Viscoelastic properties of chondrocytes from normal and osteoarthritic human cartilage

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Trickey, Wendy R.^1,2; Lee, Greta M.³; Guilak, Farshid^1,2,4

Viscoelastic properties of chondrocytes from normal and osteoarthritic human cartilage

J Orthop Res. November 2000;18(6):891-898

©2000 Orthopacdic Research Society

Affiliations

¹Orthopaedic Research Laboratories, Department of Surgery, Duke University Medical Center, Duke University, Durham

²Department of Biomedical Engineering, Duke University, Durham

³Thurston Arthritis Research Center, Department of Orthopaedics, University of North Carolina, Chapel Hill, North Carolina, U.S.A.

⁴Department of Mechanical Engineering and Material Science, Duke University, Durham
Abstract

The deformation behavior and mechanical properties of articular chondrocytes are believed to play an important role in their response to mechanical loading of the extracellular matrix. This study utilized the micropipette aspiration test to measure the viscoelastic properties of chondrocytes isolated from macroscopically normal or end-stage osteoarthritic cartilage. A three-parameter standard linear solid was used to model the viscoelastic behavior of the cells. Significant differences were found between the mechanical properties of chondrocytes isolated from normal and osteoarthritic cartilage. Specifically, osteoarthritic chondrocytes exhibited a significantly higher equilibrium modulus (0.33 ± 0.23 compared with 0.24 ± 0.11 kPa), instantaneous modulus (0.63 ± 0.51 compared with 0.41 ± 0.17 kPa), and apparent viscosity (5.8 ± 6.5 compared with 3.0 ± 1.8 kPa-s) compared with chondrocytes isolated from macroscopically normal, nonosteoarthritic cartilage. The elastic moduli and relaxation time constant determined experimentally in this study were used to estimate the apparent biphasic properties of the chondrocyte on the basis of the equation for the gel relaxation time of a biphasic material. The differences in viscoelastic properties may reflect alterations in the structure and composition of the chondrocyte cytoskeleton that have previously been associated with osteoarthritic cartilage. Coupled with earlier theoretical models of cell-matrix interactions in articular cartilage, the increased elastic and viscous properties suggest that the mechanical environment of the chondrocyte may be altered in osteoarthritic cartilage.
Links

DOI: 10.1002/jor.1100180607

PubMed: 11192248

WoS: 000166217600006
History

Received: 1999-11-08

Accepted: 2000-02-11

Cited Works (17)

Year	Entry
1982	Armstrong CG, Mow VC. Variations in the intrinsic mechanical properties of human articular cartilage with age, degeneration, and water content. J Bone Joint Surg. 1982;64A(1):88-94.
1994	Mow VC, Bachrach NM, Setton LA, Guilak F. Stress, strain, pressure and flow fields in articular cartilage and chondrocytes. In: Mow VC, Tran-Son-Tay R, Guilak F, Hochmuth RM, eds. Cell Mechanics and Cellular Engineering. Symposium on Cell Mechanics and Cellular Engineering; July 10-15, 1994. New York, NY: Springer-Verlag; 1994:345-379.
1994	Freeman PM, Natarajan RN, Kimura JH, Andriacchi TP. Chondrocyte cells respond mechanically to compressive loads. J Orthop Res. May 1994;12(3):311-320.
1999	Guilak F, Jones WR, Ting-Beall HP, Lee GM. The deformation behavior and mechanical properties of chondrocytes in articular cartilage. Osteoarthritis Cartilage. January 1999;7(1):59-70.
1996	Wong M, Wuethrich P, Eggli P, Hunziker E. Zone-specific cell biosynthetic activity in mature bovine articular cartilage: a new method using confocal microscopic stereology and quantitative autoradiography. J Orthop Res. May 1996;14(3):424-432.
1980	Mow VC, Kuei SC, Lai WM, Armstrong CG. Biphasic creep and stress relaxation of articular cartilage in compression: theory and experiments. J Biomech Eng. February 1980;102(1):73-84.
1994	Guilak F, Meyer BC, Ratcliffe A, Mow VC. The effects of matrix compression on proteoglycan metabolism in articular cartilage explants. Osteoarthritis Cartilage. June 1994;2(2):91-101.
1990	Sato M, Theret DP, Wheeler LT, Ohshima N, Nerem RM. Application of the micropipette technique to the measurement of cultured porcine aortic endothelial cell viscoelastic properties. J Biomech Eng. August 1990;112(3):263-268.
1995	Guilak F, Ratcliffe A, Mow VC. Chondrocyte deformation and local tissue strain in articular cartilage: a confocal microscopy study. J Orthop Res. May 1995;13(3):410-421.
1995	Bachrach NM, Valhmu WB, Stazzone E, Ratcliffe A, Lai WM, Mow VC. Changes in proteoglycan synthesis of chondrocytes in articular cartilage are associated with the time-dependent changes in their mechanical environment. J Biomech. December 1995;28(12):1561-1569.
2000	Hochmuth RM. Micropipette aspiration of living cells. J Biomech. January 2000;33(1):15-22.
1994	Kim Y-J, Sah RLY, Grodzinsky AJ, Plaas AHK, Sandy JD. Mechanical regulation of cartilage biosynthetic behavior: physical stimuli. Arch Biochem Biophys. May 1994;311(1):1-12.
1999	Shin D, Athanasiou K. Cytoindentation for obtaining cell biomechanical properties. J Orthop Res. November 1999;17(6):880-890.
1998	Valhmu WB, Stazzone EJ, Bachrach NM, Saed-Nejad F, Fischer SG, Mow VC, Ratcliffe A. Load-controlled compression of articular cartilage induces a transient stimulation of aggrecan gene expression. Arch Biochem Biophys. May 1, 1998;353(1):29-36.
2000	Guilak F, Mow VC. The mechanical environment of the chondrocyte: a biphasic finite element model of cell–matrix interactions in articular cartilage. J Biomech. December 2000;33(12):1663-1673.
1988	Theret DP, Levesque MJ, Sato M, Nerem RM, Wheeler LT. The application of a homogeneous half-space model in the analysis of endothelial cell micropipette measurements. J Biomech Eng. August 1988;110(3):190-199.
1999	Jones WR, Ping Ting-Beall H, Lee GM, Kelley SS, Hochmuth RM, Guilak F. Alterations in the young’s modulus and volumetric properties of chondrocytes isolated from normal and osteoarthritic human cartilage. J Biomech. February 1999;32(2):119-127.

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2005	Alexopoulos LG, Setton LA, Guilak F. The biomechanical role of the chondrocyte pericellular matrix in articular cartilage. Acta Biomater. May 2005;1(3):317-325.
2006	Guilak F, Alexopoulos LG, Upton ML, Youn I, Choi JB, Cao L, Setton LA, Haider MA. The pericellular matrix as a transducer of biomechanical and biochemical signals in articular cartilage. Annals NY Acad Sci. April 2006;1068(1):498-512.
2002	Provenzano PP, Lakes RS, Corr DT, Vanderby R. Application of nonlinear viscoelastic models to describe ligament behavior. Biomech Model Mechanobiol. June 2002;1(1):45-57.
2002	Guilak F, Erickson GR, Ting-Beall HP. The effects of osmotic stress on the viscoelastic and physical properties of articular chondrocytes. Biophys J. February 2002;82(2):720-727.
2000	Guilak F, Mow VC. The mechanical environment of the chondrocyte: a biphasic finite element model of cell–matrix interactions in articular cartilage. J Biomech. December 2000;33(12):1663-1673.
2005	Leipzig ND, Athanasiou KA. Unconfined creep compression of chondrocytes. J Biomech. January 2005;38(1):77-85.
2005	Alexopoulos LG, Williams GM, Upton ML, Setton LA, Guilak F. Osteoarthritic changes in the biphasic mechanical properties of the chondrocyte pericellular matrix in articular cartilage. J Biomech. March 2005;38(3):509-517.
2007	Choi JB, Youn I, Cao L, Leddy HA, Gilchrist CL, Setton LA, Guilak F. Zonal changes in the three-dimensional morphology of the chondron under compression: the relationship among cellular, pericellular, and extracellular deformation in articular cartilage. J Biomech. 2007;40(12):2596-2603.
2008	Darling EM, Topel M, Zauscher S, Vail TP, Guilak F. Viscoelastic properties of human mesenchymally-derived stem cells and primary osteoblasts, chondrocytes, and adipocytes. J Biomech. 2008;41(2):454-464.
2003	Baer AE, Laursen TA, Guilak F, Setton LA. The micromechanical environment of intervertebral disc cells determined by a finite deformation, anisotropic, and biphasic finite element model. J Biomech Eng. February 2003;125(1):1-11.
2003	Alexopoulos LG, Haider MA, Vail TP, Guilak F. Alterations in the mechanical properties of the human chondrocyte pericellular matrix with osteoarthritis. J Biomech Eng. June 2003;125(3):323-333.
2003	Koay EJ, Shieh AC, Athanasiou KA. Creep indentation of single cells. J Biomech Eng. June 2003;125(3):334-341.
2004	Trickey WR, Vail TP, Guilak F. The role of the cytoskeleton in the viscoelastic properties of human articular chondrocytes. J Orthop Res. January 2004;22(1):131-139.
2006	Darling EM, Zauscher S, Guilak F. Viscoelastic properties of zonal articular chondrocytes measured by atomic force microscopy. Osteoarthritis Cartilage. June 2006;14(6):571-579.
2006	Youn I, Choi JB, Cao L, Setton LA, Guilak F. Zonal variations in the three-dimensional morphology of the chondron measured in situ using confocal microscopy. Osteoarthritis Cartilage. September 2006;14(9):889-897.
2021	Dempsey M. Molecular Recognition Tools for Live-Cell Labeling and Enrichment [PhD thesis]. Brown University; October 2021.
2005	Takai E. Modulation of Bone Cell Mechanotransduction [PhD thesis]. Columbia University; 2005.
2006	Chahine NO. Multi-Scale Measurements of the Mechanical and Transport Properties of Native and Engineered Articular Cartilage [PhD thesis]. Columbia University; 2006.
2007	Likhitpanichkul M. The Cell-Matrix Mechano-Electrochemical Interactions in Articular Cartilage: Experiment and Triphasic Model [PhD thesis]. Columbia University; 2007.
2001	Baer AE. The Micromechanical Environment of Intervertebral Disc Cells [PhD thesis]. Duke University; 2001.
2001	Erickson GR. Articular Chondrocyte Response to Osmotic Stress: The Involvement of Calcium and the Cytoskeleton in Cellular Volume Adaptation and Regulation [PhD thesis]. Duke University; 2001.
2004	Alexopoulos LG. The Biomechanical Role of the Chondrocyte Pericellular Matrix in Articular Cartilage [PhD thesis]. Duke University; 2004.
2007	Upton ML. Theoretical Predictions and Experimental Measurements of the Micromechanical Environment of Meniscus Cells [PhD thesis]. Duke University; 2007.
2010	Finan JD. The Effect of Osmotic Stress on the Structure and Properties of the Cell Nucleus [PhD thesis]. Duke University; 2010.
2013	Wilusz RE. Micromechanical Properties of the Extracellular and Pericellular Matrices of Articular Cartilage [PhD thesis]. Duke University; 2013.
2005	Ng LJ. Probing Nanomechanics of Aggrecan and the Aggrecan-Rich Pericellular Matrix of Chondrocytes in Cartilage [PhD thesis]. Cambridge, MA: Massachusetts Institute of Technology; September 2005.
2009	Chen S. Regulation of Lubricin Gene Expression and Synthesis in Cartilage by Mechanical Injury [PhD thesis]. Cambridge, MA: Massachusetts Institute of Technology; September 2009.
2009	Lee B. Time-Dependent Mechanical Behavior of Newly Developing Matrix of Bovine Primary Chondrocytes and Bone Marrow Stromal Cells Using Atomic Force Microscopy [PhD thesis]. Cambridge, MA: Massachusetts Institute of Technology; September 2009.
2011	Amini S. Stress Relaxation of Growth Plate Tissue Under Uniform Compressive Load: Relationship Between Mechanical Response and Extracellular Matrix Bio-Composition and Structure [PhD thesis]. École polytechnique de Montréal; December 2011.
2018	De Mori A. Silver Nanowires and Their Potential Use as 3D Scaffolds for Biomedical Applications [PhD thesis]. Portsmouth, England: University of Portsmouth; October 2018.
2011	Jeon JE. Development of Zonal Cartilage Constructs: Effects of Chondrocyte Subpopulation, Compressive Stimulation, and Culture Models [PhD thesis]. Queensland University of Technology; 2011.
2005	Hu J. Chondrocyte Self -Assembly and Culture in Bioreactors [PhD thesis]. Houston, TX: Rice University; April 2005.
2005	Scott CC. Interferometry of Chondrocytes and Impact of Articular Cartilage [PhD thesis]. Houston, TX: Rice University; August 2005.
2006	Leipzig ND. Growth Factor Effects on Single Chondrocyte Biomechanics and Gene Expression [PhD thesis]. Houston, TX: Rice University; April 2006.
2006	Shieh AC. Mechanobiology of Single Chondrocytes [PhD thesis]. Houston, TX: Rice University; April 2006.
2007	Koay EJ. Chondrocyte Biomechanics and Chondrogenesis [PhD thesis]. Houston, TX: Rice University; December 2007.
2008	Natoli RM. Impact Loading and Functional Tissue Engineering of Articular Cartilage [PhD thesis]. Houston, TX: Rice University; October 2008.
2009	Ofek G. Biomechanics of the Single Chondrocyte and Its Developing Extracellular Matrix [PhD thesis]. Houston, TX: Rice University; May 2009.
2011	Eleswarapu SV. Multiscale Strategies for Cartilage Repair [PhD thesis]. Houston, TX: Rice University; October 2011.
2011	Willard VP. Characterization of the Temporomandibular Joint Disc and Fibrocartilage Engineering Using Human Embryonic Stem Cells [PhD thesis]. Houston, TX: Rice University; May 2011.
2012	Sanchez-Adams J. Regional Characterization of the Knee Meniscus and Tissue Engineering With Dermal Stem Cells [PhD thesis]. Houston, TX: Rice University; 2012.
2007	Malone AMD. Mechanotransduction Mechanisms in Bone Cells [PhD thesis]. Stanford University; August 2007.
2005	McGarry JG. Computational and Experimental Investigation of Bone Cell Response to Mechanical Stimuli [PhD thesis]. Trinity College Dublin; September 2005.
2009	Tripathy S. An Indentation Study of Costal Cartilage Using Atomic Force Microscopy [PhD thesis]. Charlottesville, VA: University of Virginia; May 2009.
2009	Rath AL. The Effects of Strain and Perilacunar Environment on the Mechanotransduction of Osteocytes [PhD thesis]. Winston-Salem, NC: Wake Forest University; May 2009.