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

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.

Role of pioneer neurons and neuroblast behaviors on otic ganglion assembly

“…When imaging apical protein Pard3 localization during otic delamination, Pard3 is partially kept in the apical membrane remaining's after abscission, while a different fraction travels basally in the hinge point of apical cytoplasmatic thinning, suggesting it might provide information for the apical thinning process. In our system, compared with the laterality organ of zebrafish (Pulgar et al, 2021), partial delamination does not occur, but once NB are out of the epithelium, Pard3 is dynamically rearranged while retained, similarly as in in the zebrafish heart trabeculation (Jiménez-Amilburu et al, 2016). Pard3 maintenance in pseudo-mesenchymal NB suggest that Pard3 could establish a new polarity axis in migratory cells or inform where neurites must grow, as shown in some mechanosensory neurons (Lee et al, 2021).…”

Heterotopic reduction of forelimb progenitors underpins development of the vestigial emu wing; implications for vertebrate limb evolution

“…This emphasizes that the evolution of divergent limb morphologies does not exclusively occur through post-patterning of the established limb bud primordia [29][30][31][32][33][34][35] . Rather, these findings present an alternate mechanism whereby heterotopic differences in the allocation of limb progenitors can instead influence limb size, shape, or proportions within or between species (Figure 4) 57 .…”

Meteorins regulate the formation of the left-right organizer and the establishment of vertebrate body asymmetry

“…It is therefore possible that the observed defects are due to impaired embedding of the DFCs into the cells of the EVL, the deep cell layer and the EVL. Since the proper connection between DFC and EVL enables a subset of DFCs to have apical contacts with the EVL and to be pre-polarized, one can speculate that Metrns play a role in the polarization and direct apical contacts establishment of DFCs to the EVL [17], [18], [45], [46]. We hypothesize that the observed clustering defects in metrn mutants might instead be due to a role of Metrns in DFC-DFC contact interaction [44].…”