Pluripotent stem cell-derived model of the post-implantation human embryo.
Female
Humans
Pregnancy
Bone Morphogenetic Proteins
Cell Differentiation
Embryo Implantation
Embryo, Mammalian
/ cytology
Embryoid Bodies
/ cytology
Embryonic Development
Germ Layers
/ cytology
Human Embryonic Stem Cells
/ cytology
Models, Biological
Transcription Factors
/ genetics
Pluripotent Stem Cells
/ cytology
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
Oct 2023
Oct 2023
Historique:
received:
14
11
2022
accepted:
23
06
2023
medline:
23
10
2023
pubmed:
28
6
2023
entrez:
27
6
2023
Statut:
ppublish
Résumé
The human embryo undergoes morphogenetic transformations following implantation into the uterus, but our knowledge of this crucial stage is limited by the inability to observe the embryo in vivo. Models of the embryo derived from stem cells are important tools for interrogating developmental events and tissue-tissue crosstalk during these stages
Identifiants
pubmed: 37369347
doi: 10.1038/s41586-023-06368-y
pii: 10.1038/s41586-023-06368-y
pmc: PMC10584688
doi:
Substances chimiques
Bone Morphogenetic Proteins
0
SOX17 protein, human
0
Transcription Factors
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
584-593Subventions
Organisme : Wellcome Trust
Pays : United Kingdom
Commentaires et corrections
Type : CommentIn
Type : CommentIn
Type : ErratumIn
Informations de copyright
© 2023. The Author(s).
Références
Rossant, J. & Tam, P. P. L. Early human embryonic development: blastocyst formation to gastrulation. Dev. Cell 57, 152–165 (2022).
pubmed: 35077679
doi: 10.1016/j.devcel.2021.12.022
Molè, M. A. et al. A single cell characterisation of human embryogenesis identifies pluripotency transitions and putative anterior hypoblast centre. Nat. Commun. 12, 3679 (2021).
pubmed: 34140473
pmcid: 8211662
doi: 10.1038/s41467-021-23758-w
Clark A. T, et al.Human embryo research, stem cell-derived embryo models and in vitro gametogenesis: considerations leading to the revised ISSCR guidelines. Stem Cell Rep. 16, 1416–1424 (2021).
doi: 10.1016/j.stemcr.2021.05.008
Macklon, N. S. Conception to ongoing pregnancy: the ‘black box’ of early pregnancy loss. Hum. Reprod. Update 8, 333–343 (2002).
pubmed: 12206468
doi: 10.1093/humupd/8.4.333
Ross, C. & Boroviak, T. E. Origin and function of the yolk sac in primate embryogenesis. Nat. Commun. 11, 3760 (2020).
pubmed: 32724077
pmcid: 7387521
doi: 10.1038/s41467-020-17575-w
Deglincerti, A. et al. Self-organization of the in vitro attached human embryo. Nature 533, 251–254 (2016).
pubmed: 27144363
doi: 10.1038/nature17948
Morris, S. A. et al. Dynamics of anterior–posterior axis formation in the developing mouse embryo. Nat. Commun. 3, 673–673 (2012).
pubmed: 22334076
doi: 10.1038/ncomms1671
Shahbazi, M. N. et al. Self-organization of the human embryo in the absence of maternal tissues. Nat. Cell Biol. 18, 700–708 (2016).
pubmed: 27144686
pmcid: 5049689
doi: 10.1038/ncb3347
Liu, X. et al. Modelling human blastocysts by reprogramming fibroblasts into iBlastoids. Nature 591, 627–632 (2021).
pubmed: 33731926
doi: 10.1038/s41586-021-03372-y
Sozen, B. et al. Reconstructing aspects of human embryogenesis with pluripotent stem cells. Nat. Commun. 12, 5550 (2021).
pubmed: 34548496
pmcid: 8455697
doi: 10.1038/s41467-021-25853-4
Kagawa, H. et al. Human blastoids model blastocyst development and implantation. Nature 601, 600–605 (2022).
pubmed: 34856602
doi: 10.1038/s41586-021-04267-8
Yanagida, A. et al. Naive stem cell blastocyst model captures human embryo lineage segregation. Cell Stem Cell 28, 1016–1022.e1014 (2021).
pubmed: 33957081
pmcid: 8189436
doi: 10.1016/j.stem.2021.04.031
Yu, L. et al. Blastocyst-like structures generated from human pluripotent stem cells. Nature 591, 620–626 (2021).
pubmed: 33731924
doi: 10.1038/s41586-021-03356-y
Simunovic, M. et al. A 3D model of a human epiblast reveals BMP4-driven symmetry breaking. Nat. Cell Biol. 21, 900–910 (2019).
pubmed: 31263269
doi: 10.1038/s41556-019-0349-7
Zheng, Y. et al. Controlled modelling of human epiblast and amnion development using stem cells. Nature 573, 421–425 (2019).
pubmed: 31511693
pmcid: 8106232
doi: 10.1038/s41586-019-1535-2
Moris, N. et al. An in vitro model of early anteroposterior organization during human development. Nature 582, 410–415 (2020).
pubmed: 32528178
doi: 10.1038/s41586-020-2383-9
Warmflash, A., Sorre, B., Etoc, F., Siggia, E. D. & Brivanlou, A. H. A method to recapitulate early embryonic spatial patterning in human embryonic stem cells. Nat. Methods 11, 847–854 (2014).
pubmed: 24973948
pmcid: 4341966
doi: 10.1038/nmeth.3016
Simunovic, M., Siggia, E. D. & Brivanlou, A. H. In vitro attachment and symmetry breaking of a human embryo model assembled from primed embryonic stem cells. Cell Stem Cell. 29, 962–972.e964 (2022).
Amadei, G. et al. Embryo model completes gastrulation to neurulation and organogenesis. Nature 610, 143–153 (2022).
pubmed: 36007540
pmcid: 9534772
doi: 10.1038/s41586-022-05246-3
Lau, K. Y. C. et al. Mouse embryo model derived exclusively from embryonic stem cells undergoes neurulation and heart development. Cell Stem Cell 29, 1445–1458.e1448 (2022).
pubmed: 36084657
pmcid: 9648694
doi: 10.1016/j.stem.2022.08.013
Tarazi, S. et al. Post-gastrulation synthetic embryos generated ex utero from mouse naïve ESCs. Cell 185, 3290–3306.e25 (2022).
pubmed: 35988542
pmcid: 9439721
doi: 10.1016/j.cell.2022.07.028
Yan, L. et al. Single-cell RNA-seq profiling of human preimplantation embryos and embryonic stem cells. Nat. Struct. Mol. Biol. 20, 1131–1139 (2013).
pubmed: 23934149
doi: 10.1038/nsmb.2660
Blakeley, P. et al. Defining the three cell lineages of the human blastocyst by single-cell RNA-seq. Development 142, 3613–3613 (2015).
pubmed: 26487783
pmcid: 4631772
doi: 10.1242/dev.131235
Petropoulos, S. et al. Single-cell RNA-seq reveals lineage and X chromosome dynamics in human preimplantation embryos. Cell 165, 1012–1026 (2016).
pubmed: 27062923
pmcid: 4868821
doi: 10.1016/j.cell.2016.03.023
Zhou, F. et al. Reconstituting the transcriptome and DNA methylome landscapes of human implantation. Nature 572, 660–664 (2019).
pubmed: 31435013
doi: 10.1038/s41586-019-1500-0
Xiang, L. et al. A developmental landscape of 3D-cultured human pre-gastrulation embryos. Nature 577, 537–542 (2020).
pubmed: 31830756
doi: 10.1038/s41586-019-1875-y
Wamaitha, S. E. et al. Gata6 potently initiates reprograming of pluripotent and differentiated cells to extraembryonic endoderm stem cells. Genes Dev. 29, 1239–1255 (2015).
pubmed: 26109048
pmcid: 4495396
doi: 10.1101/gad.257071.114
Séguin, C. A., Draper, J. S., Nagy, A. & Rossant, J. Establishment of endoderm progenitors by SOX transcription factor expression in human embryonic stem cells. Cell Stem Cell 3, 182–195 (2008).
pubmed: 18682240
doi: 10.1016/j.stem.2008.06.018
Krendl, C. et al. GATA2/3–TFAP2A/C transcription factor network couples human pluripotent stem cell differentiation to trophectoderm with repression of pluripotency. Proc. Natl Acad. Sci USA 114, E9579–E9588 (2017).
pubmed: 29078328
pmcid: 5692555
doi: 10.1073/pnas.1708341114
Linneberg-Agerholm, M. et al. Naïve human pluripotent stem cells respond to Wnt, Nodal and LIF signalling to produce expandable naïve extra-embryonic endoderm. Development 146, dev180620 (2019).
pubmed: 31740534
doi: 10.1242/dev.180620
Mackinlay, K. M. L. et al. An in vitro stem cell model of human epiblast and yolk sac interaction. eLife 10, e63930 (2021).
pubmed: 34403333
pmcid: 8370770
doi: 10.7554/eLife.63930
Dong, C. et al. Derivation of trophoblast stem cells from naïve human pluripotent stem cells. eLife 9, e52504 (2020).
pubmed: 32048992
pmcid: 7062471
doi: 10.7554/eLife.52504
Liu, X. et al. Reprogramming roadmap reveals route to human induced trophoblast stem cells. Nature 586, 101–107 (2020).
pubmed: 32939092
doi: 10.1038/s41586-020-2734-6
Pham, T. X. A. et al. Modeling human extraembryonic mesoderm cells using naive pluripotent stem cells. Cell Stem Cell 29, 1346–1365.e1310 (2022).
pubmed: 36055191
pmcid: 9438972
doi: 10.1016/j.stem.2022.08.001
Zeevaert, K., Elsafi Mabrouk, M. H., Wagner, W. & Goetzke, R. Cell mechanics in embryoid bodies. Cells 9, 2270 (2020).
pubmed: 33050550
pmcid: 7599659
doi: 10.3390/cells9102270
Abe, K. et al. Endoderm-specific gene expression in embryonic stem cells differentiated to embryoid bodies. Exp. Cell Res. 229, 27–34 (1996).
pubmed: 8940246
doi: 10.1006/excr.1996.0340
Tyser, R. C. V. et al. Single-cell transcriptomic characterization of a gastrulating human embryo. Nature 600, 285–289 (2021).
pubmed: 34789876
doi: 10.1038/s41586-021-04158-y
Ma, H. et al. In vitro culture of cynomolgus monkey embryos beyond early gastrulation. Science 366, eaax7890 (2019).
pubmed: 31672918
doi: 10.1126/science.aax7890
Yang, R. et al. Amnion signals are essential for mesoderm formation in primates. Nat. Commun. 12, 5126 (2021).
pubmed: 34446705
pmcid: 8390679
doi: 10.1038/s41467-021-25186-2
Nakamura, T. et al. A developmental coordinate of pluripotency among mice, monkeys and humans. Nature 537, 57–62 (2016).
pubmed: 27556940
doi: 10.1038/nature19096
Munger, C. et al. Microgel culture and spatial identity mapping elucidate the signalling requirements for primate epiblast and amnion formation. Development 149, dev200263 (2022).
pubmed: 36125063
doi: 10.1242/dev.200263
Chen, D. et al. Human primordial germ cells are specified from lineage-primed progenitors. Cell Rep. 29, 4568–4582 e4565 (2019).
pubmed: 31875561
pmcid: 6939677
doi: 10.1016/j.celrep.2019.11.083
Castillo-Venzor, A. et al. Origin and segregation of the human germline. Life Sci. Alliance 6, e202201706 (2023).
pubmed: 37217306
pmcid: 10203729
doi: 10.26508/lsa.202201706
Jo, K. et al. Efficient differentiation of human primordial germ cells through geometric control reveals a key role for Nodal signaling. eLife 11, e72811 (2022).
pubmed: 35394424
pmcid: 9106331
doi: 10.7554/eLife.72811
Luckett, W. P. Origin and differentiation of the yolk sac and extraembryonic mesoderm in presomite human and rhesus monkey embryos. Am. J. Anat. 152, 59–97 (1978).
pubmed: 98035
doi: 10.1002/aja.1001520106
Mukherjee, S. et al. Sox17 and beta-catenin co-occupy Wnt-responsive enhancers to govern the endoderm gene regulatory network. eLife 9, e58029 (2020).
pubmed: 32894225
pmcid: 7498262
doi: 10.7554/eLife.58029
Young, M. D. et al. Single-cell transcriptomes from human kidneys reveal the cellular identity of renal tumors. Science 361, 594–599 (2018).
pubmed: 30093597
pmcid: 6104812
doi: 10.1126/science.aat1699
Bredenkamp, N. et al. Wnt inhibition facilitates RNA-mediated reprogramming of human somatic cells to naive pluripotency. Stem Cell Rep. 13, 1083–1098 (2019).
doi: 10.1016/j.stemcr.2019.10.009
Amadei, G. et al. Inducible stem-cell-derived embryos capture mouse morphogenetic events in vitro. Dev. Cell 56, 366–382.e369 (2021).
pubmed: 33378662
pmcid: 7883308
doi: 10.1016/j.devcel.2020.12.004
Stuart, T. et al. Comprehensive integration of single-cell data. Cell 177, 1888–1902.e1821 (2019).
pubmed: 31178118
pmcid: 6687398
doi: 10.1016/j.cell.2019.05.031
Stuart, T., Srivastava, A., Madad, S., Lareau, C. A. & Satija, R. Single-cell chromatin state analysis with Signac. Nat. Methods 18, 1333–1341 (2021).
pubmed: 34725479
pmcid: 9255697
doi: 10.1038/s41592-021-01282-5
Germain, P. L., Lun, A., Garcia Meixide, C., Macnair, W. & Robinson, M. D. Doublet identification in single-cell sequencing data using scDblFinder. F1000Res 10, 979 (2021).
pubmed: 35814628
doi: 10.12688/f1000research.73600.1
Schep, A. N., Wu, B., Buenrostro, J. D. & Greenleaf, W. J. chromVAR: inferring transcription-factor-associated accessibility from single-cell epigenomic data. Nat. Methods 14, 975–978 (2017).
pubmed: 28825706
pmcid: 5623146
doi: 10.1038/nmeth.4401
Blanco-Carmona, E. Generating publication ready visualizations for Single Cell transcriptomics using SCpubr. Preprint at bioRxiv https://doi.org/10.1101/2022.02.28.482303 (2022).
Kiselev, V. Y., Yiu, A. & Hemberg, M. scmap: projection of single-cell RNA-seq data across data sets. Nat. Methods 15, 359–362 (2018).
pubmed: 29608555
doi: 10.1038/nmeth.4644
Li, C., Virgilio, M. C., Collins, K. L. & Welch, J. D. Multi-omic single-cell velocity models epigenome-transcriptome interactions and improves cell fate prediction. Nat. Biotechnol. 41, 387–398 (2023).
pubmed: 36229609
doi: 10.1038/s41587-022-01476-y
Campbell, K. R. & Yau, C. switchde: inference of switch-like differential expression along single-cell trajectories. Bioinformatics 33, 1241–1242 (2017).
pubmed: 28011787
doi: 10.1093/bioinformatics/btw798
Efremova, M., Vento-Tormo, M., Teichmann, S. A. & Vento-Tormo, R. CellPhoneDB: inferring cell–cell communication from combined expression of multi-subunit ligand–receptor complexes. Nat. Protoc. 15, 1484–1506 (2020).
pubmed: 32103204
doi: 10.1038/s41596-020-0292-x
Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527 (2016).
pubmed: 27043002
doi: 10.1038/nbt.3519
Melsted, P. et al. Modular, efficient and constant-memory single-cell RNA-seq preprocessing. Nat. Biotechnol. 39, 813–818 (2021).
pubmed: 33795888
doi: 10.1038/s41587-021-00870-2
Townes, F. W. & Irizarry, R. A. Quantile normalization of single-cell RNA-seq read counts without unique molecular identifiers. Genome Biol. 21, 160 (2020).
pubmed: 32620142
pmcid: 7333325
doi: 10.1186/s13059-020-02078-0