ArticleScience (New York, N.Y.)2023
Yolk sac cell atlas reveals multiorgan functions during human early development.
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Article in Science (New York, N.Y.), 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 53 papers.
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53citing papers in PubMed
14.5field-weighted citation impact, top 1% of its field
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53 citing papers in PubMed, 88 citations in OpenAlex.
- Spatially resolved multiomics of human meningeal development reveal lineage and disease dynamics.Nature cell biology · 2026Article
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- Harnessing macrophage signaling pathways and scalable engineering for next-generation immunotherapies.Signal transduction and targeted therapy · 2026Review
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- A consensus atlas of human brain development defines cell type-specific maturation trajectories across the lifespan.bioRxiv : the preprint server for biology · 2026Article
- Microglia and neuroinflammation: function, heterogeneity, and crosstalk.Cellular & molecular immunology · 2026Review
- Macrophages in embryonic development.Nature reviews. Immunology · 2026Review
- Synthetic developmental engineering of human liver organogenesis.Development (Cambridge, England) · 2026Review
- A three-dimensional spatial transcriptome atlas reconstructs early organogenesis in primate Carnegie stages 9 and 10 embryos.Nature cell biology · 2026Article
- A transgene-free, human peri-gastrulation embryo model presents trilaminar embryonic disc-, amnion- and yolk sac-like structures.Nature cell biology · 2026Article
- The vertebrate yolk sac: evolutionary origins and current advances in in vitro models.Development (Cambridge, England) · 2026Review
- Effect of a truncated mutant factor V on hemostatic function and embryonic development in mice.Scientific reports · 2026Article
- Discovery of New Markers for Haemogenic Endothelium and Haematopoietic Progenitors in the Mouse Yolk Sac.Journal of developmental biology · 2026Article
- Defining the marker and developmental trajectory of myeloid-derived suppressor cells in aging by single-cell transcriptomics.npj aging · 2025Article
- Macrophages in Hematopoiesis and Related Blood Diseases.Genomics, proteomics & bioinformatics · 2025Review
- Prpf4 sequentially regulates the expansion and maturation of erythrocyte through distinct mechanisms.Cell death discovery · 2025Article
- Primitive means first, not worst: Critical roles for primitive endoderm in embryos and embryo models.Developmental biology · 2025Review
- CD43, but not CD41 or GPI-80, marks first definitive haematopoietic stem cells in the human embryo.Development (Cambridge, England) · 2025Article
- CombinedActa biochimica et biophysica Sinica · 2025Article
- Review
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Authors and funding
61 authors at 11 institutions in 5 countries.
Issac Goh *Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-6397-3518
Rachel A Botting *Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0001-9595-4605
Antony Rose *Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0001-8494-8138
Simone Webb *Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0003-3058-8952
Justin EngelbertBiosciences Institute, Newcastle University, Newcastle upon Tyne NE2 4HH, UK.ORCID 0000-0002-4255-9668
Yorick GittonSorbonne Université, INSERM, CNRS, Institut de la Vision, Paris, France.ORCID 0000-0002-6808-6010
Emily StephensonWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-4244-4019
Mariana Quiroga LondoñoDepartment of Haematology, Wellcome-MRC Cambridge Stem Cell Institute, Cambridge CB2 0AW, UK.ORCID 0000-0003-2352-0773
Michael MatherBiosciences Institute, Newcastle University, Newcastle upon Tyne NE2 4HH, UK.
Nicole MendeDepartment of Haematology, Wellcome-MRC Cambridge Stem Cell Institute, Cambridge CB2 0AW, UK.ORCID 0000-0002-5078-2333
Ivan Imaz-RosshandlerDepartment of Haematology, Wellcome-MRC Cambridge Stem Cell Institute, Cambridge CB2 0AW, UK.ORCID 0000-0001-5975-0138
Lu YangWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-2694-1189
Dave HorsfallWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-8086-812X
Daniela Basurto-LozadaWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0003-3943-8424
Nana-Jane ChipampeWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-8802-0473
Victoria RookWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
Jimmy Tsz Hang LeeWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0003-1208-8356
Mai-Linh TonDepartment of Haematology, Wellcome-MRC Cambridge Stem Cell Institute, Cambridge CB2 0AW, UK.ORCID 0000-0001-6965-0528
Daniel KeitleyWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-6418-2849
Pavel MazinWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0001-9268-3352
M S VijayabaskarDepartment of Haematology, Wellcome-MRC Cambridge Stem Cell Institute, Cambridge CB2 0AW, UK.ORCID 0000-0002-5559-9394
Rebecca HannahDepartment of Haematology, Wellcome-MRC Cambridge Stem Cell Institute, Cambridge CB2 0AW, UK.ORCID 0000-0003-0477-7792
Laure GambardellaWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0001-5771-1565
Kile GreenTranslational and Clinical Research Institute, Newcastle University, Newcastle upon Tyne NE2 4HH, UK.ORCID 0000-0002-4777-5458
Stephane BallereauWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
Megumi InoueSorbonne Université, INSERM, CNRS, Institut de la Vision, Paris, France.ORCID 0000-0002-4201-9215
Elizabeth TuckWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-1837-7549
Valentina LorenziWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-3111-4006
Kwasi KwakwaWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
Clara AlsinetWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-7779-0667
Bayanne OlabiWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
Mohi MiahWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0001-5617-5350
Chloe AdmaneWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
Dorin-Mirel PopescuBiosciences Institute, Newcastle University, Newcastle upon Tyne NE2 4HH, UK.
Meghan AcresBiosciences Institute, Newcastle University, Newcastle upon Tyne NE2 4HH, UK.
David DixonBiosciences Institute, Newcastle University, Newcastle upon Tyne NE2 4HH, UK.ORCID 0000-0002-5904-9074
Thomas NessNovoPath, Department of Pathology, Newcastle Hospitals NHS Foundation Trust, Newcastle upon Tyne NE1 4LP, UK.ORCID 0000-0003-3587-2098
Rowen CoulthardNovoPath, Department of Pathology, Newcastle Hospitals NHS Foundation Trust, Newcastle upon Tyne NE1 4LP, UK.
Steven LisgoBiosciences Institute, Newcastle University, Newcastle upon Tyne NE2 4HH, UK.ORCID 0000-0001-5186-3971
Deborah J HendersonBiosciences Institute, Newcastle University, Newcastle upon Tyne NE2 4HH, UK.ORCID 0000-0002-2705-5998
Emma DannWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-7400-7438
Chenqu SuoWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-8813-0875
Sarah J KinstonDepartment of Haematology, Wellcome-MRC Cambridge Stem Cell Institute, Cambridge CB2 0AW, UK.ORCID 0000-0002-5217-098X
Jong-Eun ParkKorea Advanced Institute of Science and Technology, Daejeon, South Korea.ORCID 0000-0002-1687-2423
Krzysztof PolanskiWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-2586-9576
John MarioniWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0001-9092-0852
Stijn van DongenWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
Kerstin B MeyerWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0001-5906-1498
Marella de BruijnMRC Molecular Haematology Unit, MRC Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford OX3 9DS, UK.
James PalisDepartment of Pediatrics, University of Rochester Medical Center, Rochester, NY 14642, USA.ORCID 0000-0001-7324-1049
Sam BehjatiWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-6600-7665
Elisa LaurentiDepartment of Haematology, Wellcome-MRC Cambridge Stem Cell Institute, Cambridge CB2 0AW, UK.ORCID 0000-0002-9917-9092
Nicola K WilsonDepartment of Haematology, Wellcome-MRC Cambridge Stem Cell Institute, Cambridge CB2 0AW, UK.ORCID 0000-0003-0865-7333
Roser Vento-TormoWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-9870-8474
Alain ChédotalSorbonne Université, INSERM, CNRS, Institut de la Vision, Paris, France.ORCID 0000-0001-7577-3794
Omer BayraktarWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0001-6055-277X
Irene RobertsDepartment of Paediatrics, University of Oxford, Oxford OX3 9DS, UK.ORCID 0000-0002-6094-6397
Laura JardineWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0003-4495-8205
Berthold GöttgensDepartment of Haematology, Wellcome-MRC Cambridge Stem Cell Institute, Cambridge CB2 0AW, UK.ORCID 0000-0001-6302-5705
Sarah A TeichmannWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-6294-6366
Muzlifah HaniffaWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.ORCID 0000-0002-3927-2084
Wellcome Sanger Institute · GBWellcome/MRC Cambridge Stem Cell Institute · GBNewcastle University · GBCentre National de la Recherche Scientifique · FRUniversity of Cambridge · GBNewcastle upon Tyne Hospitals NHS Foundation Trust · GBUniversity of Oxford · GBEuropean Bioinformatics Institute · GBKorea Advanced Institute of Science and Technology · KRMRC Laboratory of Molecular Biology · GBUniversity of Rochester Medical Center · US
Funding
Embryonic natural killer cell development and functionR01HL151777 · NHLBI · WASHINGTON UNIVERSITY · PI PALIS, JAMES, STURGEON, CHRISTOPHER MICHAEL · 2020 to 2023
$2.3MMedical Research Council MC_PC_17230Medical Research Council MC_UU_00029/5Medical Research Council MR/M008975/1Medical Research Council MR/R006237/1Medical Research Council MR/S036113/1NHLBI NIH HHS R01 HL151777Wellcome Trust 107630Wellcome Trust 107931Wellcome Trust 206194Wellcome Trust 206328Wellcome Trust 206328/Z/17/ZWellcome Trust 211276Wellcome Trust 215116Wellcome Trust 220540
Abstract
The extraembryonic yolk sac (YS) ensures delivery of nutritional support and oxygen to the developing embryo but remains ill-defined in humans. We therefore assembled a comprehensive multiomic reference of the human YS from 3 to 8 postconception weeks by integrating single-cell protein and gene expression data. Beyond its recognized role as a site of hematopoiesis, we highlight roles in metabolism, coagulation, vascular development, and hematopoietic regulation. We reconstructed the emergence and decline of YS hematopoietic stem and progenitor cells from hemogenic endothelium and revealed a YS-specific accelerated route to macrophage production that seeds developing organs. The multiorgan functions of the YS are superseded as intraembryonic organs develop, effecting a multifaceted relay of vital functions as pregnancy proceeds.
Indexed as
Embryonic DevelopmentYolk SacAtlases as TopicBlood CoagulationFemaleGene ExpressionGene Expression ProfilingHematopoiesisHumansLiverMacrophagesPregnancy
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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.