Chondrocyte deformation under extreme tissue strain in two regions of the rabbit knee joint

Journal of Biomechanics

Volumn 46, Issue 3, 2013, Pages 554-560

  Madden, Ryan ^a   Han, Sang Kuy ^b   Herzog, Walter ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

Articular cartilage; Cell mechanics; Chondrocyte; Extracellular matrix; Large deformation

Indexed keywords

ARTICULAR CARTILAGES; CELL MECHANICS; CHONDROCYTES; EXTRACELLULAR MATRICES; LARGE DEFORMATIONS;

BODY FLUIDS; CARTILAGE; CELLS; CYTOLOGY; DEFORMATION; JOINTS (ANATOMY); TISSUE;

STRAIN;

ANIMAL TISSUE; ARTICLE; BONE STRESS; CARTILAGE CELL; CELL VOLUME; COMPRESSION; EXPLANT; EXTRACELLULAR MATRIX; FEMUR CONDYLE; KNEE; NONHUMAN; PATELLA; PRIORITY JOURNAL; RABBIT;

ANIMALS; CHONDROCYTES; KNEE JOINT; RABBITS; STRESS, PHYSIOLOGICAL; WEIGHT-BEARING;

EID: 84872602874     PISSN: 00219290     EISSN: 18732380     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2012.09.021     Document Type: Article

References (57)

1. Abusara Z., Seerattan R., Leumann A., Thompson R., Herzog W. A novel method for determining articular cartilage chondrocyte mechanics in vivo. Journal of Biomechanics 2011, 44:930-934.
2. Alexopoulos L.G., Setton L.A., Guilak F. The biomechanical role of the chondrocyte pericellular matrix in articular cartilage. Acta Biomaterialia 2005, 1:317-325.
3. Armstrong C.G., Bahrani A.S., Gardner D.L. Changes in the deformational behavior of human hip cartilage with age. Journal of Biomechanical Engineering 1980, 102:214-220.
4. Arokoski J.P.A., Hyttinen M.M., Helminen H.J., Jurvelin J.S. Biomechanical and structural characteristics of canine femoral and tibial cartilage. Journal of Biomedical Material Research 1999, 48:379-392.
5. Athanasiou K.A., Rosenwasser M.P., Buckwalter J.A., Malinin T.I., Mow V.C. Interspecies comparisons of in situ intrinsic mechanical properties of distal femoral cartilage. Journal of Orthopaedic Research 1991, 9:330-340.
6. Baer A.E., Laursen T.A., Guilak F., Setton L.A. The micromechanical environment of intervertebral disc cells determined by a finite deformation, anisotropic, and biphasic finite element model. Journal of Biomechanical Engineering 2003, 125:1-11.
7. Benjamin M., Archer C.W., Ralphs J.R. Cytoskeleton of cartilage cells. Microscopy Research and Technique 1994, 28:372-377.
8. Bevill S.L., Briant P.L., Levenston M.E., Andriacchi T.P Central and peripheral region tibial plateau chondrocytes respond differently to in vitro dynamic compression. Osteoarthritis and Cartilage 2009, 17:980-987.
9. Bonassar L.J., Frank E.H., Murray J.C., Paguio C.G., Moore V.L., Lark M.W., Sandy J.D., Wu J.-J., Eyre D.R., Grodzinsky A.J. Changes in cartilage composition and physical properties due to stromelysin degredation. Arthritis & Rheumatism 1995, 38:173-183.
10. Bush P.G., Hall A.C. The osmotic sensitivity of isolated and in situ bovine articular chondrocytes. Journal of Orthopaedic Research 2001, 19:768-778.
11. Choi J.B., Youn I., Cao L., Leddy H.A., Gilchrist C.L., Setton L.A., 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. Journal of Biomechanics 2007, 40:2596-2603.
12. Clark A.L., Barclay L.D., Matyas J.R., Herzog W. In situ chondrocyte deformation with physiological compression of the feline patellofemoral joint. Journal of Biomechanics 2003, 36:553-568.
13. Darling E.M., Wilusz R.E., Bolognesi M.P., Zauscher S., Guilak F. Spatial mapping of the biomechanical properties of the pericellular matrix of articular cartilage measured in situ via atomic force microscopy. Biophysical Journal 2010, 98:2848-2856.
14. Durrant L.A., Archer C.W., Benjamin M., Ralphs J.R. Organisation of the chondrocyte cytoskeleton and its response to changing mechanical conditions in organ culture. Journal of Anatomy 1999, 194:343-353.
15. Eggli P.S., Hunziker E.B., Schenk R.K. Quantitation of structural features characterizing weight- and less-weight-bearing regions in articular cartilage: a stereological analysis of medial femoral condyles in young adult rabbits. Anatomical Record 1988, 222:217-227.
16. Feddema, J.T., Little, C.Q., 1997. Rapid World Modeling: Fitting Range Data to Geometric Primitives. In: Proceedings of the IEEE International Conference on Robotics and Automation, Albuquerque, New Mexico, April 1997 4, 2807-2812.
17. Flachsmann R., Broom N.D., Hardy A.E. Deformation and rupture of the articular surface under dynamic and static compression. Journal of Orthopaedic Research 2001, 19:1131-1139.
18. Freeman P.M., Natarajan R.N., Kimura J.H., Andriacchi T.P. Chondrocyte cells respond mechanically to compressive loads. Journal of Orthopaedic Research 1994, 12:311-320.
19. Froimson M.I., Ratcliffe A., Gardner T.R., Mow V.C. Differences in patellofemoral joint cartilage material properties and their significance to the etiology of cartilage surface fibrillation. Osteoarthritis and Cartilage 1997, 5:377-386.
20. Guilak F. Volume and surface area measurement of viable chondrocytes in situ using geometric modelling of serial confocal sections. Journal of Microscopy 1994, 173:245-256.
21. Guilak F., Ratcliffe A., Lane N., Rosenwasser M.P., Mow V.C. Mechanical and biochemical changes in the superficial zone of articular cartilage in canine experimental osteoarthritis. Journal of Orthopaedic Research 1994, 12:474-484.
22. Guilak F. Compression-induced changes in the shape and volume of the chondrocyte nucleus. Journal of Biomechanics 1995, 28:1529-1541.
23. Guilak F., Ratcliffe A., Mow V.C. Chondrocyte deformation and local tissue strain in articular cartilage: a confocal microscopy study. Journal of Orthopaedic Research 1995, 13:410-421.
24. Guilak F., Ting-Beall H.P., Baer A.E., Trickey W.R., Erickson G.R., Setton L.A. Viscoelastic properties of intervertebral disc cells-identification of two biomechanically distinct cell populations. SPINE 1999, 24:2475-2483.
25. Guilak F., Alexopoulos L.G., Haider M.A., Ting-Beall H.P., Setton L.A. Zonal uniformity in mechanical properties of the chondrocyte pericellular matrix: micropipette aspiration of canine chondrons isolated by cartilage homogenization. Annals of Biomedical Engineering 2005, 33:1312-1318.
26. Guilak F., Alexopoulos L.G., Upton M.L., Youn I., Choi J.B., Cao L., Setton L.A., Haider M.A. The pericellular matrix as a transducer of biomechanical and biochemical signals of articular cartilage. Annals of the New York Academy of Sciences 2006, 1068:498-512.
27. Han S.-K., Colarusso P., Herzog W. Confocal microscopy indentation system for studying in situ chondrocyte mechanics. Medical Engineering & Physics 2009, 31:1038-1042.
28. Han S.-K., Seerattan R., Herzog W. Mechanical loading of in situ chondrocytes in lapine retropatellar cartilage after anterior cruciate ligament transection. Journal of the Royal Society Interface 2010, 7:895-903.
29. Han S.-K., Wouters W., Clark A., Herzog W. Mechanically induced calcium signaling in chondrocytes in situ. Journal of Orthopaedic Research 2012, 30:475-481.
30. Herberhold C., Faber S., Stammberger T., Steilechner M., Putz R., Englmeier K.H., Reiser M., Eckstein F. In situ measurement of articular cartilage deformation in intact femoropatellar joints under static loading. Journal of Biomechanics 1999, 32:1287-1295.
31. Herzog W., Diet S., Suter E., Mayzus P., Leonard T.R., Muller C., Wu J.Z., Epstein M. Material and functional properties of articular cartilage and patellofemoral contact mechanics in an experimental model of osteoarthritis. Journal of Biomechanics 1998, 31:1137-1145.
32. Jurvelin J.S., Arokoski J.P.A., Hunziker E.B., Helminen H.J. Topographical variation of the elastic properties of articular cartilage in the canine knee. Journal of Biomechanics 2000, 33:669-675.
33. Knight M.M., Ghori S.A., Lee D.A., Bader D.L. Measurement of the deformation of isolated chondrocytes in agarose subjected to cyclic compression. Medical Engineering & Physics 1998, 20:684-688.
34. Korhonen R.K., Laasanen M.S., Toyras J., Rieppo J., Hirvonen J., Helminen H.J., Jurvelin J.S. Comparison of the equilibrium response of articular cartilage in unconfined compression, confined compression and indentation. Journal of Biomechanics 2002, 35:903-909.
35. Korhonen R.K., Herzog W. Depth-dependent analysis of the role of collagen fibrils, fixed charges and fluid in the pericellular matrix of articular cartilage on chondrocyte mechanics. Journal of Biomechanics 2008, 41:480-485.
36. Korhonen R.K., Julkunen P., Wilson W., Herzog W. Importance of collagen orientation and depth-dependent fixed charge densities of cartilage on mechanical behavior of chondrocytes. Journal of Biomechanical Engineering 2008, 130:021003.
37. Krueger J.A., Thisse P., Ewers B.J., Dvoracek-Driksna D., Orth M.W., Haut R.C. The extent and distribution of cell death and matrix damage in impacted chondral explants varies with the presence of underlying bone. Journal of Biomechanical Engineering 2003, 125:114-119.
38. Lee D.A., Knight M.M., Bolton J.F., Idowu B.D., Kayser M.V., Bader D.L. Chondrocyte deformation within compressed agarose constructs at the cellular and sub-cellular levels. Journal of Biomechanics 2000, 33:81-95.
39. Little C.B., Ghosh P. Variation in proteoglycan metabolism by articular chondrocytes in different joint regions is determined by post-natal mechanical loading. Osteoarthritis and Cartilage 1997, 5:49-62.
40. Lyyra T., Kiviranta I., Vaatainen U., Helminen H.J., Jurvelin J.S. In vivo characterization of indentation stiffness of articular cartilage in the normal human knee. Journal of Biomedical Materials Research 1999, 48:482-487.
41. Morel V., Merçay A., Quinn T.M. Prestrain decreases cartilage susceptibility to injury by ramp compression in vitro. Osteroarthritis and Cartilage 2005, 13:964-970.
42. Mow V.C., Ratcliffe A. Cartilage and diarthrodial joints as paradigms for hierarchical materials and structures. Biomaterials 1992, 13:67-97.
43. Nugent A.E., McBurney D.L., Horton W.E. The presence of extracellular matrix alters the chondrocyte response to endoplasmic reticulum stress. Journal of Cellular Biochemistry 2011, 112:1118-1129.
44. Nguyen B.V., Wang Q., Kuiper N.J., El Haj A.J., Thomas C.R., Zhang Z. Strain-dependent viscoelastic behaviour and rupture force of single chondrons under compression. Biotechnology Letters 2009, 31:803-809.
45. Nguyen B.V., Wang Q.G., Kuiper N.J., El Haj A.J., Thomas C.R., Zhang Z. Biomechanical properties of single chondrocytes and chondrons determined by micromanipulation and finite-element modeling. Journal of the Royal Society Interface 2010, 7:1723-1733.
46. Poole C.A. Articular cartilage chondrons: form, function and failure. Journal of Anatomy 1997, 191:1-13.
47. Sah R.L., Kim Y.-J., Doong J.-Y.H., Grodzinsky A.J., Plaas A.H.K., Sandy J.D. Biosynthetic response of cartilage explants to dynamic compression. Journal of Orthopaedic Research 1989, 7:619-636.
48. Schachar N.S., Cucheran D.J., McGann L.E., Novak K.A., Frank C.B. Metabolic activity of bovine articular cartilage during refrigerated storage. Journal of Orthopaedic Research 1994, 12:15-20.
49. Schinagl R.M., Gurskis D., Chen A.C., Sah R.L. Depth-dependent confined compression modulus of full-thickness bovine articular cartilage. Journal of Orthopaedic Research 1997, 15:499-506.
50. Stockwell R.A. Biology of Cartilage Cells 1979, Cambridge University Press, Cambridge, England.
51. Treppo S., Koepp H., Quan E.C., Cole A.A., Kuettner K.E., Grodzinsky A.J. Comparison of biomechanical and biochemical properties of cartilage from human knee and ankle pairs. Journal of Orthopaedic Research 2000, 18:739-748.
52. Trickey W.R., Vail T.P., Guilak F. The role of the cytoskeleton in the viscoelastic properties of human articular chondrocytes. Journal of Orthopaedic Research 2004, 22:131-139.
53. Turunen S.M., Lammi M.J., Saarakkala S., Koistinen A., Korhonen R.K. Hypotonic challenge modulates cell volumes differently in the superficial zone of intact articular cartilage and cartilage explant. Biomechanics and Modeling in Mechanobiology 2011, 1-11. 10.1007/s10237-011-0341-z.
54. Wieland H.A., Michaelis M., Kirschbaum B.J., Rudolphi K.A. Osteoarthritis: an untreatable disease?. Nature Reviews 2005, 4:331-345.
55. 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. Journal of Orthopaedic Research 1996, 14:424-432.
56. Wong M., Wuethrich P., Buschmann M.D., Eggli P., Hunziker E. Chondrocyte biosynthesis correlates with local tissue strain in statically compressed adult articular cartilage. Journal of Orthopaedic Research 1997, 15:189-196.
57. Youn I., Choi J.B., Cao L., Setton L.A., Guilak F. Zonal variations in the three-dimensional morphology of the chondron measured in situ using confocal microscopy. Osteoarthritis and Cartilage 2006, 14:889-897.