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

Abstract

Embryos are growing organisms with highly heterogeneous properties in space and time. Understanding the mechanical properties is a crucial prerequisite for the investigation of morphogenesis. During the last 10 years, new techniques have been developed to evaluate the mechanical properties of biological tissues in vivo. To address this need, we employed a new instrument that, via the combination of micro‐indentation with Optical Coherence Tomography (OCT), allows us to determine both, the spatial distribution of mechanical properties of chick embryos, and the structural changes in real‐time. We report here the stiffness measurements on the live chicken embryo, from the mesenchymal tailbud to the epithelialized somites. The storage modulus of the mesoderm increases from (176 ± 18) Pa in the tail to (716 ± 117) Pa in the somitic region (mean ± SEM, n = 12). The midline has a mean storage modulus of (947 ± 111) Pa in the caudal (PSM) presomitic mesoderm (mean ± SEM, n = 12), indicating a stiff rod along the body axis, which thereby mechanically supports the surrounding tissue. The difference in stiffness between midline and presomitic mesoderm decreases as the mesoderm forms somites. This study provides an efficient method for the biomechanical characterization of soft biological tissues in vivo and shows that the mechanical properties strongly relate to different morphological features of the investigated regions.

A mechanical model of early somite segmentation

“…TLater in segmentation, we see a gradual mesenchymal to epithelial transition progressing caudally along the PSM ( Figure 1 ). During axis elongation and segmentation, the PSM becomes stiffer with a caudal-to-rostral stiffness gradient ( Marrese et al., 2020 ) which is associated with increasing cell polarity and expression of adhesion molecules like cadherins ( Duband et al., 1987 ), which are sufficient to reproduce boundary formation in models of somite formation ( Glazier et al., 2008 ). Higher cadherin density corresponds to faster actin reassembly ( Yonemura et al., 1995 ) and myosin enrichment in epithelial cells ( Maddugoda et al., 2007 ), since faster actin turnover and higher levels of myosin correlate with greater apical contractility, these patterns are compatible with a model in which contractility gradually builds up with a caudal-rostral gradient along the PSM.…”

Molecular and Mechanical Cues for Somite Periodicity

“…Truskinovsky et al (2014) made the case that also somite periodicity may be due to differential strain. With the presence of a contractile, coherent anterior PM and a physical connection to resistive surrounding tissues expanding at a different rates (like the ectoderm, the neural tube, the notochord or the intermediate mesoderm) (Bénazéraf et al, 2017;Marrese et al, 2020), the physical requirements for periodic differential strain are met. It is important to stress that the degree of tissue cohesiveness required for a pattern of differential strain to form is probably only met by the epithelium of the PM.…”

Mechanics of neural tube morphogenesis

“…More recently, methods that can be applied in intact, live embryos are being developed to overcome some of the limitations of more invasive methods [22]. These new methods include magnetically controlled droplets [170], atomic force microscopy [195] (AFM), Brillouin microscopy and optical coherence tomography [196][197][198] and optically trapped nanoparticles [199]. The droplets provide a local and dynamic measurement of tissue mechanics leading to the finding of solid-fluid jamming transition in the paraxial mesoderm of zebrafish [21].…”