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Cao Science 2020.Pdf RESEARCH ◥ CONCLUSION: The single-cell data resource RESEARCH ARTICLE SUMMARY presented here is notable for its scale, its fo- cus on human fetal development, the breadth HUMAN GENOMICS of tissues analyzed, and the parallel gener- ation of gene expression (this study) and chro- A human cell atlas of fetal gene expression matin accessibility data (Domcke et al.,this issue). We furthermore consolidate the tech- Junyue Cao, Diana R. O’Day, Hannah A. Pliner, Paul D. Kingsley, Mei Deng, Riza M. Daza, nical framework for individual laboratories to Michael A. Zager, Kimberly A. Aldinger, Ronnie Blecher-Gonen, Fan Zhang, Malte Spielmann, generate and analyze gene expression and James Palis, Dan Doherty, Frank J. Steemers, Ian A. Glass, Cole Trapnell*, Jay Shendure* chromatin accessibility data from millions of single cells. Looking forward, we envision that the somewhat narrow window of mid- INTRODUCTION: A reference atlas of human cell 72 to 129 days in estimated postconceptual age gestational human development studied here typesisamajorgoalforthefield.Here,weset and representing 15 organs, altogether profiling will be complemented by additional atlases out to generate single-cell atlases of both gene 4 million single cells. We developed and applied of earlier and later time points, as well as expression (this study) and chromatin acces- a framework for quantifying cell type specificity, similarly comprehensive profiling and inte- sibility (Domcke et al., this issue) using diverse identifying 657 cell subtypes, which we prelimi- gration of data from model organisms. The human tissues obtained during midgestation. narily annotated based on cross-matching to continued development and application of mouse cell atlases. We identified and validated methods for ascertaining gene expression RATIONALE: Contemporary knowledge of the potentially circulating trophoblast-like and and chromatin accessibility—in concert with Downloaded from molecular basis of in vivo human development hepatoblast-like cells in unexpected tissues. Pro- spatial, epigenetic, proteomic, lineage history, mostly derives from a combination of human filing gene expression in diverse tissues facilitated and other information—will be necessary to genetics, in vivo investigations of model or- the cross-tissue analyses of broadly distributed obtain a comprehensive view of the temporal ganisms, and in vitro studies of differentiating cell types, including blood, endothelial, and unfolding of human cell type diversity that human cell lines, rather than through direct epithelial cells. For blood cells, this yielded a begins at the single-cell zygote. An interactive investigations of developing human tissues. multiorgan map of cell state trajectories from website facilitates the exploration of these http://science.sciencemag.org/ Several challenges have historically limited hematopoietic stem cells to all major subline- freely available data by tissue, cell type, or the study of developing human tissues at the ages. Multiple lines of evidence support the gene (descartes.brotmanbaty.org).▪ molecular level, including limited access, tissue adrenal gland as a normal, albeit minor, site degradation, and cell type heterogeneity. For of erythropoiesis during fetal development. It this and the companion study (Domcke et al., was notably straightforward to integrate these The list of author affiliations is available in the full article online. this issue), we were able to overcome these human fetal data with a mouse embryonic cell *Corresponding author. Email: [email protected] (C.T.); challenges. atlas, despite differences in species and devel- [email protected] (J.S.) Cite this article as J. Cao et al., Science 370, eaba7721 opmental stage. For some systems, this essen- (2020). DOI: 10.1126/science.aba7721 RESULTS: We applied three-level single-cell com- tially permitted us to bridge gene expression READ THE FULL ARTICLE AT binatorial indexing for gene expression (sci-RNA- dynamics from the embryonic to the fetal stages on December 13, 2020 seq3) to 121 human fetal samples ranging from of mammalian development. https://doi.org/10.1126/science.aba7721 15 human fetal organs Single-cell gene expression profiles Cell type annotation Genes 4,062,980 cells Main cell types Main cell Integrated analyses of broadly distributed cell types 121 samples Blood cells 1. Indexed reverse transcription AAAA TTTT AAAA TTTT 2. Indexed hairpin ligation AAAA TTTT Cross-species integration U AAAA TTTT U sci-RNA-seq3 3. Indexed PCR AAAA TTTT AAAA TTTT A human cell atlas of fetal gene expression enables the exploration of in vivo gene expression across diverse cell types. We used a three-level combinatorial indexing assay (sci-RNA-seq3) to profile gene expression in ~4,000,000 single cells from 15 fetal organs. This rich resource enables, for example, the identification and annotation of cell types, cross-tissue integration of broadly distributed cell types (e.g., blood, endothelial, and epithelial), and interspecies integration of mouse embryonic and human fetal cell atlases. PCR, polymerase chain reaction. Cao et al., Science 370, 808 (2020) 13 November 2020 1of1 RESEARCH ◥ matin accessibility in 1.6 million cells from RESEARCH ARTICLE the same organs using an overlapping set of samples (12). The profiled organs span diverse HUMAN GENOMICS systems; however, some systems were not accessible—bone marrow, bone, gonads, and A human cell atlas of fetal gene expression skin are notably absent. Tissues were obtained from 28 fetuses rang- Junyue Cao1*, Diana R. O’Day2, Hannah A. Pliner3, Paul D. Kingsley4, Mei Deng2, Riza M. Daza1, ing from 72 to 129 days in estimated post- Michael A. Zager3,5, Kimberly A. Aldinger2,6, Ronnie Blecher-Gonen1, Fan Zhang7, Malte Spielmann8,9, conceptual age. We applied a method for James Palis4, Dan Doherty2,3,6, Frank J. Steemers7, Ian A. Glass2,3,6, extracting nuclei directly from cryopreserved Cole Trapnell1,3,10†, Jay Shendure1,3,10,11† tissues that works across a variety of tissue types and produces homogenates suitable for The gene expression program underlying the specification of human cell types is of fundamental interest. both sci-RNA-seq3 and sci-ATAC-seq3 (single- We generated human cell atlases of gene expression and chromatin accessibility in fetal tissues. For cell combinatorial indexing assay for transposase- gene expression, we applied three-level combinatorial indexing to >110 samples representing 15 organs, accessible chromatin with high-throughput ultimately profiling ~4 million single cells. We leveraged the literature and other atlases to identify sequencing) (12). For most organs, extracted and annotate hundreds of cell types and subtypes, both within and across tissues. Our analyses focused nuclei were fixed with paraformaldehyde. on organ-specific specializations of broadly distributed cell types (such as blood, endothelial, and For renal and digestive organs where ribo- epithelial), sites of fetal erythropoiesis (which notably included the adrenal gland), and integration nucleases (RNases) and proteases are abun- with mouse developmental atlases (such as conserved specification of blood cells). These data represent dant, we used fixed cells rather than nuclei, Downloaded from a rich resource for the exploration of in vivo human gene expression in diverse tissues and cell types. which increased cell and mRNA recovery (13). For each experiment, nuclei or cells from a given tissue were deposited to different wells, o date, most investigations of human de- of Mendelian disorders), in vivo investiga- such that the first index of sci-RNA-seq3 pro- velopment have been anatomical or his- tions of model organisms (in particular, of tocol also identified the source. As a batch tological in nature (1–3). However, it is the mouse), and in vitro studies of differentiat- control for experiments on nuclei, we spiked a http://science.sciencemag.org/ T clear that variation in the genetic and ing human cell lines (in particular, of embry- mixture of human HEK293T and mouse NIH/ molecular programs unfolding within onic or induced pluripotent stem cells), rather 3T3 nuclei, or nuclei from a common sentinel cells during development can cause disease. than from direct investigations of developing tissue (trisomy 21 cerebrum), into one or sev- For example, most Mendelian disorders have human tissues. eral wells. As a batch control for experiments a major developmental component (4). More- A reference human cell atlas based on de- on cells, we spiked cells derived from a tissue common and often devastating developmental veloping tissues could serve as the foundation (pancreas) into one or several wells. conditions to which genetic factors substan- for a systematic effort to better understand the We sequenced sci-RNA-seq3 libraries from tially contribute include congenital heart de- molecular and cellular events that give rise to seven experiments across seven Illumina NovaSeq fects, other birth defects, intellectual disabilities, all rare and common disorders of develop- 6000 sequencer runs, altogether generating and autism (5). ment, which collectively account for a major 68.6 billion raw reads. Processing data as pre- Several challenges have historically limited proportion of pediatric morbidity and mor- viously described (11), we recovered 4,979,593 on December 13, 2020 the study of developing human tissues at the tality (6, 7). Furthermore, although pioneer- single-cell gene expression profiles [unique molecular level. First, access to human embry- ing cell atlases have already
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