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Elastic Anisotropy Governs the Range of Cell-Induced Displacements.

ABSTRACT: The unique nonlinear mechanics of the fibrous extracellular matrix (ECM) facilitates long-range cell-cell mechanical communications that would be impossible for linear elastic substrates. Past research has described the contribution of two separated effects on the range of force transmission, including ECM elastic nonlinearity and fiber alignment. However, the relation between these different effects is unclear, and how they combine to dictate force transmission range is still elusive. Here, we combine discrete fiber simulations with continuum modeling to study the decay of displacements induced by a contractile cell in fibrous networks. We demonstrate that fiber nonlinearity and fiber reorientation both contribute to the strain-induced elastic anisotropy of the cell's local environment. This elastic anisotropy is a "lumped" parameter that governs the slow decay of displacements, and it depends on the magnitude of applied strain, either an external tension or an internal contraction, as a model of the cell. Furthermore, we show that accounting for artificially prescribed elastic anisotropy dictates the decay of displacements induced by a contracting cell. Our findings unify previous single effects into a mechanical theory that explains force transmission in fibrous networks. This work may provide insights into biological processes that involve communication of distant cells mediated by the ECM, such as those occurring in morphogenesis, wound healing, angiogenesis, and cancer metastasis. It may also provide design parameters for biomaterials to control force transmission between cells as a way to guide morphogenesis in tissue engineering.

SUBMITTER: Goren S

PROVIDER: S-EPMC7063433 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Elastic Anisotropy Governs the Range of Cell-Induced Displacements.

Goren Shahar S Koren Yoni Y Xu Xinpeng X Lesman Ayelet A

Biophysical journal 20200109 5

The unique nonlinear mechanics of the fibrous extracellular matrix (ECM) facilitates long-range cell-cell mechanical communications that would be impossible for linear elastic substrates. Past research has described the contribution of two separated effects on the range of force transmission, including ECM elastic nonlinearity and fiber alignment. However, the relation between these different effects is unclear, and how they combine to dictate force transmission range is still elusive. Here, we ...[more]

PMID: 31995739

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Project description:Knowledge of the nature of the elastic symmetry of trabecular bone is fundamental to the study of bone adaptation and failure. Previous studies have classified human vertebral trabecular bone as orthotropic or transversely isotropic but have typically obtained samples from only selected regions of the centrum. In this study, the elastic symmetry of human vertebral trabecular bone was characterized using microfinite element (?FE) analyses performed on 1019 cubic regions of side length equal to 5 mm, obtained via thorough sampling of the centrums of 18 human L1 vertebrae (age?=?81.17?±?7.7?yr; eight males and ten females). An optimization procedure was used to find the closest orthotropic representation of the resulting stiffness tensor for each cube. The orthotropic elastic constants and orientation of the principal elastic axes were then recorded for each cube and were compared to the constants predicted from Cowin's fabric-based constitutive model (Cowin, 1985, "The Relationship Between the Elasticity Tensor and the Fabric Tensor," Mech. Mater., 4(2), pp. 137-147.) and the orientation of the principal axes of the fabric tensor, respectively. Deviations from orthotropy were quantified by the "orthotropic error" (van Rietbergen et al., 1996, "Direct Mechanics Assessment of Elastic Symmetries and Properties of Trabecular Bone Architecture," J. Biomech., 29(12), pp. 1653-1657), and deviations from transverse isotropy were determined by statistical comparison of the secondary and tertiary elastic moduli. The orthotropic error was greater than 50% for nearly half of the cubes, and the secondary and tertiary moduli differed from one another (p?<?0.0001). Both the orthotropic error and the difference between secondary and tertiary moduli decreased with increasing bone volume fraction (BV/TV; p???0.007). Considering only the cubes with an orthotropic error less than 50%, only moderate correlations were observed between the fabric-based and the ?FE-computed elastic moduli (R2???0.337; p?<?0.0001). These results indicate that when using a criterion of 5?mm for a representative volume element (RVE), transverse isotropy or orthotropy cannot be assumed for elderly human vertebral trabecular bone. Particularly at low values of BV/TV, this criterion does not ensure applicability of theories of continuous media. In light of the very sparse and inhomogeneous microstructure found in the specimens analyzed in this study, further work is needed to establish guidelines for selecting a RVE within the aged vertebral centrum.

Dataset Information

Elastic Anisotropy Governs the Range of Cell-Induced Displacements.

Publications

Elastic Anisotropy Governs the Range of Cell-Induced Displacements.

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