Biomechanical properties and mechanobiology of the articular chondrocyte

American Journal of Physiology - Cell Physiology

Volumn 305, Issue 12, 2013, Pages

  Chen, Cheng ^a   Tambe, Dhananjay T ^b   Deng, Linhong ^c   Yang, Liu ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c CHANGZHOU UNIVERSITY   (China)

Author keywords

Articular cartilage; Chondrocyte; Joint loading; Mechanobiology; Osteoarthritis

Indexed keywords

ARTICULAR CARTILAGE; CARTILAGE CELL; CARTILAGE MATRIX; CELL NUCLEUS; DEGRADATION; HUMAN; INJURY; JOINT; JOINT DEGENERATION; MACROMOLECULE; OSTEOARTHRITIS; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SYNTHESIS;

ARTICULAR CARTILAGE; CHONDROCYTE; JOINT LOADING; MECHANOBIOLOGY; OSTEOARTHRITIS;

BIOMECHANICAL PHENOMENA; CARTILAGE, ARTICULAR; CHONDROCYTES; HUMANS; OSTEOARTHRITIS;

EID: 84890352903     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00242.2013     Document Type: Review

References (93)

1. Alexopoulos LG, Haider MA, Vail TP, Guilak F. Alterations in the mechanical properties of the human chondrocyte pericellular matrix with osteoarthritis. J Biomech Eng 125: 323-333, 2003.
2. Alexopoulos LG, Setton LA, Guilak F. The biomechanical role of the chondrocyte pericellular matrix in articular cartilage. Acta Biomater 1: 317-325, 2005.
3. 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 38: 509-517, 2005.
4. Allen DM, Mao JJ. Heterogeneous nanostructural and nanoelastic properties of pericellular and interterritorial matrices of chondrocytes by atomic force microscopy. J Struct Biol 145: 196-204, 2004.
5. Bader DL, Ohashi T, Knight MM, Lee DA, Sato M. Deformation properties of articular chondrocytes: a critique of three separate techniques. Biorheology 39: 69-78, 2002.
6. Buckwalter JA. The role of mechanical forces in the initiation and progression of osteoarthritis. HSS J 8: 37-38, 2012.
7. Buckwalter JA, Mankin HJ. Articular cartilage: degeneration and osteoarthritis, repair, regeneration, and transplantation. Instr Course Lect 47: 487-504, 1998.
8. Buckwalter JA, Mankin HJ. Articular cartilage: tissue design and chondrocyte-matrix interactions. Instr Course Lect 47: 477-486, 1998.
9. Buckwalter JA, Martin JA, Brown TD. Perspectives on chondrocyte mechanobiology and osteoarthritis. Biorheology 43: 603-609, 2006.
10. Buschmann MD, Hunziker EB, Kim YJ, Grodzinsky AJ. Altered aggrecan synthesis correlates with cell and nucleus structure in statically compressed cartilage. J Cell Sci 109: 499-508, 1996.
11. Chahine NO, Blanchette C, Thomas CB, Lu J, Haudenschild D, Loots GG. Effect of age and cytoskeletal elements on the indentation-dependent mechanical properties of chondrocytes. PLos One 8: e61651, 2013.
12. Clark AL, Votta BJ, Kumar S, Liedtke W, Guilak F. Chondroprotective role of the osmotically sensitive ion channel transient receptor potential vanilloid 4: age-and sex-dependent progression of osteoarthritis in Trpv4-deficient mice. Arthritis Rheum 62: 2973-2983, 2010.
13. Dahl KN, Kalinowski A. Nucleoskeleton mechanics at a glance. J Cell Sci 124: 675-678, 2011.
14. Darling EM, Pritchett PE, Evans BA, Superfine R, Zauscher S, Guilak F. Mechanical properties and gene expression of chondrocytes on micropatterned substrates following dedifferentiation in monolayer. Cell Mol Bioeng 2: 395-404, 2009.
15. Darling EM, Zauscher S, Guilak F. Viscoelastic properties of zonal articular chondrocytes measured by atomic force microscopy. Osteoarthritis Cartilage 14: 571-579, 2006.
16. Degala S, Williams R, Zipfel W, Bonassar LJ. Calcium signaling in response to fluid flow by chondrocytes in 3D alginate culture. J Orthop Res 30: 793-799, 2012.
17. Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science 310: 1139-1143, 2005.
18. Duan W, Wei L, Zhang J, Hao Y, Li C, Li H, Li Q, Zhang Q, Chen W, Wei X. Alteration of viscoelastic properties is associated with a change in cytoskeleton components of ageing chondrocytes from rabbit knee articular cartilage. Mol Cell Biomech 8: 253-274, 2011.
19. Egloff C, Hugle T, Valderrabano V. Biomechanics and pathomechanisms of osteoarthritis. Swiss Med Weekly 142: w13583, 2012.
20. Elder BD, Athanasiou KA. Hydrostatic pressure in articular cartilage tissue engineering: from chondrocytes to tissue regeneration. Tissue Eng 15: 43-53, 2009.
21. Enomoto-Iwamoto M, Iwamoto M, Nakashima K, Mukudai Y, Boettiger D, Pacifici M, Kurisu K, Suzuki F. Involvement of α5β1 integrin in matrix interactions and proliferation of chondrocytes. J Bone Miner Res 12: 1124-1132, 1997.
22. Felson DT. Osteoarthritis as a disease of mechanics. Osteoarthritis Cartilage 21: 10-15, 2013.
23. Felson DT, Lawrence RC, Hochberg MC, McAlindon T, Dieppe PA, Minor MA, Blair SN, Berman BM, Fries JF, Weinberger M, Lorig KR, Jacobs JJ, Goldberg V. Osteoarthritis: new insights. 2. Treatment approaches. Ann Intern Med 133: 726-737, 2000.
24. Fioravanti A, Collodel G, Petraglia A, Nerucci F, Moretti E, Galeazzi M. Effect of hydrostatic pressure of various magnitudes on osteoarthritic chondrocytes exposed to IL-1β. Indian J Med Res 132: 209-217, 2010.
25. Fitzgerald JB, Jin M, Chai DH, Siparsky P, Fanning P, Grodzinsky AJ. Shear-and compression-induced chondrocyte transcription requires MAPK activation in cartilage explants. J Biol Chem 283: 6735-6743, 2008.
26. Fitzgerald JB, Jin M, Dean D, Wood DJ, Zheng MH, Grodzinsky AJ. Mechanical compression of cartilage explants induces multiple timedependent gene expression patterns and involves intracellular calcium and cyclic AMP. J Biol Chem 279: 19502-19511, 2004.
27. Fletcher DA, Mullins RD. Cell mechanics and the cytoskeleton. Nature 463: 485-492, 2010.
28. Forsyth CB, Pulai J, Loeser RF. Fibronectin fragments and blocking antibodies to α2β1 and α5β1 integrins stimulate mitogen-activated protein kinase signaling and increase collagenase 3 (matrix metalloproteinase 13) production by human articular chondrocytes. Arthritis Rheum 46: 2368-2376, 2002.
29. Freeman PM, Natarajan RN, Kimura JH, Andriacchi TP. Chondrocyte cells respond mechanically to compressive loads. J Orthop Res 12: 311-320, 1994.
30. Griffin TM, Guilak F. The role of mechanical loading in the onset and progression of osteoarthritis. Exerc Sport Sci Rev 33: 195-200, 2005.
31. Grodzinsky AJ, Levenston ME, Jin M, Frank EH. Cartilage tissue remodeling in response to mechanical forces. Annu Rev Biomed Eng 2: 691-713, 2000.
32. Guilak F. Biomechanical factors in osteoarthritis. Best Pract Res Clin Rheumatol 25: 815-823, 2011.
33. Guilak F. Compression-induced changes in the shape and volume of the chondrocyte nucleus. J Biomech 28: 1529-1541, 1995.
34. Guilak F, Alexopoulos LG, Haider MA, Ting-Beall HP, Setton LA. 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, 2005.
35. 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. Ann NY Acad Sci 1068: 498-512, 2006.
36. Guilak F, Erickson GR, Ting-Beall HP. The effects of osmotic stress on the viscoelastic and physical properties of articular chondrocytes. Biophys J 82: 720-727, 2002.
37. Guilak F, Leddy HA, Liedtke W. Transient receptor potential vanilloid 4: the sixth sense of the musculoskeletal system? Ann NY Acad Sci 1192: 404-409, 2010.
38. Guilak F, Mow VC. The mechanical environment of the chondrocyte: a biphasic finite element model of cell-matrix interactions in articular cartilage. J Biomech 33: 1663-1673, 2000.
39. Guilak F, Tedrow JR, Burgkart R. Viscoelastic properties of the cell nucleus. Biochem Biophys Res Commun 269: 781-786, 2000.
40. Han SK, Madden R, Abusara Z, Herzog W. In situ chondrocyte viscoelasticity. J Biomech 45: 2450-2456, 2012.
41. Han SK, Wouters W, Clark A, Herzog W. Mechanically induced calcium signaling in chondrocytes in situ. J Orthop Res 30: 475-481, 2012.
42. Haudenschild DR, Chen J, Pang N, Steklov N, Grogan SP, Lotz MK, D'Lima DD. Vimentin contributes to changes in chondrocyte stiffness in osteoarthritis. J Orthop Res 29: 20-25, 2011.
43. Haudenschild DR, D'Lima DD, Lotz MK. Dynamic compression of chondrocytes induces a Rho kinase-dependent reorganization of the actin cytoskeleton. Biorheology 45: 219-228, 2008.
44. Herberhold C, Faber S, Stammberger T, Steinlechner M, Putz R, Englmeier KH, Reiser M, Eckstein F. In situ measurement of articular cartilage deformation in intact femoropatellar joints under static loading. J Biomech 32: 1287-1295, 1999.
45. Hsieh CH, Lin YH, Lin S, Tsai-Wu JJ, Herbert Wu CH, Jiang CC. Surface ultrastructure and mechanical property of human chondrocyte revealed by atomic force microscopy. Osteoarthritis Cartilage 16: 480-488, 2008.
46. Hung CT, Henshaw DR, Wang CC, Mauck RL, Raia F, Palmer G, Chao PH, Mow VC, Ratcliffe A, Valhmu WB. Mitogen-activated protein kinase signaling in bovine articular chondrocytes in response to fluid flow does not require calcium mobilization. J Biomech 33: 73-80, 2000.
47. Huselstein C, Netter P, de Isla N, Wang Y, Gillet P, Decot V, Muller S, Bensoussan D, Stoltz JF. Mechanobiology, chondrocyte and cartilage. Biomed Mater Eng 18: 213-220, 2008.
48. Ingber DE. Tensegrity: the architectural basis of cellular mechanotransduction. Annu Rev Physiol 59: 575-599, 1997.
49. Jeon JE, Schrobback K, Hutmacher DW, Klein TJ. Dynamic compression improves biosynthesis of human zonal chondrocytes from osteoarthritis patients. Osteoarthritis Cartilage 20: 906-915, 2012.
50. Knight MM, van de Breevaart Bravenboer J, Lee DA, van Osch GJ, Weinans H, Bader DL. Cell and nucleus deformation in compressed chondrocyte-alginate constructs: temporal changes and calculation of cell modulus. Biochim Biophys Acta 1570: 1-8, 2002.
51. Koay EJ, Shieh AC, Athanasiou KA. Creep indentation of single cells. J Biomech Eng 125: 334-341, 2003.
52. Korhonen RK, Han SK, Herzog W. Osmotic loading of in situ chondrocytes in their native environment. Mol Cell Biomech 7: 125-134, 2010.
53. Lammerding J. Mechanics of the nucleus. Compr Physiol 1: 783-807, 2011.
54. Lammi MJ. Current perspectives on cartilage and chondrocyte mechanobiology. Biorheology 41: 593-596, 2004.
55. Lee GM, Poole CA, Kelley SS, Chang J, Caterson B. Isolated chondrons: a viable alternative for studies of chondrocyte metabolism in vitro. Osteoarthritis Cartilage 5: 261-274, 1997.
56. Leipzig ND, Athanasiou KA. Static compression of single chondrocytes catabolically modifies single-cell gene expression. Biophys J 94: 2412-2422, 2008.
57. Leipzig ND, Athanasiou KA. Unconfined creep compression of chondrocytes. J Biomech 38: 77-85, 2005.
58. 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 43: 2091-2099, 2000.
59. Millward-Sadler SJ, Wright MO, Lee H, Nishida K, Caldwell H, Nuki G, Salter DM. Integrin-regulated secretion of interleukin 4: a novel pathway of mechanotransduction in human articular chondrocytes. J Cell Biol 145: 183-189, 1999.
60. Mizuno S, Ogawa R. Using changes in hydrostatic and osmotic pressure to manipulate metabolic function in chondrocytes. Am J Physiol Cell Physiol 300: C1234-C1245, 2011.
61. Moo EK, Herzog W, Han SK, Abu Osman NA, Pingguan-Murphy B, Federico S. Mechanical behaviour of in-situ chondrocytes subjected to different loading rates: a finite element study. Biomech Modeling Mechanobiol 11: 983-993, 2012.
62. Morgenroth DC, Gellhorn AC, Suri P. Osteoarthritis in the disabled population: a mechanical perspective. PM R 4: S20-S27, 2012.
63. Muramatsu S, Wakabayashi M, Ohno T, Amano K, Ooishi R, Sugahara T, Shiojiri S, Tashiro K, Suzuki Y, Nishimura R, Kuhara S, Sugano S, Yoneda T, Matsuda A. Functional gene screening system identified TRPV4 as a regulator of chondrogenic differentiation. J Biol Chem 282: 32158-32167, 2007.
64. Ng L, Hung HH, Sprunt A, Chubinskaya S, Ortiz C, Grodzinsky A. Nanomechanical properties of individual chondrocytes and their developing growth factor-stimulated pericellular matrix. J Biomech 40: 1011-1023, 2007.
65. Nguyen BV, Wang Q, Kuiper NJ, El Haj AJ, Thomas CR, Zhang Z. Strain-dependent viscoelastic behaviour and rupture force of single chondrocytes and chondrons under compression. Biotechnol Lett 31: 803-809, 2009.
66. Nguyen BV, Wang QG, Kuiper NJ, El Haj AJ, Thomas CR, Zhang Z. Biomechanical properties of single chondrocytes and chondrons determined by micromanipulation and finite-element modelling. J R Soc Interface 7: 1723-1733, 2010.
67. Nilius B, Vriens J, Prenen J, Droogmans G, Voets T. TRPV4 calcium entry channel: a paradigm for gating diversity. Am J Physiol Cell Physiol 286: C195-C205, 2004.
68. Ofek G, Dowling EP, Raphael RM, McGarry JP, Athanasiou KA. Biomechanics of single chondrocytes under direct shear. Biomech Model Mechanobiol 9: 153-162, 2010.
69. Ofek G, Natoli RM, Athanasiou KA. In situ mechanical properties of the chondrocyte cytoplasm and nucleus. J Biomech 42: 873-877, 2009.
70. Phan MN, Leddy HA, Votta BJ, Kumar S, Levy DS, Lipshutz DB, Lee SH, Liedtke W, Guilak F. Functional characterization of TRPV4 as an osmotically sensitive ion channel in porcine articular chondrocytes. Arthritis Rheum 60: 3028-3037, 2009.
71. Poole CA. Articular cartilage chondrons: form, function and failure. J Anat 191: 1-13, 1997.
72. Poole CA, Flint MH, Beaumont BW. Chondrons extracted from canine tibial cartilage: preliminary report on their isolation and structure. J Orthop Res 6: 408-419, 1988.
73. Poole CA, Honda T, Skinner SJ, Schofield JR, Hyde KF, Shinkai H. Chondrons from articular cartilage. II. Analysis of the glycosaminoglycans in the cellular microenvironment of isolated canine chondrons. Connect Tissue Res 24: 319-330, 1990.
74. Pravincumar P, Bader DL, Knight MM. Viscoelastic cell mechanics and actin remodelling are dependent on the rate of applied pressure. PLos One 7: e43938, 2012.
75. Raizman I, De Croos JN, Pilliar R, Kandel RA. Calcium regulates cyclic compression-induced early changes in chondrocytes during in vitro cartilage tissue formation. Cell Calcium 48: 232-242, 2010.
76. Ruwhof C, van Wamel JT, Noordzij LA, Aydin S, Harper JC, van der Laarse A. Mechanical stress stimulates phospholipase C activity and intracellular calcium ion levels in neonatal rat cardiomyocytes. Cell Calcium 29: 73-83, 2001.
77. Salter DM, Millward-Sadler SJ, Nuki G, Wright MO. Integrin-interleukin-4 mechanotransduction pathways in human chondrocytes. Clin Orthop Relat Res S49-S60, 2001.
78. Shieh AC, Athanasiou KA. Biomechanics of single zonal chondrocytes. J Biomech 39: 1595-1602, 2006.
79. Shieh AC, Athanasiou KA. Dynamic compression of single cells. Osteoarthritis Cartilage 15: 328-334, 2007.
80. Shin D, Athanasiou K. Cytoindentation for obtaining cell biomechanical properties. J Orthop Res 17: 880-890, 1999.
81. Smith RL, Carter DR, Schurman DJ. Pressure and shear differentially alter human articular chondrocyte metabolism: a review. Clin Orthop Related Res S89-S95, 2004.
82. Stamenovic D, Mijailovich SM, Tolic-Norrelykke IM, Chen J, Wang N. Cell prestress. II. Contribution of microtubules. Am J Physiol Cell Physiol 282: C617-C624, 2002.
83. Steklov N, Srivastava A, Sung KL, Chen PC, Lotz MK, D'Lima DD. Aging-related differences in chondrocyte viscoelastic properties. Mol Cell Biomech 6: 113-119, 2009.
84. Tew SR, Vasieva O, Peffers MJ, Clegg PD. Post-transcriptional gene regulation following exposure of osteoarthritic human articular chondrocytes to hyperosmotic conditions. Osteoarthritis Cartilage 19: 1036-1046, 2011.
85. Toyoda T, Seedhom BB, Kirkham J, Bonass WA. Upregulation of aggrecan and type II collagen mRNA expression in bovine chondrocytes by the application of hydrostatic pressure. Biorheology 40: 79-85, 2003.
86. Trickey WR, Lee GM, Guilak F. Viscoelastic properties of chondrocytes from normal and osteoarthritic human cartilage. J Orthop Res 18: 891-898, 2000.
87. Trickey WR, Vail TP, Guilak F. The role of the cytoskeleton in the viscoelastic properties of human articular chondrocytes. J Orthop Res 22: 131-139, 2004.
88. Urban JP. The chondrocyte: a cell under pressure. Br J Rheumatol 33: 901-908, 1994.
89. Waldman SD, Spiteri CG, Grynpas MD, Pilliar RM, Hong J, Kandel RA. Effect of biomechanical conditioning on cartilaginous tissue formation in vitro. J Bone Joint Surg Am 85A Suppl 2: 101-105, 2003.
90. Wang N, Tolic-Norrelykke IM, Chen J, Mijailovich SM, Butler JP, Fredberg JJ, Stamenovic D. Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am J Physiol Cell Physiol 282: C606-C616, 2002.
91. Wang P, Zhu F, Tong Z, Konstantopoulos K. Response of chondrocytes to shear stress: antagonistic effects of the binding partners Toll-like receptor 4 and caveolin-1. FASEB J 25: 3401-3415, 2011.
92. Yellowley CE, Hancox JC, Donahue HJ. Effects of cell swelling on intracellular calcium and membrane currents in bovine articular chondrocytes. J Cell Biochem 86: 290-301, 2002.
93. Zwerger M, Ho CY, Lammerding J. Nuclear mechanics in disease. Annu Rev Biomed Eng 13: 397-428, 2011.