Biomechanical properties of single chondrocytes and chondrons determined by micromanipulation and finite-element modelling

Journal of the Royal Society Interface

Volumn 7, Issue 53, 2010, Pages 1723-1733

  Nguyen, Bac V ^a   Wang, Qi Guang ^b   Kuiper, Nicola J ^b   El Haj, Alicia J ^b   Thomas, Colin R ^a   Zhang, Zhibing ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b KEELE UNIVERSITY   (United Kingdom)

Author keywords

Chondrocyte; Chondron; Finite element modelling; Micromanipulation; Nonlinear elasticity; Viscoelasticity

Indexed keywords

BIOMECHANICS; BODY FLUIDS; CARTILAGE; COMPUTER SIMULATION; DEFORMATION; ELASTIC MODULI; ELASTICITY; FINITE ELEMENT METHOD; MICROMANIPULATORS; MODELS; STRAIN; VISCOELASTICITY; VISCOSITY;

CHONDROCYTES; CHONDRON; FINITE ELEMENT MODELLING; MICRO MANIPULATION; NONLINEAR ELASTICITY;

MECHANICAL PROPERTIES;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; BIOMECHANICS; CARTILAGE CELL; CELL NUCLEUS; COW; CYTOSKELETON; FINITE ELEMENT ANALYSIS; FORCE; MICROMANIPULATION; NONHUMAN; VISCOELASTICITY; YOUNG MODULUS;

BOVINAE;

EID: 78649891998     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2010.0207     Document Type: Article

References (54)

1. ABAQUS 2005 Analysis user's manual, v. 6.5. Pawtucket, RI: Hibbit, Karlsson and Sorensen Inc.
2. Alexopoulos, L. G., Haider, M. A., Vail, T. P. & Guilak, F. 2003 Alterations in the mechanical properties of the human chondrocyte pericellular matrix with osteoarthritis. J. Biomech. Eng. (Trans. ASME) 125, 323-333. (doi:10.1115/1.1579047)
3. Alexopoulos, L. G., Setton, L. A. & Guilak, F. 2005 The biomechanical role of the chondrocyte pericellular matrix in articular cartilage. Acta Biomater. 1, 317-325. (doi:10.1016/j.actbio.2005.02.001) (Pubitemid 43348791)
4. Allen, D. M. & Mao, J. J. 2004 Heterogeneous nanostructural and nanoelastic properties of pericellular and interterritorial matrices of chondrocytes by atomic force microscopy. J. Struct. Biol. 145, 196-204. (doi:10.1016/j.jsb.2003.10.003)
5. Andrei, D. C., Briscoe, B. J., Luckham, P. F. & Williams, D. R. 1996 The deformation of microscopic gel particles. J. Chim. Phys. Phys. Chim. Biol. 93, 960-976.
6. Athanasiou, K. A., Thoma, B. S., Lanctot, D. R., Shin, D., Agrawal, C. M. & LeBaron, R. G. 1999 Development of the cytodetachment technique to quantify mechanical adhesiveness of the single cell. Biomaterials 20, 2405-2415. (doi:10.1016/S0142-9612(99)00168-4)
7. Buckwalter, J. & Mankin, H. 1998 Articular cartilage: tissue design and chondrocyte-matrix interactions. Instr. Course Lect. 47, 477-486.
8. Budinski, K. G. 1979 Engineering materials: properties and selection. Reston, VA: Reston Publishing Company, Inc.
9. Caille, N., Thoumine, O., Tardy, Y. & Meister, J. 2002 Contribution of the nucleus to the mechanical properties of endothelial cells. J. Biomech. 35, 177-187. (doi:10.1016/S0021-9290(01)00201-9)
10. Darling, E. M., Zauscher, S. & Guilak, F. 2006 Viscoelastic properties of zonal articular chondrocytes measured by atomic force microscopy. Osteoarthritic Cartilage 14, 571-579. (doi:10.1016/j.joca.2005.12.003)
11. Dong, C., Skalak, R. & Sung, L. P. 1991 Cytoplasmic rheology of passive neutrophils. Biorheology 28, 557-567.
12. Gilbert, N. 1981 Statistics, pp. 328-340, 2nd edn. Japan: Saunders College Publishing.
13. Guilak, F. 1995 Compression-induced changes in the shape and volume of the chondrocyte nucleus. J. Biomech. 28, 1529-1541. (doi:10.1016/0021-9290(95) 00100-X)
14. Guilak, F. & Mow, V. C. 2000 The mechanical environment of the chondrocyte: a biphasic finite element model of cell-matrix interactions in articular cartilage. J. Biomech. 33, 1663-1673. (doi:10.1016/S0021-9290(00) 00105-6)
15. Guilak, F., Ratcliffe, A. & Mow, V. C. 1997 Physical regulation of cartilage metabolism. In Basic orthopedic biomechanics (eds W. C. Hayes & V. C. Mow), pp. 179-207. Philadelphia, PA: Lipincott-Ravenwood.
16. Guilak, F., Jones, W. R., Ting-Beall, H. P. & Lee, G. M. 1999 The deformation behavior and mechanical properties of chondrocytes in articular cartilage. Osteoarthritis Cartilage 7, 59-70. (doi:10.1053/joca.1998.0162)
17. Guilak, F., Tedrowa, J. R. & Burgkartb, R. 2000 Viscoelastic properties of the cell nucleus. Biochem. Biophys. Res. Commun. 269, 781-786. (doi:10.1006/bbrc.2000.2360)
18. Guilak, F., Erickson, G. R. & Ting-Beall, H. P. 2002 The effects of osmotic stress on the viscoelastic and physical properties of articular chondrocytes. Biophys. J. 82, 720-727. (doi:10.1016/S0006-3495(02)75434-9)
19. Guilak, F., Alexopoulos, L. G., Haider, M. A., Ting-Beall, H. P. & Setton, L. A. 2005 Zonal uniformity in mechanical properties of the chondrocyte pericellular matrix: micropipette aspiration of canine chondrons isolated by cartilage homogenization. Ann. Biomed. Eng. 33, 1312-1318. (doi:10.1007/s10439- 005-4479-7)
20. Knight, M. M., van de Breevaart Bravenboer, J., Lee, D. A., van Osh, G. J. V. M., Weinans, H. & Bader, D. L. 2002 Cell and nucleus deformation in compressed chondrocyte-alginate constructs: temporal changes and calculation of cell modulus. Biochim. Biophys. Acta 1570, 1-8.
21. Koay, E. J., Shieh, A. C. & Athanasiou, K. A. 2003 Creep indentation of single cells. J. Biomech. Eng. 125, 334-341. (doi:10.1115/1.1572517)
22. Koay, E. J., Ofek, G. & Athanasiou, K. A. 2008 Effects of TGF- β1 and IGF-I on the compressibility, biomechanics, and strain-dependent recovery behavior of single chondrocytes. J. Biomech. 41, 1044-1052. (doi:10.1016/j.jbiomech.2007.12.006)
23. Kuettner, K. E., Pauli, B. U., Gallm, G., Memoli, V. A. & Schenk, R. K. 1982 Synthesis of cartilage matrix by mammalian chondrocytes in vitro. I. Isolation, culture characteristics, and morphology. J. Cell Biol. 93, 743-750. (doi:10.1083/jcb.93.3.743)
24. Lee, G. M., Poole, C. A., Kelley, S. S., Chang, J. & Caterson, B. 1997 Isolated chondrons: a viable alternative for studies of chondrocyte metabolism in vitro. Osteoarthritis Cartilage 5, 261-274. (doi:10.1016/S1063- 4584(97)80022-2) (Pubitemid 27315905)
25. Lee, D. A., Knight, M. M., Bolton, J. F., Idowu, B. D., Kayser, M. V. & Bader, M. 2000 Chondrocyte deformation within compressed agarose constructs at the cellular and subcellular levels. J. Biomech. 33, 81-95. (doi:10.1016/S0021-9290(99)00160-8)
26. Lee, B., Han, L., Frank, E. H., Chubinskaya, S., Ortiz, C. & Grodzinsky, A. J. 2010 Dynamic mechanical properties of the tissue-engineered matrix associated with individual chondrocytes. J. Biomech. 43, 469-476. (doi:10.1016/j.jbiomech.2009.09.053)
27. Leipzig, N. D. & Athanasiou, K. A. 2005 Unconfined creep compression of chondrocytes. J. Biomech. 38, 77-85.
28. Leipzig, N. D. & Athanasiou, K. A. 2008 Static compression of single chondrocytes catabolically modifies single-cell gene expression. Biophys. J. 94, 2412-2422. (doi:10.1529/biophysj.107.114207)
29. Mathur, A. B., Truskey, G. A. & Reichert, W. M. 2000 Atomic force and total internal reflection fluorescence microscopy for the study of force transmission in endothelial cells. Biophys. J. 78, 1725-1735. (doi:10.1016/S0006-3495(00)76724-5)
30. Ng, L., Hung, H.-H., Sprunt, A., Chubinskaya, S., Ortiz, C. & Grodzinsky, A. 2007 Nanomechanical properties of individual chondrocytes and their developing growth factor-stimulated pericellular matrix. J. Biomech. 40, 1011-1023. (doi:10.1016/j.jbiomech.2006.04.004)
31. Nguyen, V. B., Wang, C. X., Thomas, C. R. & Zhang, Z. 2009a Mechanical properties of single alginate microspheres determined by microcompression and finite element modelling. Chem. Eng. Sci. 64, 821-829. (doi:10.1016/j.ces.2008.10.050)
32. Nguyen, V. B., Wang, Q. G., Kuiper, N. J., El Haj, A. J., Thomas, C. R. & Zhang, Z. 2009b Strain-dependent viscoelastic behaviour and rupture force of single chondrocytes and chondrons under compression. Biotechnol. Lett. 31, 803-809. (doi:10.1007/s10529-009-9939-y)
33. Nussinovitch, A., Pleg, M. & Normand, M. D. 1989 A modified Maxwell and a nonexponential model for characterization of the stress relaxation of agar and alginate gels. J. Food Sci. 54, 1013-1016. (doi:10.1111/j.1365-2621.1989. tb07934.x)
34. Ofek, G. & Athanasiou, K. A. 2007 Micromechanical properties of chondrocytes and chondrons: relevance to articular cartilage tissue engineering. J. Mech. Mater. Struct. 2, 1059-1086. (doi:10.2140/jomms.2007.2.1059)
35. Ofek, G., Natoli, R. M. & Athanasiou, K. 2009a In situ mechanical properties of the chondrocyte cytoplasm and nucleus. J. Biomech. 42, 873-877. (doi:10.1016/j.jbiomech.2009.01.024)
36. Ofek, G., Wiltz, D. C. & Athanasiou, K. 2009b Contribution of the cytoskeleton to the compressive properties and recovery behavior of single cells. Biophys. J. 97, 1873-1882. (doi:10.1016/j.bpj.2009.07.050)
37. Peeters, E. A. G., Oomens, C. W. J., Bouten, C. V. C., Bader, D. L. & Baaijens, F. P. T. 2005 Mechanical and failure properties of single attached cells under compression. J. Biomech. 38, 1685-1693. (doi:10.1016/j.jbiomech. 2004.07.018)
38. Poole, C. A. 1997 Articular cartilage chondrons: form, function, and failure. J. Anat. 191, 1-13. (doi:10.1046/j.1469-7580.1997.19110001.x)
39. Poole, C. A., Flint, M. H. & Beaumont, B. W. 1988 Chondrons extracted from canine tibial cartilage: preliminary report on their isolation and structure. J. Orthop. Res. 6, 408-419. (doi:10.1002/jor.1100060312)
40. Rivlin, R. S. 1948 Large elastic deformations of isotropic materials. IV. Further development of the general theory. Phil. Trans. R. Soc. Lond. A 241, 379-397.
41. Shieh, A. C. & Athanasiou, K. A. 2006 Biomechanics of single zonal chondrocytes. J. Biomech. 39, 1595-1602. (doi:10.1016/j.jbiomech.2005.05.002)
42. Shieh, A. C., Koay, E. J. & Athanasiou, K. A. 2006 Straindependent recovery behavior of single chondrocytes. Biomech. Model Mechanobiol. 5, 172-179. (doi:10.1007/s10237-006-0028-z)
43. Spencer, A. J. M. 2009 Ronald Rivlin and invariant theory. Int. J. Eng. Sci. 47, 1066-1078. (doi:10.1016/j.ijengsci.2009.01.004)
44. Szirmai, J. A. 1974 The concept of the chondron as a biomechanical unit. In Biopolymer und Biomechanik von Bindegewebssystemen (ed. F. Hartmann), pp. 87-91. Berlin, Germany: Academic Press.
45. Thomas, C. R., Zhang, Z. & Cowen, C. 2000 Micromanipulation measurements of biological materials. Biotechnol. Lett. 22, 531-537. (doi:10.1023/A:1005644412588)
46. Trickey, W. R., Lee, G. M. & Guilak, F. 2000 Viscoelastic properties of chondrocytes from normal and osteoarthritic human cartilage. J. Orthop. Res. 18, 891-898. (doi:10.1002/jor.1100180607)
47. Trickey, W. R., Vail, T. P. & Guilak, F. 2004 The role of the cytoskeleton in the viscoelastic properties of human articular chondrocytes. J. Orthop. Res. 22, 131-139. (doi:10.1016/S0736-0266(03)0150-5)
48. Wang, N. & Ingber, D. E. 1994 Control of cytoskeletal mechanics by extracellular matrix, cell shape, and mechanical tension. Biophys. J. 66, 2181-2189. (doi:10.1016/S0006-3495(94)81014-8)
49. Wang, N., Butler, J. P. & Ingber, D. E. 1993 Mechanotransduction across the cell surface and through the cytoskeleton. Science 260, 1124-1127. (doi:10.1126/science.7684161)
50. Wang, Q. G., El Haj, A. J. & Kuiper, N. J. 2008 Glycosaminoglycans in the pericellular matrix of chondrons and chondrocytes. J. Anat. 213, 266-273. (doi:10.1111/j.1469-7580.2008.00942.x)
51. Wang, Q. G., Magnay, J. L., Nguyen, V. B., Thomas, C. R., Zhang, Z., El Haj, A. J. & Kuiper, N. J. 2009 Gene expression profiles of dynamically compressed single chondrocytes and chondrons. Biochem. Biophys. Res. Commun. 379, 738-742. (doi:10.1016/j.bbrc.2008.12.111)
52. Wang, Q. G., Nguyen, B., Thomas, C. R., Zhang, Z., El Haj, A. J. & Kuiper, N. J. 2010 Molecular profiling of single cells in response to mechanical force: comparison of chondrocytes, chondrons and encapsulated chondrocytes.Biomaterials 31, 1619-1625. (doi:10.1016/j.biomaterials.2009.11. 021)
53. Wikes, R. P. & Athanasiou, K. A. 1996 The intrinsic incompressibility of osteoblast-like cells. Tissue Eng. 2, 167-181.
54. Wong, M. & Carter, D. R. 2003 Articular cartilage functional histomorphology and mechanobiology: a research perspective. Bone 33, 1-13. (doi:10.1016/S8756-3282(03)00083-8)