Abstract

Tissue morphogenesis is essential for metazoan development, yet is poorly understood as it requires the coordination of multiple cellular events such as migration, adhesion and shape changes. Furthermore, cells from neighboring tissues also must be coordinated during development, but few studies have addressed this. Caenorhabditis elegans is an ideal model to study tissue morphogenesis, since tissues are formed in a highly reproducible manner from a relatively small number of cells of known origin.

I study C. elegans ventral enclosure, when epidermal cells migrate over the ventral side of the embryo using cues from the underlying neurons. F-actin accumulates into a supracellular ring along the margins of the ventral epidermal cells, which was predicted to close by non-muscle myosin contractility. We found that anillin (ani-1), an actomyosin binding protein, and RhoA (rho-1), an upstream regulator of myosin contractility, are required for ventral enclosure. Interestingly, we found that anillin is required for neuroblast cytokinesis, and non-autonomously facilitates ventral epidermal cell migration. We also found that ventral enclosure phenotypes caused by ani-1 depletion were alleviated or strengthened by mutants that altered actomyosin contractility. Based on these data, we hypothesized that myosin contractility regulates ventral enclosure, and that tissue-tissue interactions are crucial for this process.
Further studies revealed that myosin is indeed required for ventral enclosure. In ventral epidermal cells, myosin localizes as foci in a pattern reminiscent of F-actin. However, myosin also localizes as dynamic foci that form intercellular networks in the neuroblasts, and we found that myosin is required in the neuroblasts for ventral enclosure. In the area underlying the ventral epidermal pocket cells, neuroblasts organize into a rosette-like pattern, and their exposed surface area decreases as the epidermal cells are drawn together. Interestingly, myosin distribution is altered in epidermal cells when neuroblast shape is altered, suggesting that they sense changes in neuroblast tension.
We propose that mechanical forces in the neuroblasts may influence actomyosin in the epidermal cells to facilitate ventral enclosure. This work emphasizes the importance of the interplay between different cell types during tissue morphogenesis, where contractility could be uniquely organized in non-epidermal tissues.