Distinct regimes of elastic response and deformation modes of cross-linked cytoskeletal and semiflexible polymer networks.

Semiflexible polymers such as filamentous actin (F-actin) play a vital role in the mechanical behavior of cells, yet the basic properties of cross-linked F-actin networks remain poorly understood. To address this issue, we have performed numerical studies of the linear response of homogeneous and isotropic two-dimensional networks subject to an applied strain at zero temperature. The elastic moduli are found to vanish for network densities at a rigidity percolation threshold. For higher densities, two regimes are observed: one in which the deformation is predominately affine and the filaments stretch and compress; and a second in which bending modes dominate. We identify a dimensionless scalar quantity, being a combination of the material length scales, that specifies to which regime a given network belongs. A scaling argument is presented that approximately agrees with this crossover variable. By a direct geometric measure, we also confirm that the degree of affinity under strain correlates with the distinct elastic regimes. We discuss the implications of our findings and suggest possible directions for future investigations.

[1]  Theo Odijk,et al.  The statistics and dynamics of confined or entangled stiff polymers , 1983 .

[2]  David C. Morse,et al.  VISCOELASTICITY OF TIGHTLY ENTANGLED SOLUTIONS OF SEMIFLEXIBLE POLYMERS , 1998 .

[3]  Sami Saarinen,et al.  Microscopic mechanics of fiber networks , 1994 .

[4]  T. Stossel On the crawling of animal cells. , 1993, Science.

[5]  P. Gennes Scaling Concepts in Polymer Physics , 1979 .

[6]  D. Wirtz,et al.  Mechanics of living cells measured by laser tracking microrheology. , 2000, Biophysical journal.

[7]  E. Sackmann,et al.  First-order transition between adhesion states in a system mimicking cell-tissue interaction , 2001 .

[8]  Åström,et al.  Rigidity and Dynamics of Random Spring Networks. , 1996, Physical review letters.

[9]  David C. Morse,et al.  Viscoelasticity of Concentrated Isotropic Solutions of Semiflexible Polymers. 1. Model and Stress Tensor , 1998 .

[10]  E. Siggia,et al.  Entropic elasticity of lambda-phage DNA. , 1994, Science.

[11]  G. Schatten,et al.  Adhesion of cells to surfaces coated with polylysine. Applications to electron microscopy , 1975, The Journal of cell biology.

[12]  D. Weitz,et al.  Strain Hardening of Fractal Colloidal Gels , 1999 .

[13]  A. C. Maggs,et al.  Dynamics and rheology of actin solutions , 1996 .

[14]  E. Sackmann,et al.  Quasielastic light scattering study of thermal excitations of F‐actin solutions and of growth kinetics of actin filaments , 1992, Biopolymers.

[15]  Radial Distribution Function of Semiflexible Polymers. , 1996, Physical review letters.

[16]  F. MacKintosh,et al.  Deformation of cross-linked semiflexible polymer networks. , 2003, Physical review letters.

[17]  T. Stossel,et al.  The machinery of cell crawling. , 1994, Scientific American.

[18]  C F Dewey,et al.  Theoretical estimates of mechanical properties of the endothelial cell cytoskeleton. , 1996, Biophysical journal.

[19]  S. Edwards,et al.  The computer study of transport processes under extreme conditions , 1972 .

[20]  Andrea J. Liu,et al.  Effect of Random Packing on Stress Relaxation in Foam , 1997 .

[21]  J. Ralphs,et al.  Actin stress fibres and cell-cell adhesion molecules in tendons: organisation in vivo and response to mechanical loading of tendon cells in vitro. , 2002, Matrix biology : journal of the International Society for Matrix Biology.

[22]  J. Timonen,et al.  Rigidity of random networks of stiff fibers in the low-density limit. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[23]  F. MacKintosh,et al.  Dynamic shear modulus of a semiflexible polymer network , 1998 .

[24]  D. Ingber,et al.  Mechanotransduction across the cell surface and through the cytoskeleton , 1993 .

[25]  S. Timoshenko,et al.  Theory Of Elasticity. 2nd Ed. , 1951 .

[26]  D. Navajas,et al.  Scaling the microrheology of living cells. , 2001, Physical review letters.

[27]  S. Timoshenko,et al.  Theory of elasticity , 1975 .

[28]  Muhammad Sahimi,et al.  Non-linear and non-local transport processes in heterogeneous media: from long-range correlated percolation to fracture and materials breakdown , 1998 .

[29]  J. Trempe Molecular biology of the cell, 3rd edition Bruce Alberts, Dennis Bray, Julian Lewis, Martin Raff, Keith Roberts and James D. Watson, Garland Publishing, 1994, 559.95 (xiii + 1294 pages), ISBN 0-815-31619-4 , 1995, Trends in Endocrinology & Metabolism.

[30]  Frey,et al.  Force-Extension Relation and Plateau Modulus for Wormlike Chains. , 1996, Physical review letters.

[31]  David C. Morse,et al.  Viscoelasticity of concentrated isotropic solutions of semiflexible polymers. 2. Linear response , 1998 .

[32]  J. Timonen,et al.  Rigidity transition in two-dimensional random fiber networks. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[33]  Erwin Frey,et al.  Elasticity of stiff polymer networks. , 2003, Physical review letters.

[34]  E. Elson,et al.  Cellular mechanics as an indicator of cytoskeletal structure and function. , 1988, Annual review of biophysics and biophysical chemistry.

[35]  M. Magnasco,et al.  Measurement of the persistence length of polymerized actin using fluorescence microscopy. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[36]  Avi Caspi,et al.  Semiflexible Polymer Network: A View From Inside , 1998 .

[37]  P. Fromherz,et al.  Fluorescence Interferometry of Neuronal Cell Adhesion on Microstructured Silicon , 1998 .

[38]  P. Janmey,et al.  Elasticity of semiflexible biopolymer networks. , 1995, Physical review letters.

[39]  J. Kovac,et al.  Polymer conformational statistics. III. Modified Gaussian models of stiff chains , 1973 .

[40]  P. Janmey,et al.  Mechanical properties of cytoskeletal polymers. , 1991, Current opinion in cell biology.

[41]  M. Djabourov,et al.  All Gelatin Networks: 2. The Master Curve for Elasticity† , 2002 .

[42]  S. Smith,et al.  Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. , 1992, Science.

[43]  C. H. Seager,et al.  Percolation and conductivity: A computer study. II , 1974 .

[44]  M. Plischke,et al.  Entropic Elasticity of Diluted Central Force Networks , 1998 .

[45]  E. Sackmann,et al.  Entanglement, Elasticity, and Viscous Relaxation of Actin Solutions , 1998 .

[46]  Paul A. Janmey,et al.  Resemblance of actin-binding protein/actin gels to covalently crosslinked networks , 1990, Nature.

[47]  F. MacKintosh,et al.  Nonuniversality of elastic exponents in random bond-bending networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[48]  Christoph F. Schmidt,et al.  Chain dynamics, mesh size, and diffusive transport in networks of polymerized actin. A quasielastic light scattering and microfluorescence study , 1989 .

[49]  D. Morse,et al.  Viscoelasticity of dilute solutions of semiflexible polymers. , 2000, Physical review. E, Statistical, nonlinear, and soft matter physics.

[50]  J. Howard,et al.  Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape , 1993, The Journal of cell biology.

[51]  Elasticity of Poissonian fiber networks , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[52]  R. Ball,et al.  ELASTICITY OF RIGID NETWORKS , 1991 .

[53]  A. Semenov Dynamics of concentrated solutions of rigid-chain polymers. Part 1.—Brownian motion of persistent macromolecules in isotropic solution , 1986 .