Apical membrane maturation and cellular rosette formation during morphogenesis of the zebrafish lateral line

Abstract

Tissue morphogenesis and cell sorting are major forces during organ development. Here, we characterize the process of tissue morphogenesis within the zebrafish lateral line primordium, a migratory sheet of cells that gives rise to the neuromasts of the posterior lateral line organ. We find that cells within this epithelial tissue constrict actin-rich membranes and enrich apical junction proteins at apical focal points. The coordinated apical membrane constriction in single Delta D-positive hair cell progenitors and in their neighbouring prospective support cells generates cellular rosettes. Live imaging reveals that cellular rosettes subsequently separate from each other and give rise to individual neuromasts. Genetic analysis uncovers an involvement of Lethal giant larvae proteins in the maturation of apical junction belts during cellular rosette formation. Our findings suggest that apical constriction of cell membranes spatially confines regions of strong cell-cell adhesion and restricts the number of tightly interconnected cells into cellular rosettes, which ensures the correct deposition of neuromasts during morphogenesis of the posterior lateral line organ.

Fgfr-Ras-MAPK signaling is required for apical constriction via apical positioning of Rho-associated kinase during mechanosensory organ formation

“…The Fgfr-Ras-MAPK signaling cascade is required for apical constriction in leading pLLp cells Apical constriction has been suggested to underlie pLLp rosette formation (Hava et al, 2009;Chitnis et al, 2012). Cell shape analysis during live imaging of rosette formation revealed that, over a 1-hour period, columnar cells become apically constricted as nascent rosettes form (Fig.…”

Tuning Collective Cell Migration by Cell–Cell Junction Regulation

“…Cells of the primordium express E-cadherin and show foci of the TJ protein ZO1 and aPKC at the center of the tightly packaged primordium (Revenu et al 2014), similar to mature epithelium. On the other hand, cells particularly located at the edge of this cell group display typical mesenchymal characteristics, such as reduced apicobasal polarity and the presence of highly dynamic actin-rich lamellipodia-like protrusions at the basal interactions to the tissue (Lecaudey et al 2008;Hava et al 2009). Thus, within the same moving cell group, different interaction types are found, with strong cell -cell adhesions at the center of the migrating cluster and more mesenchymal cells with weaker adhesions but higher actinmediated mobility at the periphery and in leader cells.…”

Apical constriction is driven by a pulsatile apical myosin network in delaminating Drosophila neuroblasts

“…Through a lateral inhibition process mediated by Notch-Delta signaling activity, one cell from a proneural cluster is specified as a neuroblast, while the rest of the cells in the cluster that have higher Notch signaling activity remain epithelial cells. During the formation of proneuromast rosettes in the zebrafish posterior lateral line primordium, morphogenesis is independent of cell fate-determining Notch-Delta signaling activity (Hava et al, 2009). In Drosophila embryos, it has been shown that overexpression of the Notch intracellular domain (NICD) leads to premature cell division in the ventral neuroectoderm (Hartenstein et al, 1994).…”