Journal of Biomechanics
Volume 43, Issue 3 , Pages 469-476 , 10 February 2010

Dynamic mechanical properties of the tissue-engineered matrix associated with individual chondrocytes

  • BoBae Lee

      Affiliations

    • Department of Materials Science and Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA
    • ,
  • Lin Han

      Affiliations

    • Department of Materials Science and Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA
    • ,
  • Eliot H. Frank

      Affiliations

    • Center for Biomedical Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA
    • ,
  • Susan Chubinskaya

      Affiliations

    • Department of Biochemistry, Rush University Medical Center, Chicago, IL 60612, USA
    • ,
  • Christine Ortiz

      Affiliations

    • Department of Materials Science and Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA
    • ,
  • Alan J. Grodzinsky

      Affiliations

    • Center for Biomedical Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA
    • Electrical Engineering and Computer Science, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA
    • Mechanical Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA
    • Biological Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA
    • Corresponding Author InformationCorresponding author at: Electrical Engineering and Computer Science, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA. Tel.: +6172534969; fax: +6172585239.

,Accepted 28 September 2009.

References 

  1. Alcaraz J, Busceme L, Puig-de-Morales M, Colchero J, Baró A, Navajas D. Correction of microrheological measurements of soft samples with atomic force microscopy for the hydrodynamic drag on the cantilever. Langmuir. 2002;18:716–721
  2. Alcaraz J, Buscemi L, Grabulosa M, Trepat X, Fabry B, Farre R, et al. Microrheology of human lung epithelial cells measured by atomic force microscopy. Biophys. J. 2003;84:2071–2079
  3. Alexopoulos LG, Haider MA, Vail TP, Guilak F. Alterations in the mechanical properties of the human chondrocyte pericellular matrix with osteoarthritis. J. Biomech. Eng. 2003;125:323–333
  4. 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. 2005;38:509–517
  5. Buschmann MD, Gluzband YA, Grodzinsky AJ, Hunziker EB. Mechanical compression modulates matrix biosynthesis in chondrocyte/agarose culture. J. Cell Sci. 1995;108:1497–1508
  6. Buschmann MD, Gluzband YA, Grodzinsky AJ, Kimura JH, Hunziker EB. Chondrocytes in agarose culture synthesize a mechanically functional extracellular matrix. J. Orthop. Res. 1992;10:745–758
  7. Buschmann MD, Kim Y-J, Wong M, Frank E, Hunziker EB, Grodzinsky AJ. Stimulation of aggrecan synthesis in cartilage explants by cyclic loading is localized to regions of high interstitial fluid flow. Arch. Biochem. Biophys. 1999;366(1):1–7
  8. Chao PG, Tang Z, Angelini E, West AC, Costa KD, Hung CT. Dynamic osmotic loading of chondrocytes using a novel microfluidic device. J. Biomech. 2005;38:1273–1281
  9. Darling EM, Zauscher S, Guilak F. A thin-layer model for viscoelastic, stress-relaxation testing of cells using atomic force microscopy: do cell properties reflect metastatic potential?. Biophys. J. 2007;92:1784–1791
  10. DiMicco MA, Kisiday JD, Gong H, Grodzinsky AJ. Structure of pericellular matrix around agarose-embedded chondrocytes. Osteoarthr. Cartilage. 2007;15(10):1207–1216
  11. Dudhia J. Aggrecan, aging and assembly in articular cartilage. Cell Mol. Life Sci. 2005;62:2241–2256
  12. Eisenberg SR, Grodzinsky AJ. Electrokinetic micromodel of extracellular matrix and other polyelectrolyte networks. Physicochem. Hydrodyn. 1988;10(4):517–539
  13. Flory PJ. Configurational and frictional properties of the polymer molecule in dilute solution. In: Principles of Polymer Chemistry. Ithaca: Cornell Univ. Press; 1953;p. 595–639
  14. Frank EH, Grodzinsky AJ. Cartilage Electromechanics - II. Continuum model of cartilage electrokinetics and correlation with experiments. J. Biomech. 1987;20:629–639
  15. Freeman PM, Natarajan RN, Kimura JH, Andriacchi TP. Chondrocyte cells respond mechanically to compressive loads. J. Orthop. Res. 1994;12:311–320
  16. Grodzinsky AJ, Roth V, Myers E, Grossman WD, Mow VC. The significance of electromechanical and osmotic forces in the nonequilibrium swelling behavior of articular cartilage in tension. J. Biomech. Eng. 1981;103:221–231
  17. Han, L., Greene J.J., Frank E.H., Hung H.-H.K., Grodzinsky A.J., Ortiz, C., 2008. Effect of length scale on frequency-dependent cartilage oscillatory nanomechanics. 54th Annual Meeting of the Orthopaedic Research Society, San Francisco, CA.
  18. Happel J. Viscous flow relative to arrays of cylinders. AIChE J. 1959;5(2):174–177
  19. Huang C-Y, Soltz MA, Kopacz M, Ateshian GA. Experimental verification of the roles of intrinsic matrix compression nonlinearity in the biphasic response of cartilage. J. Biomech. Eng. 2003;125:84–93
  20. Huang W, Anvari B, Torres JH, LeBaron RG, Athanasiou KA. Temporal effects of cell adhesion on mechanical characteristics of the single chondrocyte. J. Orthop. Res. 2003;21:88–95
  21. Johnson KL, Greenwood JA. An adhesion map for the contact of elastic spheres. J. Colloid Interface Sci. 1997;192:326–333
  22. Kim E, Guilak F, Haider MA. The dynamic mechanical environment of the chondrocyte: a biphasic finite element model of cell-matrix interactions under cyclic compressive loading. J. Biomech. Eng. 2008;130:061009.1–061009.10
  23. Kim Y-J, Bonassar LJ, Grodzinsky AJ. The role of cartilage streaming potential, fluid flow and pressure in the stimulation of chondrocyte biosynthesis during dynamic compression. J. Biomech. 1995;28(9):1055–1066
  24. Lee GM, Johnstone B, Jacobson K, Caterson B. The dynamic structure of the pericellular matrix on living cells. J. Cell Biol. 1993;123(6):1899–1907
  25. Lee GM, Loeser RF. Interactions of the chondrocyte with its pericellular matrix. Cell Mater. 1998;8:135–149
  26. Lee RC, Frank EH, Grodzinsky AJ, Roylance DK. Oscillatory compressional behavior of articular cartilage and its associated electromechanical properties. J. Biomech. Eng. 1981;103:280–292
  27. Loeser RF, Pacione CA, Chubinskaya S. The combination of insulin-like growth factor 1 and osteogenic protein 1 promotes increased survival of and matrix synthesis by normal and osteoarthritic human articular chondrocytes. Arthritis Rheum. 2003;48:2188–2196
  28. Mahaffy RE, Park S, Gerde E, Käs J, Shih CK. Quantitative analysis of the viscoelastic properties of thin regions of fibroblasts using atomic force microscopy. Biophys. J. 2004;86:1777–1793
  29. Mahaffy RE, Shih CK, MacKintosh FC, Käs J. Scanning probe-based frequency-dependent microrheology of polymer gels and biological cells. Phys. Rev. Lett. 2000;85(4):880–883
  30. Mauck RL, Soltz MA, Wang CCB, Wong DD, Chao P-HG, Valhmu WB, et al. Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. J. Biomech. Eng. 2000;122:252–260
  31. Millward-Sadler SJ, Salter DM. Integrin-dependent signal cascades in chondrocyte mechanotransduction. Ann. Biomed. Eng. 2004;32(3):435–446
  32. Millward-Sadler SJ, Wright MO, Davies LW, Nuki G, Salter DM. Mechanotransduction via integrins and interleukin-4 results in altered aggrecan and matrix metalloproteinase 3 gene expression in normal, but not osteoarthritic, human articular chondrocytes. Arthritis Rheum. 2000;43(9):2091–2099
  33. Morel V, Quinn TM. Cartilage injury by ramp compression near the gel diffusion rate. J. Orthop. Res. 2004;22:145–151
  34. Mow VC, Kuei SC, Lai WM, Armstrong CG. Biphasic creep and stress relaxation of articular cartilage in compression: theory and experiments. J. Biomech. Eng. 1980;102(73):73–84
  35. Ng L, Hung H-H, Sprunt A, Chubinskaya S, Ortiz C, Grodzinsky AJ. Nanomechanical properties of individual chondrocytes and their developing growth factor-stimulated pericellular matrix. J. Biomech. 2007;40(5):1011–1023
  36. Park S, Koch D, Cardenas R, Käs J, Shih CK. Cell motility and local viscoelasticity of fibroblasts. Biophys. J. 2005;89:4330–4342
  37. Radmacher M. Measuring the elastic properties of biological samples with the AFM. IEEE Eng. Med. Biol. 1997;16(2):47–57
  38. Shepherd DET, Seedhom BB. A technique for measuring the compressive modulus of articular cartilage under physiological loading rates with preliminary results. Pro. Instn. Mech. Engrs. Part H. 1997;211:155–165
  39. Shieh AC, Athanasiou KA. Biomechanics of single zonal chondrocytes. J. Biomech. 2006;39:1595–1602
  40. Shieh AC, Athanasiou KA. Dynamic compression of single cells. Osteoarthr. Cartilage. 2006;15(3):328–334
  41. Smith B, Tolloczko B, Martin J, Grutter P. Probing the viscoelastic behavior of cultured airway smooth muscle cells with atomic force microscopy: stiffening induced by contractile agonist. Biophys. J. 2005;88:2994–3007
  42. Soltz MA, Ateshian GA. Interstitial fluid pressurization during confined compression cyclical loading of articular cartilage. Ann. Biomed. Eng. 2000;28:150–159
  43. Trickey WR, Vail TP, Guilak F. The role of the cytoskeleton in the viscoelastic properties of human articular chondrocytes. J. Orthop. Res. 2004;22:131–139

PII: S0021-9290(09)00574-0

doi: 10.1016/j.jbiomech.2009.09.053

Journal of Biomechanics
Volume 43, Issue 3 , Pages 469-476 , 10 February 2010

Article Tools

* Image Usage & Resolution