Mechanical forces drive neuroblast morphogenesis and are required for epidermal closure

Abstract

Tissue morphogenesis requires myosin-dependent events such as cell shape changes and migration to be coordinated between cells within a tissue, and/or with cells from other tissues. However, few studies have investigated the simultaneous morphogenesis of multiple tissues in vivo. We found that during Caenorhabditis elegans ventral enclosure, when epidermal cells collectively migrate to cover the ventral surface of the embryo, the underlying neuroblasts (neuronal precursor cells) also undergo morphogenesis. We found that myosin accumulates as foci along the junction-free edges of the ventral epidermal cells to form a ring, whose closure is myosin-dependent. We also observed the accumulation of myosin foci and the adhesion junction proteins E-cadherin and α-catenin in the underlying neuroblasts. Myosin may help to reorganize a subset of neuroblasts into a rosette-like pattern, and decrease their surface area as the overlying epidermal cells constrict. Since myosin is required in the neuroblasts for ventral enclosure, we propose that mechanical forces in the neuroblasts influence constriction of the overlying epidermal cells. In support of this model, disrupting neuroblast cell division or altering their fate influences myosin localization in the overlying epidermal cells. The coordination of myosin-dependent events and forces between cells in different tissues could be a common theme for coordinating morphogenetic events during metazoan development.

PCP and SAX-3/Robo Pathways Cooperate to Regulate Convergent Extension-Based Nerve Cord Assembly in C. elegans

“…These single-cell intercalations lead the neurons to cross the midline and eventually form a single file along the ventral midline prior to the onset of embryonic twitching (Figures 1C–E). These three phases occur simultaneously with ventral enclosure and constriction of the epiderm which has been shown to depend on forces generated in the VNC neurons (Wernike et al, 2016). Taken together, our observations show that the C. elegans VNC undergoes CE to assemble into a linear structure.…”

Sequential Rosettes Drive C. elegans Ventral Nerve Cord Assembly

“…On the orthogonal axis, regulated enrichment of adhesion molecules can drive shrinkage or elongation of cell-cell contacts, which also drives cell movements. Inspired by images from Harding et al (2014), Butler and Wallingford (2017), Wernike et al (2016), and Shah et al (2017).…”

“…Shah, Tanner and colleagues (2017), have developed tools for live imaging past the early embryonic stage. Wernike and colleagues (2016) recently discovered that C. elegans neuroblasts can form a ventral rosette, and that this process requires myosin/NMY-2. The elegant 3D live imaging and lineage tracing in the current work by Shah et al (2017) shows that specific ventral cord neuroblasts undergo rosette formation and resolution followed by single cell intercalation.…”

“…SAX-3/ROBO may also act upstream of actin regulators in the neuroblasts to promote mediolateral movements of CE. However, in the neuroblasts the target of SAX-3 could be the Rho-1 GTPase, as Rho-1 regulators promote ventral cord cell movements (Wernike et al, 2016). It will be interesting to determine if there are global asymmetries to the patterns of SAX-3 in the multiple tissues that pattern the embryo, and to further investigate how SAX-3/ROBO separately mediates anteroposterior and dorsoventral polarity.…”

RhoGAP RGA-8 supports morphogenesis inC. elegansby polarizing epithelia through CDC-42

“…6A). Myosin is enriched as puncta at the front of migrating epidermal pocket cells that later converge at the ventral midline as the contralateral pocket cells meet[41,42] (green arrows inFig. 6B).…”