Temporal variability and cell mechanics control robustness in mammalian embryogenesis

Dimitri Fabrèges; Bernat Corominas-Murtra; Prachiti Moghe; Alison Kickuth; Takafumi Ichikawa; Chizuru Iwatani; Tomoyuki Tsukiyama; Nathalie Daniel; Julie Gering; Anniek Stokkermans; Adrian Wolny; Anna Kreshuk; Véronique Duranthon; Virginie Uhlmann; Edouard Hannezo; Takashi Hiiragi

doi:10.1126/science.adh1145

Temporal variability and cell mechanics control robustness in mammalian embryogenesis

Dimitri Fabrèges, Bernat Corominas-Murtra, Prachiti Moghe, Alison Kickuth, Takafumi Ichikawa, Chizuru Iwatani, Tomoyuki Tsukiyama, Nathalie Daniel, Julie Gering, Anniek Stokkermans, Adrian Wolny, Anna Kreshuk, Véronique Duranthon, Virginie Uhlmann, Edouard Hannezo, Takashi Hiiragi

Hubrecht Institute

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

4 Citations (Scopus)

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.

Original language	English
Pages (from-to)	eadh1145
Journal	Science
Volume	386
Issue number	6718
DOIs	https://doi.org/10.1126/science.adh1145
Publication status	Published - 11 Oct 2024

Keywords

Animals
Mice
Rabbits
Actomyosin/metabolism
Blastocyst/physiology
Blastomeres/cytology
Cell Division
Embryo, Mammalian/cytology
Embryonic Development
Stochastic Processes

Access to Document

10.1126/science.adh1145

Cite this

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., Uhlmann, V., Hannezo, E., & Hiiragi, T. (2024). Temporal variability and cell mechanics control robustness in mammalian embryogenesis. Science, 386(6718), eadh1145. https://doi.org/10.1126/science.adh1145

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title = "Temporal variability and cell mechanics control robustness in mammalian embryogenesis",

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.",

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author = "Dimitri Fabr{\`e}ges and Bernat Corominas-Murtra and Prachiti Moghe and Alison Kickuth and Takafumi Ichikawa and Chizuru Iwatani and Tomoyuki Tsukiyama and Nathalie Daniel and Julie Gering and Anniek Stokkermans and Adrian Wolny and Anna Kreshuk and V{\'e}ronique Duranthon and Virginie Uhlmann and Edouard Hannezo and Takashi Hiiragi",

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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, Uhlmann, V, Hannezo, E & Hiiragi, T 2024, 'Temporal variability and cell mechanics control robustness in mammalian embryogenesis', Science, vol. 386, no. 6718, pp. eadh1145. https://doi.org/10.1126/science.adh1145

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AU - Fabrèges, Dimitri

AU - Corominas-Murtra, Bernat

AU - Moghe, Prachiti

AU - Kickuth, Alison

AU - Ichikawa, Takafumi

AU - Iwatani, Chizuru

AU - Tsukiyama, Tomoyuki

AU - Daniel, Nathalie

AU - Gering, Julie

AU - Stokkermans, Anniek

AU - Wolny, Adrian

AU - Kreshuk, Anna

AU - Duranthon, Véronique

AU - Uhlmann, Virginie

AU - Hannezo, Edouard

AU - Hiiragi, Takashi

PY - 2024/10/11

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AB - 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.

KW - Animals

KW - Mice

KW - Rabbits

KW - Actomyosin/metabolism

KW - Blastocyst/physiology

KW - Blastomeres/cytology

KW - Cell Division

KW - Embryo, Mammalian/cytology

KW - Embryonic Development

KW - Stochastic Processes

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