell.2018.10.012 · Cited by 243 · see citing works
Epigenomic State Transitions Characterize Tumor Progression in Mouse Lung Adenocarcinoma
LaFave, L. M., Kartha, V. K., Ma, S., Meli, K., Priore, I. S. D., Lareau, C. A., Naranjo, S., Westcott, P. M. K., Duarte, F. M., Sankar, V., et al. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.06.006 · Cited by 207 · see citing works
Self-citationLien, W.-H., Guo, X., Polak, L., Lawton, L. N., Young, R. A., Zheng, D., & Fuchs, E. (2011) · Cell Stem Cell · doi:10.1016/j.stem.2011.07.015 · Cited by 199 · see citing works
Joost, S., Jacob, T., Sun, X., Annusver, K., Manno, G. L., Sur, I., & Kasper, M. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.09.059 · Cited by 196 · see citing works
Homeostasis of protein and mRNA concentrations in growing cells
Lin, J., & Amir, A. (2018) · Nature Communications · doi:10.1038/s41467-018-06714-z · Cited by 180 · see citing works
BMP Signaling and Its pSMAD1/5 Target Genes Differentially Regulate Hair Follicle Stem Cell Lineages
Genander, M., Cook, P. J., Ramsköld, D., Keyes, B. E., Mertz, A. F., Sandberg, R., & Fuchs, E. V. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.09.009 · Cited by 174 · see citing works
Legué, E., & Nicolas, J.-F. (2005) · Development · doi:10.1242/dev.01975 · Cited by 169 · see citing works
Single-cell and single-molecule epigenomics to uncover genome regulation at unprecedented resolution
Shema, E., Bernstein, B., & Buenrostro, J. D. (2018) · Nature Genetics · doi:10.1038/s41588-018-0290-x · Cited by 164 · see citing works
Self-citationA Genome-wide Framework for Mapping Gene Regulation via Cellular Genetic Screens
Gasperini, M. J., Hill, A. J., McFaline‐Figueroa, J. L., Martin, B., Kim, S., Zhang, M. D., Jackson, D., Leith, A., Schreiber, J. M., Noble, W. S., et al. (2019) · Cell · doi:10.1016/j.cell.2019.02.027 · Cited by 150 · 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
Cohen, I., Zhao, D., Bar, C., Valdés, V. J., Dauber-Decker, K. L., Nguyen, M. B., Nakayama, M., Rendl, M., Bickmore, W. A., Koseki, H., et al. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.04.005 · Cited by 126 · see citing works
Systematic comparative analysis of single cell RNA-sequencing methodsPreprint
Ding, J., Adiconis, X., Simmons, S., Kowalczyk, M. S., Hession, C. C., Marjanovic, N. D., Hughes, T. K., Wadsworth, M. H., Burks, T., Nguyễn, L., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/632216 · Cited by 106 · see citing works
Self-citationZhang, B., Tsai, P.-C., Gonzalez-Celeiro, M., Chung, O., Boumard, B., Perdigoto, C. N., Ezhkova, E., & Hsu, Y. (2016) · Genes & Development · doi:10.1101/gad.285429.116 · Cited by 97 · see citing works
Self-citationCo-ChIP enables genome-wide mapping of histone mark co-occurrence at single-molecule resolution
Weiner, A., Lara‐Astiaso, D., Krupalnik, V., Gafni, O., David, E., Winter, D. R., Hanna, J. H., & Amit, I. (2016) · Nature Biotechnology · doi:10.1038/nbt.3652 · Cited by 88 · see citing works
González, A. J., Setty, M. N., & Leslie, C. S. (2015) · Nature Genetics · doi:10.1038/ng.3402 · Cited by 82 · see citing works
Single Cell and Open Chromatin Analysis Reveals Molecular Origin of Epidermal Cells of the Skin
Fan, X., Wang, D., Burgmaier, J. E., Teng, Y., Romano, R., Sinha, S., & Yi, R. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.08.010 · Cited by 68 · see citing works
Accurate loop calling for 3D genomic data with cLoops
Cao, Y., Chen, Z., Chen, X., Ai, D., Chen, G., McDermott, J., Huang, Y., Guo, X., & Han, J. J. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz651 · Cited by 66 · see citing works
Huang, D., Lin, Y., Jan, P. C., Hwang, Y., Liang, S., Peng, Y. G., Huang, C., Wu, H., & Lin, C. (2007) · The Journal of Pathology · doi:10.1002/path.2299 · Cited by 57 · see citing works
Emerging roles of transit-amplifying cells in tissue regeneration and cancer
Zhang, B., & Hsu, Y.-C. (2017) · Wiley Interdisciplinary Reviews: Developmental Biology · doi:10.1002/wdev.282 · Cited by 48 · see citing works
Self-citationSnapATAC: 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
Flexible fate determination ensures robust differentiation in the hair follicle
Xin, T., Gonzalez, D. G., Rompolas, P., & Greco, V. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0232-y · Cited by 42 · see citing works
Single Cell and Open Chromatin Analysis Reveals Molecular Origin of Epidermal Cells of the Skin
Fan, X., Wang, D., Burgmaier, J. E., Teng, Y., Romano, R., Sinha, S., & Yi, R. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.09.019 · Cited by 17 · see citing works
Multi-omics single-cell analysis
Rusk, N. (2019) · Nature Methods · doi:10.1038/s41592-019-0519-3 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Integrated analysis of multimodal single-cell data
Hao, Y., Hao, S., Andersen-Nissen, E., Mauck, W. M., Zheng, S., Butler, A., Lee, M. J., Wilk, A. J., Darby, C., Zagar, M., et al. (2020) · doi:10.1101/2020.10.12.335331 · Cited by 15,508 · see citing works
Dictionary learning for integrative, multimodal and scalable single-cell analysis
Hao, Y., Stuart, T., Kowalski, M. H., Choudhary, S., Hoffman, P., Hartman, A., Srivastava, A., Molla, G., Madad, S., Fernandez-Granda, C., et al. (2024) · Nature Biotechnology · doi:10.1038/s41587-023-01767-y · Cited by 5,631 · see citing works
Microglia states and nomenclature: A field at its crossroads
Paolicelli, R. C., Sierra, A., Stevens, B., Tremblay, M.-E., Aguzzi, A., Ajami, B., Amit, I., Audinat, E., Bechmann, I., Bennett, M., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.10.020 · Cited by 1,973 · see citing works
Self-citationSingle-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
Self-citationMethods 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
Deep learning and alignment of spatially resolved single-cell transcriptomes with Tangram
Biancalani, T., Scalia, G., Buffoni, L., Avasthi, R., Lu, Z., Sanger, A., Tokcan, N., Vanderburg, C. R., Segerstolpe, Å., Zhang, M., et al. (2021) · Nature Methods · doi:10.1038/s41592-021-01264-7 · Cited by 931 · see citing works
Self-citationFleming, S. J., Chaffin, M. D., Arduini, A., Akkad, A.-D., Banks, E., Marioni, J. C., Philippakis, A. A., Ellinor, P. T., & Babadi, M. (2023) · Nature Methods · doi:10.1038/s41592-023-01943-7 · Cited by 867 · 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
SCENIC+: 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
Large-scale foundation model on single-cell transcriptomics
Hao, M., Gong, J., Zeng, X., Liu, C., Guo, Y., Cheng, X., Wang, T., Ma, J., Zhang, X., & Song, L. (2024) · Nature Methods · doi:10.1038/s41592-024-02305-7 · Cited by 628 · see citing works
Multi-omics single-cell data integration and regulatory inference with graph-linked embedding
Cao, Z.-J., & Gao, G. (2022) · Nature Biotechnology · doi:10.1038/s41587-022-01284-4 · Cited by 616 · 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
Self-citationTrevino, A. E., Müller, F., Andersen, J., Sundaram, L., Kathiria, A., Shcherbina, A., Farh, K., Chang, H. Y., Pașca, A. M., Kundaje, A., et al. (2021) · Cell · doi:10.1016/j.cell.2021.07.039 · Cited by 478 · see citing works
Spatial epigenome–transcriptome co-profiling of mammalian tissues
Zhang, D., Deng, Y., Kukanja, P., Agirre, E., Bartosovic, M., Dong, M., Ma, C., Ma, S., Su, G., Bao, S., et al. (2023) · Nature · doi:10.1038/s41586-023-05795-1 · Cited by 483 · see citing works
Self-citationGene regulatory network inference in the era of single-cell multi-omics
Badia-i-Mompel, P., Wessels, L., Müller‐Dott, S., Trimbour, R., Flores, R. O. R., Argelaguet, R., & Sáez-Rodríguez, J. (2023) · Nature Reviews Genetics · doi:10.1038/s41576-023-00618-5 · Cited by 475 · see citing works
Computational principles and challenges in single-cell data integration
Argelaguet, R., Cuomo, A. S. E., Stegle, O., & Marioni, J. C. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-00895-7 · Cited by 472 · see citing works
Molecular logic of cellular diversification in the mouse cerebral cortex
Di Bella, D. J., Habibi, E., Stickels, R. R., Scalia, G., Brown, J., Yadollahpour, P., Yang, S. M., Abbate, C., Biancalani, T., Macosko, E. Z., et al. (2021) · Nature · doi:10.1038/s41586-021-03670-5 · Cited by 464 · see citing works
Self-citationMapping transcriptomic vector fields of single cells
Qiu, X., Zhang, Y., Martin-Rufino, J. D., Weng, C., Hosseinzadeh, S., Yang, D., Pogson, A. N., Hein, M. Y., Min, K. H., Wang, L., et al. (2022) · Cell · doi:10.1016/j.cell.2021.12.045 · Cited by 436 · see citing works
Applications of single-cell RNA sequencing in drug discovery and development
de Sande, B. V., Lee, J. S., Mutasa-Gottgens, E., Naughton, B. J., Bacon, W., Manning, J. R., Wang, Y., Pollard, J. R., Mendez, M., Hill, J., et al. (2023) · Nature Reviews Drug Discovery · doi:10.1038/s41573-023-00688-4 · Cited by 441 · see citing works
Zhu, Y., Ouyang, Z., Du, H., Wang, M., Wang, J., Sun, H., Kong, L., Xu, Q., Ma, H., & Sun, Y. (2022) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2022.08.022 · Cited by 422 · see citing works
Single-nucleus cross-tissue molecular reference maps toward understanding disease gene function
Eraslan, G., Drokhlyansky, E., Anand, S. K., Fiškin, E., Subramanian, A., Slyper, M., Wang, J., Wittenberghe, N. V., Rouhana, J. M., Waldman, J., et al. (2022) · Science · doi:10.1126/science.abl4290 · Cited by 396 · see citing works
Self-citationSpatial-CUT&Tag: Spatially resolved chromatin modification profiling at the cellular level
Deng, Y., Bartosovic, M., Kukanja, P., Zhang, D., Liu, Y., Su, G., Enninful, A., Bai, Z., Castelo-Branco, G., & Fan, R. (2022) · Science · doi:10.1126/science.abg7216 · Cited by 393 · see citing works
The Specious Art of Single-Cell Genomics
Chari, T., & Pachter, L. (2021) · doi:10.1101/2021.08.25.457696 · Cited by 379 · see citing works
Cis-regulatory sequences in plants: Their importance, discovery, and future challenges
Schmitz, R. J., Grotewold, E., & Stam, M. E. (2021) · The Plant Cell · doi:10.1093/plcell/koab281 · Cited by 358 · see citing works
Single-cell proteomics enabled by next-generation sequencing or mass spectrometry
Bennett, H. M., Stephenson, W., Rose, C. M., & Darmanis, S. (2023) · Nature Methods · doi:10.1038/s41592-023-01791-5 · Cited by 351 · see citing works
Lineage tracing reveals the phylodynamics, plasticity, and paths of tumor evolution
Yang, D., Jones, M. G., Naranjo, S., Rideout, W. M., Min, K. H., Ho, R., Wu, W., Replogle, J. M., Page, J. L., Quinn, J. J., et al. (2022) · Cell · doi:10.1016/j.cell.2022.04.015 · Cited by 333 · see citing works
Epigenetic regulation of T cell exhaustion
Belk, J. A., Dániel, B., & Satpathy, A. T. (2022) · Nature Immunology · doi:10.1038/s41590-022-01224-z · Cited by 334 · see citing works
Where Are the Disease-Associated eQTLs?
Umans, B. D., Battle, A., & Gilad, Y. (2021) · Trends in Genetics · doi:10.1016/j.tig.2020.08.009 · Cited by 296 · see citing works
Epigenetic memory of coronavirus infection in innate immune cells and their progenitors
Cheong, J.-G., Ravishankar, A., Sharma, S., Parkhurst, C. N., Grassmann, S. A., Wingert, C. K., Laurent, P., Ma, S., Paddock, L., Miranda, I. C., et al. (2023) · Cell · doi:10.1016/j.cell.2023.07.019 · Cited by 309 · see citing works
Self-citationRNA velocity—current challenges and future perspectives
Bergen, V., Soldatov, R. A., Kharchenko, P. V., & Theis, F. J. (2021) · Molecular Systems Biology · doi:10.15252/msb.202110282 · Cited by 271 · see citing works
Datlinger, P., Rendeiro, A. F., Boenke, T., Senekowitsch, M., Krausgruber, T., Barreca, D., & Bock, C. (2021) · Nature Methods · doi:10.1038/s41592-021-01153-z · Cited by 261 · see citing works
Chromatin profiles classify castration-resistant prostate cancers suggesting therapeutic targets
Tang, F., Xu, D., Wang, S., Wong, C. K., Martinez‐Fundichely, A., Lee, C. J., Cohen, S. M., Park, J., Hill, C. E., Eng, K. W., et al. (2022) · Science · doi:10.1126/science.abe1505 · Cited by 261 · see citing works
Swanson, E., Lord, C., Reading, J., Heubeck, A. T., Genge, P. C., Thomson, Z., Weiss, M. D., Li, X.-J., Savage, A. K., Green, R. R., et al. (2021) · eLife · doi:10.7554/elife.63632 · Cited by 267 · see citing works
Deep learning-based approaches for multi-omics data integration and analysis
Ballard, J. L., Wang, Z., Li, W., Shen, L., & Long, Q. (2024) · BioData Mining · doi:10.1186/s13040-024-00391-z · Cited by 287 · see citing works
Epigenetic scars of CD8+ T cell exhaustion persist after cure of chronic infection in humans
Yates, K. B., Tonnerre, P., Martin, G. E., Gerdemann, U., Abosy, R. A., Comstock, D. E., Weiss, S. A., Wolski, D., Tully, D. C., Chung, R. T., et al. (2021) · Nature Immunology · doi:10.1038/s41590-021-00979-1 · Cited by 253 · see citing works
Characterizing cis-regulatory elements using single-cell epigenomics
Preissl, S., Gaulton, K. J., & Ren, B. (2023) · Nature Reviews Genetics · doi:10.1038/s41576-022-00509-1 · Cited by 251 · see citing works
Functional inference of gene regulation using single-cell multi-omics
Kartha, V. K., Duarte, F. M., Hu, Y., Ma, S., Chew, J. G., Lareau, C. A., Earl, A., Burkett, Z. D., Kohlway, A. S., Lebofsky, R., et al. (2022) · Cell Genomics · doi:10.1016/j.xgen.2022.100166 · Cited by 224 · see citing works
Self-citationMulti-omics integration in the age of million single-cell data
Miao, Z., Humphreys, B. D., McMahon, A. P., & Kim, J. (2021) · Nature Reviews Nephrology · doi:10.1038/s41581-021-00463-x · Cited by 249 · see citing works
Uzquiano, A., Kedaigle, A. J., Pigoni, M., Paulsen, B. D. S., Adiconis, X., Kim, K., Faits, T., Nagaraja, S., Antón-Bolaños, N., Gerhardinger, C., et al. (2022) · Cell · doi:10.1016/j.cell.2022.09.010 · Cited by 250 · see citing works
Self-citationA Review of Single-Cell RNA-Seq Annotation, Integration, and Cell–Cell Communication
Cheng, C., Chen, W., Jin, H., & Chen, X. '. (2023) · Cells · doi:10.3390/cells12151970 · Cited by 237 · see citing works
Microfluidics-free single-cell genomics with templated emulsification
Clark, I. C., Fontanez, K. M., Meltzer, R. H., Xue, Y., Hayford, C. E., May-Zhang, A. A., D’Amato, C., Osman, A., Zhang, J. Q., Hettige, P., et al. (2023) · Nature Biotechnology · doi:10.1038/s41587-023-01685-z · Cited by 225 · see citing works
A transcription factor atlas of directed differentiation
Joung, J., Ma, S., Tay, T., Geiger-Schuller, K., Kirchgatterer, P. C., Verdine, V. K., Guo, B., Arias-García, M. A., Allen, W. E., Singh, A., et al. (2023) · Cell · doi:10.1016/j.cell.2022.11.026 · Cited by 223 · see citing works
Self-citationSEACells infers transcriptional and epigenomic cellular states from single-cell genomics data
Persad, S., Choo, Z.-N., Dien, C., Sohail, N., Masilionis, I., Chaligné, R., Nawy, T., Brown, C. C., Sharma, R., Pe’er, I., et al. (2023) · Nature Biotechnology · doi:10.1038/s41587-023-01716-9 · Cited by 222 · see citing works
Gene regulation by gonadal hormone receptors underlies brain sex differences
Gegenhuber, B., Wu, M. V., Bronstein, R., & Tollkuhn, J. (2022) · Nature · doi:10.1038/s41586-022-04686-1 · Cited by 221 · see citing works
Advances and Opportunities in Single-Cell Transcriptomics for Plant Research
Seyfferth, C., Renema, J., Wendrich, J. R., Eekhout, T., Seurinck, R., Vandamme, N., Blob, B., Saeys, Y., Helariutta, Y., Birnbaum, K. D., et al. (2021) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-081720-010120 · Cited by 216 · see citing works
Liu, I., Jiang, L., Samuelsson, E. R., Salas, S. M., Beck, A., Hack, O. A., Jeong, D., Shaw, M. L., Englinger, B., LaBelle, J. J., et al. (2022) · Nature Genetics · doi:10.1038/s41588-022-01236-3 · Cited by 213 · see citing works
Li, H., Dixon, E. E., Wu, H., & Humphreys, B. D. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2022.09.026 · Cited by 211 · see citing works
Epigenetic regulation during cancer transitions across 11 tumour types
Terekhanova, N. V., Karpova, A. Y., Liang, W.-W., Strzalkowski, A. J., Chen, S., Li, Y., Southard-Smith, A. N., Iglesia, M. D., Wendl, M. C., Jayasinghe, R. G., et al. (2023) · Nature · doi:10.1038/s41586-023-06682-5 · Cited by 205 · 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
Dissecting the treatment-naive ecosystem of human melanoma brain metastasis
Biermann, J., Melms, J. C., Amin, A. D., Wang, Y., Caprio, L., Karz, A., Tagore, S., Barrera, I., Ibarra-Arellano, M. A., Andreatta, M., et al. (2022) · Cell · doi:10.1016/j.cell.2022.06.007 · Cited by 203 · see citing works
Wilson, P. C., Muto, Y., Wu, H., Karihaloo, A. K., Waikar, S. S., & Humphreys, B. D. (2022) · Nature Communications · doi:10.1038/s41467-022-32972-z · Cited by 190 · see citing works
Human and mouse trigeminal ganglia cell atlas implicates multiple cell types in migraine
Yang, L., Xu, M., Bhuiyan, S. A., Li, J., Zhao, J., Cohrs, R. J., Susterich, J. T., Signorelli, S., Green, U., Stone, J. R., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.03.003 · Cited by 188 · see citing works
Advances in single-cell omics and multiomics for high-resolution molecular profiling
Lim, J., Park, C., Kim, M., Kim, H., Kim, J., & Lee, D.-S. (2024) · Experimental & Molecular Medicine · doi:10.1038/s12276-024-01186-2 · Cited by 193 · see citing works
Statistical and machine learning methods for spatially resolved transcriptomics data analysis
Zeng, Z., Li, Y., Li, Y., & Luo, Y. (2022) · Genome Biology · doi:10.1186/s13059-022-02653-7 · Cited by 186 · see citing works
A fast, scalable and versatile tool for analysis of single-cell omics data
Zhang, K., Zemke, N. R., Armand, E. J., & Ren, B. (2024) · Nature Methods · doi:10.1038/s41592-023-02139-9 · Cited by 185 · see citing works
Enhancers in disease: molecular basis and emerging treatment strategies
Claringbould, A., & Zaugg, J. B. (2021) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2021.07.012 · Cited by 171 · see citing works
FOXA2 drives lineage plasticity and KIT pathway activation in neuroendocrine prostate cancer
Han, M., Li, F., Zhang, Y., Dai, P., He, J., Li, Y., Zhu, Y., Zheng, J., Huang, H., Bai, F., et al. (2022) · Cancer Cell · doi:10.1016/j.ccell.2022.10.011 · Cited by 166 · see citing works
Linking genome structures to functions by simultaneous single-cell Hi-C and RNA-seq
Liu, Z., Chen, Y., Xia, Q., Liu, M., Xu, H., Chi, Y., Deng, Y., & Xing, D. (2023) · Science · doi:10.1126/science.adg3797 · Cited by 169 · see citing works
Single nucleus multi-omics identifies human cortical cell regulatory genome diversity
Luo, C., Liu, H., Xie, F., Armand, E. J., Siletti, K., Bakken, T. E., Fang, R., Doyle, W. I., Stuart, T., Hodge, R. D., et al. (2022) · Cell Genomics · doi:10.1016/j.xgen.2022.100107 · Cited by 167 · 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
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
Fleming, S. J., Chaffin, M. D., Arduini, A., Akkad, A.-D., Banks, E., Marioni, J. C., Philippakis, A. A., Ellinor, P. T., & Babadi, M. (2019) · doi:10.1101/791699 · Cited by 164 · see citing works
BABEL enables cross-modality translation between multiomic profiles at single-cell resolution
Wu, K., Yost, K. E., Chang, H. Y., & Zou, J. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2023070118 · Cited by 164 · see citing works
The Human Cell Atlas from a cell census to a unified foundation model
Rood, J., Wynne, S., Robson, L., Hupalowska, A., Randell, J., Teichmann, S. A., & Regev, A. (2024) · Nature · doi:10.1038/s41586-024-08338-4 · Cited by 168 · see citing works
Self-citationLi, L., Bowling, S., McGeary, S. E., Yu, Q., Lemke, B., Alcedo, K., Jia, Y., Liu, X., Ferreira, M., Klein, A. M., et al. (2023) · Cell · doi:10.1016/j.cell.2023.09.019 · Cited by 167 · see citing works
Turner, A. W., Hu, S. S., Mosquera, J. V., Feng, W., Hodonsky, C. J., Wong, D., Auguste, G. E., Song, Y., Sol‐Church, K., Farber, E., et al. (2022) · Nature Genetics · doi:10.1038/s41588-022-01069-0 · Cited by 151 · see citing works
Mapping cells through time and space with moscot
Klein, D., Palla, G., Lange, M., Klein, M., Piran, Z., Gander, M., Meng-Papaxanthos, L., Sterr, M., Saber, L., Jing, C., et al. (2025) · Nature · doi:10.1038/s41586-024-08453-2 · Cited by 202 · see citing works
Chromatin accessibility: methods, mechanisms, and biological insights
Mansisidor, A., & Risca, V. I. (2022) · Nucleus · doi:10.1080/19491034.2022.2143106 · Cited by 150 · see citing works
Multimodal single-cell chromatin analysis with SignacPreprint
Stuart, T., Srivastava, A., Lareau, C. A., & Satija, R. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.09.373613 · Cited by 150 · see citing works
Self-citationA mixture-of-experts deep generative model for integrated analysis of single-cell multiomics data
Minoura, K., Abe, K., Nam, H., Nishikawa, H., & Shimamura, T. (2021) · Cell Reports Methods · doi:10.1016/j.crmeth.2021.100071 · Cited by 147 · see citing works
Joint single-cell measurements of nuclear proteins and RNA in vivo
Chung, H., Parkhurst, C. N., Magee, E. M., Phillips, D., Habibi, E., Chen, F., Yeung, B. Z., Waldman, J., Artis, D., & Regev, A. (2021) · Nature Methods · doi:10.1038/s41592-021-01278-1 · Cited by 144 · see citing works
Self-citationRecent 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
A multi-omic single-cell landscape of human gynecologic malignancies
Regner, M. J., Wiśniewska, K., García‐Recio, S., Thennavan, A., Méndez-Giráldez, R., Malladi, V. S., Hawkins, G. M., Parker, J. S., Perou, C. M., Bae-Jump, V. L., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.10.013 · Cited by 139 · see citing works
Chen, A. F., Parks, B., Kathiria, A. S., Ober-Reynolds, B., Goronzy, J. J., & Greenleaf, W. J. (2022) · Nature Methods · doi:10.1038/s41592-022-01461-y · Cited by 139 · see citing works
Lyu, P., Hoang, T. V., Santiago, C. P., Thomas, E. D., Timms, A. E., Appel, H., Gimmen, M. Y., Le, N., Jiang, L., Kim, D. W., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109994 · Cited by 137 · see citing works
Clustering of single-cell multi-omics data with a multimodal deep learning method
Lin, X., Tian, T., Wei, Z., & Hakonarson, H. (2022) · Nature Communications · doi:10.1038/s41467-022-35031-9 · Cited by 135 · see citing works
Li, C., Virgilio, M. C., Collins, K. L., & Welch, J. D. (2023) · Nature Biotechnology · doi:10.1038/s41587-022-01476-y · Cited by 130 · see citing works
Taavitsainen, S., Engedal, N., Cao, S., Handle, F., Erickson, A. M., Preković, S., Wetterskog, D., Tolonen, T. T., Vuorinen, E. M., Kiviaho, A., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25624-1 · Cited by 124 · see citing works
Towards multimodal foundation models in molecular cell biology
Cui, H., Tejada-Lapuerta, A., Brbić, M., Sáez-Rodríguez, J., Cristea, S., Goodarzi, H., Lotfollahi, M., Theis, F. J., & Wang, B. (2025) · Nature · doi:10.1038/s41586-025-08710-y · Cited by 131 · see citing works
Genetic and epigenetic coordination of cortical interneuron development
Allaway, K. C., Gabitto, M. I., Wapinski, O. L., Saldi, G.-A., Wang, C., Bandler, R. C., Wu, S. J., Bonneau, R., & Fishell, G. (2021) · Nature · doi:10.1038/s41586-021-03933-1 · Cited by 122 · see citing works
Jiang, F., Zhou, X., Qian, Y., Zhu, M., Wang, L., Li, Z., Shen, Q., Wang, M., Qu, F., Cui, G., et al. (2023) · Nature Methods · doi:10.1038/s41592-023-01884-1 · Cited by 127 · see citing works
Multi-omic profiling of the developing human cerebral cortex at the single-cell level
Zhu, K., Bendl, J. M., Rahman, S., Vicari, J. M., Coleman, C., Clarence, T., Latouche, O., Tsankova, N. M., Li, A., Brennand, K., et al. (2023) · Science Advances · doi:10.1126/sciadv.adg3754 · Cited by 116 · see citing works
Single-cell technologies: From research to application
Wen, L., Li, G., Huang, T., Geng, W., Pei, H., Yang, J., Zhu, M., Zhang, P., Hou, R., Tian, G., et al. (2022) · The Innovation · doi:10.1016/j.xinn.2022.100342 · Cited by 118 · see citing works
Xu, W. Q., Yang, W., Zhang, Y., Chen, Y., Hong, N., Zhang, Q., Wang, X. J., Hu, Y., Song, K., Jin, W., et al. (2022) · Nature Methods · doi:10.1038/s41592-022-01601-4 · Cited by 115 · see citing works
Self-citationLarge Scale Foundation Model on Single-cell Transcriptomics
Hao, M., Gong, J., Zeng, X., Liu, C., Guo, Y., Cheng, X., Wang, T., Ma, J., Song, L., & Zhang, X. (2023) · doi:10.1101/2023.05.29.542705 · Cited by 639 · see citing works
Dictys: dynamic gene regulatory network dissects developmental continuum with single-cell multiomics
Wang, L., Trasanidis, N., Wu, T., Dong, G., Hu, M., Bauer, D. E., & Pinello, L. (2023) · Nature Methods · doi:10.1038/s41592-023-01971-3 · Cited by 117 · see citing works
Single cell cancer epigenetics
Casado-Peláez, M., Bueno-Costa, A., & Esteller, M. (2022) · Trends in cancer · doi:10.1016/j.trecan.2022.06.005 · Cited by 113 · see citing works
Computational strategies for single-cell multi-omics integration
Adossa, N. A., Khan, S., Rytkönen, K. T., & Elo, L. L. (2021) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2021.04.060 · Cited by 106 · see citing works
Ameen, M., Sundaram, L., Shen, M., Banerjee, A., Kundu, S., Nair, S., Shcherbina, A., Gu, M., Wilson, K. D., Varadarajan, A., et al. (2022) · Cell · doi:10.1016/j.cell.2022.11.028 · Cited by 109 · see citing works
Solid-phase capture and profiling of open chromatin by spatial ATAC
Llorens-Bobadilla, E., Zamboni, M., Marklund, M., Bhalla, N., Chen, X.-S., Hartman, J., Frisén, J., & Ståhl, P. L. (2023) · Nature Biotechnology · doi:10.1038/s41587-022-01603-9 · Cited by 94 · 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
Thibodeau, A., Eroğlu, A., McGinnis, C. S., Lawlor, N. T., Nehar-Belaid, D., Kursawe, R., Marcheş, R., Conrad, D. N., Kuchel, G. A., Gartner, Z. J., et al. (2021) · Genome biology · doi:10.1186/s13059-021-02469-x · Cited by 98 · see citing works
Gene regulatory network reconstruction: harnessing the power of single-cell multi-omic data
Kim, D. J., Tran, A., Kim, H. J., Lin, Y., Yang, J. Y. H., & Yang, P. (2023) · npj Systems Biology and Applications · doi:10.1038/s41540-023-00312-6 · Cited by 110 · see citing works
A deep generative model for multi-view profiling of single-cell RNA-seq and ATAC-seq data
Li, G., Fu, S., Wang, S., Zhu, C., Duan, B., Tang, C., Chen, X., Chuai, G., Wang, P. Q., & Liu, Q. (2022) · Genome biology · doi:10.1186/s13059-021-02595-6 · Cited by 100 · see citing works
Integrated analysis of multimodal single-cell data with structural similarity
Cao, Y., Fu, L., Wu, J., Peng, Q., Nie, Q. H., Zhang, J., & Xie, X. S. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac781 · Cited by 106 · see citing works
A generalization of t-SNE and UMAP to single-cell multimodal omics
Do, V. H., & Canzar, S. (2021) · Genome biology · doi:10.1186/s13059-021-02356-5 · Cited by 102 · see citing works
Le, J., Dian, Y., Zhao, D., Guo, Z., Luo, Z., Chen, X., Zeng, F., & Deng, G. (2025) · Molecular Cancer · doi:10.1186/s12943-025-02426-3 · Cited by 109 · see citing works
Wang, M., Song, W., Chen, M., Wang, Q., Zhou, X., Xu, P., Krek, A., Yoon, Y., Ho, L., Orr, M. E., et al. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00517-z · Cited by 100 · see citing works
Self-citation
- Authors
- Ma, S., Zhang, B., LaFave, L. M., Earl, A. S., Chiang, Z., Hu, Y., Ding, J., Brack, A., Kartha, V. K., Tay, T., Law, T., Lareau, C., Hsu, Y.-C., Regev, A., & Buenrostro, J. D.
- Affiliations
- Broad Institute (US)
- Harvard University (US)
- Corresponding author
- Regev, Aviv
- Buenrostro, Jason D.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2020-11
- Volume
- 183
- Issue
- 4
- Pages
- 1103-1116.e20
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC7669735
- OpenAlex
- W3093858607
- Cited by
- 1,146
- References
- 95
- Citations by year
- 2026: 223 · 2025: 224 · 2024: 215 · 2023: 183 · 2022: 175 · 2021: 107 · 2020: 15 · 2019: 2 · 2013: 1
- FWCI
- 39.26
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 376 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- Funders
- Chan Zuckerberg Initiative
- Klarman Cell Observatory, Broad Institute
- National Institutes of Health
- Richard and Susan Smith Family Foundation
- Allen Institute
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- chromatin accessibility, single-cell multi-omics, cis-regulatory interactions, super-enhancers, cell fate prediction, lineage commitment, mouse skin, cell differentiation
- MeSH terms
- Animals, Cell Differentiation, Cell Line, Chromatin, Enhancer Elements, Genetic, Female, Gene Expression Regulation, Histones, Mice, Inbred C57BL, Protein Processing, Post-Translational, RNA, Cell Lineage, Gene Expression Profiling, Single-Cell Analysis
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