Multiscale analysis of architecture, cell size and the cell cortex reveals cortical F-actin density and composition are major contributors to mechanical properties during convergent extension

Abstract

The large-scale movements that construct complex three-dimensional tissues during development are governed by universal physical principles. Fine-grained control of both mechanical properties and force production is crucial to the successful placement of tissues and shaping of organs. Embryos of the frog provide a dramatic example of these physical processes, as dorsal tissues increase in Young's modulus by six-fold to 80 Pascal over 8 h as germ layers and the central nervous system are formed. These physical changes coincide with emergence of complex anatomical structures, rounds of cell division, and cytoskeletal remodeling. To understand the contribution of these diverse structures, we adopt the cellular solids model to relate bulk stiffness of a solid foam to the unit size of individual cells, their microstructural organization, and their material properties. Our results indicate that large-scale tissue architecture and cell size are not likely to influence the bulk mechanical properties of early embryonic or progenitor tissues but that F-actin cortical density and composition of the F-actin cortex play major roles in regulating the physical mechanics of embryonic multicellular tissues.

Insight into Mechanobiology: How Stem Cells Feel Mechanical Forces and Orchestrate Biological Functions

“…The first evidences of the role that mechanics play in developmental processes came from non-mammalians, such as Drosophila [5,139], avians [140], amphibians [141], and fish [142], in which became clear how eggs fertilization and maturation strongly depend on osmotic pressure gradients that influence cells shape [143,144]. On the other hand, significantly less is known about the influence of mechanical forces in the development of human embryos inside uterus because of the limited amount of material available for experimentations on animal models used for recapitulating human physiology [145] and because of ethical restrictions regarding human embryos manipulation [143].…”

Elasticity spectra as a tool to investigate actin cortex mechanics

“…The AC consists of the plasma membrane and the underlying actin cytoskeleton, linked together by a rich pool of transmembrane and adaptor proteins [10]. The structure and biomechanics of the AC are tightly intertwined [11,12] and they in turn influence the functionality of molecular mechanosensors, such as Piezo mechanosensitive ion channels [13,14] or G-protein coupled receptors [15,16]. These are incorporated into the plasma membrane and directly convert mechanical stimuli into downstream biochemical signals.…”

Micro-Engineered Models of Development Using Induced Pluripotent Stem Cells

“…The role of physical forces in embryonic development has been studied in model systems for fish (Petridou et al, 2019), amphibians (Shawky et al, 2018), and avians (Saadaoui et al, 2018) providing evidence for the irrefutable contributions of mechanics in the development process. In the case of mammals and their in-utero development, the embryo is believed to be more susceptible to local physical forces, geometry and general biomechanics because of their embedded development.…”