Apical contacts stemming from incomplete delamination guide progenitor cell allocation through a dragging mechanism

Elife. 2021 Aug 27:10:e66483. doi: 10.7554/eLife.66483.

Abstract

The developmental strategies used by progenitor cells to allow a safe journey from their induction place towards the site of terminal differentiation are still poorly understood. Here, we uncovered a mechanism of progenitor cell allocation that stems from an incomplete process of epithelial delamination that allows progenitors to coordinate their movement with adjacent extra-embryonic tissues. Progenitors of the zebrafish laterality organ originate from the superficial epithelial enveloping layer by an apical constriction process of cell delamination. During this process, progenitors retain long-lasting apical contacts that enable the epithelial layer to pull a subset of progenitors on their way to the vegetal pole. The remaining delaminated cells follow the movement of apically attached progenitors by a protrusion-dependent cell-cell contact mechanism, avoiding sequestration by the adjacent endoderm, ensuring their collective fate and allocation at the site of differentiation. Thus, we reveal that incomplete delamination serves as a cellular platform for coordinated tissue movements during development.

Keywords: apical constriction; cell delamination; collective locomotion; developmental biology; dorsal forerunner cells; dragging; mechanical forces; zebrafish.

Publication types

  • Research Support, Non-U.S. Gov't
  • Video-Audio Media

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Cell Adhesion
  • Cell Communication*
  • Cell Differentiation*
  • Cell Lineage
  • Cell Movement*
  • Embryo, Nonmammalian / physiology
  • Epithelial Cells / physiology*
  • Gene Expression Regulation, Developmental
  • Morphogenesis
  • Stem Cells / physiology*
  • Time Factors
  • Zebrafish / embryology
  • Zebrafish / genetics

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.