Nanomechanical properties of individual chondrocytes and their developing growth factor-stimulated pericellular matrix

Journal of Biomechanics

Volumn 40, Issue 5, 2007, Pages 1011-1023

  Ng, Laurel ^a   Hung, Han Hwa ^b   Sprunt, Alexander ^b   Chubinskaya, Susan ^c   Ortiz, Christine ^b   Grodzinsky, Alan ^a,b,d  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c RUSH UNIVERSITY MEDICAL CENTER   (United States)

^d USA   (United States)

Author keywords

Cartilage; Chondrocytes; Growth factors; Nanoindentation; Nanomechanics; Pericellular matrix

Indexed keywords

CHONDROCYTES; GROWTH FACTORS; PERICELLULAR MATRIX;

ATOMIC FORCE MICROSCOPY; BIOMECHANICS; CARTILAGE; GELS; GROWTH KINETICS; NANOINDENTATION; NANOMECHANICS;

ANIMAL CELL CULTURE;

AGGRECAN; ALGINIC ACID; COLLAGEN; GROWTH FACTOR; INSULIN GROWTH FACTOR 1; OSTEOGENIC PROTEIN 1; SILICON; SOMATOMEDIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; BIOCHIP; BIOMECHANICS; CARTILAGE CELL; CELL CULTURE; CELL ISOLATION; CELL STIMULATION; CELL VIABILITY; EVOLUTION; EXTRACELLULAR MATRIX; FETUS; FINITE ELEMENT ANALYSIS; FORCE; GEL; IMMOBILIZED CELL; INTROSPECTION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RIGIDITY; SERUM; TIME; TISSUE ENGINEERING;

ANIMALS; BIOMECHANICS; CATTLE; CELLS, CULTURED; CHONDROCYTES; EXTRACELLULAR MATRIX; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROSCOPY, ATOMIC FORCE; NANOSTRUCTURES;

EID: 33847401967     PISSN: 00219290     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2006.04.004     Document Type: Article

References (69)

1. A-Hassan E., Heinz W.F., Antonik M.D., D'Costa N.P., Nageswaran S., Schoenenberger C.-A., and Hoh J.H. Relative microelastic mapping of living cells by atomic force microscopy. Biophysical Journal 74 (1998) 1564-1578
2. Alcaraz J., Buscemi L., Grabulosa M., Trepat X., Fabry B., Farre R., and Navajas D. Microrheology of human lung epithelial cells measured by atomic force microscopy. Biophysical Journal 84 (2003) 2071-2079
3. Alexopoulos L.G., Haider M.A., Vail T.P., and Guilak F. Alterations in the mechanical properties of the human chondrocyte pericellular matrix with osteoarthritis. Journal of Biomechanical Engineering 125 (2003) 323-333
4. Allen D.M., and Mao J.J. Heterogeneous nanostructural and nanoelastic properties of pericellular and interterritorial matrices of chondrocytes by atomic force microscopy. Journal of Structural Biology 145 (2004) 196-204
5. Benya P.D., and Padilla S.R. Dihydrocytochalasin B enhances transforming growth factor-beta-induced reexpression of the differentiated chondrocyte phenotype without stimulaiton of collagen synthesis. Experimental Cell Research 204 (1993) 268-277
6. Buschmann M., Gluzband Y.A., Grodzinsky A.J., and Hunziker E.B. Mechanical compression modulates matrix biosynthesis in chondrocyte/agarose culture. Journal of Cell Science 108 (1995) 1497-1508
7. Chang J., and Poole C.A. Confocal analysis of the molecular heterogeneity in the pericellular microenvironment produced by adult canine chondrocytes cultured in agarose gel. Histochemistry Journal 29 (1997) 515-528
8. Charras G.T., and Horton M.A. Single cell mechanotransduction and its modulation analyzed by atomic force microscope indentation. Biophysical Journal 82 (2002) 2970-2981
9. Charras G.T., Yarrow J.C., Horton M.A., Mahadevan L., and Mitchison T.J. Non-equilibration of hydrostatic pressure in blebbing cells. Nature 435 (2005) 365-369
10. Chasiotis I., Fillmore H.L., and Gillies G.T. Atomic force microscopy measurement of cytostructural elements involved in the nanodynamics of tumour cell invasion. Nanotechnology 14 (2003) 557-561
11. Cheng L., Xia X., Scriven L.E., and Gerberich W.W. Spherical-tip indentation of viscoelastic material. Mechanics of Materials 37 (2005) 213-226
12. Collinsworth A.M., Zhang S., Kraus W.E., and Truskey G.A. Apparent elastic modulus and hysteresis of skeletal muscle cells throughout differentiation. American Journal of Physiology: Cellular Physics 283 (2002) 1219-1227
13. Dimicco, M.A., Kisiday, J.D., Gong, H., Grodzinsky, A.J., 2005. Fibrillar structure of type VI collagen-rich pericellular matrix assembled by agarose-embedded chondrocytes. Transactions of the Orthopaedic Research Society 30, 258.
14. Eyre, D., 2005. Personal communication.
15. Eyre D.R., Apon S., Wu J.-J., Ericsson L.H., and Walsh K.A. Collagen type IX: evidence for covalent linkages to type II collagen in cartilage. Federation of European Biochemical Societies (FEBS) Letters 220 (1987) 337-341
16. Farndale R.W., Buttle D.J., and Barrett A.J. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochimica et Biophysica Acta 883 (1986) 173-177
17. Fitzgerald J.B., Jin M., Dean D., Wood D.J., Zheng M.H., and Grodzinsky A.J. Mechanical compression of cartilage explants induces multiple time-dependent gene expression patterns and involves intracellular calcium and cyclic AMP. Journal of Biological Chemistry 279 (2004) 19502-19511
18. Flechtenmacher J., Huch K., Thonar E.J.-M.A., Mollenhauer J.A., Davies S.R., Schmid T.M., Puhl W., Sampath T.K., Aydelotte M.B., and Kuettner K.E. Recombinant human osteogenic protein 1 is a potent stimulator of the synthesis of cartilage proteoglycans and collagens by human articular chondrocytes. Arthritis and Rheumatism 39 (1996) 1896-1904
19. Freeman P.M., Natarajan R.N., Kimura J.H., and Andriacchi T.P. Chondrocyte cells respond mechanically to compressive loads. Journal of Orthopaedic Research 12 (1994) 311-320
20. Graff R.D., Kelley S.S., and Lee G.M. Role of pericellular matrix in development of a mechanically functional neocartilage. Biotechnology and Bioengineering 82 (2003) 457-464
21. Guilak F. The deformation behavior and viscoelastic properties of chondrocytes in articular cartilage. Biorheology 37 (2000) 27-44
22. Guilak F., Jones W.R., Ting-Beall H.P., and Lee G.M. The deformation behavior and mechanical properties of chondrocytes in articular cartilage. Osteoarthritis and Cartilage 7 (1999) 59-70
23. Guilak F., Meyer B.C., Ratcliffe A., and Mow V.C. The effects of matrix compression on proteoglycan metabolism in articular cartilage explants. Osteoarthritis and Cartilage 2 (1994) 91-101
24. Hategan A., Law R., Kahn S., and Discher D.E. Adhesively tensed cell membranes: lysis kinetics and atomic force microscopy probing. Biophysical Journal 85 (2003) 2746-2759
25. Hauselmann H.J., Aydelotte M.B., Schumacher B.L., Kuettner K.E., Gitelis S.H., and Thonar E.J.-M.A. Synthesis and turnover of proteglycans by human and bovine adult articular chondrocytes cultured in alginate beads. Matrix 12 (1992) 116-129
26. Hodge A.J. Structure at the electron microscope level. In: Ramachandran G.N. (Ed). Treatise on Collagen. Chemistry of Collagen (1967), Academic Press, London 185-205
27. Hunziker E.B., Herrmann W., and Schenk R.K. Improved cartilage fixation by ruthenium hexammine trichloride (RHT). A prerequisite for morphometry in growth cartilage. Journal of Ultrastructure Research 81 (1982) 1-12
28. Hutter J.L., and Bechhoefer J. Calibration of atomic-force microscope tips. Review of Scientific Instruments 64 (1993) 1868-1873
29. Johnson K.L., and Greenwood J.A. An adhesion map for the contact of elastic spheres. Journal of Colloid and Interface Science 192 (1997) 326-333
30. Jones W.R., Ting-Beall H.P., Lee G.M., Kelley S.S., Hochmuth R.M., and Guilak F. Alterations in the Young's modulus and volumetric properties of chondrocytes isolated from normal and osteoarthritic human cartilage. Journal of Biomechanics 32 (1999) 119-127
31. Jurvelin J.S., Muller D.J., Wong M., Studer D., Engel A., and Hunziker E.B. Surface and subsurface morphology of bovine humeral articular cartilage as assessed by atomic force and transmission electron microscopy. Journal of Structural Biology 117 (1996) 45-54
32. Kim Y.-J., Sah R.L.Y., Grodzinsky A.J., Plaas A.H.K., and Sandy J.D. Mechanical regulation of cartilage biosynthetic behavior: physical stimuli. Archives of Biochemistry and Biophysics 311 (1994) 1-12
33. Knight M.M., Ross J.M., Sherwin A.F., Lee D.A., Bader D.L., and Poole C.A. Chondrocyte deformation within mechanically and enzymatically extracted chondrons compressed in agarose. Biochimica et Biophysica Acta 1526 (2001) 141-146
34. Koay E.J., Shieh A.C., and Athanasiou K.A. Creep indentation of single cells. Journal of Biomechanical Engineering 125 (2003) 334-341
35. Kovacs G.T.A., Maluf N.I., and Petersen K.E. Bulk micromachining of silicon. Proceedings of the IEEE 86 (1998) 1536-1551
36. Lee G.M., and Loeser R.F. Interactions of the chondrocyte with its pericellular matrix. Cells and Materials 8 (1998) 135-149
37. Lehenkari P.P., Charras G.T., Nesbitt S.A., and Horton M.A. New technologies in scanning probe microscopy for studying molecular interactions in cells. Expert Reviews in Molecular Medicine (2000) 1-19
38. Lehenkari P.P., Charras G.T., Nykanen A., and Horton M.A. Adapting atomic force microscopy for cell biology. Ultramicroscopy 82 (2000) 289-295
39. Leipzig N.D., and Athanasiou K.A. Unconfined creep compression of chondrocytes. Journal of Biomechanics 38 (2005) 77-85
40. Lodish H., Berk A., Zipursky S.L., Matsudaira P., Baltimore D., and Darnell J. Molecular Cell Biology (2000), W.H. Freeman and Company, New York (pp. 981-985)
41. Loeser R.F., Pacione C.A., and 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 and Rheumatism 48 (2003) 2188-2196
42. Luna E.G. Manual of Histological Staining Methods (1968), McGraw-Hill Publication, New York (p. 94)
43. Mahaffy R.E., Park S., Gerde E., Käs J., and Shih C.K. Quantitative analysis of the viscoelastic properties of thin regions of fibroblasts using atomic force microscopy. Biophysical Journal 86 (2004) 1777-1793
44. Masuda K., Sah R.L., Hejna M.J., and Thonar E.J.-M.A. A novel two-step method for the formation of tissue-engineered cartilage by mature bovine chondrocytes: the alginate recovered chondrocyte (ARC) method. Journal of Orthopaedic Research 21 (2003) 139-148
45. McQuillan D.J., Handley C.J., Campbell M.A., Bolis S., Milway V.E., and Herington A.C. Stimulation of proteoglycan biosynthesis by serum and insulin-like growth factor-I in cultured bovine articular cartilage. Biochemistry Journal 240 (1986) 423-430
46. Nishida Y., Knudson C.B., Kuettner K.E., and Knudson W. Osteogenic protein-1 promotes the synthesis and retention of extracellular matrix within bovine articular cartilage and chondrocyte cultures. Osteoarthritis and Cartilage 8 (2000) 127-136
47. Ortolani F., Giordano M., and Marchini M. A model for type II collagen fibrils: distinctive D-band patterns in native and reconstituted fibrils compared with sequence data for helix and telopeptide domains. Biopolymers 54 (2000) 448-463
48. Oyen M.L., and Cook R.F. Load-displacement behavior during sharp indentation of viscous-elastic-plastic materials. Journal of Materials Research 18 (2003) 139-150
49. Petersen K.E. Silicon as a mechanical material. Proceedings of the IEEE 70 (1982) 420-457
50. Petit B., Masuda K., D'Souza A.L., Otten L., Pietryla D., Hartmann D.J., Morris N.P., Uebelhart D., Schmid T.M., and Thonar E.J.-M.A. Characterization of crosslinked collagens synthesized by mature articular chondrocytes cultured in alginate beads: comparison of two distinct matrix compartments. Experimental Cell Research 225 (1996) 151-161
51. Poole C.A. Articular cartilage chondrons: form, function and failure. Journal of Anatomy 191 (1997) 1-13
52. Poole C.A., Ayad S., and Gilbert R.T. Chondrons from articular cartilage. V. Immunohistochemical evaluation of type VI collagen organisation in isolated chondrons by light, confocal and electron microscopy. Journal of Cell Science 103 (1992) 1101-1110
53. Poole C.A., Ayad S., and Schofield J.R. Chondrons from articular cartilage: (I). Immunolocalization of type VI collagen in the pericellular capsule of isolated canine tibial chondrons. Journal of Cell Science 90 (1988) 635-643
54. Poole C.A., Flint M.H., and Beaumont B.W. Chondrons extracted from canine tibial cartilage: preliminary report on their isolation and structure. Journal of Orthopaedic Research 6 (1988) 408-419
55. Radmacher M. Measuring the elastic properties of biological samples with the AFM. IEEE Engineering in Medicine and Biology Magazine 16 (1997) 47-57
56. Ragan P.M., Chin V.I., Hung H.H., Masuda K., Thonar E.J.-M.A., Arner E.C., Grodzinsky A.J., and Sandy J.D. Chondrocyte extracellular matrix synthesis and turnover are influenced by static compression in a new alginate disk culture system. Archives of Biochemistry and Biophysics 383 (2000) 256-264
57. Rico, F., Roca-Cusachs, P., Gavara, N., Farre, R., Rotger, M., Navajas, D., 2005. Probing mechanical properties of living cells by atomic force microscopy with blunted pyramidal cantilever tips. Physical Review Letters E 72, Art. No. 021914.
58. Rotsch C., and Radmacher M. Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: An atomic force microscopy study. Biophysical Journal 78 (2000) 520-535
59. Shao Z., Mou J., Czajkowsky D.M., Yang J., and Yuan J.Y. Biological atomic force microscopy: what is achieved & what is needed. Advances in Physics 45 (1996) 1-86
60. Shieh, A.C., Athanasiou, K.A., 2005. Biomechanics of single zonal chondrocytes. Journal of Biomechanics, in press, doi:10.1016/j.biomech.2005.05.002.
61. Smith B.A., Tolloczko B., Martin J.G., and Grütter P. Probing the viscoelastic behavior of cultured airway smooth muscle cells with atomic force microscopy: stiffening induced by contractile agonist. Biophysical Journal 88 (2005) 2994-3007
62. Stockwell R.A., and Meachim G. The chondrocytes. In: Freeman M.A.R. (Ed). Adult Articular Cartilage (1979), Pitman Medical Publishing Co Ltd, Kent 69-144
63. Stolz M., Raiteri R., Daniels A.U., Vanlandingham M.R., Baschong W., and Aebi U. Dynamic elastic modulus of porcine articular cartilage determined at two different levels of tissue organization by indentation-type atomic force microscopy. Biophysical Journal 86 (2004) 3269-3283
64. Tsui T.Y., and Pharr G.M. Substrate effects on nanoindentation mechanical property measurement of soft films on hard substrates. Journal of Material Research 14 (1999) 292-301
65. Valhmu W.B., Stazzone E.J., Bachrach N.M., Saed-Nejad F., Fischer S.G., Mow V.C., and Ratcliffe A. Load-controlled compression of articular cartilage induces a transient stimulation of aggrecan gene expression. Archives of Biochemistry and Biophysics 353 (1998) 29-36
66. van Osch G.J., van den Berg W.B., Hunziker E.B., and Hauselmann H.J. Differential effects of IGF-1 and TGF beta-2 on the assembly of proteoglycans in pericellular and territorial matrix by cultured bovine articular chondrocytes. Osteoarthritis and Cartilage 6 (1998) 187-195
67. Vanlandingham M.R., Chang N.K., Drzal P.L., White C.C., and Chang S.-H. Viscoelastic characterization of polymers using instrumented indentation. I. Quasi-static testing. Journal of Polymer Science Part B-Polymer Physics 43 (2005) 1794-1811
68. White C.C., Vanlandingham M.R., Drzal P.L., Chang N.-K., and Chang S.-H. Viscoelastic characterization of polymers using instrumented indentation. II. Dynamic testing. Journal of Polymer Science Part B-Polymer Physics 43 (2005) 1812-1824
69. Woessner Jr. J.F. The determination of hydroxyproline in tissue and protein samples containing small amounts of this imino acid. Archives of Biochemistry and Biophysics 93 (1961) 440-447