Architecture and Composition Dictate Viscoelastic Properties of Organ-Derived Extracellular Matrix Hydrogels.

Francisco Drusso Martinez-Garcia,Martin Conrad Harmsen,Prashant Kumar Sharma,Theo Borghuis,Machteld Nelly Hylkema,Roderick Harold Jan De Hilster,Janette Kay Burgess

doi:10.3390/polym13183113

Francisco Drusso Martinez-Garcia, Martin Conrad Harmsen + Show 5 more

Open Access

https://doi.org/10.3390/polym13183113

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Abstract

The proteins and polysaccharides of the extracellular matrix (ECM) provide architectural support as well as biochemical and biophysical instruction to cells. Decellularized, ECM hydrogels replicate in vivo functions. The ECM’s elasticity and water retention renders it viscoelastic. In this study, we compared the viscoelastic properties of ECM hydrogels derived from the skin, lung and (cardiac) left ventricle and mathematically modelled these data with a generalized Maxwell model. ECM hydrogels from the skin, lung and cardiac left ventricle (LV) were subjected to a stress relaxation test under uniaxial low-load compression at a 20%/s strain rate and the viscoelasticity determined. Stress relaxation data were modelled according to Maxwell. Physical data were compared with protein and sulfated GAGs composition and ultrastructure SEM. We show that the skin-ECM relaxed faster and had a lower elastic modulus than the lung-ECM and the LV-ECM. The skin-ECM had two Maxwell elements, the lung-ECM and the LV-ECM had three. The skin-ECM had a higher number of sulfated GAGs, and a highly porous surface, while both the LV-ECM and the lung-ECM had homogenous surfaces with localized porous regions. Our results show that the elasticity of ECM hydrogels, but also their viscoelastic relaxation and gelling behavior, was organ dependent. Part of these physical features correlated with their biochemical composition and ultrastructure.

Highlights

The extracellular matrix (ECM) is the acellular component of all organs and tissues:a three-dimensional (3D) mixture of proteins embedded in a gel of water-retaining negatively charged polysaccharides such as glycosaminoglycans (GAGs) [1]
ECM mechanics were solely evaluated in terms of elasticity—the resistance of an object to undergo reversible deformation in response to applied force (Stress, σ) [6,7]
Measuring the gelation kinetics of ECM hydrogels using turbidimetric analysis is based on the increased turbidity during gelling, i.e., increased absorbance

Summary

Introduction

The extracellular matrix (ECM) is the acellular component of all organs and tissues:a three-dimensional (3D) mixture of proteins embedded in a gel of water-retaining negatively charged polysaccharides such as glycosaminoglycans (GAGs) [1]. Due to variations in ECM composition and organization, the response to mechanical stress and strain differs among organs [9]. More recent studies have shown that due to a large water content, the ECM is not elastic but viscoelastic in nature [7,10,11], where viscosity plays an active role in matrix mechanics [7]. Viscosity is a material property that arises from the resistance of a fluid to deformation The combination of both elastic and viscous responses leads to a time-dependent stress dissipation (i.e., stress relaxation), a phenomenon known as viscoelasticity [8]. Unlike purely elastic materials that store and retain energy, a viscoelastic material will dissipate energy in the presence of stress over time, making the elastic modulus strain rate dependent. Viscoelasticity is an inherent property of the ECM, that has only recently been recognized within biological systems [7,10,11]

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