A model for compression-weakening materials and the elastic fields due to contractile cells

We construct a homogeneous, nonlinear elastic constitutive law that models aspects of the mechanical behavior of inhomogeneous fibrin networks. Fibers in such networks buckle when in compression. We model this as a loss of stiffness in compression in the stress–strain relations of the homogeneous constitutive model. Problems that model a contracting biological cell in a finite matrix are solved. It is found that matrix displacements and stresses induced by cell contraction decay slower (with distance from the cell) in a compression weakening material than linear elasticity would predict. This points toward a mechanism for long-range cell mechanosensing. In contrast, an expanding cell would induce displacements that decay faster than in a linear elastic matrix.

[1]  F. MacKintosh,et al.  Cross-linked networks of stiff filaments exhibit negative normal stress. , 2008, Physical review letters.

[2]  P. Janmey,et al.  Nonlinear elasticity in biological gels , 2004, Nature.

[3]  M. Dembo,et al.  Cell movement is guided by the rigidity of the substrate. , 2000, Biophysical journal.

[4]  G. Ravichandran,et al.  Three-dimensional Full-field Measurements of Large Deformations in Soft Materials Using Confocal Microscopy and Digital Volume Correlation , 2007 .

[5]  K. Billiar,et al.  Nonlinear strain stiffening is not sufficient to explain how far cells can feel on fibrous protein gels. , 2013, Biophysical journal.

[6]  M. Sheetz,et al.  Local force and geometry sensing regulate cell functions , 2006, Nature Reviews Molecular Cell Biology.

[7]  Ben Fabry,et al.  Stress controls the mechanics of collagen networks , 2015, Proceedings of the National Academy of Sciences.

[8]  Dennis E. Discher,et al.  Multiscale Mechanics of Fibrin Polymer: Gel Stretching with Protein Unfolding and Loss of Water , 2009, Science.

[9]  A. Goriely,et al.  Positive or negative Poynting effect? The role of adscititious inequalities in hyperelastic materials , 2011, Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[10]  P. Friedl,et al.  Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. , 2011, Trends in cell biology.

[11]  Huajian Gao,et al.  Some basic questions on mechanosensing in cell–substrate interaction , 2014 .

[12]  J. Notbohm,et al.  Quantifying cell-induced matrix deformation in three dimensions based on imaging matrix fibers. , 2015, Integrative biology : quantitative biosciences from nano to macro.

[13]  J. Weisel,et al.  Foam-like compression behavior of fibrin networks , 2015, Biomechanics and modeling in mechanobiology.

[14]  Paul A. Janmey,et al.  Non-Linear Elasticity of Extracellular Matrices Enables Contractile Cells to Communicate Local Position and Orientation , 2009, PloS one.

[15]  J. Weisel,et al.  Structural basis for the nonlinear mechanics of fibrin networks under compression. , 2014, Biomaterials.

[16]  P. Janmey,et al.  Tissue Cells Feel and Respond to the Stiffness of Their Substrate , 2005, Science.

[17]  J. Paul Robinson,et al.  Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure. , 2002, Journal of biomechanical engineering.

[18]  S. Safran,et al.  Scaling laws for the response of nonlinear elastic media with implications for cell mechanics. , 2012, Physical review letters.

[19]  Christopher S. Chen,et al.  Long Range Force Transmission in Fibrous Matrices Enabled by Tension-Driven Alignment of Fibers , 2014, bioRxiv.

[20]  A. Ruina,et al.  Microbuckling instability in elastomeric cellular solids , 1993, Journal of Materials Science.

[21]  Sebastian Rammensee,et al.  Negative normal stress in semiflexible biopolymer gels. , 2007, Nature materials.

[22]  Micah Dembo,et al.  Cell-cell mechanical communication through compliant substrates. , 2008, Biophysical journal.

[23]  Max Potters,et al.  Structural hierarchy governs fibrin gel mechanics. , 2010, Biophysical journal.

[24]  J. Notbohm Dynamics of Cell–Matrix Mechanical Interactions in Three Dimensions , 2013 .

[25]  Chris H. Rycroft,et al.  Rapid disorganization of mechanically interacting systems of mammary acini , 2013, Proceedings of the National Academy of Sciences.

[26]  John Henry Poynting,et al.  On pressure perpendicular to the shear planes in finite pure shears , and on the lengthening of loaded wires when twisted , 1909 .

[27]  P. Rosakis,et al.  Microbuckling of fibrin provides a mechanism for cell mechanosensing , 2014, Journal of The Royal Society Interface.