How dynamic prestress governs the shape of living systems, from the subcellular to tissue scale

Abstract

Cells and tissues change shape both to carry out their function and during pathology. In most cases, these deformations are driven from within the systems themselves. This is permitted by a range of molecular actors, such as active crosslinkers and ion pumps, whose activity is biologically controlled in space and time. The resulting stresses are propagated within complex and dynamical architectures like networks or cell aggregates. From a mechanical point of view, these effects can be seen as the generation of prestress or prestrain, resulting from either a contractile or growth activity. In this review, we present this concept of prestress and the theoretical tools available to conceptualize the statics and dynamics of living systems. We then describe a range of phenomena where prestress controls shape changes in biopolymer networks (especially the actomyosin cytoskeleton and fibrous tissues) and cellularized tissues. Despite the diversity of scale and organization, we demonstrate that these phenomena stem from a limited number of spatial distributions of prestress, which can be categorized as heterogeneous, anisotropic or differential. We suggest that in addition to growth and contraction, a third type of prestress—topological prestress—can result from active processes altering the microstructure of tissue.

Editorial: theme issue on complex rheology in biological systems

“…The challenge of understanding intra- and extracellular biomolecular networks across length scales requires identification of whether the network is passive or active [ 3 ], and the level of pre-stress [ 4 ]. To assess this information, the contributed review by Erlich et al [ 4 ] argues it is necessary to develop novel non-perturbative methodologies to probe the network at a small length scale.…”

“…The challenge of understanding intra- and extracellular biomolecular networks across length scales requires identification of whether the network is passive or active [ 3 ], and the level of pre-stress [ 4 ]. To assess this information, the contributed review by Erlich et al [ 4 ] argues it is necessary to develop novel non-perturbative methodologies to probe the network at a small length scale. Lecinski et al address this using single-bead tracking passive rheology in live S. cerevisiae yeast cells [ 1 ], and Jory et al discuss new methodologies to probe mucus adhesion at the microscopic scale using optical tweezers [ 10 ].…”

“…Questions on such mechanical properties and phenomena are rarely addressed. At the tissue biology level, there are new challenges especially in the highly nonlinear range of deformations [ 3 , 4 ], coupling to smaller structures, and pathologies. Vascular biology (e.g.…”

A Low‐Cost, User‐Friendly Rheo‐Optical Compression Assay to Measure Mechanical Properties of Cell Spheroids in Standard Cell Culture Plates

“…Additionally, mechanical properties are also dependent on size [ 36 ] and growth conditions of the cell spheroids, [ 37 ] showing a time‐dependent viscoelastic behavior, influenced by factors such as cell‐cell adhesion and extracellular matrix production.…”

“…Here, we propose an innovative rheo‐optical compression assay based on simple materials and equipment usually available in a biology lab. Our approach is based on the combination of a constant stress test (creep) by a using a microscope coverslip to apply the load and data fitting of the resulting deformation with rheological models [ 36 ] to extract mechanical parameters. The assay is first validated on agarose gel particles and then carried out on two different cell lines to exemplify its application.…”