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Scientific article
Open access
English

In Vivo Force Application Reveals a Fast Tissue Softening and External Friction Increase during Early Embryogenesis

Published inCurrent biology, vol. 29, no. 9, p. 1564-1571.e6
Publication date2019-05
Abstract

During development, cell-generated forces induce tissue-scale deformations to shape the organism [1,2]. The pattern and extent of these deformations depend not solely on the temporal and spatial profile of the generated force fields but also on the mechanical properties of the tissues that the forces act on. It is thus conceivable that, much like the cell-generated forces, the mechanical properties of tissues are modulated during development in order to drive morphogenesis toward specific developmental endpoints. Although many approaches have recently emerged to assess effective mechanical parameters of tissues [3-8], they could not quantitatively relate spatially localized force induction to tissue-scale deformations in vivo. Here, we present a method that overcomes this limitation. Our approach is based on the application of controlled forces on a single microparticle embedded in an individual cell of an embryo. Combining measurements of bead displacement with the analysis of induced deformation fields in a continuum mechanics framework, we quantify material properties of the tissue and follow their changes over time. In particular, we uncover a rapid change in tissue response occurring during Drosophila cellularization, resulting from a softening of the blastoderm and an increase of external friction. We find that the microtubule cytoskeleton is a major contributor to epithelial mechanics at this stage. We identify developmentally controlled modulations in perivitelline spacing that can account for the changes in friction. Overall, our method allows for the measurement of key mechanical parameters governing tissue-scale deformations and flows occurring during morphogenesis.

eng
Keywords
  • Drosophila embryo
  • Cellularization
  • Continuum mechanics
  • Cytoskeleton
  • Force manipulation
  • Magnetic tweezer
  • Morphogenesis
  • Physical modeling
  • Tissue mechanics
  • Vitelline envelope
Affiliation Not a UNIGE publication
Funding
  • Wellcome Trust - Theoretical Physics of Biology Laboratory [FC001317]
  • Cancer Research UK - [21144]
  • The Francis Crick Institute - [10317]
  • Plan Nacional - [BFU2015-68754]
  • CERCA Programme/Generalitat de Catalunya -
  • Spanish Ministry of Economy and Competitiveness (MEIC) to the EMBL partnership -
  • Francis Crick Institute -
Citation (ISO format)
D’ANGELO, Arturo et al. <i>In Vivo</i> Force Application Reveals a Fast Tissue Softening and External Friction Increase during Early Embryogenesis. In: Current biology, 2019, vol. 29, n° 9, p. 1564–1571.e6. doi: 10.1016/j.cub.2019.04.010
Main files (1)
Article (Published version)
Identifiers
ISSN of the journal0960-9822
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