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Kinematic analysis of cell lineage reveals coherent and robust mechanical deformation patterns in zebrafish gastrulation

View ORCID ProfileDavid Pastor-Escuredo, Benoît Lombardot, Thierry Savy, Adeline Boyreau, View ORCID ProfileJose M. Goicolea, View ORCID ProfileAndrés Santos, Paul Bourgine, View ORCID ProfileJuan C. del Álamo, View ORCID ProfileNadine Peyriéras, María J. Ledesma-Carbayo
doi: https://doi.org/10.1101/054353
David Pastor-Escuredo
1Biomedical Image Technologies, ETSIT, Technical University Madrid, Spain.
2Biomedical Research Center in Bioengineering, Biomaterials and Nanomedicine (CIBERBBN), Spain.
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  • ORCID record for David Pastor-Escuredo
Benoît Lombardot
3UPS3611 Complex Systems Institute Paris Ile-de-France (ISC-PIF), CNRS, Paris, France
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Thierry Savy
3UPS3611 Complex Systems Institute Paris Ile-de-France (ISC-PIF), CNRS, Paris, France
4USR3695 BioEmergences, CNRS, Paris-Saclay University, Gif-sur-Yvette, France.
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Adeline Boyreau
4USR3695 BioEmergences, CNRS, Paris-Saclay University, Gif-sur-Yvette, France.
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Jose M. Goicolea
5Computational Mechanics Group, Technical University Madrid, Spain.
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Andrés Santos
1Biomedical Image Technologies, ETSIT, Technical University Madrid, Spain.
2Biomedical Research Center in Bioengineering, Biomaterials and Nanomedicine (CIBERBBN), Spain.
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Paul Bourgine
3UPS3611 Complex Systems Institute Paris Ile-de-France (ISC-PIF), CNRS, Paris, France
4USR3695 BioEmergences, CNRS, Paris-Saclay University, Gif-sur-Yvette, France.
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Juan C. del Álamo
6Mechanical and Aerospace Engineering Department, University of California San Diego, La Jolla, CA 92093, United States.
7Institute for Engineering in Medicine, University of California San Diego, La Jolla, CA 92093, United States.
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Nadine Peyriéras
3UPS3611 Complex Systems Institute Paris Ile-de-France (ISC-PIF), CNRS, Paris, France
4USR3695 BioEmergences, CNRS, Paris-Saclay University, Gif-sur-Yvette, France.
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  • For correspondence: nadine.peyrieras@cnrs.fr mledesma@die.upm.es
María J. Ledesma-Carbayo
1Biomedical Image Technologies, ETSIT, Technical University Madrid, Spain.
2Biomedical Research Center in Bioengineering, Biomaterials and Nanomedicine (CIBERBBN), Spain.
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  • For correspondence: nadine.peyrieras@cnrs.fr mledesma@die.upm.es
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Abstract

Digital cell lineages reconstructed from 3D+time imaging data provide unique information to unveil mechanical cues and their role in morphogenetic processes. Our methodology based on a kinematic analysis of cell lineage data reveals deformation patterns and quantitative morphogenetic landmarks for a new type of developmental table. The characteristic spatial and temporal length scales of mechanical deformation patterns derived from a continuous approximation of cell displacements indicate a compressible fluid-like behavior of zebrafish gastrulating tissues. The instantaneous deformation rate at the mesoscopic level of the cell’s neighborhood is spatially and temporally heterogeneous. The robustness of mechanical patterns results from their cumulative history along cell trajectories. Unsupervised classification of mechanical descriptor profiles was used to assess the homogeneity of biomechanical cues in cell populations. Further clustering of cell trajectories according to their cumulative mesoscopic biomechanical history during gastrulation revealed ordered and coherent spatiotemporal patterns comparable to that of the embryonic fate map.

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Posted October 19, 2016.
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Kinematic analysis of cell lineage reveals coherent and robust mechanical deformation patterns in zebrafish gastrulation
David Pastor-Escuredo, Benoît Lombardot, Thierry Savy, Adeline Boyreau, Jose M. Goicolea, Andrés Santos, Paul Bourgine, Juan C. del Álamo, Nadine Peyriéras, María J. Ledesma-Carbayo
bioRxiv 054353; doi: https://doi.org/10.1101/054353
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Kinematic analysis of cell lineage reveals coherent and robust mechanical deformation patterns in zebrafish gastrulation
David Pastor-Escuredo, Benoît Lombardot, Thierry Savy, Adeline Boyreau, Jose M. Goicolea, Andrés Santos, Paul Bourgine, Juan C. del Álamo, Nadine Peyriéras, María J. Ledesma-Carbayo
bioRxiv 054353; doi: https://doi.org/10.1101/054353

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