Abstract
How epithelial cell behaviors are coordinately regulated to sculpt tissue architecture is a fundamental question in biology. Kupffer's vesicle (KV), a transient organ with a fluid-filled lumen, provides a simple system to investigate the interplay between intrinsic cellular mechanisms and external forces during epithelial morphogenesis. Using 3-dimensional (3D) analyses of single cells we identify asymmetric cell volume changes along the anteroposterior axis of KV that coincide with asymmetric cell shape changes. Blocking ion flux prevents these cell volume changes and cell shape changes. Vertex simulations suggest cell shape changes do not depend on lumen expansion. Consistent with this prediction, asymmetric changes in KV cell volume and shape occur normally when KV lumen growth fails due to leaky cell adhesions. These results indicate ion flux mediates cell volume changes that contribute to asymmetric cell shape changes in KV, and that these changes in epithelial morphology are separable from lumen-generated forces.
Highlights
In an embryo, epithelial cells undergo tightly regulated shape changes to drive tissue remodeling and organ development
We developed methods to analyze single Kupffer’s vesicle (KV) cells in 3-dimensions (3D) and created novel mathematical vertex models of KV development to identify mechanisms that contribute to AP asymmetric epithelial cell shape changes in KV. 3D analyses revealed that KV-ant cells increase their volume and KV-post cells decrease their volume during KV morphogenesis
Models predicted that when external tissues are solid-like, asymmetric cell volume changes in KV cells contribute to cell shape changes even in the absence of lumen expansion
Summary
Epithelial cells undergo tightly regulated shape changes to drive tissue remodeling and organ development. The mechanical properties of neighboring cells can help shape how an epithelium develops (Luu et al, 2011; Sedzinski et al, 2016). Another source of extrinsic force found in many organs is a fluid-filled lumen. Forces generated by increased fluid pressure during lumen expansion can have an impact on individual cell shapes and the overarching epithelial architecture (Bagnat et al, 2010). Exactly how intrinsic molecular mechanisms and extrinsic mechanical forces interact to regulate epithelial cell shape changes during organogenesis remains an open and intriguing question
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