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Long Range Force Transmission in Fibrous Matrices Enabled by Tension-Driven Alignment of Fibers

Hailong Wang, A.S. Abhilash, Christopher S. Chen, Rebecca G. Wells, Vivek B. Shenoy
doi: https://doi.org/10.1101/048579
Hailong Wang
1Department of Materials Science and Engineering
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A.S. Abhilash
1Department of Materials Science and Engineering
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Christopher S. Chen
2Department of Biomedical Engineering, Boston University, Boston MA 02215
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Rebecca G. Wells
3Departments of Medicine (GI) and Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104
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Vivek B. Shenoy
1Department of Materials Science and Engineering
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  • For correspondence: vshenoy@seas.upenn.edu
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Abstract

Cells can sense and respond to mechanical signals over relatively long distances across fibrous extracellular matrices. Recently proposed models suggest that long-range force transmission can be attributed to the nonlinear elasticity or fibrous nature of collagen matrices, yet the mechanism whereby fibers align remains unknown. Moreover, cell shape and anisotropy of cellular contraction are not considered in existing models, although recent experiments have shown that they play crucial roles. 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.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted April 13, 2016.
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Long Range Force Transmission in Fibrous Matrices Enabled by Tension-Driven Alignment of Fibers
Hailong Wang, A.S. Abhilash, Christopher S. Chen, Rebecca G. Wells, Vivek B. Shenoy
bioRxiv 048579; doi: https://doi.org/10.1101/048579
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Long Range Force Transmission in Fibrous Matrices Enabled by Tension-Driven Alignment of Fibers
Hailong Wang, A.S. Abhilash, Christopher S. Chen, Rebecca G. Wells, Vivek B. Shenoy
bioRxiv 048579; doi: https://doi.org/10.1101/048579

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