Mechanobiology of cell migration in the context of dynamic two-way cell–matrix interactions

Kurniawan, Nicholas A.; Chaudhuri, Parthiv Kant; Lim, Chwee Teck

doi:10.1016/j.jbiomech.2015.12.023

Cited by 44 publications

(42 citation statements)

References 218 publications

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“…Values of displacement, strain, stress (logarithmic/true tensile and compressive strains and stresses), SED and reaction force were calculated at the nodes and/or centroids of all showing that contraction of neighboring cells causes densification and realignment of the ECM fibers stretched between the cells; cells may respond to such structural changes, for example by migrating along the aligned fibers (34). All aforementioned outcomes were derived for both cells contained in each model variant; the mean of the outcomes of the two cells was then calculated, and is regarded as the model outcome (as presented below).…”

Section: Outcome Measuresmentioning

confidence: 99%

Nonlinear Elasticity of the ECM Fibers Facilitates Efficient Intercellular Communication

Sopher¹,

Tokash²,

Natan³

et al. 2018

Biophysical Journal

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Biological cells embedded in fibrous matrices have been observed to form intercellular bands of dense and aligned fibers through which they mechanically interact over long distances. Such matrix-mediated cellular interactions have been shown to regulate various biological processes. This study aimed to explore the effects of elastic nonlinearity of the fibers contained in the extracellular matrix (ECM) on the transmission of mechanical loads between contracting cells. Based on our biological experiments, we developed a finite-element model of two contracting cells embedded within a fibrous network. The individual fibers were modeled as showing linear elasticity, compression microbuckling, tension stiffening, or both of the latter two. Fiber compression buckling resulted in smaller loads in the ECM, which were primarily directed toward the neighboring cell. These loads decreased with increasing cell-to-cell distance; when cells were >9 cell diameters apart, no such intercellular interaction was observed. Tension stiffening further contributed to directing the loads toward the neighboring cell, though to a smaller extent. The contraction of two neighboring cells resulted in mutual attraction forces, which were considerably increased by tension stiffening and decayed with increasing cell-to-cell distances. Nonlinear elasticity contributed also to the onset of force polarity on the cell boundaries, manifested by larger contractile forces pointing toward the neighboring cell. The density and alignment of the fibers within the intercellular band were greater when fibers buckled under compression, with tension stiffening further contributing to this structural remodeling. Although previous studies have established the role of the ECM nonlinear mechanical behavior in increasing the range of force transmission, our model demonstrates the contribution of nonlinear elasticity of biological gels to directional and efficient mechanical signal transfer between distant cells, and rehighlights the importance of using fibrous gels in experimental settings for facilitating intercellular communication. VIDEO ABSTRACT.

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Section: Outcome Measuresmentioning

confidence: 99%

Nonlinear Elasticity of the ECM Fibers Facilitates Efficient Intercellular Communication

Sopher¹,

Tokash²,

Natan³

et al. 2018

Biophysical Journal

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“…The second mechanism instead involves plastic (or inelastic) deformation. Similar to the case with metals, where defects reduce local stresses and slow down cracks (5), Nature effectively utilizes plasticity to toughen cells and tissues against the mechanical demands of their environment (6)(7)(8). It is unclear how biomaterials balance elastic nonlinearity and plasticity, especially across the large range of physiological strains encountered throughout the body (9)(10)(11)(12).…”

Section: Introductionmentioning

confidence: 99%

Fibrin Networks Support Recurring Mechanical Loads by Adapting their Structure across Multiple Scales

Kurniawan

Vos

Biebricher

et al. 2016

Biophysical Journal

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Tissues and cells sustain recurring mechanical loads that span a wide range of loading amplitudes and timescales as a consequence of exposure to blood flow, muscle activity, and external impact. Both tissues and cells derive their mechanical strength from fibrous protein scaffolds, which typically have a complex hierarchical structure. In this study, we focus on a prototypical hierarchical biomaterial, fibrin, which is one of the most resilient naturally occurring biopolymers and forms the structural scaffold of blood clots. We show how fibrous networks composed of fibrin utilize irreversible changes in their hierarchical structure at different scales to maintain reversible stress stiffening up to large strains. To trace the origin of this paradoxical resilience, we systematically tuned the microstructural parameters of fibrin and used a combination of optical tweezers and fluorescence microscopy to measure the interactions of single fibrin fibers for the first time, to our knowledge. We demonstrate that fibrin networks adapt to moderate strains by remodeling at the network scale through the spontaneous formation of new bonds between fibers, whereas they adapt to high strains by plastic remodeling of the fibers themselves. This multiscale adaptation mechanism endows fibrin gels with the remarkable ability to sustain recurring loads due to shear flows and wound stretching. Our findings therefore reveal a microscopic mechanism by which tissues and cells can balance elastic nonlinearity and plasticity, and thus can provide microstructural insights into cell-driven remodeling of tissues.

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“…Moreover, the mitochondrial oxidative metabolism is viewed as a critical suppressor of metastasis and thus, lower OXPHOS activity may help promote metastasis (Lu et al, 2015). Cell migration is an early requirement for tumor metastasis (Findlay et al, 2014), but is a complex phenomenon that involves cycling of adhesion and cell detachment (Kurniawan et al, 2016;Pankova et al, 2010;Tozluoglu et al, 2013). Strongly adherent cells may increase their migration capacity through a decrease of their adhesion to extracellular matrix.…”

Section: Discussionmentioning

confidence: 99%

Cross-Talk between Alternatively Spliced UGT1A Isoforms and Colon Cancer Cell Metabolism

Audet-Delage

Rouleau

et al. 2017

Mol Pharmacol

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Mechanobiology of cell migration in the context of dynamic two-way cell–matrix interactions

Cited by 44 publications

References 218 publications

Nonlinear Elasticity of the ECM Fibers Facilitates Efficient Intercellular Communication

Nonlinear Elasticity of the ECM Fibers Facilitates Efficient Intercellular Communication

Fibrin Networks Support Recurring Mechanical Loads by Adapting their Structure across Multiple Scales

Cross-Talk between Alternatively Spliced UGT1A Isoforms and Colon Cancer Cell Metabolism

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