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Activity-driven extracellular volume expansion drives vertebrate axis elongation

Arthur Michaut, Alessandro Mongera, Anupam Gupta, Mattia Serra, Pietro Rigoni, Jong Gwan Lee, Felipe Duarte, Adam R. Hall, View ORCID ProfileL. Mahadevan, Karine Guevorkian, Olivier Pourquié
doi: https://doi.org/10.1101/2022.06.27.497799
Arthur Michaut
1Department of Genetics, Harvard Medical School; Boston, MA, USA
2Department of Pathology, Brigham and Women’s Hospital; Boston, MA, USA
10Department of Developmental and Stem Cell Biology, Institute Pasteur; Paris, France
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Alessandro Mongera
1Department of Genetics, Harvard Medical School; Boston, MA, USA
2Department of Pathology, Brigham and Women’s Hospital; Boston, MA, USA
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Anupam Gupta
3Department of Physics, IIT Hyderabad, Telengana, India
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Mattia Serra
4Department of Physics, University of California at San Diego; San Diego, CA, USA
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Pietro Rigoni
1Department of Genetics, Harvard Medical School; Boston, MA, USA
2Department of Pathology, Brigham and Women’s Hospital; Boston, MA, USA
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Jong Gwan Lee
1Department of Genetics, Harvard Medical School; Boston, MA, USA
2Department of Pathology, Brigham and Women’s Hospital; Boston, MA, USA
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Felipe Duarte
5Virginia Tech-Wake Forest School of Biomedical Engineering and Sciences, Wake Forest University School of Medicine; Winston-Salem, NC, USA
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Adam R. Hall
5Virginia Tech-Wake Forest School of Biomedical Engineering and Sciences, Wake Forest University School of Medicine; Winston-Salem, NC, USA
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L. Mahadevan
6Paulson School of Engineering and Applied Sciences, Harvard University; Cambridge, MA, USA
7Department of Organismic and Evolutionary Biology, Harvard University; Cambridge, MA, USA
8Department of Physics, Harvard University; Cambridge, MA, USA
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  • ORCID record for L. Mahadevan
  • For correspondence: lmahadev@g.harvard.edu karine.guevorkian@curie.fr pourquie@genetics.med.harvard.edu
Karine Guevorkian
9Institut Curie, Université PSL, Sorbonne Université; CNRS UMR168, Laboratoire Physico-Chimie Curie, 75005 Paris, France
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  • For correspondence: lmahadev@g.harvard.edu karine.guevorkian@curie.fr pourquie@genetics.med.harvard.edu
Olivier Pourquié
1Department of Genetics, Harvard Medical School; Boston, MA, USA
2Department of Pathology, Brigham and Women’s Hospital; Boston, MA, USA
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  • For correspondence: lmahadev@g.harvard.edu karine.guevorkian@curie.fr pourquie@genetics.med.harvard.edu
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Abstract

The vertebrate bauplan is primarily established via the formation of embryonic tissues in a head-to-tail progression. The biomechanics of this elongation, which requires the presomitic mesoderm (PSM), remains poorly understood. Here, we find that avian PSM explants can elongate autonomously when physically confined in vitro, producing a pushing force that can largely account for the posterior elongation of the embryo. Tissue elongation results from volumetric expansion that is driven by cellular activity and accompanied by inhomogeneous increase of the extracellular fraction along the AP axis. We show that FGF signaling promotes glycolysis-dependent production of Hyaluronic Acid (HA), which is required for expansion of the posterior PSM. Our findings link body axis elongation to tissue expansion through the metabolic control of extracellular matrix production downstream of FGF signaling.

One-Sentence Summary Active tissue expansion propels body elongation independent of cell proliferation-driven growth

Competing Interest Statement

A.R.H. is listed as inventor on a patent describing nanopore analysis of HA. The other authors declare no competing interests.

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-ND 4.0 International license.
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Posted June 28, 2022.
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Activity-driven extracellular volume expansion drives vertebrate axis elongation
Arthur Michaut, Alessandro Mongera, Anupam Gupta, Mattia Serra, Pietro Rigoni, Jong Gwan Lee, Felipe Duarte, Adam R. Hall, L. Mahadevan, Karine Guevorkian, Olivier Pourquié
bioRxiv 2022.06.27.497799; doi: https://doi.org/10.1101/2022.06.27.497799
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Activity-driven extracellular volume expansion drives vertebrate axis elongation
Arthur Michaut, Alessandro Mongera, Anupam Gupta, Mattia Serra, Pietro Rigoni, Jong Gwan Lee, Felipe Duarte, Adam R. Hall, L. Mahadevan, Karine Guevorkian, Olivier Pourquié
bioRxiv 2022.06.27.497799; doi: https://doi.org/10.1101/2022.06.27.497799

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