Understanding how cells respond to and remodel their extracellular environment is foundational to morphogenesis. Intricate apical or luminal matrices are vital components of numerous epithelial organs and yet shaped by elusive mechanisms. In my thesis research, I have used the molting cycle in the nematode C. elegans to study how the actin cytoskeleton is coupled to the extracellular matrix and functions as a key effector of cellular behavior.

In this thesis, I characterize the mechanical networks and successive changes in tissue morphology that give rise to long ridges called alae on certain cuticles of C.�elegans. We show that knockdowns of apical constriction components lead to maze-like cuticle deformities overlying lateral epidermal syncytia (seam). Transient apical constriction leads to the formation of three actin filament bundles in the seam and adjacent syncytia that presage the forthcoming ridges of the alae. The rapid constriction and gradual expansion of the epidermis generates transient protuberances from the surface that organize provisional matrix macromolecules. The provisional matrix enables power from apical constriction to shape durable substructures in apical extracellular matrix. The proposed mechanism integrates changes in cell and extracellular matrix morphology over time and might apply to significant developmental transitions in other systems.  

I also reveal the extensive dynamic rearrangements of the epidermal actin cytoskeleton over the course of the last larval stage and molt. My findings show that the propagation of annular folds from larval to adult-stage cuticles does not rely on a subset of circumferential actin filament bundles present at the cortex of the major epidermal syncytium across the larval-to-adult transition. This leads to a revised understanding of patterning in which matrix proteins themselves shape the cuticle and regulate the organization of the transient molting sheath as well as the actin cytoskeleton with the epidermis. Lastly, I present preliminary evidence of regulators of the actin cytoskeleton within the epidermis, which may act downstream of the matrix.