Single-cell multi-omics sequencing of mouse early embryos and embryonic stem cells
Open accessAbstract
Single-cell epigenome sequencing techniques have recently been developed. However, the combination of different layers of epigenome sequencing in an individual cell has not yet been achieved. Here, we developed a single-cell multi-omics sequencing technology (single-cell COOL-seq) that can analyze the chromatin state/nucleosome positioning, DNA methylation, copy number variation and ploidy simultaneously from the same individual mammalian cell. We used this method to analyze the reprogramming of the chromatin state and DNA methylation in mouse preimplantation embryos. We found that within < 12 h of fertilization, each individual cell undergoes global genome demethylation together with the rapid and global reprogramming of both maternal and paternal genomes to a highly opened chromatin state. This was followed by decreased openness after the late zygote stage. Furthermore, from the late zygote to the 4-cell stage, the residual DNA methylation is preferentially preserved on intergenic regions of the paternal alleles and intragenic regions of maternal alleles in each individual blastomere. However, chromatin accessibility is similar between paternal and maternal alleles in each individual cell from the late zygote to the blastocyst stage. The binding motifs of several pluripotency regulators are enriched at distal nucleosome depleted regions from as early as the 2-cell stage. This indicates that the cis-regulatory elements of such target genes have been primed to an open state from the 2-cell stage onward, long before pluripotency is eventually established in the ICM of the blastocyst. Genes may be classified into homogeneously open, homogeneously closed and divergent states based on the chromatin accessibility of their promoter regions among individual cells. This can be traced to step-wise transitions during preimplantation development. Our study offers the first single-cell and parental allele-specific analysis of the genome-scale chromatin state and DNA methylation dynamics at single-base resolution in early mouse embryos and provides new insights into the heterogeneous yet highly ordered features of epigenomic reprogramming during this process.
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Multiple teams have created methods that jointly profile DNA methylation and RNA.
“Many groups have built from this foundation to develop technologies that co-profile the DNA methylome and transcriptome28–31.”
From The technological landscape and applications of single-cell multi-omics (2023) · cites this paper as [30]
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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
Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications
Krueger, F., & Andrews, S. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr167 · Cited by 5,161 · see citing works
Tumour evolution inferred by single-cell sequencing
Navin, N., Kendall, J., Troge, J., Andrews, P., Rodgers, L., McIndoo, J., Cook, K., Stepansky, A., Levy, D., Esposito, D., et al. (2011) · Nature · doi:10.1038/nature09807 · Cited by 2,598 · 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
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
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
The Technology and Biology of Single-Cell RNA Sequencing
Kolodziejczyk, A. A., Kim, J. K., Svensson, V., Marioni, J. C., & Teichmann, S. A. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.04.005 · Cited by 1,487 · see citing works
Single-Cell RNA-Seq Reveals Dynamic, Random Monoallelic Gene Expression in Mammalian Cells
Deng, Q., Ramsköld, D., Reinius, B., & Sandberg, R. (2014) · Science · doi:10.1126/science.1245316 · Cited by 1,345 · see citing works
Single-cell genome sequencing: current state of the science
Gawad, C., Koh, W., & Quake, S. R. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2015.16 · Cited by 1,334 · see citing works
Demethylation of the zygotic paternal genome
Mayer, W., Niveleau, A., Walter, J., Fundele, R. H., & Haaf, T. (2000) · Nature · doi:10.1038/35000656 · Cited by 1,330 · 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
Genome-Wide Detection of Single-Nucleotide and Copy-Number Variations of a Single Human Cell
Zong, C., Lu, S., Chapman, A. R., & Xie, X. S. (2012) · Science · doi:10.1126/science.1229164 · Cited by 1,154 · see citing works
The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes
Gu, T., Guo, F., Yang, H., Wu, H.-P., Xu, G., Liu, W., Xie, Z.-G., Shi, L., He, X., Jin, S., et al. (2011) · Nature · doi:10.1038/nature10443 · Cited by 1,144 · see citing works
Self-citationSingle-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
Active demethylation of the paternal genome in the mouse zygote
Oswald, J., Engemann, S., Lane, N., Mayer, W., Olek, A., Fundele, R. H., Dean, W., Reik, W., & Walter, J. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00448-6 · Cited by 983 · see citing works
A unique regulatory phase of DNA methylation in the early mammalian embryo
Smith, Z. D., Chan, M. M., Mikkelsen, T. S., Gu, H., Gnirke, A., Regev, A., & Meissner, A. (2012) · Nature · doi:10.1038/nature10960 · Cited by 964 · see citing works
The DNA methylation landscape of human early embryos
Guo, H., Zhu, P., Yan, L., Li, R., Hu, B., Lian, Y., Yan, J., Ren, X., Lin, S., Li, J., et al. (2014) · Nature · doi:10.1038/nature13544 · Cited by 919 · see citing works
Self-citationTopologically associating domains are stable units of replication-timing regulation
Pope, B. D., Ryba, T., Dileep, V., Yue, F., Wu, W.-S., Denas, O., Vera, D. L., Wang, Y., Hansen, R. S., Canfield, T. K., et al. (2014) · Nature · doi:10.1038/nature13986 · Cited by 902 · 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
Epigenetic Dynamics of Imprinted X Inactivation During Early Mouse Development
Okamoto, I., Otte, A. P., Allis, C. D., Reinberg, D., & Heard, É. (2003) · Science · doi:10.1126/science.1092727 · Cited by 811 · see citing works
DNA methylation dynamics during epigenetic reprogramming in the germline and preimplantation embryosPreprint
Messerschmidt, D. M., Knowles, B. B., & Solter, D. (2014) · Genes & Development · doi:10.1101/gad.234294.113 · Cited by 734 · 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
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
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
Self-citationBroad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition
Dahl, J. A., Jung, I., Aanes, H., Greggains, G. D., Manaf, A., Lerdrup, M., Li, G., Kuan, S., Li, B., Lee, A. Y., et al. (2016) · Nature · doi:10.1038/nature19360 · Cited by 628 · see citing works
Allelic reprogramming of the histone modification H3K4me3 in early mammalian development
Zhang, B., Zheng, H., Huang, B., Li, W., Xiang, Y.-L., Peng, X., Jia, M., Wu, X., Zhang, Y., Xu, Q.-H., et al. (2016) · Nature · doi:10.1038/nature19361 · Cited by 627 · see citing works
Self-citationAdvances and Applications of Single-Cell Sequencing Technologies
Wang, Y., & Navin, N. E. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.05.005 · Cited by 610 · see citing works
The Transcriptome and DNA Methylome Landscapes of Human Primordial Germ Cells
Guo, F., Yan, L., Guo, H., Li, L., Hu, B., Zhao, Y., Yong, J., Hu, Y., Wang, X., Wei, Y., et al. (2015) · Cell · doi:10.1016/j.cell.2015.05.015 · Cited by 603 · see citing works
Self-citationTargets and dynamics of promoter DNA methylation during early mouse development
Borgel, J., Guibert, S., Li, Y., Chiba, H., Schübeler, D., Sasaki, H., Forné, T., & Weber, M. (2010) · Nature Genetics · doi:10.1038/ng.708 · Cited by 602 · see citing works
Global Reorganization of Replication Domains During Embryonic Stem Cell Differentiation
Hiratani, I., Ryba, T., Itoh, M., Yokochi, T., Schwaiger, M., Chang, C., Lyou, Y., Townes, T. M., Schübeler, D., & Gilbert, D. M. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060245 · Cited by 548 · see citing works
Programming and Inheritance of Parental DNA Methylomes in Mammals
Wang, L., Zhang, J., Duan, J., Gao, X., Zhu, W. Z., Lu, X., Yang, L., Zhang, J., Li, G., Ci, W., et al. (2014) · Cell · doi:10.1016/j.cell.2014.04.017 · Cited by 532 · see citing works
Self-citationReactivation of the Paternal X Chromosome in Early Mouse Embryos
Mak, W., Nesterova, T. B., de Napoles, M., Appanah, R., Yamanaka, S., Otte, A. P., & Brockdorff, N. (2004) · Science · doi:10.1126/science.1092674 · Cited by 532 · 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
Self-citationGenome-wide Single-Cell Analysis of Recombination Activity and De Novo Mutation Rates in Human Sperm
Wang, J., Fan, H. C., Behr, B. R., & Quake, S. R. (2012) · Cell · doi:10.1016/j.cell.2012.06.030 · Cited by 511 · 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
Replication-Dependent Loss of 5-Hydroxymethylcytosine in Mouse Preimplantation Embryos
Inoue, A., & Zhang, Y. (2011) · Science · doi:10.1126/science.1212483 · Cited by 489 · see citing works
Hirasawa, R., Chiba, H., Kaneda, M., Tajima, S., Li, E., Jaenisch, R., & Sasaki, H. (2008) · Genes & Development · doi:10.1101/gad.1667008 · Cited by 488 · see citing works
Heterogeneity in Oct4 and Sox2 Targets Biases Cell Fate in 4-Cell Mouse Embryos
Goolam, M., Scialdone, A., Graham, S. J. L., Macaulay, I. C., Jedrusik, A., Hupalowska, A., Voet, T., Marioni, J. C., & Zernicka-Goetz, M. (2016) · Cell · doi:10.1016/j.cell.2016.01.047 · Cited by 484 · see citing works
Genome-wide Maps of Nuclear Lamina Interactions in Single Human Cells
Kind, J., Pagie, L., de Vries, S., Nahidiazar, L., Dey, S. S., Bienko, M., Zhan, Y., Lajoie, B. R., de Graaf, C. A., Amendola, M., et al. (2015) · Cell · doi:10.1016/j.cell.2015.08.040 · Cited by 467 · see citing works
Genome-wide mapping of nucleosome positioning and DNA methylation within individual DNA molecules
Kelly, T. K., Liu, Y., Lay, F. D., Liang, G., Berman, B. P., & Jones, P. A. (2012) · Genome Research · doi:10.1101/gr.143008.112 · Cited by 455 · see citing works
Resetting Epigenetic Memory by Reprogramming of Histone Modifications in Mammals
Zheng, H., Huang, B., Zhang, B., Xiang, Y., Du, Z., Xu, Q., Li, Y., Wang, Q., Ma, J., Xu, P., et al. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.08.032 · Cited by 432 · see citing works
Single-cell DNA methylome sequencing and bioinformatic inference of epigenomic cell-state dynamics
Farlik, M., Sheffield, N. C., Nuzzo, A., Datlinger, P., Schönegger, A., Klughammer, J., & Bock, C. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.02.001 · Cited by 422 · see citing works
Single-Cell Whole-Genome Amplification and Sequencing: Methodology and Applications
Huang, L., Ma, F., Chapman, A. R., Lü, S., & Xie, X. S. (2015) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-090413-025352 · Cited by 419 · see citing works
Epigenetic reversion of post-implantation epiblast to pluripotent embryonic stem cells
Bao, S., Tang, F., Li, X., Hayashi, K., Gillich, A., Lao, K., & Surani, M. A. (2009) · Nature · doi:10.1038/nature08534 · Cited by 384 · see citing works
Self-citationActive and Passive Demethylation of Male and Female Pronuclear DNA in the Mammalian Zygote
Guo, F., Li, X., Liang, D., Li, T., Zhu, P., Guo, H., Wu, X., Wen, L., Gu, T., Hu, B., et al. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.08.003 · Cited by 375 · see citing works
Self-citationEstablishing Chromatin Regulatory Landscape during Mouse Preimplantation Development
Lu, F., Liu, Y., Inoue, A., Suzuki, T., Zhao, K., & Zhang, Y. (2016) · Cell · doi:10.1016/j.cell.2016.05.050 · Cited by 342 · 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
Genome-wide dynamics of replication timing revealed by in vitro models of mouse embryogenesisPreprint
Hiratani, I., Ryba, T., Itoh, M., Rathjen, J., Kulik, M. J., Papp, B., Fussner, E., Bazett‐Jones, D. P., Plath, K., Dalton, S., et al. (2009) · Genome Research · doi:10.1101/gr.099796.109 · Cited by 318 · see citing works
Probing Meiotic Recombination and Aneuploidy of Single Sperm Cells by Whole-Genome Sequencing
Lü, S., Zong, C. C., Fan, W., Yang, M., Li, J., Chapman, A. R., Zhu, P., Hu, X., Xu, L., Yan, L., et al. (2012) · Science · doi:10.1126/science.1229112 · Cited by 294 · see citing works
Self-citationHa, G., Roth, A. J. L., Lai, D., Bashashati, A., Ding, J., Goya, R., Giuliany, R., Rosner, J., Oloumi, A., Shumansky, K., et al. (2012) · Genome Research · doi:10.1101/gr.137570.112 · Cited by 269 · see citing works
Shen, L., Inoue, A., He, J., Liu, Y., Lu, F., & Zhang, Y. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.09.002 · Cited by 268 · see citing works
Chromatin dynamics in the regulation of cell fate allocation during early embryogenesis
Burton, A., & Torres‐Padilla, M. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3885 · Cited by 256 · see citing works
De novo DNA methylation drives 5hmC accumulation in mouse zygotes
Amouroux, R., Nashun, B., Shirane, K., Nakagawa, S., Hill, P. W. S., D’Souza, Z., Nakayama, M., Matsuda, M., Turp, A., Ndjetehe, E., et al. (2016) · Nature Cell Biology · doi:10.1038/ncb3296 · Cited by 233 · see citing works
Taberlay, P. C., Statham, A. L., Kelly, T. K., Clark, S. J., & Jones, P. A. (2014) · Genome Research · doi:10.1101/gr.163485.113 · Cited by 183 · see citing works
Polycomb-Repressed Genes Have Permissive Enhancers that Initiate Reprogramming
Taberlay, P. C., Kelly, T. K., Liu, C.-C., You, J. S., Carvalho, D. D. D., Miranda, T. B., Zhou, X. J., Liang, G., & Jones, P. A. (2011) · Cell · doi:10.1016/j.cell.2011.10.040 · Cited by 172 · see citing works
Peat, J. R., Dean, W., Clark, S. J., Krueger, F., Smallwood, S. A., Ficz, G., Kim, J. K., Marioni, J. C., Hore, T. A., & Reik, W. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.11.034 · Cited by 130 · see citing works
The role of DNA methylation in directing the functional organization of the cancer epigenomePreprint
Lay, F. D., Liu, Y., Kelly, T. K., Witt, H. N., Farnham, P., Jones, P. A., & Berman, B. P. (2015) · Genome Research · doi:10.1101/gr.183368.114 · Cited by 109 · see citing works
Single-cell nucleosome mapping reveals the molecular basis of gene expression heterogeneity
Small, E. C., Xi, L., Wang, J.-P., Widom, J., & Licht, J. D. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400517111 · Cited by 105 · see citing works
Nabilsi, N. H., Deleyrolle, L. P., Darst, R. P., Riva, A., Reynolds, B. A., & Kladde, M. P. (2013) · Genome Research · doi:10.1101/gr.161737.113 · Cited by 53 · see citing works
DNA methylation dynamics in mouse preimplantation embryos revealed by mass spectrometry
Okamoto, Y., Yoshida, N., Suzuki, T., Shimozawa, N., Asami, M., Matsuda, T., Kojima, N., Perry, A. C. F., & Takada, T. (2016) · Scientific Reports · doi:10.1038/srep19134 · Cited by 43 · see citing works
Guenatri, M., Duffié, R., Iranzo, J., Fauque, P., & Bourc’his, D. (2013) · Development · doi:10.1242/dev.089268 · Cited by 42 · see citing works
Single-Cell Transcriptomics Enters the Age of Mass Production
Junker, J. P., & van Oudenaarden, A. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.05.019 · Cited by 20 · see citing works
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Single-cell RNA sequencing technologies and bioinformatics pipelines
Hwang, B., Lee, J. H., & Bang, D. (2018) · Experimental & Molecular Medicine · doi:10.1038/s12276-018-0071-8 · Cited by 1,793 · see citing works
Mapping the Mouse Cell Atlas by Microwell-Seq
Han, X., Wang, R., Zhou, Y., Fei, L., Sun, H., Lai, S., Saadatpour, A., Zhou, Z., Chen, H., Ye, F., et al. (2018) · Cell · doi:10.1016/j.cell.2018.02.001 · Cited by 1,597 · see citing works
Multi-Omics Factor Analysis—a framework for unsupervised integration of multi-omics data sets
Argelaguet, R., Velten, B., Arnol, D., Dietrich, S., Zenz, T., Marioni, J. C., Buettner, F., Huber, W., & Stegle, O. (2018) · Molecular Systems Biology · doi:10.15252/msb.20178124 · Cited by 1,510 · see citing works
MOFA+: a statistical framework for comprehensive integration of multi-modal single-cell data
Argelaguet, R., Arnol, D., Bredikhin, D., Deloro, Y., Velten, B., Marioni, J. C., & Stegle, O. (2020) · Genome Biology · doi:10.1186/s13059-020-02015-1 · Cited by 1,091 · 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
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
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
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
Dynamics of the epigenetic landscape during the maternal-to-zygotic transition
Eckersley-Maslin, M. A., Alda-Catalinas, C., & Reik, W. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0008-z · Cited by 431 · 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 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
Integrating genetic and non-genetic determinants of cancer evolution by single-cell multi-omics
Nam, A. S., Chaligné, R., & Landau, D. A. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-020-0265-5 · Cited by 381 · 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
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Simultaneous profiling of transcriptome and DNA methylome from a single cell
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Sperm RNA code programmes the metabolic health of offspring
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Xu, Q., & Xie, W. (2017) · Trends in Cell Biology · doi:10.1016/j.tcb.2017.10.008 · Cited by 214 · see citing works
Understanding tumor ecosystems by single-cell sequencing: promises and limitations
Ren, X., Kang, B., & Zhang, Z. (2018) · Genome biology · doi:10.1186/s13059-018-1593-z · Cited by 214 · see citing works
Single-cell multi-omics sequencing of human early embryos
Li, L., Guo, F., Gao, Y., Ren, Y., Yuan, P., Yan, L., Li, R., Lian, Y., Li, J., Hu, B., et al. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0123-2 · Cited by 209 · see citing works
Self-citationSingle-Cell (Multi)omics Technologies
Chappell, L., Russell, A. J. C., & Voet, T. (2018) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-091416-035324 · Cited by 206 · 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
Chromatin Accessibility Landscape in Human Early Embryos and Its Association with Evolution
Gao, L., Wu, K., Liu, Z., Yao, X., Yuan, S., Tao, W., Yi, L., Yu, G., Hou, Z., Fan, D., et al. (2018) · Cell · doi:10.1016/j.cell.2018.02.028 · Cited by 200 · see citing works
Single-cell sequencing to multi-omics: technologies and applications
Wu, X., Yang, X., Dai, Y., Zhao, Z., Zhu, J., Guo, H., & Yang, R. (2024) · Biomarker Research · doi:10.1186/s40364-024-00643-4 · Cited by 195 · see citing works
“Additionally, single-cell multi-omics technologies have been employed for multiple stages of embryonic development, including preimplantation [188, 189], implantation [190], gastrulation [191], and early organogenesis [192], to explore cell fate decisions of embryonic development from multiple…”
MethodSelf-citationAdvances 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
Single Cell Multi-Omics Technology: Methodology and Application
Hu, Y., An, Q., Sheu, K. M., Trejo, B. M., Fan, S., & Guo, Y. Q. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00028 · Cited by 192 · see citing works
Gu, C., Liu, S., Wu, Q., Zhang, L., & Guo, F. (2018) · Cell Research · doi:10.1038/s41422-018-0125-4 · Cited by 185 · see citing works
Self-citationLatest techniques to study DNA methylation
Gouil, Q. A., & Keniry, A. (2019) · Essays in Biochemistry · doi:10.1042/ebc20190027 · Cited by 177 · see citing works
Chromatin accessibility: biological functions, molecular mechanisms and therapeutic application
Chen, Y., Liang, R., Li, Y., Jiang, L., Ma, D., Luo, Q., & Song, G. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-02030-9 · Cited by 174 · see citing works
Single-cell DNA methylation profiling: technologies and biological applications
Karemaker, I. D., & Vermeulen, M. (2018) · Trends in Biotechnology · doi:10.1016/j.tibtech.2018.04.002 · Cited by 170 · 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
Single-cell multiomics sequencing reveals the functional regulatory landscape of early embryos
Wang, Y., Yuan, P., Yan, Z., Yang, M., Huo, Y., Nie, Y., Zhu, X., Qiao, J., & Yan, L. (2021) · Nature Communications · doi:10.1038/s41467-021-21409-8 · Cited by 161 · see citing works
High-throughput single-сell sequencing in cancer research
Jia, Q., Chu, H., Jin, Z., Long, H., & Zhu, B. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-00990-4 · Cited by 152 · see citing works
Microfluidics applications for high-throughput single cell sequencing
Zhou, W.-M., Yan, Y., Guo, Q.-R., Ji, H., Wang, H., Xu, T.-T., Makabel, B., Pilarsky, C. P., He, G., Yu, X.-Y., et al. (2021) · Journal of Nanobiotechnology · doi:10.1186/s12951-021-01045-6 · Cited by 146 · see citing works
Single-cell RNAseq for the study of isoforms—how is that possible?
Arzalluz-Luque, Á., & Conesa, A. (2018) · Genome biology · doi:10.1186/s13059-018-1496-z · Cited by 135 · see citing works
f-scLVM: scalable and versatile factor analysis for single-cell RNA-seq
Buettner, F., Pratanwanich, P. N., McCarthy, D. J., Marioni, J. C., & Stegle, O. (2017) · Genome biology · doi:10.1186/s13059-017-1334-8 · Cited by 127 · see citing works
Single-cell omics in ageing: a young and growing field
He, X., Memczak, S., Qu, J. T., Belmonte, J. C. I., & Liu, G. (2020) · Nature Metabolism · doi:10.1038/s42255-020-0196-7 · Cited by 128 · 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
Self-citationEpigenetic regulation in development: is the mouse a good model for the human?
Hanna, C. W., Demond, H., & Kelsey, G. (2018) · Human Reproduction Update · doi:10.1093/humupd/dmy021 · Cited by 126 · see citing works
Genetic Control of Early Cell Lineages in the Mammalian Embryo
Rossant, J. (2018) · Annual Review of Genetics · doi:10.1146/annurev-genet-120116-024544 · Cited by 126 · see citing works
Decoding dynamic epigenetic landscapes in human oocytes using single-cell multi-omics sequencing
Yan, R., Gu, C., You, D., Huang, Z., Qian, J., Yang, Q., Cheng, X., Zhang, L., Wang, H., Wang, P., et al. (2021) · Cell stem cell · doi:10.1016/j.stem.2021.04.012 · Cited by 125 · see citing works
Self-citationSingle-cell measurement of higher-order 3D genome organization with scSPRITE
Arrastia, M. V., Jachowicz, J. W., Ollikainen, N., Curtis, M. S., Lai, C., Quinodoz, S. A., Selck, D. A., Ismagilov, R. F., & Guttman, M. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-00998-1 · Cited by 126 · see citing works
Desta, G. M., & Birhanu, A. G. (2025) · Acta Biochimica Polonica · doi:10.3389/abp.2025.13922 · Cited by 121 · 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
Self-citationDeconstructing the pluripotency gene regulatory network
Li, M., & Belmonte, J. C. I. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0067-6 · Cited by 116 · see citing works
Ruan, Q., Ruan, W., Lin, X., Wang, Y., Zou, F., Zhou, L., Zhu, Z., & Yang, C. J. (2020) · Science Advances · doi:10.1126/sciadv.abd6454 · Cited by 116 · 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
Dynamics of DNA hydroxymethylation and methylation during mouse embryonic and germline development
Yan, R., Cheng, X., Gu, C., Xu, Y., Long, X., Zhai, J., Sun, F., Qian, J., Du, Y., Wang, H., et al. (2022) · Nature Genetics · doi:10.1038/s41588-022-01258-x · Cited by 115 · see citing works
Self-citationSingle 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
A Comparative Overview of Epigenomic Profiling Methods
Mehrmohamadi, M., Sepehri, M. H., Nazer, N., & Norouzi, M. R. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.714687 · Cited by 112 · see citing works
Rebooting the Epigenomes during Mammalian Early Embryogenesis
Xia, W., & Xie, W. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.09.005 · Cited by 111 · see citing works
Ivanova, E., Cánovas, S., García-Martínez, S., Romar, R., Lopes, J. S., Rizos, D. V., Sánchez‐Calabuig, M. J., Krueger, F., Andrews, S., Pérez-Sánz, F., et al. (2020) · Clinical Epigenetics · doi:10.1186/s13148-020-00857-x · Cited by 110 · see citing works
Best practices on the differential expression analysis of multi-species RNA-seq
Chung, M. C., Bruno, V. M., Rasko, D. A., Cuomo, C. A., Muñoz, J. F., Livny, J., Shetty, A. C., Mahurkar, A., & Hotopp, J. C. D. (2021) · Genome biology · doi:10.1186/s13059-021-02337-8 · Cited by 108 · 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
Single-cell RNA sequencing in cancer: Applications, advances, and emerging challenges
Sun, G., Li, Z., Rong, D., Zhang, H., Shi, X., Yang, W., Zheng, W., Sun, G., Wu, F., Cao, H., et al. (2021) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2021.04.001 · Cited by 104 · see citing works
Advances in bulk and single-cell multi-omics approaches for systems biology and precision medicine
Li, Y., Ma, L., Wu, D., & Chen, G. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab024 · Cited by 101 · 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
Single-cell sequencing technology applied to epigenetics for the study of tumor heterogeneity
Hu, Y., Shen, F., Yang, X., Han, T., Long, Z., Wen, J., Huang, J., Shen, J., & Guo, Q. (2023) · Clinical Epigenetics · doi:10.1186/s13148-023-01574-x · Cited by 95 · see citing works
Stem cell bioengineering: building from stem cell biology
Tewary, M., Shakiba, N., & Zandstra, P. W. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0040-z · Cited by 93 · see citing works
Zhang, J., Song, C., Tian, Y. F., & Yang, X. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2021.802080 · Cited by 87 · see citing works
Alda-Catalinas, C., Bredikhin, D., Hernando-Herraez, I., Santos, F., Kubinyecz, O., Eckersley-Maslin, M. A., Stegle, O., & Reik, W. (2020) · Cell Systems · doi:10.1016/j.cels.2020.06.004 · Cited by 86 · see citing works
Reprogramming of the histone H3.3 landscape in the early mouse embryo
Ishiuchi, T., Abe, S., Inoue, K., Yeung, W. K. A., Miki, Y., Ogura, A., & Sasaki, H. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-00521-1 · Cited by 86 · see citing works
Spatial transcriptomics technology in cancer research
Yu, Q., Jiang, M., & Wu, L. L. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.1019111 · Cited by 86 · see citing works
DNA Methylation and Psychiatric Disorders
Liu, C., Jiao, C., Wang, K., & Yuan, N. (2018) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2018.01.006 · Cited by 85 · see citing works
Dynamic Enhancer DNA Methylation as Basis for Transcriptional and Cellular Heterogeneity of ESCs
Song, Y., van den Berg, P. R., Markoulaki, S., Soldner, F., Dall’Agnese, A., Henninger, J. E., Drotar, J., Rosenau, N., Cohen, M. A., Young, R. A., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.06.045 · Cited by 84 · 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
Invited Review: Epigenetics in neurodevelopment
Salinas, R. D., Connolly, D. R., & Song, H. (2020) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12608 · Cited by 81 · see citing works
Single-cell sequencing and its applications in head and neck cancer
Qi, Z., Barrett, T. F., Parikh, A. S., Tirosh, I., & Puram, S. V. (2019) · Oral Oncology · doi:10.1016/j.oraloncology.2019.104441 · Cited by 79 · see citing works
Advances and Challenges in Spatial Transcriptomics for Developmental Biology
Choe, K., Pak, U., Pang, Y., Hao, W., & Yang, X. (2023) · Biomolecules · doi:10.3390/biom13010156 · Cited by 78 · see citing works
Single cell transcriptome research in human placenta
Li, H., Huang, Q., Liu, Y., & Garmire, L. X. (2020) · Reproduction · doi:10.1530/rep-20-0231 · Cited by 77 · see citing works
Yao, C., Lyu, R., Rong, B., Zheng, Y., Lin, Z., Dai, R., Zhang, X., Xie, N., Wang, S., Tang, F., et al. (2020) · Cell Research · doi:10.1038/s41422-020-0281-1 · Cited by 74 · see citing works
Self-citationSingle-Cell Dissection of the Multiomic Landscape of High-Grade Serous Ovarian Cancer
Wang, Y., Xie, H., Chang, X., Hu, W., Li, M., Li, Y., Liu, H., Cheng, H., Wang, S., Zhou, L., et al. (2022) · Cancer Research · doi:10.1158/0008-5472.can-21-3819 · Cited by 75 · see citing works
Self-citationSingle-Cell RNA Sequencing: Technological Progress and Biomedical Application in Cancer Research
Xu, C., Zheng, Y., & Xu, K. (2023) · Molecular Biotechnology · doi:10.1007/s12033-023-00777-0 · Cited by 74 · see citing works
Statistical single cell multi-omics integration
Colomé‐Tatché, M., & Theis, F. J. (2018) · Current Opinion in Systems Biology · doi:10.1016/j.coisb.2018.01.003 · Cited by 70 · see citing works
Human Germline Cell Development: from the Perspective of Single-Cell Sequencing
Wen, L., & Tang, F. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.08.025 · Cited by 69 · see citing works
Self-citationAdvances and applications in single-cell and spatial genomics
Wang, J., Ye, F., Chai, H., Jiang, Y., Wang, T., Ran, X., Xia, Q., Xu, Z., Fu, Y., Zhang, G., et al. (2024) · Science China Life Sciences · doi:10.1007/s11427-024-2770-x · Cited by 69 · see citing works
A plate-based single-cell ATAC-seq workflow for fast and robust profiling of chromatin accessibility
Xu, W., Wen, Y., Liang, Y., Xu, Q., Wang, X., Jin, W., & Chen, X. (2021) · Nature Protocols · doi:10.1038/s41596-021-00583-5 · Cited by 67 · see citing works
Introduction to Single-Cell DNA Methylation Profiling Methods
Ahn, J., Heo, S., Lee, J., & Bang, D. (2021) · Biomolecules · doi:10.3390/biom11071013 · Cited by 67 · see citing works
Dissecting the epigenomic dynamics of human fetal germ cell development at single-cell resolution
Li, L., Li, L., Li, Q., Liu, X., Ma, X., Yong, J., Gao, S., Wu, X., Wei, Y., Wang, X., et al. (2020) · Cell Research · doi:10.1038/s41422-020-00401-9 · Cited by 65 · see citing works
Self-citationEpigenetics, microbiota, and intraocular inflammation: New paradigms of immune regulation in the eye
Wen, X., Hu, X., Li, M., Ge, X., Deng, Y., Bible, P. W., & Wei, L. (2018) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2018.01.001 · Cited by 64 · see citing works
Collin, J., Zerti, D., Queen, R. A., Santos‐Ferreira, T., Bauer, R., Coxhead, J. M., Hussain, R., STEEL, D. H., Mellough, C., Ader, M., et al. (2019) · Stem Cells · doi:10.1002/stem.2974 · Cited by 64 · see citing works
Glioma Stem Cells: Novel Data Obtained by Single-Cell Sequencing
Gisina, A. M., Kholodenko, I. V., Kim, Y. S., Abakumov, M. A., Lupatov, A. Y., & Yarygin, K. N. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232214224 · Cited by 63 · see citing works
Technologies and applications of single-cell DNA methylation sequencing
Liu, F., Wang, Y., Gu, H., & Wang, X. (2023) · Theranostics · doi:10.7150/thno.82582 · Cited by 63 · see citing works
Genome-coverage single-cell histone modifications for embryo lineage tracing
Liu, M., Yue, Y., Chen, X., Xian, K., Dong, C. F., Shi, M., Xiong, H., Tian, K., Li, Y., Zhang, Q. C., et al. (2025) · Nature · doi:10.1038/s41586-025-08656-1 · Cited by 63 · see citing works
Huang, Y., Li, L., An, G., Yang, X., Cui, M., Song, X., Lin, J., Zhang, X., Yao, Z., Wan, C., et al. (2023) · Nature Cell Biology · doi:10.1038/s41556-023-01232-7 · Cited by 59 · see citing works
Self-citationBrown, A. J., Snapkov, I., Akbar, R., Pavlović, M., Miho, E., Sandve, G. K., & Greiff, V. (2019) · Molecular Systems Design & Engineering · doi:10.1039/c9me00071b · Cited by 59 · see citing works
Zhu, L., Marjani, S. L., & Jiang, Z. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.557934 · Cited by 58 · see citing works
Chen, M., Fu, R., Chen, Y., Li, L., & Wang, S. (2025) · Nature Methods · doi:10.1038/s41592-024-02567-1 · Cited by 56 · see citing works
Self-citationFan, X., Lü, P., Wang, H., Bian, S., Wu, X., Zhang, Y., Liu, Y., Fu, D., Wen, L., Hao, J., et al. (2022) · Cell Discovery · doi:10.1038/s41421-021-00366-y · Cited by 54 · see citing works
Self-citationJoint single-cell profiling resolves 5mC and 5hmC and reveals their distinct gene regulatory effects
Fabyanic, E. B., Hu, P., Qiu, Q., Berríos, K. N., Connolly, D. R., Wang, T., Flournoy, J., Zhou, Z., Kohli, R. M., & Wu, H. (2023) · Nature Biotechnology · doi:10.1038/s41587-023-01909-2 · Cited by 53 · see citing works
Mapping chromatin modifications at the single cell level
Ludwig, C., & Bintu, L. (2019) · Development · doi:10.1242/dev.170217 · Cited by 53 · see citing works
The landscape of accessible chromatin in bovine oocytes and early embryos
Ming, H., Sun, J., Pasquariello, R., Gatenby, L., Herrick, J. R., Yuan, Y., Pinto, C. R. F., Bondioli, K. R., Krisher, R. L., & Jiang, Z. (2020) · Epigenetics · doi:10.1080/15592294.2020.1795602 · Cited by 53 · see citing works
Single-Cell Multiomics Techniques: From Conception to Applications
Dimitriu, M. A., Lazar-Contes, I., Roszkowski, M., & Mansuy, I. M. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.854317 · Cited by 52 · see citing works
Single‐cell RNA sequencing in Drosophila: Technologies and applications
Li, H. (2020) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.396 · Cited by 52 · see citing works
- Authors
- Guo, F., Li, L., Li, J., Wu, X., Hu, B., Zhu, P., Wen, L., & Tang, F.
- Affiliations
- Peking University (CN)
- Corresponding author
- Guo, Fan
- Tang, Fuchou
- Venue
- Cell Research
- Published
- 2017-06-16
- Volume
- 27
- Issue
- 8
- Pages
- 967-988
- ISSN
- 1001-0602 (ISSN-L)
- 1748-7838
- PMC
- PMC5539349
- OpenAlex
- W2626695356
- Cited by
- 374
- References
- 62
- Citations by year
- 2026: 20 · 2025: 32 · 2024: 34 · 2023: 42 · 2022: 58 · 2021: 54 · 2020: 48 · 2019: 35 · 2018: 42 · 2017: 6 · 2016: 1
- FWCI
- 14.75
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell Research (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (31625018, 81521002, 81561138005)
- Peking University
- Beijing Municipal Science and Technology Commission (Z131100005213006)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Keywords
- chromatin accessibility, DNA methylation, copy number variation, ploidy, preimplantation embryo, embryonic stem cells, epigenetic reprogramming, nucleosome positioning, cis-regulatory elements, blastocyst, early mouse embryo
- MeSH terms
- Mouse Embryonic Stem Cells, Animals, Blastocyst, Cell Line, Chromatin, Female, Male, Gene Expression Regulation, Developmental, DNA Methylation, Genomics, Mice
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