Hierarchical micro-adaptation of biological structures by mechanical stimuli

Abstract The objective of this work is to develop a remodeling model for biological matter coupling two different processes in a 3D framework: reorientation of the preferential direction of a given fibered structure and reorientation of the fibrils or filaments that make up such a structure. This work uses the microsphere-based approach to take into account the micro mechanics involved in biological fibered structures regarding both their passive behavior and the reorientation of their micro constituents. Moreover, the macro behavior of the material as a whole is obtained by means of homogenizing the underlying micro response. We associate the orientation space of the integration directions to the physical space of micro-fibrils. To approximate the directional distribution of the fibrils within each fiber bundle, a Bingham probability orientation density function is introduced into the Helmholtz energy function. With all these assumptions, the problem is studied from an energetic point of view, describing the dissipation inherent to remodeling processes, and the evolution equations for both reorientations (change in preferential direction of the network and change in shape of the fibril distribution) re obtained. The model is included in a finite element code which allows computing different geometries and boundary value problems. This results in a complete methodology for characterizing the reorientation evolution of different fibered biological structures, such as cells. Our results show remodeling of fibered structures in two different scales, presenting a qualitatively good agreement with experimental findings in cell mechanics. Hierarchical structures align in the direction of the maximum principal direction of the considered stimulus and narrow in the perpendicular direction. The dissipation rates follows predictable trends although there are no experimental findings to date for comparison. The incorporation of metabolic processes and an insight into cell-oriented mechano-sensing processes can help to overcome the limitations involved.

[1]  William E. Kraus,et al.  Orientation and length of mammalian skeletal myocytes in response to a unidirectional stretch , 2000, Cell and Tissue Research.

[2]  Byung H. Oh,et al.  Microplane Model for Progressive Fracture of Concrete and Rock , 1985 .

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

[4]  Alain Goriely,et al.  On the definition and modeling of incremental, cumulative, and continuous growth laws in morphoelasticity , 2007, Biomechanics and modeling in mechanobiology.

[5]  O. Kratky,et al.  Röntgenuntersuchung gelöster Fadenmoleküle , 1949 .

[6]  Frank Baaijens,et al.  Modeling collagen remodeling. , 2010, Journal of biomechanics.

[7]  Jay D. Humphrey,et al.  A CONSTRAINED MIXTURE MODEL FOR GROWTH AND REMODELING OF SOFT TISSUES , 2002 .

[8]  R M Nerem,et al.  Correlation of Endothelial Cell Shape and Wall Shear Stress in a Stenosed Dog Aorta , 1986, Arteriosclerosis.

[9]  J D Humphrey,et al.  Perspectives on biological growth and remodeling. , 2011, Journal of the mechanics and physics of solids.

[10]  Yuan Xu,et al.  Constructing fully symmetric cubature formulae for the sphere , 2001, Math. Comput..

[11]  E Kuhl,et al.  Computational modeling of arterial wall growth , 2007, Biomechanics and modeling in mechanobiology.

[12]  Yuzhi Zhang,et al.  Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and -resistant regions of human vasculature. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Jeffrey E. Bischoff,et al.  A microstructurally based orthotropic hyperelastic constitutive law , 2002 .

[14]  Paul Steinmann,et al.  Time‐dependent fibre reorientation of transversely isotropic continua—Finite element formulation and consistent linearization , 2008 .

[15]  Donald E. Ingber,et al.  Tensegrity-based mechanosensing from macro to micro. , 2008, Progress in biophysics and molecular biology.

[16]  M. Doblaré,et al.  On the use of the Bingham statistical distribution in microsphere-based constitutive models for arterial tissue , 2010 .

[17]  Andreas Menzel,et al.  Anisotropic micro-sphere-based finite elasticity applied to blood vessel modelling , 2009 .

[18]  D. Ingber Tensegrity I. Cell structure and hierarchical systems biology , 2003, Journal of Cell Science.

[19]  L. Taber Biomechanics of Growth, Remodeling, and Morphogenesis , 1995 .

[20]  Stephen C Cowin,et al.  Tissue growth and remodeling. , 2004, Annual review of biomedical engineering.

[21]  M. Vianello Optimization of the stored energy and coaxiality of strain and stress in finite elasticity , 1996 .

[22]  Milan Jirásek,et al.  A thermodynamically consistent approach to microplane theory. Part I. Free energy and consistent microplane stresses , 2001 .

[23]  Pere C. Prat,et al.  Microplane Model for Brittle-Plastic Material: I. Theory , 1988 .

[24]  S. Safran,et al.  Dynamical theory of active cellular response to external stress. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[25]  Stephen C. Cowin,et al.  Optimization of the strain energy density in linear anisotropic elasticity , 1994 .

[26]  Pascal Silberzan,et al.  Is the mechanical activity of epithelial cells controlled by deformations or forces? , 2005, Biophysical journal.

[27]  Frank P. T. Baaijens,et al.  Remodelling of the angular collagen fiber distribution in cardiovascular tissues , 2007, Biomechanics and modeling in mechanobiology.

[28]  Carlo Sansour,et al.  The modelling of fibre reorientation in soft tissue , 2009, Biomechanics and modeling in mechanobiology.

[29]  K. Hayakawa,et al.  Dynamic reorientation of cultured cells and stress fibers under mechanical stress from periodic stretching. , 2001, Experimental cell research.

[30]  M. Doblaré,et al.  On the use of non‐linear transformations for the evaluation of anisotropic rotationally symmetric directional integrals. Application to the stress analysis in fibred soft tissues , 2009 .

[31]  Ignacio Carol,et al.  Microplane constitutive model and computational framework for blood vessel tissue. , 2006, Journal of biomechanical engineering.

[32]  P. Flory,et al.  Thermodynamic relations for high elastic materials , 1961 .

[33]  A K Harris,et al.  Connective tissue morphogenesis by fibroblast traction. I. Tissue culture observations. , 1982, Developmental biology.

[34]  Paul Steinmann,et al.  Geometrically non‐linear anisotropic inelasticity based on fictitious configurations: Application to the coupling of continuum damage and multiplicative elasto‐plasticity , 2003 .

[35]  M. Kroon A continuum mechanics framework and a constitutive model for remodelling of collagen gels and collagenous tissues , 2010 .

[36]  Ekkehard Ramm,et al.  An anisotropic gradient damage model for quasi-brittle materials , 2000 .

[37]  Alain Goriely,et al.  Growth and instability in elastic tissues , 2005 .

[38]  Serdar Göktepe,et al.  A micro-macro approach to rubber-like materials—Part I: the non-affine micro-sphere model of rubber elasticity , 2004 .

[39]  K Garikipati,et al.  In silico estimates of the free energy rates in growing tumor spheroids , 2010, Journal of physics. Condensed matter : an Institute of Physics journal.

[40]  Toshiro Ohashi,et al.  Remodeling of vascular endothelial cells exposed to fluid shear stress: experimental and numerical approach , 2005 .

[41]  Huajian Gao,et al.  Cyclic Stretch Induces Cell Reorientation on Substrates by Destabilizing Catch Bonds in Focal Adhesions , 2012, PloS one.

[42]  Gérard A. Maugin,et al.  A constitutive model for material growth and its application to three-dimensional finite element analysis , 2002 .

[43]  M. Jirásek,et al.  A framework for microplane models at large strain, with application to hyperelasticity , 2004 .

[44]  P. Bazant,et al.  Efficient Numerical Integration on the Surface of a Sphere , 1986 .

[45]  S Chien,et al.  Shear stress induces spatial reorganization of the endothelial cell cytoskeleton. , 1998, Cell motility and the cytoskeleton.

[46]  K. Garikipati,et al.  Material Forces in the Context of Biotissue Remodelling , 2003, q-bio/0312002.

[47]  Huajian Gao,et al.  Two characteristic regimes in frequency-dependent dynamic reorientation of fibroblasts on cyclically stretched substrates. , 2008, Biophysical journal.

[48]  Gerard A Ateshian,et al.  On the theory of reactive mixtures for modeling biological growth , 2007, Biomechanics and modeling in mechanobiology.

[49]  E Otten,et al.  Analytical description of growth. , 1982, Journal of theoretical biology.

[50]  Jerrold E. Marsden,et al.  Introduction to Mechanics and Symmetry: A Basic Exposition of Classical Mechanical Systems , 1999 .

[51]  Jean-François Ganghoffer,et al.  Mechanical modeling of growth considering domain variation. Part I: constitutive framework , 2005 .

[52]  Jean-François Ganghoffer,et al.  On Eshelby tensors in the context of the thermodynamics of open systems: Application to volumetric growth , 2010 .

[53]  M. Janmaleki,et al.  Effect of uniaxial stretch on morphology and cytoskeleton of human mesenchymal stem cells: static vs. dynamic loading , 2011, Biomedizinische Technik. Biomedical engineering.

[54]  J D Humphrey,et al.  Stress, strain, and mechanotransduction in cells. , 2001, Journal of biomechanical engineering.

[55]  Larry A Taber,et al.  Towards a unified theory for morphomechanics , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[56]  R. Ogden,et al.  A New Constitutive Framework for Arterial Wall Mechanics and a Comparative Study of Material Models , 2000 .

[57]  Andreas Menzel,et al.  Modelling of anisotropic growth in biological tissues , 2005 .

[58]  Günther Meschke,et al.  A computational remodeling approach to predict the physiological architecture of the collagen fibril network in corneo-scleral shells , 2010, Biomechanics and modeling in mechanobiology.

[59]  Roger D. Kamm,et al.  Cytoskeletal mechanics : models and measurements , 2006 .

[60]  K. Grosh,et al.  A continuum treatment of growth in biological tissue: the coupling of mass transport and mechanics , 2003, q-bio/0312001.

[61]  Samuel A. Safran,et al.  Dynamics of cell orientation , 2007 .

[62]  W. Goldmann,et al.  Mechanotransduction in cells 1 , 2012, Cell biology international.

[63]  M. Boyce,et al.  A three-dimensional constitutive model for the large stretch behavior of rubber elastic materials , 1993 .

[64]  E. Kuhl,et al.  A continuum model for remodeling in living structures , 2007 .

[65]  J. D. Humphrey,et al.  Need for a Continuum Biochemomechanical Theory of Soft Tissue and Cellular Growth and Remodeling , 2009 .

[66]  Christopher Bingham An Antipodally Symmetric Distribution on the Sphere , 1974 .

[67]  U. Schwarz,et al.  Cell organization in soft media due to active mechanosensing , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[68]  R. Ogden,et al.  Hyperelastic modelling of arterial layers with distributed collagen fibre orientations , 2006, Journal of The Royal Society Interface.

[69]  Paul Steinmann,et al.  A thermodynamically consistent approach to microplane theory. Part II. Dissipation and inelastic constitutive modeling , 2001 .

[70]  L. Taber A model for aortic growth based on fluid shear and fiber stresses. , 1998, Journal of biomechanical engineering.

[71]  R. Kaunas,et al.  A Dynamic Stochastic Model of Frequency-Dependent Stress Fiber Alignment Induced by Cyclic Stretch , 2009, PloS one.

[72]  A. Menzel,et al.  Towards an orientation-distribution-based multi-scale approach for remodelling biological tissues , 2008, Computer methods in biomechanics and biomedical engineering.

[73]  Serdar Göktepe,et al.  A multiscale model for eccentric and concentric cardiac growth through sarcomerogenesis. , 2010, Journal of theoretical biology.

[74]  R. Leask,et al.  The development of 3-D, in vitro, endothelial culture models for the study of coronary artery disease , 2009, Biomedical engineering online.

[75]  J. Humphrey,et al.  A Mixture Model of Arterial Growth and Remodeling in Hypertension: Altered Muscle Tone and Tissue Turnover , 2004, Journal of Vascular Research.

[76]  A. Menzel,et al.  A fibre reorientation model for orthotropic multiplicative growth , 2007, Biomechanics and modeling in mechanobiology.

[77]  H. Narayanan,et al.  Biological remodelling: Stationary energy, configurational change, internal variables and dissipation , 2005, q-bio/0506023.

[78]  C. Bustamante,et al.  Ten years of tension: single-molecule DNA mechanics , 2003, Nature.

[79]  Y. Fung,et al.  Biomechanics: Mechanical Properties of Living Tissues , 1981 .

[80]  S. Safran,et al.  Cyclic Stress at mHz Frequencies Aligns Fibroblasts in Direction of Zero Strain , 2011, PloS one.

[81]  S. Safran,et al.  Do cells sense stress or strain? Measurement of cellular orientation can provide a clue. , 2008, Biophysical journal.

[82]  Jay D Humphrey,et al.  Growth and remodeling in a thick-walled artery model: effects of spatial variations in wall constituents , 2008, Biomechanics and modeling in mechanobiology.

[83]  Jean-François Ganghoffer,et al.  Mechanical modeling of growth considering domain variation―Part II: Volumetric and surface growth involving Eshelby tensors , 2010 .

[84]  K. Grosh,et al.  Remodeling of biological tissue: Mechanically induced reorientation of a transversely isotropic chain network , 2004, q-bio/0411037.

[85]  F P T Baaijens,et al.  A computational model for collagen fibre remodelling in the arterial wall. , 2004, Journal of theoretical biology.

[86]  P. Bovendeerd,et al.  Stability against dynamic remodeling of an arterial tissue , 2010 .

[87]  Victor H Barocas,et al.  Image-based multiscale modeling predicts tissue-level and network-level fiber reorganization in stretched cell-compacted collagen gels , 2009, Proceedings of the National Academy of Sciences.

[88]  A. McCulloch,et al.  Stress-dependent finite growth in soft elastic tissues. , 1994, Journal of biomechanics.

[89]  Andreas Menzel,et al.  A micro‐sphere‐based remodelling formulation for anisotropic biological tissues , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[90]  P. Bovendeerd,et al.  A model for arterial adaptation combining microstructural collagen remodeling and 3D tissue growth , 2010, Biomechanics and modeling in mechanobiology.