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Gastruloids develop the three body axes in the absence of extraembryonic tissues and spatially localised signalling

View ORCID ProfileD.A. Turner, L. Alonso-Crisostomo, M. Girgin, View ORCID ProfileP. Baillie-Johnson, C. R. Glodowski, P. C. Hayward, J. Collignon, C. Gustavsen, P. Serup, View ORCID ProfileB. Steventon, M. Lutolf, A. Martinez Arias
doi: https://doi.org/10.1101/104539
D.A. Turner
1Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, United Kingdom
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  • For correspondence: ama11@cam.ac.uk dat40@cam.ac.ku
L. Alonso-Crisostomo
1Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, United Kingdom
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M. Girgin
2Laboratory of Stem Cell Bioengineering, Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland
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P. Baillie-Johnson
1Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, United Kingdom
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C. R. Glodowski
1Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, United Kingdom
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P. C. Hayward
1Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, United Kingdom
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J. Collignon
3Université Paris-Diderot, CNRS, Institut Jacques Monod, UMR 7592, Development and Neurobiology Programme, F-75013 Paris, France
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C. Gustavsen
4Danish Stem Cell Center, University of Copenhagen, DK-2200 Copenhagen, Denmark
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P. Serup
4Danish Stem Cell Center, University of Copenhagen, DK-2200 Copenhagen, Denmark
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B. Steventon
1Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, United Kingdom
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M. Lutolf
2Laboratory of Stem Cell Bioengineering, Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland
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A. Martinez Arias
1Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, United Kingdom
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  • For correspondence: ama11@cam.ac.uk dat40@cam.ac.ku
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Abstract

Establishment of the three body axes is a critical step during animal development. In mammals, genetic studies have shown that a combination of precisely deployed signals from extraembryonic tissues position the anteroposterior axis (AP) within the embryo and lead to the emergence of the dorsoventral (DV) and left-right (LR) axes. We have used Gastruloids, embryonic organoids, as a model system to understand this process and find that they are able to develop AP, DV and LR axes as well as to undergo axial elongation in a manner that mirror embryos. The Gastruloids can be grown for 160 hours and form derivatives from ectoderm, mesoderm and endoderm. We focus on the AP axis and show that in the Gastruloids this axis is registered in the expression of T/Bra at one pole that corresponds to the tip of the elongation. We find that localisation of T/Bra expression depends on the combined activities of Wnt/β-Catenin and Nodal/Smad2,3 signalling, and that BMP signalling is dispensable for this process. Furthermore, AP axis specification occurs in the absence of both extraembryonic tissues and of localised sources of signalling. Our experiments show that Nodal, together with Wnt/β-Catenin signalling, is essential for the expression of T/Bra but that Wnt signalling has a separable activity in the elongation of the axis. The results lead us to suggest that, in the embryo, the role of the extraembryonic tissues might not be to induce the axes but to bias an intrinsic ability of the embryo to break its initial symmetry and organise its axes.

One sentence summary Culture of aggregates of defined number of Embryonic Stem cells leads to self-organised embryo-like structures which, in the absence of localised signalling from extra embryonic tissues and under the autonomous influence of Wnt and Nodal signalling, develop the three main axes of the body.

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Posted January 31, 2017.
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Gastruloids develop the three body axes in the absence of extraembryonic tissues and spatially localised signalling
D.A. Turner, L. Alonso-Crisostomo, M. Girgin, P. Baillie-Johnson, C. R. Glodowski, P. C. Hayward, J. Collignon, C. Gustavsen, P. Serup, B. Steventon, M. Lutolf, A. Martinez Arias
bioRxiv 104539; doi: https://doi.org/10.1101/104539
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Gastruloids develop the three body axes in the absence of extraembryonic tissues and spatially localised signalling
D.A. Turner, L. Alonso-Crisostomo, M. Girgin, P. Baillie-Johnson, C. R. Glodowski, P. C. Hayward, J. Collignon, C. Gustavsen, P. Serup, B. Steventon, M. Lutolf, A. Martinez Arias
bioRxiv 104539; doi: https://doi.org/10.1101/104539

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