Embryo model completes gastrulation to neurulation and organogenesis

Gianluca Amadei, Charlotte E. Handford, Chengxiang Qiu, Joachim De Jonghe, Hannah Greenfeld, Martin Tran, Beth K. Martin, Dong-Yuan Chen, Alejandro Aguilera-Castrejon, Jacob H. Hanna, Michael B. Elowitz, Florian Hollfelder, Jay Shendure, David M. Glover and Magdalena Zernicka-Goetz ()
Additional contact information
Gianluca Amadei: University of Cambridge
Charlotte E. Handford: University of Cambridge
Chengxiang Qiu: University of Washington
Joachim De Jonghe: University of Cambridge
Hannah Greenfeld: California Institute of Technology
Martin Tran: California Institute of Technology
Beth K. Martin: University of Washington
Dong-Yuan Chen: California Institute of Technology
Alejandro Aguilera-Castrejon: Weizmann Institute of Science
Jacob H. Hanna: Weizmann Institute of Science
Michael B. Elowitz: California Institute of Technology
Florian Hollfelder: University of Cambridge
Jay Shendure: University of Washington
David M. Glover: California Institute of Technology
Magdalena Zernicka-Goetz: University of Cambridge

Nature, 2022, vol. 610, issue 7930, 143-153

Abstract: Abstract Embryonic stem (ES) cells can undergo many aspects of mammalian embryogenesis in vitro1–5, but their developmental potential is substantially extended by interactions with extraembryonic stem cells, including trophoblast stem (TS) cells, extraembryonic endoderm stem (XEN) cells and inducible XEN (iXEN) cells6–11. Here we assembled stem cell-derived embryos in vitro from mouse ES cells, TS cells and iXEN cells and showed that they recapitulate the development of whole natural mouse embryo in utero up to day 8.5 post-fertilization. Our embryo model displays headfolds with defined forebrain and midbrain regions and develops a beating heart-like structure, a trunk comprising a neural tube and somites, a tail bud containing neuromesodermal progenitors, a gut tube, and primordial germ cells. This complete embryo model develops within an extraembryonic yolk sac that initiates blood island development. Notably, we demonstrate that the neurulating embryo model assembled from Pax6-knockout ES cells aggregated with wild-type TS cells and iXEN cells recapitulates the ventral domain expansion of the neural tube that occurs in natural, ubiquitous Pax6-knockout embryos. Thus, these complete embryoids are a powerful in vitro model for dissecting the roles of diverse cell lineages and genes in development. Our results demonstrate the self-organization ability of ES cells and two types of extraembryonic stem cells to reconstitute mammalian development through and beyond gastrulation to neurulation and early organogenesis.

Date: 2022
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DOI: 10.1038/s41586-022-05246-3

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