The geometric basis of epithelial convergent extension

Elife. 2024 Dec 19:13:RP95521. doi: 10.7554/eLife.95521.

Abstract

Shape changes of epithelia during animal development, such as convergent extension, are achieved through the concerted mechanical activity of individual cells. While much is known about the corresponding large-scale tissue flow and its genetic drivers, fundamental questions regarding local control of contractile activity on the cellular scale and its embryo-scale coordination remain open. To address these questions, we develop a quantitative, model-based analysis framework to relate cell geometry to local tension in recently obtained time-lapse imaging data of gastrulating Drosophila embryos. This analysis systematically decomposes cell shape changes and T1 rearrangements into internally driven, active, and externally driven, passive, contributions. Our analysis provides evidence that germ band extension is driven by active T1 processes that self-organize through positive feedback acting on tensions. More generally, our findings suggest that epithelial convergent extension results from the controlled transformation of internal force balance geometry which combines the effects of bottom-up local self-organization with the top-down, embryo-scale regulation by gene expression.

Keywords: D. melanogaster; active cell intercalation; convergent extension; developmental biology; passive cell intercalation; physics of living systems; self-organization; tissue mechanics.

MeSH terms

  • Animals
  • Cell Shape
  • Drosophila / embryology
  • Drosophila / physiology
  • Drosophila melanogaster* / embryology
  • Drosophila melanogaster* / genetics
  • Drosophila melanogaster* / physiology
  • Embryo, Nonmammalian / physiology
  • Epithelial Cells / physiology
  • Epithelium / embryology
  • Epithelium / physiology
  • Gastrulation / physiology
  • Models, Biological
  • Morphogenesis
  • Time-Lapse Imaging