Composition of the pericellular matrix modulates the deformation behaviour of chondrocytes in articular cartilage under static loading

The aim was to assess the role of the composition changes in the pericellular matrix (PCM) for the chondrocyte deformation. For that, a three-dimensional finite element model with depth-dependent collagen density, fluid fraction, fixed charge density and collagen architecture, including parallel planes representing the split-lines, was created to model the extracellular matrix (ECM). The PCM was constructed similarly as the ECM, but the collagen fibrils were oriented parallel to the chondrocyte surfaces. The chondrocytes were modelled as poroelastic with swelling properties. Deformation behaviour of the cells was studied under 15% static compression. Due to the depth-dependent structure and composition of cartilage, axial cell strains were highly depth-dependent. An increase in the collagen content and fluid fraction in the PCMs increased the lateral cell strains, while an increase in the fixed charge density induced an inverse behaviour. Axial cell strains were only slightly affected by the changes in PCM composition. We conclude that the PCM composition plays a significant role in the deformation behaviour of chondrocytes, possibly modulating cartilage development, adaptation and degeneration. The development of cartilage repair materials could benefit from this information.

[1]  M J Glimcher,et al.  In vitro wear of articular cartilage. , 1975, The Journal of bone and joint surgery. American volume.

[2]  F Guilak,et al.  Viscoelastic properties of chondrocytes from normal and osteoarthritic human cartilage , 2000, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[3]  Walter Herzog,et al.  Analysis of the mechanical behavior of chondrocytes in unconfined compression tests for cyclic loading. , 2006, Journal of biomechanics.

[4]  V. Mow,et al.  Biphasic creep and stress relaxation of articular cartilage in compression? Theory and experiments. , 1980, Journal of biomechanical engineering.

[5]  T. Laursen,et al.  Determination of the Poisson's ratio of the cell: recovery properties of chondrocytes after release from complete micropipette aspiration. , 2006, Journal of biomechanics.

[6]  A Shirazi-Adl,et al.  Role of cartilage collagen fibrils networks in knee joint biomechanics under compression. , 2008, Journal of biomechanics.

[7]  E B Hunziker,et al.  Mechanical compression alters proteoglycan deposition and matrix deformation around individual cells in cartilage explants. , 1998, Journal of cell science.

[8]  W. Herzog,et al.  Finite Element Simulation of Location- and Time-Dependent Mechanical Behavior of Chondrocytes in Unconfined Compression Tests , 2000, Annals of Biomedical Engineering.

[9]  W Wouter Wilson,et al.  Mechanical regulation of the chondron collagen fiber network structure , 2005 .

[10]  Petro Julkunen,et al.  Stress-relaxation of human patellar articular cartilage in unconfined compression: prediction of mechanical response by tissue composition and structure. , 2008, Journal of biomechanics.

[11]  Walter Herzog,et al.  NOVEL IN SITU CHONDROCYTE INDENTATION STUDY , 2007 .

[12]  H. P. Ting-Beall,et al.  The effects of osmotic stress on the viscoelastic and physical properties of articular chondrocytes. , 1999, Biophysical journal.

[13]  Gerard A Ateshian,et al.  In-situ measurements of chondrocyte deformation under transient loading. , 2007, European cells & materials.

[14]  J M Huyghe,et al.  A composition-based cartilage model for the assessment of compositional changes during cartilage damage and adaptation. , 2006, Osteoarthritis and cartilage.

[15]  Petro Julkunen,et al.  Characterization of articular cartilage by combining microscopic analysis with a fibril-reinforced finite-element model. , 2007, Journal of biomechanics.

[16]  A Ratcliffe,et al.  Mechanical and biochemical changes in the superficial zone of articular cartilage in canine experimental osteoarthritis , 1994, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[17]  Albert C. Chen,et al.  Depth‐dependent confined compression modulus of full‐thickness bovine articular cartilage , 1997, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[18]  Van C Mow,et al.  The effect of matrix tension-compression nonlinearity and fixed negative charges on chondrocyte responses in cartilage. , 2005, Molecular & cellular biomechanics : MCB.

[19]  Farshid Guilak,et al.  The biomechanical role of the chondrocyte pericellular matrix in articular cartilage. , 2005, Acta biomaterialia.

[20]  H Shinkai,et al.  Chondrons from articular cartilage (II): Analysis of the glycosaminoglycans in the cellular microenvironment of isolated canine chondrons. , 1990, Connective tissue research.

[21]  Walter Herzog,et al.  Depth-dependent analysis of the role of collagen fibrils, fixed charges and fluid in the pericellular matrix of articular cartilage on chondrocyte mechanics. , 2008, Journal of biomechanics.

[22]  Mauro Alini,et al.  9 – Cellular Biology of Cartilage Degradation , 1995 .

[23]  J. M. Huyghe,et al.  An ionised/non-ionised dual porosity model of intervertebral disc tissue , 2003, Biomechanics and modeling in mechanobiology.

[24]  A. Maroudas,et al.  Measurement of swelling pressure in cartilage and comparison with the osmotic pressure of constituent proteoglycans. , 1981, Biorheology.

[25]  E B Hunziker,et al.  Stimulation of aggrecan synthesis in cartilage explants by cyclic loading is localized to regions of high interstitial fluid flow. , 1999, Archives of biochemistry and biophysics.

[26]  A. Maroudas,et al.  Physicochemical properties of cartilage in the light of ion exchange theory. , 1968, Biophysical journal.

[27]  W. R. Jones,et al.  The deformation behavior and mechanical properties of chondrocytes in articular cartilage. , 1999, Osteoarthritis and cartilage.

[28]  L. Dahners,et al.  The collagenous architecture of articular cartilage. Correlation of scanning electron microscopy and polarized light microscopy observations. , 1979, Clinical orthopaedics and related research.

[29]  S. Ayad,et al.  Chondrons from articular cartilage. V. Immunohistochemical evaluation of type VI collagen organisation in isolated chondrons by light, confocal and electron microscopy. , 1992, Journal of cell science.

[30]  Farshid Guilak,et al.  Alterations in the mechanical properties of the human chondrocyte pericellular matrix with osteoarthritis. , 2003, Journal of biomechanical engineering.

[31]  Farshid Guilak,et al.  Zonal changes in the three-dimensional morphology of the chondron under compression: the relationship among cellular, pericellular, and extracellular deformation in articular cartilage. , 2007, Journal of biomechanics.

[32]  Zhanfeng Cui,et al.  Measurement of the chondrocyte membrane permeability to Me2SO, glycerol and 1,2-propanediol. , 2003, Medical engineering & physics.

[33]  A. Grodzinsky,et al.  Nanomechanical properties of individual chondrocytes and their developing growth factor-stimulated pericellular matrix. , 2007, Journal of biomechanics.

[34]  W M Lai,et al.  Electrical signals for chondrocytes in cartilage. , 2002, Biorheology.

[35]  A Ratcliffe,et al.  Changes in proteoglycan synthesis of chondrocytes in articular cartilage are associated with the time-dependent changes in their mechanical environment. , 1995, Journal of biomechanics.

[36]  F. Guilak,et al.  The role of the cytoskeleton in the viscoelastic properties of human articular chondrocytes. , 2004, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[37]  A. Borthakur,et al.  Water distribution patterns inside bovine articular cartilage as visualized by 1H magnetic resonance imaging. , 2001, Osteoarthritis and cartilage.

[38]  S. Ayad,et al.  Chondrons from articular cartilage: I. Immunolocalization of type VI collagen in the pericellular capsule of isolated canine tibial chondrons. , 1988, Journal of cell science.

[39]  R. G. Richards,et al.  Deformation of Chondrocytes in Articular Cartilage under Compressive Load: A Morphological Study , 2003, Cells Tissues Organs.

[40]  R. Schugart,et al.  Mathematical Models and Numerical Methods for Analysis of Mechanical and Chemical Loading in Articular Cartilage , 2005 .

[41]  J. M. Huyghe,et al.  Depth-dependent Compressive Equilibrium Properties of Articular Cartilage Explained by its Composition , 2007, Biomechanics and modeling in mechanobiology.

[42]  Petro Julkunen,et al.  Collagen Network of Articular Cartilage Modulates Fluid Flow and Mechanical Stresses in Chondrocyte , 2006, Biomechanics and modeling in mechanobiology.

[43]  P J Basser,et al.  Mechanical properties of the collagen network in human articular cartilage as measured by osmotic stress technique. , 1998, Archives of biochemistry and biophysics.

[44]  Farshid Guilak,et al.  Zonal Uniformity in Mechanical Properties of the Chondrocyte Pericellular Matrix: Micropipette Aspiration of Canine Chondrons Isolated by Cartilage Homogenization , 2005, Annals of Biomedical Engineering.

[45]  R K Korhonen,et al.  Mechanical characterization of articular cartilage by combining magnetic resonance imaging and finite-element analysis—a potential functional imaging technique , 2008, Physics in medicine and biology.

[46]  E B Hunziker,et al.  Mechanical compression modulates matrix biosynthesis in chondrocyte/agarose culture. , 1995, Journal of cell science.

[47]  G A Ateshian,et al.  A Theoretical Analysis of Water Transport Through Chondrocytes , 2007, Biomechanics and modeling in mechanobiology.

[48]  LePing Li,et al.  Three-dimensional fibril-reinforced finite element model of articular cartilage , 2009, Medical & Biological Engineering & Computing.

[49]  F. Guilak.  The deformation behavior and viscoelastic properties of chondrocytes in articular cartilage. , 2000, Biorheology.

[50]  V. Mow,et al.  The mechanical environment of the chondrocyte: a biphasic finite element model of cell-matrix interactions in articular cartilage. , 2000, Journal of biomechanics.

[51]  W Wilson,et al.  A fibril-reinforced poroviscoelastic swelling model for articular cartilage. , 2005, Journal of biomechanics.

[52]  R. Schneiderman,et al.  Depth-dependent compressive properties of normal aged human femoral head articular cartilage: relationship to fixed charge density. , 2001, Osteoarthritis and cartilage.

[53]  W A Hing,et al.  The influence of the pericellular microenvironment on the chondrocyte response to osmotic challenge. , 2002, Osteoarthritis and cartilage.

[54]  V. Mow,et al.  Chondrocyte deformation and local tissue strain in articular cartilage: A confocal microscopy study , 1995, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[55]  Walter Herzog,et al.  Importance of collagen orientation and depth-dependent fixed charge densities of cartilage on mechanical behavior of chondrocytes. , 2008, Journal of biomechanical engineering.

[56]  C A Poole,et al.  Chondrons extracted from canine tibial cartilage: Preliminary report on their isolation and structure , 1988, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[57]  Farshid Guilak,et al.  Osteoarthritic changes in the biphasic mechanical properties of the chondrocyte pericellular matrix in articular cartilage. , 2005, Journal of biomechanics.