Abstract
The spreading of mesenchymal-like cell layers is critical for embryo morphogenesis and tissue repair, yet we know little of this process in vivo. Here we take advantage of unique developmental features of the non-conventional annual killifish embryo to study the principles underlying tissue spreading in a simple cellular environment, devoid of patterning signals and major morphogenetic cell movements. Using in vivo experimentation and physical modelling we reveal that the extra-embryonic epithelial enveloping cell layer, thought mainly to provide protection to the embryo, directs cell migration and the spreading of embryonic tissue during early development. This function relies on the ability of embryonic cells to couple their autonomous random motility to non-autonomous signals arising from the expansion of the extra-embryonic epithelium, mediated by cell membrane adhesion and tension. Thus, we present a mechanism of extra-embryonic control of embryo morphogenesis that couples the mechanical properties of adjacent tissues in the early killifish embryo.
Highlights
The spreading of mesenchymal-like cell layers is critical for embryo morphogenesis and tissue repair, yet we know little of this process in vivo
This function is mediated by cell adhesion and tension and relies on the ability of embryonic cells to couple their autonomous random motility to non-autonomous mechanical signals arising from the expansion of the enveloping cell layer (EVL), which is used by embryonic cells as a substrate for migration
The hypoblast coordinates cell signalling and movements of the epiblast in the pre-gastrula chick embryos[22], while extracellular matrix (ECM) proteins derived from the mouse trophectoderm/visceral endoderm and zebrafish yolk syncytial layer (YSL) are required for morphogenesis of the egg cylinder[23] and heart[24], respectively
Summary
The spreading of mesenchymal-like cell layers is critical for embryo morphogenesis and tissue repair, yet we know little of this process in vivo. Using in vivo experimentation and physical modelling we reveal that the extra-embryonic epithelial enveloping cell layer, thought mainly to provide protection to the embryo, directs cell migration and the spreading of embryonic tissue during early development. This function relies on the ability of embryonic cells to couple their autonomous random motility to non-autonomous signals arising from the expansion of the extra-embryonic epithelium, mediated by cell membrane adhesion and tension. We present a previously undescribed function for extra-embryonic control of embryo morphogenesis that couples the mechanical properties of adjacent tissues in the early vertebrate embryo
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