Basal filopodia and vascular mechanical stress organize fibronectin into pillars bridging the mesoderm-endoderm gap

Abstract

Cells may exchange information with other cells and tissues by exerting forces on the extracellular matrix (ECM). Fibronectin (FN) is an important ECM component that forms fibrils through cell contacts and creates directionally biased geometry. Here, we demonstrate that FN is deposited as pillars between widely separated germ layers, namely the somitic mesoderm and the endoderm, in quail embryos. Alongside the FN pillars, long filopodia protrude from the basal surfaces of somite epithelial cells. Loss-of-function of Ena/VASP, α5β1-integrins or talin in the somitic cells abolished the FN pillars, indicating that FN pillar formation is dependent on the basal filopodia through these molecules. The basal filopodia and FN pillars are also necessary for proper somite morphogenesis. We identified a new mechanism contributing to FN pillar formation by focusing on cyclic expansion of adjacent dorsal aorta. Maintenance of the directional alignment of the FN pillars depends on pulsatile blood flow through the dorsal aortae. These results suggest that the FN pillars are specifically established through filopodia-mediated and pulsating force-related mechanisms.

Weakening of resistance force by cell–ECM interactions regulate cell migration directionality and pattern formation

“…Cells move dynamically in the surrounding ECM, which is an essential scaffold composed of proteins such as collagen that supplies chemical and mechanical cues for tissue morphogenesis 23 , by degrading the ECM to increase the pore size of the scaffold and alter adhesion 24 , 25 . In addition, cells also produce ECM proteins, such as fibronectin (FN), which contribute to cell rearrangement by forming cell adhesion sites 26 , 27 . These remodelling events in the cellular microenvironment are known to modulate the forces exerted on cells and affect individual cell migration in fibroblasts and mesenchymal cells 25 , 28 , 29 as well as in endothelial cells during vascularisation and angiogenesis 30 – 33 .…”

In vivo characterization of chick embryo mesoderm by optical coherence tomography‐assisted microindentation

“…This aids in anchoring the PSM cells by providing a substrate on which they can undergo collective migration and mesenchymal-epithelial transition (MET) to form epithelial spheres. [28][29][30][31] The PSM cells compact together, adhere to the ECM and each other, and become more contractile (Figure 2A confocal section, compare caudal PSM with rostral PSM), [30][31][32] thereby promoting fibronectin assembly. Concurrently, the notochord and neural plate quickly develop a high stiffness (Figure 2, lines 8 to 6).…”