Long Range Force Transmission in Fibrous Matrices Enabled by Tension-Driven Alignment of Fibers
arXiv:1409.6377 · doi:10.1016/j.bpj.2014.09.044
Abstract
Cells can sense and respond to mechanical signals over relatively long distances across fibrous extracellular matrices. Here, we explore all of the key factors that influence long range force transmission in cell-populated collagen matrices: alignment of collagen fibers, responses to applied force, strain stiffening properties of the aligned fibers, aspect ratios of the cells, and the polarization of cellular contraction. A constitutive law accounting for mechanically-driven collagen fiber reorientation is proposed. We systematically investigate the range of collagen fiber alignment using both finite element simulations and analytical calculations. Our results show that tension-driven collagen fiber alignment plays a crucial role in force transmission. Small critical stretch for fiber alignment, large fiber stiffness and fiber strain hardening behavior enable long-range interaction. Furthermore, the range of collagen fiber alignment for elliptical cells with polarized contraction is much larger than that for spherical cells with diagonal contraction. A phase diagram showing the range of force transmission as a function of cell shape and polarization and matrix properties is presented. Our results are in good agreement with recent experiments, and highlight the factors that influence long-range force transmission, in particular tension-driven alignment of fibers. Our work has important relevance to biological processes including development, cancer metastasis and wound healing, suggesting conditions whereby cells communicate over long distances.
arXiv commentAccepted for publication in the Biophysical Journal
References in corpus (1)
Cited by in corpus (26)
- Cell contraction induces long-ranged stress stiffening in the extracellular matrix
- Nonlinear elasticity of the extracellular matrix fibers facilitates efficient inter-cellular mechanical communication
- A Model for Compression-Weakening Materials and the Elastic Fields due to Contractile Cells
- Heterogeneous Force Chains in Cellularized Biopolymer Network
- A computational framework for modeling cell-matrix interactions in soft biological tissues
- Modeling cell migration regulated by cell-ECM micromechanical coupling
- Cells exploit a phase transition to mechanically remodel the fibrous extracellular matrix
- Mechanical and Systems Biology of Cancer
- The Role of Cell-Matrix Interactions in Connective Tissue Mechanics
- Nonlinear Poisson effect governed by mechanical critical transition
- Mechanical Interaction Between Cells Facilitates Molecular Transport
- Shape regulation generates elastic interaction between living cells
- Fiber plucking by molecular motors yields large emergent contractility in stiff biopolymer networks
- Continuum elastic models for force transmissions in biopolymer gels
- Anomalous linear elasticity of disordered networks
- Modeling Multi-Cellular Dynamics Regulated by ECM-Mediated Mechanical Communication via Active Particles with Polarized Effective Attraction
- Mean-field interactions between living cells in linear and nonlinear elastic matrices
- Towards understanding structure-function relationships in random fiber networks
- Design framework for programmable three-dimensional woven metamaterials
- In-silico modeling of the micromechanics of fibrous scaffolds and stiffness sensing by cells
- Structural features and nonlinear rheology of self-assembled networks of cross-linked semiflexible polymers
- Nonlinear Poisson effect in affine semiflexible polymer networks
- Elastic Anisotropy Governs the Decay of Cell-induced Displacements
- Criticality enhances the reinforcement of disordered networks by rigid inclusions
- Variational approximation method for the long-range force transmission in biopolymer gels
- Collective dynamics and self-organization of active particles on random networks