Active shape programming drives <i>Drosophila</i> wing disc eversion
How complex 3D tissue shape emerges during animal development remains an important open question in biology and biophysics. Here, we discover a mechanism for 3D epithelial shape change based on active, in-plane cellular events that is analogous to inanimate "shape programmable" materials, which undergo blueprinted 3D shape transformations from in-plane gradients of spontaneous strains. We study eversion of the <i>Drosophila</i> wing disc pouch, when the epithelium transforms from a dome into a curved fold, quantifying 3D tissue shape changes and mapping spatial patterns of cellular behaviors on the evolving geometry using cellular topology. Using a physical model inspired by shape programming, we find that active cell rearrangements are the major contributor to pouch eversion and validate this conclusion using a knockdown of MyoVI, which reduces rearrangements and disrupts morphogenesis. This work shows that shape programming is a mechanism for animal tissue morphogenesis and suggests that patterns in nature could present design strategies for shape-programmable materials.
Authors
- Marko Popović (ORCID: https://orcid.org/0000-0003-2360-3982)
- Carl D. Modes (ORCID: https://orcid.org/0000-0001-9940-0730)
- Suzanne Eaton (ORCID: https://orcid.org/0000-0002-8319-284X)
- Abhijeet Krishna (ORCID: https://orcid.org/0000-0002-9291-500X)
- Jana F. Fuhrmann (ORCID: https://orcid.org/0000-0003-3949-5242)
- Charlie Duclut (ORCID: https://orcid.org/0000-0002-8595-6815)
- Joris Paijmans (ORCID: https://orcid.org/0000-0002-4274-7925)
- Natalie A. Dye (ORCID: https://orcid.org/0000-0002-4859-6670)
- Frank Jülicher (ORCID: https://orcid.org/0000-0003-4731-9185)
- Greta Cwikla (ORCID: https://orcid.org/0009-0001-6390-4299)
Institutions
- Centre National de la Recherche Scientifique (FR)
- Université Paris Sciences et Lettres (FR)
- Sorbonne Université (FR)
- Max Planck Institute for the Physics of Complex Systems (DE)
- Center for Systems Biology Dresden (DE)
- Max Planck Institute of Molecular Cell Biology and Genetics (DE)
- Physique des Cellules et Cancers (FR)
- Technische Universität Dresden (DE)
- Institut Curie (FR)
Publication Details
- Journal
- Science Advances
- Published
- 2024-08-09
- DOI
- https://doi.org/10.1126/sciadv.adp0860
- Citations
- 17
- Primary Topic
- Advanced Materials and Mechanics
- Type
- article
- Field-Weighted Citation Impact
- 3.61