Temporal variability and cell mechanics control robustness in mammalian embryogenesis
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.
Authors
- Adrian Wolny (ORCID: https://orcid.org/0000-0003-2794-4266)
- Dimitri Fabrèges (ORCID: https://orcid.org/0000-0001-6603-1510)
- Nathalie Daniel (ORCID: https://orcid.org/0000-0002-2251-1296)
- Bernat Corominas‐Murtra (ORCID: https://orcid.org/0000-0001-9806-5643)
- Édouard Hannezo (ORCID: https://orcid.org/0000-0001-6005-1561)
- Anna Kreshuk (ORCID: https://orcid.org/0000-0003-1334-6388)
- Julie Gering (ORCID: https://orcid.org/0000-0001-6917-9860)
- Alison Kickuth (ORCID: https://orcid.org/0000-0002-8571-7902)
- Takafumi Ichikawa (ORCID: https://orcid.org/0000-0002-0490-4176)
- Anniek Stokkermans (ORCID: https://orcid.org/0000-0002-9013-9983)
- Tomoyuki Tsukiyama (ORCID: https://orcid.org/0000-0002-2657-7719)
- Takashi Hiiragi (ORCID: https://orcid.org/0000-0003-4964-7203)
- Véronique Duranthon (ORCID: https://orcid.org/0000-0001-8120-7481)
- Prachiti Moghe (ORCID: https://orcid.org/0000-0002-7924-9671)
- Virginie Uhlman
- Chizuru Iwatani
Institutions
- European Bioinformatics Institute (GB)
- Institute of Science and Technology Austria (AT)
- University of Graz (AT)
- Shiga University of Medical Science (JP)
- École Nationale Vétérinaire d'Alfort (FR)
- Université de Versailles Saint-Quentin-en-Yvelines (FR)
- Kyoto University (JP)
- Université Paris-Saclay (FR)
- Microbiologie de l’alimentation au service de la santé (FR)
- Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
- Hubrecht Institute for Developmental Biology and Stem Cell Research (NL)
- European Molecular Biology Laboratory (DE)
- Biologie de la Reproduction, Environnement, Epigénétique et Développement (FR)
Publication Details
- Journal
- Science
- Published
- 2024-10-10
- DOI
- https://doi.org/10.1126/science.adh1145
- Citations
- 19
- Primary Topic
- Pluripotent Stem Cells Research
- Type
- article
- Field-Weighted Citation Impact
- 4.44