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Tissue self-organization underlies morphogenesis of the notochord.

Publication ,  Journal Article
Norman, J; Sorrell, EL; Hu, Y; Siripurapu, V; Garcia, J; Bagwell, J; Charbonneau, P; Lubkin, SR; Bagnat, M
Published in: Philos Trans R Soc Lond B Biol Sci
September 24, 2018

The notochord is a conserved axial structure that in vertebrates serves as a hydrostatic scaffold for embryonic axis elongation and, later on, for proper spine assembly. It consists of a core of large fluid-filled vacuolated cells surrounded by an epithelial sheath that is encased in extracellular matrix. During morphogenesis, the vacuolated cells inflate their vacuole and arrange in a stereotypical staircase pattern. We investigated the origin of this pattern and found that it can be achieved purely by simple physical principles. We are able to model the arrangement of vacuolated cells within the zebrafish notochord using a physical model composed of silicone tubes and water-absorbing polymer beads. The biological structure and the physical model can be accurately described by the theory developed for the packing of spheres and foams in cylinders. Our experiments with physical models and numerical simulations generated several predictions on key features of notochord organization that we documented and tested experimentally in zebrafish. Altogether, our data reveal that the organization of the vertebrate notochord is governed by the density of the osmotically swelling vacuolated cells and the aspect ratio of the notochord rod. We therefore conclude that self-organization underlies morphogenesis of the vertebrate notochord.This article is part of the Theo Murphy meeting issue on 'Mechanics of development'.

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Published In

Philos Trans R Soc Lond B Biol Sci

DOI

EISSN

1471-2970

Publication Date

September 24, 2018

Volume

373

Issue

1759

Location

England

Related Subject Headings

  • Zebrafish
  • Notochord
  • Morphogenesis
  • Models, Biological
  • Evolutionary Biology
  • Embryonic Development
  • Cell Count
  • Animals
  • 32 Biomedical and clinical sciences
  • 31 Biological sciences
 

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Norman, J., Sorrell, E. L., Hu, Y., Siripurapu, V., Garcia, J., Bagwell, J., … Bagnat, M. (2018). Tissue self-organization underlies morphogenesis of the notochord. Philos Trans R Soc Lond B Biol Sci, 373(1759). https://doi.org/10.1098/rstb.2017.0320
Norman, James, Emma L. Sorrell, Yi Hu, Vaishnavi Siripurapu, Jamie Garcia, Jennifer Bagwell, Patrick Charbonneau, Sharon R. Lubkin, and Michel Bagnat. “Tissue self-organization underlies morphogenesis of the notochord.Philos Trans R Soc Lond B Biol Sci 373, no. 1759 (September 24, 2018). https://doi.org/10.1098/rstb.2017.0320.
Norman J, Sorrell EL, Hu Y, Siripurapu V, Garcia J, Bagwell J, et al. Tissue self-organization underlies morphogenesis of the notochord. Philos Trans R Soc Lond B Biol Sci. 2018 Sep 24;373(1759).
Norman, James, et al. “Tissue self-organization underlies morphogenesis of the notochord.Philos Trans R Soc Lond B Biol Sci, vol. 373, no. 1759, Sept. 2018. Pubmed, doi:10.1098/rstb.2017.0320.
Norman J, Sorrell EL, Hu Y, Siripurapu V, Garcia J, Bagwell J, Charbonneau P, Lubkin SR, Bagnat M. Tissue self-organization underlies morphogenesis of the notochord. Philos Trans R Soc Lond B Biol Sci. 2018 Sep 24;373(1759).
Journal cover image

Published In

Philos Trans R Soc Lond B Biol Sci

DOI

EISSN

1471-2970

Publication Date

September 24, 2018

Volume

373

Issue

1759

Location

England

Related Subject Headings

  • Zebrafish
  • Notochord
  • Morphogenesis
  • Models, Biological
  • Evolutionary Biology
  • Embryonic Development
  • Cell Count
  • Animals
  • 32 Biomedical and clinical sciences
  • 31 Biological sciences