Abstract
The inner/apical surface of the embryonic brain wall is important as a major site for cell production by neural progenitor cells (NPCs). We compared the mechanical properties of the apical surfaces of two neighboring but morphologically distinct cerebral wall regions in mice from embryonic day (E) E12–E14. Through indentation measurement using atomic force microscopy (AFM), we first found that Young’s modulus was higher at a concave-shaped apical surface of the pallium than at a convex-shaped apical surface of the ganglionic eminence (GE). Further AFM analysis suggested that contribution of actomyosin as revealed with apical surface softening by blebbistatin and stiffness of dissociated NPCs were both comparable between pallium and GE, not accounting for the differential apical surface stiffness. We then found that the density of apices of NPCs was greater, with denser F-actin meshwork, in the apically stiffer pallium than in GE. A similar correlation was found between the decreasing density between E12 and E14 of NPC apices and the declining apical surface stiffness in the same period in both the pallium and the GE. Thus, one plausible explanation for the observed difference (pallium > GE) in apical surface stiffness may be differential densification of NPC apices. In laser ablation onto the apical surface, the convex-shaped GE apical surface showed quicker recoils of edges than the pallial apical surface did, with a milder inhibition of recoiling by blebbistatin than in pallium. This greater pre-stress in GE may provide an indication of how the initially apically concave wall then becomes an apically convex “eminence.”
Highlights
During development, tissue morphogenesis requires the coordination of cell behaviors such as proliferation, differentiation, and migration
Further atomic force microscopy (AFM) analysis with pharmacological assessments (Figure 2) or on single dissociated neural progenitor cells (NPCs) (Figure 3) and laser ablation-mediated mechanical analysis (Figure 4) suggested that each dissociated NPC stiffness and the activity of actomyosin at the in vivo NPC apices were comparable between the pallium and the ganglionic eminence (GE) and that the apical surface tension was greater in the convex-shaped GE, which do not apparently account for the observed difference in the apical surface stiffness
Through further examinations to determine how the pallial apical surface was stiffer than the GE apical surface, we found that the density of apices of NPCs in the ventricular zone (VZ) was greater in the apically stiffer pallium than in the GE (Figure 5) and found a similar correlation between the decreasing density of the apices between embryonic day 12 (E12) and E14 and the declining apical surface stiffness in the same period in both the pallium and the GE (Figure 5)
Summary
Tissue morphogenesis requires the coordination of cell behaviors such as proliferation, differentiation, and migration. These behaviors are well known to respond to chemical signals (Briscoe and Small, 2015). There are an increasing number of studies showing that cells respond to mechanical cues. Mechanical forces imposed by developing smooth muscle layers are necessary for the emergence of villi in the developing intestine (Shyer et al, 2013), and the interplay between tissue stress and cell intercalations contributes. How do cells to form brain structures generate, sense, and utilize mechanical forces? Such an understanding would be supported by the assessment of the mechanical properties of developing brain walls. The present study applies these techniques to the embryonic mouse cerebral wall, especially on its inner surface, which faces a fluid-containing space called the ventricle in vivo
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