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Multiscale quantification of tissue behavior during amniote embryo axis elongation

Bertrand Bénazéraf, Mathias Beaupeux, Martin Tchernookov, Allison Wallingford, Tasha Salisbury, Amelia Shirtz, Andrew Shirtz, Dave Huss, Olivier Pourquié, Paul François, Rusty Lansford
doi: https://doi.org/10.1101/053124
Bertrand Bénazéraf
1Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), CNRS (UMR 7104), Inserm U964, Université de Strasbourg, 67400 Illkirch Graffenstaden, France.
2Department of Radiology and Developmental Neuroscience Program, Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, CA 90027, USA.
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  • For correspondence: bertrand.benazeraf@univ-tlse3.fr pourquie@genetics.med.harvard.edu paulf@physics.mcgill.ca rustylansford@gmail.com
Mathias Beaupeux
4Ernest Rutherford Physics Building, McGill University, 3600 rue University, Montréal, QC, Canada.
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Martin Tchernookov
4Ernest Rutherford Physics Building, McGill University, 3600 rue University, Montréal, QC, Canada.
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Allison Wallingford
2Department of Radiology and Developmental Neuroscience Program, Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, CA 90027, USA.
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Tasha Salisbury
2Department of Radiology and Developmental Neuroscience Program, Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, CA 90027, USA.
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Amelia Shirtz
2Department of Radiology and Developmental Neuroscience Program, Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, CA 90027, USA.
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Andrew Shirtz
7Northern Michigan University Computer Science and Mathematics Department, Marquette, MI, 49855, USA.
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Dave Huss
2Department of Radiology and Developmental Neuroscience Program, Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, CA 90027, USA.
6Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089, USA.
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Olivier Pourquié
1Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), CNRS (UMR 7104), Inserm U964, Université de Strasbourg, 67400 Illkirch Graffenstaden, France.
8Department of Genetics, Harvard Medical School and Department of Pathology, Brigham and Woman's Hospital, 77 Avenue Louis Pasteur, Boston, MA 02115, USA.
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  • For correspondence: bertrand.benazeraf@univ-tlse3.fr pourquie@genetics.med.harvard.edu paulf@physics.mcgill.ca rustylansford@gmail.com
Paul François
4Ernest Rutherford Physics Building, McGill University, 3600 rue University, Montréal, QC, Canada.
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  • For correspondence: bertrand.benazeraf@univ-tlse3.fr pourquie@genetics.med.harvard.edu paulf@physics.mcgill.ca rustylansford@gmail.com
Rusty Lansford
2Department of Radiology and Developmental Neuroscience Program, Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, CA 90027, USA.
5Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA.
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  • For correspondence: bertrand.benazeraf@univ-tlse3.fr pourquie@genetics.med.harvard.edu paulf@physics.mcgill.ca rustylansford@gmail.com
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Summary

Embryonic axis extension is a complex multi-tissue morphogenetic process responsible for the formation of the posterior part of the amniote body. Cells located in the caudal part of the embryo divide and rearrange to participate in the elongation of the different embryonic tissues (e.g. neural tube, axial and paraxial mesoderm, lateral plate, ectoderm, endoderm). We previously identified the paraxial mesoderm as a crucial player of axis elongation, but how movements and growth are coordinated between the different posterior tissues to drive morphogenesis remain largely unknown. Here we use the quail embryo as a model system to quantify cell behavior and movements in the various tissues of the elongating embryo. We first quantify the tissue-specific contribution to axis elongation by using 3D volumetric techniques, then quantify tissue-specific parameters such as cell density and proliferation at different embryonic stages. To be able to study cell behavior at a multi-tissue scale we used high-resolution 4D imaging of transgenic quail embryos expressing constitutively expressed fluorescent proteins. We developed specific tracking and image analysis techniques to analyze cell motion and compute tissue deformations in 4D. This analysis reveals extensive sliding between tissues during axis extension. Further quantification of “tissue tectonics” showed patterns of rotations, contractions and expansions, which are coherent with the multi-tissue behavior observed previously. Our results confirm the central role of the PSM in axis extension; we propose that the PSM specific cell proliferation and migration programs control the coordination of elongation between tissues during axis extension.

Footnotes

  • ↵3 Centre de Biologie du Développement (CBD), Centre de Biologie Intégrative (CBI), Université de Toulouse, CNRS, UPS, France. (current address)

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Posted February 10, 2017.
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Multiscale quantification of tissue behavior during amniote embryo axis elongation
Bertrand Bénazéraf, Mathias Beaupeux, Martin Tchernookov, Allison Wallingford, Tasha Salisbury, Amelia Shirtz, Andrew Shirtz, Dave Huss, Olivier Pourquié, Paul François, Rusty Lansford
bioRxiv 053124; doi: https://doi.org/10.1101/053124
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Multiscale quantification of tissue behavior during amniote embryo axis elongation
Bertrand Bénazéraf, Mathias Beaupeux, Martin Tchernookov, Allison Wallingford, Tasha Salisbury, Amelia Shirtz, Andrew Shirtz, Dave Huss, Olivier Pourquié, Paul François, Rusty Lansford
bioRxiv 053124; doi: https://doi.org/10.1101/053124

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