Squamous epithelial morphogenesis and mechanobiology across the lifetime of dynamic barrier tissues.

Abstract

Barrier epithelia perform crucial protective and regulatory roles, with their development occurring in careful coordination with the tissues that they enclose. Many barrier epithelia are transient tissues with precise mechanisms of morphogenesis on spatial scales spanning over an order of magnitude, encompassing both early transitions to a squamous shape and wholesale remodeling at the end of the tissue's lifetime. Here, we compare exemplar tissues from Drosophila, Tribolium, and other insects: the extraembryonic, larval epidermal, peripodial, and follicular epithelia. We consider the extent to which these tissues share key structural features - such as a switch to the endocycle, secretion of an apical extracellular matrix, and apoptosis - and their implications for morphogenesis and physical interactions with other tissues. We also explore the process of becoming squamous from diverse precursor cell states, with the goal of identifying mechanistic commonalities. We emphasize the role of vesicle trafficking and cell adhesion remodeling at the cell-autonomous level, and we discuss the putative instructive role of mechanical forces as non-tissue-autonomous inputs in squamous shape acquisition. Further, we evaluate the time-evolution of cell deformability during squamous morphogenesis, measured with Brillouin microscopy, an emerging optical tool that maps material properties (e.g., stiffness) of cells and tissues of intact organisms in 4D. Finally, we examine the extent to which epithelial cell shape can be reversible during end-stage morphogenesis. Our comparative approach highlights general principles and open questions on the emergent properties of transient, squamous epithelia.