Stress management in composite biopolymer networks

Burla, Federica; Tauber, Justin; Dussi, Simone; Gucht, Jasper van der; Koenderink, Gijsje H.

doi:10.1038/s41567-019-0443-6

Cited by 67 publications

(70 citation statements)

References 38 publications

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“…This is in contrast to previous works that concentrated on the classification of different mechanical regimes of fibrous networks, according to connectivity, bending rigidity and internal pre-stresses (39,(49)(50)(51)(52)(53). Note that high-connectivity networks can represent fibrous biopolymer gels that are more vigorously cross-linked (54)(55)(56) or combined with synthetic gels (57). We take the advantage of the near-affine deformation in such high-connectivity networks to develop and compare with continuum models, which allows us to gain deeper insights into the associated mechanisms.…”

Section: Discrete Fiber Simulations Of a Contracting Cell In An Isotrmentioning

confidence: 57%

Elastic Anisotropy Governs the Range of Cell-Induced Displacements

Goren

Koren

et al. 2020

Biophysical Journal

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SignificanceTissues are made up of cells and an extracellular matrix (ECM), a cross-linked network of stiff biopolymers. Cells actively alter the ECM structure and mechanics by applying contractile forces, which allow them to sense other distant cells and regulate many tissue functions. We study theoretically the decay of cell-induced displacements in fibrous networks, while quantifying the changes in the elastic properties of the cell's local environment. We demonstrate that cell contraction induce an anisotropic elastic state, i.e., unequal principal elastic moduli, in the ECM which dictates the slow decay of displacements. These observations suggest a new mechanical mechanism through which cells can mechanically communicate over long distances, and may provide biomaterials design parameters to guide morphogenesis in tissue engineering. AbstractThe unique nonlinear mechanics of the fibrous extracellular matrix (ECM) facilitates long-range cell-cell mechanical communications that would be impossible on linear elastic substrates. Past research has described the contribution of two separated effects on the range of force transmission, including ECM elastic non-linearity 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 non-linearity and fiber reorientation both contribute to the Page 2 of 32 strain-induced anisotropy of the elastic moduli of the cell's local environment. This elastic anisotropy is a "lumped" parameter that governs the slow decay of the 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 displacement decay induced by a contracting cell. Our findings unify previous single effects into a mechanical theory that explains force transmission in fibrous networks. This work provides important insights into biological processes that involve the coordinated action of distant cells mediated by the ECM, such that occur 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.In addition, we find in Fig. 3C that the data points of 2 / 1 for all types of fibers can be approximately fitted by a master curve if plotted versus the normalized strain, / crit . Here crit is the critical strain, a characteristic parameter of the network, in which 2 / 1 becomes smaller than 0.9, and the strain-induced elastic anisotropy is significant. The normalized strain, / crit , similar to the normalized cell contraction, / crit in cell contraction networks, is another "emergent" dimensionless p...

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Section: Discrete Fiber Simulations Of a Contracting Cell In An Isotrmentioning

confidence: 57%

Elastic Anisotropy Governs the Range of Cell-Induced Displacements

Goren

Koren

et al. 2020

Biophysical Journal

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“…S5c). At concentrations lower than 3 mg mL À1 , as we previously reported, 53 the samples were too soft to reliably measure an elastic modulus. We note that the ISFs for 4 mg mL À1 and 1 mg mL À1 hyaluronan networks were homogeneous across different fields of view, whereas the ISFs at 2 mg mL À1 showed substantial heterogeneity (see ESI, † Fig.…”

Section: Effect Of Crosslinking On Particle Diffusivity In Hyaluronanmentioning

confidence: 64%

“…However, in this case previous macroscopic rheology data indicated that the network is not fully percolated. 53 This likely explains why we observe heterogeneous dynamics for the 0.6 mm particles with large differences among ISFs measured in different sample regions (see ESI, † Fig. S4).…”

Section: Effect Of Crosslinking On Particle Diffusivity In Hyaluronanmentioning

confidence: 82%

Particle diffusion in extracellular hydrogels

et al. 2020

Self Cite

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“…Last, an improved understanding of ECM–ECM (e.g., GAG‐collagen) interactions in health and disease will further our understanding of the ways ECM‐protein interactions influence mechanical properties and how to properly model them in vitro. [ 118 ]…”

Section: Remaining Questions and Emerging Materials To Study Fibrosismentioning

confidence: 99%

Engineered Biomaterial Platforms to Study Fibrosis

Davidson

Burdick

Wells

2020

Adv Healthcare Materials

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Many pathologic conditions lead to the development of tissue scarring and fibrosis, which are characterized by the accumulation of abnormal extracellular matrix (ECM) and changes in tissue mechanical properties. Cells within fibrotic tissues are exposed to dynamic microenvironments that may promote or prolong fibrosis, which makes it difficult to treat. Biomaterials have proved indispensable to better understand how cells sense their extracellular environment and are now being employed to study fibrosis in many tissues. As mechanical testing of tissues becomes more routine and biomaterial tools become more advanced, the impact of biophysical factors in fibrosis are beginning to be understood. Herein, fibrosis from a materials perspective is reviewed, including the role and mechanical properties of ECM components, the spatiotemporal mechanical changes that occur during fibrosis, current biomaterial systems to study fibrosis, and emerging biomaterial systems and tools that can further the understanding of fibrosis initiation and progression. This review concludes by highlighting considerations in promoting wide‐spread use of biomaterials for fibrosis investigations and by suggesting future in vivo studies that it is hoped will inspire the development of even more advanced biomaterial systems.

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Stress management in composite biopolymer networks

Cited by 67 publications

References 38 publications

Elastic Anisotropy Governs the Range of Cell-Induced Displacements

Elastic Anisotropy Governs the Range of Cell-Induced Displacements

Particle diffusion in extracellular hydrogels

Engineered Biomaterial Platforms to Study Fibrosis

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