Temporal variability and cell mechanics control robustness in mammalian embryogenesis
Fabrèges D, Corominas-Murtra B, Moghe P, Kickuth A, Ichikawa T, Iwatani C, Tsukiyama T, Daniel N, Gering J, Stokkermans A, Wolny A, Kreshuk A, Duranthon V, Uhlman V, Hannezo EB, Hiiragi T. 2024. Temporal variability and cell mechanics control robustness in mammalian embryogenesis. Science. 386(6718), eadh1145.
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Journal Article
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Author
Fabrèges, Dimitri;
Corominas-Murtra, BernatISTA ;
Moghe, Prachiti;
Kickuth, Alison;
Ichikawa, Takafumi;
Iwatani, Chizuru;
Tsukiyama, Tomoyuki;
Daniel, Nathalie;
Gering, Julie;
Stokkermans, Anniek;
Wolny, Adrian;
Kreshuk, Anna
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All
Corresponding author has ISTA affiliation
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Abstract
How living systems achieve precision in form and function despite their intrinsic stochasticity is a fundamental yet ongoing question in biology. We generated morphomaps of preimplantation embryogenesis in mouse, rabbit, and monkey embryos, and these morphomaps revealed that although blastomere divisions desynchronized passively, 8-cell embryos converged toward robust three-dimensional shapes. Using topological analysis and genetic perturbations, we found that embryos progressively changed their cellular connectivity to a preferred topology, which could be predicted by a physical model in which actomyosin contractility and noise facilitate topological transitions, lowering surface energy. This mechanism favored regular embryo packing and promoted a higher number of inner cells in the 16-cell embryo. Synchronized division reduced embryo packing and generated substantially more misallocated cells and fewer inner-cell–mass cells. These findings suggest that stochasticity in division timing contributes to robust patterning.
Publishing Year
Date Published
2024-10-11
Journal Title
Science
Publisher
AAAS
Acknowledgement
We are grateful to the members of the Hiiragi laboratory for discussions and comments on the manuscript: R. Bloehs, S. Friese, S. Hozeifi, L. Pérez, and W. Schwarzer for their technical support; V. Janssen for establishing the PAB protocol; members of the Tsukiyama group for the animal care with monkeys, in particular H. Tsuchiya and M. Nakaya; Unité Commune d’Expérimentation Animale (UCEA, Jouy-en-Josas, France) for the animal care with rabbits; the EMBL electronic and mechanical workshops and the EMBL animal facility for their support; We thank Luxendo for the close collaboration in developing the light-sheet microscopy for mammalian embryos.
Funding: This work was funded by the following: EMBL Interdisciplinary Postdoc Program (EIPOD) under Marie Sklodowska Curie Actions COFUND III RTD (to D.F.); JSPS Overseas Research Fellowship (to T.I.); Field of excellence “Complexity of life in basic research and innovation” of the University of Graz (to B.C.M.); European Research Council, ERC Advanced Grant “SelforganisingEmbryo”, grant agreement 742732; ERC Advanced Grant “COORDINATION” grant agreement 101055287 (to T.H.); Stichting LSH-TKI, grant LSHM21020 (to T.H.) JSPS KAKENHI grants JP21H05038 and JP22H05166 (to T.H.)
Volume
386
Issue
6718
Article Number
eadh1145
eISSN
IST-REx-ID
Cite this
Fabrèges D, Corominas-Murtra B, Moghe P, et al. Temporal variability and cell mechanics control robustness in mammalian embryogenesis. Science. 2024;386(6718). doi:10.1126/science.adh1145
Fabrèges, D., Corominas-Murtra, B., Moghe, P., Kickuth, A., Ichikawa, T., Iwatani, C., … Hiiragi, T. (2024). Temporal variability and cell mechanics control robustness in mammalian embryogenesis. Science. AAAS. https://doi.org/10.1126/science.adh1145
Fabrèges, Dimitri, Bernat Corominas-Murtra, Prachiti Moghe, Alison Kickuth, Takafumi Ichikawa, Chizuru Iwatani, Tomoyuki Tsukiyama, et al. “Temporal Variability and Cell Mechanics Control Robustness in Mammalian Embryogenesis.” Science. AAAS, 2024. https://doi.org/10.1126/science.adh1145.
D. Fabrèges et al., “Temporal variability and cell mechanics control robustness in mammalian embryogenesis,” Science, vol. 386, no. 6718. AAAS, 2024.
Fabrèges D, Corominas-Murtra B, Moghe P, Kickuth A, Ichikawa T, Iwatani C, Tsukiyama T, Daniel N, Gering J, Stokkermans A, Wolny A, Kreshuk A, Duranthon V, Uhlman V, Hannezo EB, Hiiragi T. 2024. Temporal variability and cell mechanics control robustness in mammalian embryogenesis. Science. 386(6718), eadh1145.
Fabrèges, Dimitri, et al. “Temporal Variability and Cell Mechanics Control Robustness in Mammalian Embryogenesis.” Science, vol. 386, no. 6718, eadh1145, AAAS, 2024, doi:10.1126/science.adh1145.
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