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Stem cell-derived mouse embryos develop within an extra-embryonic yolk sac to form anterior brain regions and a beating heart

Gianluca Amadei, Charlotte E Handford, Joachim De Jonghe, Florian Hollfelder, David Glover, Magdalena Zernicka-Goetz

Preprint posted on 2 August 2022 https://www.biorxiv.org/content/10.1101/2022.08.01.502375v1

Article now published in at https://www.nature.com/articles/s41586-022-05246-3

and

Mouse-embryo model derived exclusively from embryonic stem cells undergo neurulation and heart development

Kasey Y.C. Lau, Hernan Rubinstein, Carlos W. Gantner, Gianluca Amadei, Yonatan Stelzer, Magdalena Zernicka-Goetz

Preprint posted on 2 August 2022 https://www.biorxiv.org/content/10.1101/2022.08.01.502371v1

Embryonic stem cells, mixed with trophoblast cells and extra-embryonic endodermal cells, make the recipe for a synthetic mouse embryo!

Selected by Monica Tambalo, Juan Moriano, Martin Estermann

Background

Soon after the mouse egg is fertilized, successive cell divisions will increase the number of cells exponentially to form a compact mass of cells. Cells in the outer part of this compact mass will become the trophectoderm, while the inner cells will acquire two alternative fates: either primitive endoderm or epiblast. These distinctive specializations will differentially contribute to the development of the future embryo: while the epiblast will be responsible for the generation of the embryo proper, the extra-embryonic structures will be formed by both the trophectoderm (e.g., placenta) and the primitive endoderm (e.g., yolk sac). Around embryonic day 6.5 (E6.5) in the mouse, a process of finely orchestrated rearrangements of epiblast cells, known as gastrulation, begins which results in the formation of the three primary germ layers: ectoderm, mesoderm, and endoderm (Shahbazi and Zernicka-Goetz, 2018). As the basic body plan of the animal is established, specialized tissues and organs next develop from these germ layers. For example, the neural tube is formed through a process called neurulation, where a portion of the ectoderm (the neuroectoderm) folds into a tube at the midline of the embryo, eventually differentiating into specific regions such as the forebrain at the most anterior part or the spinal cord more posteriorly. The endoderm gives rise to the gastrointestinal and respiratory tract, whereas the mesoderm will form the urogenital system and the somites.

In mammals, embryos develop inside the mother’s body, making the study of early embryogenesis a very difficult task. To solve this problem and identify the key mechanisms required for building an embryo, scientists have been trying to develop in vitro systems that can recapitulate the early developmental stages of mammalian embryogenesis. Several stem cell models of the mouse embryo have been generated in the past decade (Harrison et al., 2017; Rivron et al., 2018; Sozen et al., 2018), suggesting a remarkable self-organizing capacity of the early mammalian embryo (Zhu and Zernicka-goetz, 2020). Scientists were also able to generate human blastocysts in vitro from induced pluripotent stem cells (Liu et al., 2021; Sozen et al., 2021). Additionally, gastruloids and trunk-like structures with a neural tube and somites were generated using mouse embryonic stem cells (Beccari et al., 2018; van den Brink et al., 2020; Sozen et al., 2021; Turner et al., 2017; Veenvliet et al., 2020), but these models are unable to recapitulate post-implantation embryogenesis since patterning signals originating form extraembryonic tissues are absent (Shahbazi and Zernicka-Goetz, 2018).

The Zernicka-Goetz Lab has experimented with different recipes to generate a synthetic mouse embryo and has now found two protocols that support the development of a synthetic embryo through post-implantation stages (Amadei et al., 2022a; Lau et al., 2022). The work led by Amadei (Amadei et al., 2022a) has now been published in Nature (Amadei et al., 2022b). In these two preprints, they describe how they were able to generate in vitro mouse embryoids, using two different approaches, that resemble E8.5 natural mouse embryos. These post-implantation-like embryos went through neurulation, developing forebrain and midbrain, produced pairs of somites, developed a beating heart, and initiated gut development. All this is remarkably similar to the development of a natural mouse embryo (Table 1,2).

Main findings

The ETiX-embryoids

In the first preprint from the Zernicka-Goetz Lab (Amadei et al., 2022a), synthetic embryos were generated by aggregating (1) embryonic stem cells (ESCs) from the epiblast, with (2) trophoblast stem cells (TSC; derived from the extraembryonic ectoderm) and (3) extraembryonic endodermal cells. These last ones were differentiated from ESCs by transiently inducing the expression of the extraembryonic visceral endoderm master regulator Gata4. These ETiX embryos developed structures that are remarkably similar to the ones observed in natural mouse embryos from E7.5 to E8.5 (Table 1).

Table 1. Summary table with the main features of the ETiX embryo

The EiTiX-embryoids

In a second preprint, the members of the Zernicka-Goetz Lab aimed to reconstruct mouse early development by solely using embryonic stem cells and transcription factor-mediated reprogramming (Lau et al., 2022). Synthetic mouse embryos, here named EiTiX-embryoids, were generated aggregating: (1) mESCs for epiblast formation; (2) mESCs with inducible Gata4 expression for extraembryonic endoderm formation; and (3) mESCs with inducible Cdx2 expression for trophectoderm formation. This new culture system using mouse embryonic stem cells simplifies the culture conditions since the three cell types use the same culture media.

Table 2. Summary table with the main features of the EiTiX embryo

 

Of note, a similar approach has been developed by Tarazi and colleagues which was recently published in the journal Cell (Tarazi et al., 2022). Similar to the EiTiX system, their synthetic embryos (sEmbryos) were formed by aggregating non-transduced ESCs with Cdx2-ESCs for the formation of the trophectoderm lineage and Gata4-ESCs to promote primitive endoderm lineage formation. These sEmbryos were grown on an adapted electronic platform which the researchers had previously deployed to grow ex utero mouse embryos for prolonged periods of time (Aguilera-Castrejon et al., 2021).

All these three recent works – ETiX (Amadei et al., 2022a), EiTiX (Lau et al., 2022), as well as the sEmbryos model (Tarazi et al., 2022) – reveal that embryoids recapitulate the development of both embryonic and extraembryonic lineages of the natural mouse embryo, thanks to a detailed analysis of morphology, marker gene expression, and single-cell RNA-seq analyses. Of note, the EiTiX-embryoid model presents some limitations, such as depletion of cell types from the ectoplacental cone lineage, frequently enlarged heart structures, or asynchronicity in cell differentiation. Similarly, sEmbryos presented some differences and/or abnormalities when their development was carefully compared to natural mouse embryos (Tarazi et al., 2022). Nevertheless, these three recipes, even with their current limitations, show that synthetic embryos can adequately complete gastrulation, neurulation, and organogenesis of embryonic and extraembryonic tissues; thus, highlighting the intrinsic capability of naïve pluripotent stem cells to self-organize and give rise to the whole organism in a dish.

Things we like

We are amazed by the striking resemblance of synthetic embryos to natural ones. If one had to blindly assign images to synthetic or natural embryos, it would be a very hard game to play. This resemblance was carefully evaluated by the authors, comparing the embryoids to the natural mouse embryos by immunofluorescence, as well as with a detailed molecular characterization using single-cell RNA-seq. Lastly, the fact that the authors could rescue, to some extent, neural tube defects in the embryoids reveals the great potential of these technologies to model neurodevelopmental disorders and find appropriate treatments. 

When the two preprints, along with the Cell paper from the laboratory of Jacob H. Hanna, became available online we immediately thought that they would have a huge impact on the scientific community and beyond. We were right! After just a few weeks, one of the preprints was published in Nature (Amadei et al., 2022b), and the great resemblance of the synthetic embryos to natural ones was quickly picked up by the press (example: https://www.bbc.com/news/health-62679322). Of course, Twitter has also been buzzing with comments and great discussion points.

The peer-reviewed version (Amadei et al., 2022b) of the preprint (Amadei et al., 2022a) that we’ve highlighted here includes some exciting and noteworthy changes. Some that we particularly liked are: the catchier new title, implementations of the histological characterization, more in-depth analysis of the single-cell RNA-sequencing used to compare cell identities in EiTX-embryoids to natural embryos, new experiments evaluating the consequences of Pax6 deletion, and the more elaborate discussion section. We are now looking forward to seeing the second preprint (Lau et al., 2022) appear in a peer-reviewed journal!

Questions for the authors

  • What is the proportion of aggregates that successfully become ETiX or EiTiX? Do you have thoughts on how the efficiency could be improved?
  • Did you check whether patterning mechanisms (e.g., organizers, signaling centers, the somitogenesis clock) are correctly in place within the ETiX/EiTiX-embryoids?
  • Can you speculate on the requirements for longer culture of ETiX/EiTiX-embryoids? How far do you think the system can be pushed?
  • Do you think a similar approach could be used for building human synthetic embryoids? What are the ethical restrictions on synthetic embryoids currently in place?

References

 Aguilera-Castrejon, A., Oldak, B., Shani, T., Ghanem, N., Itzkovich, C., Slomovich, S., Tarazi, S., Bayerl, J., Chugaeva, V., Ayyash, M., et al. (2021). Ex utero mouse embryogenesis from pre-gastrulation to late organogenesis. Nature 593, 119–124.

Amadei, G., Handford, C.E., De Jonghe, J., Hollfelder, F., Glover, D., and Zernicka-Goetz, M. (2022a). Stem cell-derived mouse embryos develop within an extra-embryonic yolk sac to form anterior brain regions and a beating heart. BioRxiv 2022.08.01.502375.

Amadei, G., Handford, C.E., Qiu, C., De Jonghe, J., Greenfeld, H., Tran, M., Martin, B.K., Chen, D.-Y., Aguilera-castrejon, A., Hanna, J.H., et al. (2022b). Synthetic embryos complete gastrulation to neurulation and organogenesis. Nature 0–1.

Beccari, L., Moris, N., Girgin, M., Turner, D.A., Baillie-Johnson, P., Cossy, A.-C., Lutolf, M.P., Duboule, D., and Arias, A.M. (2018). Multi-axial self-organization properties of mouse embryonic stem cells into gastruloids. Nature 562, 272–276.

van den Brink, S.C., Alemany, A., van Batenburg, V., Moris, N., Blotenburg, M., Vivié, J., Baillie-Johnson, P., Nichols, J., Sonnen, K.F., Martinez Arias, A., et al. (2020). Single-cell and spatial transcriptomics reveal somitogenesis in gastruloids. Nature 582, 405–409.

Harrison, S.E., Sozen, B., Christodoulou, N., Kyprianou, C., and Zernicka-Goetz, M. (2017). Assembly of embryonic and extraembryonic stem cells to mimic embryogenesis in vitro. Science (80-. ). 356, eaal1810.

Lau, K.Y.C., Rubinstein, H., Gantner, C.W., Amadei, G., Stelzer, Y., and Zernicka-Goetz, M. (2022). Mouse-embryo model derived exclusively from embryonic stem cells undergo neurulation and heart development. BioRxiv 2022.08.01.502371.

Liu, X., Tan, J.P., Schröder, J., Aberkane, A., Ouyang, J.F., Mohenska, M., Lim, S.M., Sun, Y.B.Y., Chen, J., Sun, G., et al. (2021). Modelling human blastocysts by reprogramming fibroblasts into iBlastoids. Nature 591, 627–632.

Rivron, N.C., Frias-Aldeguer, J., Vrij, E.J., Boisset, J.-C., Korving, J., Vivié, J., Truckenmüller, R.K., van Oudenaarden, A., van Blitterswijk, C.A., and Geijsen, N. (2018). Blastocyst-like structures generated solely from stem cells. Nature 557, 106–111.

Shahbazi, M.N., and Zernicka-Goetz, M. (2018). Deconstructing and reconstructing the mouse and human early embryo. Nat. Cell Biol. 22.

Sozen, B., Amadei, G., Cox, A., Wang, R., Na, E., Czukiewska, S., Chappell, L., Voet, T., Michel, G., Jing, N., et al. (2018). Self-assembly of embryonic and two extra-embryonic stem cell types into gastrulating embryo-like structures. Nat. Cell Biol. 20, 979–989.

Sozen, B., Jorgensen, V., Zernicka-Goetz, M., and Chen, S. (2021). Reconstructing aspects of human embryogenesis with pluripotent stem cells. Nat. Commun. 1–13.

Tarazi, S., Aguilera-castrejon, A., Joubran, C., Ghanem, N., Roncato, F., Wildschutz, E., Haddad, M., Gomez-cesar, E., Livnat, N., Viukov, S., et al. (2022). Post-Gastrulation Synthetic Embryos Generated Ex Utero from Mouse Naïve ESCs. Cell.

Turner, D.A., Girgin, M., Alonso-crisostomo, L., Trivedi, V., Baillie-johnson, P., Glodowski, C.R., Hayward, P.C., Steventon, B., Lutolf, M.P., and Arias, A.M. (2017). Anteroposterior polarity and elongation in the absence of extra- embryonic tissues and of spatially localised signalling in gastruloids : mammalian embryonic organoids. Development 3894–3906.

Veenvliet, J. V, Bolondi, A., Kretzmer, H., Haut, L., Scholze-Wittler, M., Schifferl, D., Koch, F., Guignard, L., Kumar, A.S., Pustet, M., et al. (2020). Mouse embryonic stem cells self-organize into trunk-like structures with neural tube and somites. Science (80-. ). 370, eaba4937.

Zhu, M., and Zernicka-goetz, M. (2020). ll Principles of Self-Organization of the Mammalian Embryo. Cell 183, 1467–1478.

Tags: stem cells, synthetic embryo

Posted on: 5 September 2022 , updated on: 6 September 2022

doi: https://doi.org/10.1242/prelights.32657

(No Ratings Yet)

4 comments

3 months

Monica Tambalo

As a developmental neurobiologist growing brain organoids myself, I was amazed by the complexity of the synthetic embryos generated by these works. Building a ball of progenitors and neurons is now relatively easy with the right protocol, but there is no proper patterning in the majority of current brain organoid protocols (Tambalo and Lodato, 2020). Seeing the synthetic mouse embryos forming with an anterio-posterior axis, a proper neural tube with dorso-ventral patterning, somite pairs, a beating heart, and many other cool features truly amazed me! I personally think that these works will be instrumental for the understanding of the early phases of mammalian embryogenesis. While reading the preprints, I liked how the authors worked on describing the system they have built with a detailed characterization that resembles how developmental biologists study the similarities and differences of embryos from different species. An ethical debate has also arisen since, to our knowledge, there are no current regulations concerning synthetic embryos and the possibility of building similar embryoids starting from human pluripotent stem cells, which is why we’ve asked the authors to comment on this.

3 months

Juan Moriano

How does a single cell generate a complete organism? The concerted changes in shape and function that take place during development, with commonalities and differences among species, and the specification of a rich variety of cell types truly amazed me when I was an undergraduate student. Currently, as a PhD student, it’s exciting to know that we are witnessing remarkable progress in the field of developmental biology with the help of the organoid technology. The works highlighted in this preLights’ post are milestones in the path to model embryonic development with enough fidelity and reproducibility. I was very happy to collaborate with Monica and Martin while writing this post. It wasn’t an easy task to summarize all relevant aspects of the two preprints, but they made the writing easier and smoother. Also, it was enriching to exchange our opinions while writing drafts, where I found we, very often, held similar views.

3 months

Martin Estermann

As a developmental geneticist, it still fascinates me that aggregated cells in culture have the capacity to form complex embryonic structures with such resemblance to in utero grown embryos. As a young postdoctoral researcher switching from birds to mammalian embryonic models, I now understand the difficulties of in utero development when studying embryonic development. These in vitro embryonic models will allow us to monitor and study mammalian embryonic development, under the microscope, in real time!. Particularly, as I study gonadal development and sex determination, which occurs around E10.5-E12.5 in mice, I am interested to see if these models can continue their development in vitro past the E8.5 developmental stage. The preprints and articles discussed here are the starting point of a new era for mammalian developmental biologists. I can’t wait to see where the science takes us.

1 month

Monica Tambalo

Just a few months after the preprint from Lau and colleagues was posted on bioRxiv it got published in Cell Stem Cell (https://doi.org/10.1016/j.stem.2022.08.013). After comparing the two versions of the manuscript, I did not spot any major differences. The main figures in the published paper are almost identical to the ones in the preprint with just some minor esthetical changes. One difference I could observe is in Figure 4C as part of which – in the published version – a less magnified embryo is shown in the right corner and a few labels were added to help understand the anatomy. The supplementary figures are almost identical between the preprint and the published paper. Now Supplementary Figure 5 has a more detailed analysis of the cellular composition of neurulating embryoids using the single-cell RNA-sequencing data. A few impressive movies have also been included in the published paper showing the beating heart of the synthetic embryos!

The text is very similar when comparing the preprint and published version of this paper and the only real difference is that the latter has a longer discussion section. Just when the preprint was posted on bioRxiv, another group published a similar approach (Tarazi et al., 2022), and related work from the Zernicka-Goetz lab, also discussed in our preLight, was published in Nature (Amadei et al., 2022). The discussion section in the published paper has therefore been extended and comments on these parallel approaches. This also covers the question we asked the authors as part of the preLight about the comparison between the two methods. Lastly, there is a new section covering the limitations of the study, which I really enjoyed reading since it gives a few more details about the successful recipe to generate synthetic mouse embryos.

Amadei, G., Handford, C.E., Qiu, C., De Jonghe, J., Greenfeld, H., Tran, M., Martin, B.K., Chen, D.-Y., Aguilera-castrejon, A., Hanna, J.H., et al. (2022b). Synthetic embryos complete gastrulation to neurulation and organogenesis. Nature 0–1.

Tarazi, S., Aguilera-castrejon, A., Joubran, C., Ghanem, N., Roncato, F., Wildschutz, E., Haddad, M., Gomez-cesar, E., Livnat, N., Viukov, S., et al. (2022). Post-Gastrulation Synthetic Embryos Generated Ex Utero from Mouse Naïve ESCs. Cell.

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