Abstract
During embryonic morphogenesis, tissues undergo dramatic deformations in order to form functional organs. Similarly, in adult animals, living cells and tissues are continually subjected to forces and deformations. Therefore, the success of embryonic development and the proper maintenance of physiological functions rely on the ability of cells to withstand mechanical stresses as well as their ability to flow in a collective manner. During these events, mechanical perturbations can originate from active processes at the single-cell level, competing with external stresses exerted by surrounding tissues and organs. However, the study of tissue mechanics has been somewhat limited to either the response to external forces or to intrinsic ones. In this work, we use an active vertex model of a 2D confluent tissue to study the interplay of external deformations that are applied globally to a tissue with internal active stresses that arise locally at the cellular level due to cell motility. We elucidate, in particular, the way in which this interplay between globally external and locally internal active driving determines the emergent mechanical properties of the tissue as a whole. For a tissue in the vicinity of a solid-fluid jamming or unjamming transition, we uncover a host of fascinating rheological phenomena, including yielding, shear thinning, continuous shear thickening, and discontinuous shear thickening. These model predictions provide a framework for understanding the recently observed nonlinear rheological behaviors in vivo.
- Received 23 April 2023
- Revised 27 November 2023
- Accepted 16 January 2024
DOI:https://doi.org/10.1103/PhysRevX.14.011027
Published by the American Physical Society under the terms of the Creative Commons Attribution 4.0 International license. Further distribution of this work must maintain attribution to the author(s) and the published article’s title, journal citation, and DOI.
Published by the American Physical Society
Physics Subject Headings (PhySH)
Popular Summary
Biological tissues have mechanical integrity yet allow for gradual structural rearrangement. The transition between liquidlike and solidlike properties resembles the well-studied jamming or glass response in granular materials. Recent work has shown that this jamming behavior underpins many important processes such as wound healing, cancer development, and morphogenesis. In this study, we delve into the interplay between cell motility, structure, and globally applied deformation to understand how it leads to the diverse mechanical properties observed in biological tissues. Using a theoretical model, we shed light on this fascinating phenomenon and uncover new insights into the mechanics of biological systems.
To simulate epithelial monolayers, we use a vertex-based model, in which cells are represented as a tiling of polygons. This model incorporates several essential parameters for biological tissues, such as cell shape and motility. While previous research has focused on small shear mechanical behavior, our study imposes large strains, leading to a significant spatially coherent alignment and rigid behavior. However, this alignment is challenged by the random motility that disrupts the large-scale organization. The interplay between the competing solidlike and liquidlike behaviors leads to abrupt shear thickening, which effectively separates the two regimes.
Overall, our results demonstrate the complex mechanical behavior of epithelial monolayers and offer insights into the dynamic interplay between various physical forces that shape tissues. This provides a general framework for understanding nonlinear behaviors in several important processes including morphogenesis, tumor spreading, and wound healing.
