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Mechanics of human embryo compaction

Julie Firmin, Nicolas Ecker, Diane Rivet Danon, Virginie Barraud Lange, Hervé Turlier, Catherine Patrat, View ORCID ProfileJean-Léon Maître
doi: https://doi.org/10.1101/2022.01.09.475429
Julie Firmin
1Institut Curie, Université PSL, CNRS UMR3215, INSERM U934, 75005 Paris, France
2Université de Paris, Paris, France
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Nicolas Ecker
3Center for Interdisciplinary Research in Biology, Collège de France, CNRS, INSERM, Université PSL, FHU Prema, Paris, France
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Diane Rivet Danon
4Service de Biologie de la Reproduction - CECOS, Paris Centre Hospital, APHP centre, FHU Prema, 75014
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Virginie Barraud Lange
4Service de Biologie de la Reproduction - CECOS, Paris Centre Hospital, APHP centre, FHU Prema, 75014
5Institut Cochin, Université de Paris, CNRS UMR1016, 75014 Paris, France
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Hervé Turlier
3Center for Interdisciplinary Research in Biology, Collège de France, CNRS, INSERM, Université PSL, FHU Prema, Paris, France
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Catherine Patrat
4Service de Biologie de la Reproduction - CECOS, Paris Centre Hospital, APHP centre, FHU Prema, 75014
5Institut Cochin, Université de Paris, CNRS UMR1016, 75014 Paris, France
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Jean-Léon Maître
1Institut Curie, Université PSL, CNRS UMR3215, INSERM U934, 75005 Paris, France
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  • ORCID record for Jean-Léon Maître
  • For correspondence: jean-leon.maitre@curie.fr
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Abstract

The shaping of the human embryo begins with compaction, during which cells come into close contact and form a tighter structure1,2. Assisted reproductive technology (ART) studies suggest that human embryos fail compaction primarily because of defective adhesion3,4. Based on our current understanding of animal morphogenesis5,6, other morphogenetic engines, such as cell contractility, could be involved in shaping the human embryo. However, the molecular, cellular and physical mechanisms driving human embryo morphogenesis remain uncharacterized. Using micropipette aspiration on human embryos donated to research, we have mapped cell surface tensions during compaction. This reveals a 4-fold increase of tension at the cellmedium interface while cell-cell contacts keep a steady tension. Comparison between human and mouse reveals qualitatively similar but quantitively different mechanical strategies, with human embryos being mechanically least efficient. Inhibition of cell contractility and cell-cell adhesion in human embryos reveal that only contractility controls the surface tension responsible for compaction. Interestingly, if both cellular processes are required for compaction, they exhibit distinct mechanical signatures when faulty. Analyzing the mechanical signature of naturally failing embryos, we find evidence that non-compacting embryos or partially compacting embryos with excluded cells have defective contractility. Together, our study reveals that an evolutionarily conserved increase in cell contractility is required to generate the forces driving the first morphogenetic movement shaping the human body.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted January 11, 2022.
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Mechanics of human embryo compaction
Julie Firmin, Nicolas Ecker, Diane Rivet Danon, Virginie Barraud Lange, Hervé Turlier, Catherine Patrat, Jean-Léon Maître
bioRxiv 2022.01.09.475429; doi: https://doi.org/10.1101/2022.01.09.475429
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Mechanics of human embryo compaction
Julie Firmin, Nicolas Ecker, Diane Rivet Danon, Virginie Barraud Lange, Hervé Turlier, Catherine Patrat, Jean-Léon Maître
bioRxiv 2022.01.09.475429; doi: https://doi.org/10.1101/2022.01.09.475429

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