Asymmetry of tensile versus compressive elasticity and permeability contributes to the regulation of exchanges in collagen gels

Abstract

The Starling principle describes exchanges between blood and tissues based on the balance of hydrostatic and osmotic flows. However, the permeation properties of the main constituent of tissues, namely, collagen, in response to the stress exerted by blood pressure remain poorly characterized. Here, we develop an instrument to determine the elasticity and permeability of collagen gels under tensile and compressive stress based on measuring the temporal change in pressure in an air cavity sealed at the outlet of a collagen slab. Data analysis with an analytical model reveals a drop in the permeability and enhanced strain stiffening of native collagen gels under compression versus tension, both effects being essentially lost after chemical cross-linking. Furthermore, we report the control of the permeability of native collagen gels using sinusoidal fluid injection, an effect explained by the asymmetric response in tension and compression. We lastly suggest that blood-associated pulsations could contribute to exchanges within tissues.

Cellular elasticity in cancer: a review of altered biomechanical features

“…These findings highlight the importance of the nonlinear elasticity of fibrillary arrays in regulating mechanical cell interactions with the ECM in a 3D context, and the principle of cell force regulation that we explored may contribute to the rapid mechanical stiffening of tissues that occurs in several diseases, including cancer and fibrosis. 109–111…”

Flow and deformation due to periodic loading in a soft porous material

“…For example, soft tissues in the body can experience pulsating loads from the surrounding blood vessels or, on a larger scale, can be cyclically loaded during their basic mechanical function. The former scenario has attracted great interest recently as a potential driver of transport in brain tissue (Franceschini et al 2006;Kedarasetti, Drew & Costanzo 2020;Bojarskaite et al 2023) and the latter is important for load-bearing and transport in cartilage (Riches et al 2002;Mauck, Hung & Ateshian 2003;Ferguson, Ito & Pyrak-Nolte 2004;Sengers, Oomens & Baaijens 2004;Schmidt et al 2010;Zhang 2011;Di Domenico, Wang & Bonassar 2017;Cacheux et al 2023) and bone (Piekarski & Munro 1977;Zhang & Cowin 1994;Manfredini et al 1999;Nguyen, Lemaire & Naili 2010;Witt et al 2014). Periodic loads are also commonly applied in regenerative medicine to improve cell differentiation in scaffolds via mechanotransduction (Kim et al 1999;Butler, Goldstein & Guilak 2000;Mauck et al 2000;Grenier et al 2005;Haj, Hampson & Gogniat 2009;Gauvin et al 2011;Amrollahi & Tayebi 2015;Peroglio et al 2018).…”