The structure and function of the pericellular matrix of articular cartilage

Matrix Biology

Volumn 39, Issue , 2014, Pages 25-32

  Wilusz, Rebecca E ^a   Sanchez Adams, Johannah ^a   Guilak, Farshid ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Aggrecan; Chondron; Decorin; Mechanobiology; Mechanotransduction; Osteoarthritis; Perlecan; Territorial matrix; Type II collagen; Type VI collagen

Indexed keywords

COLLAGEN TYPE 6; PERLECAN; COLLAGEN;

ARTICULAR CARTILAGE; ASPIRATION; ATOMIC FORCE MICROSCOPY; BIOMECHANICS; CARTILAGE; CARTILAGE CELL; CELL FUNCTION; CELL STRUCTURE; EXTRACELLULAR MATRIX; EXTRACELLULAR SPACE; MICROPIPETTE; PERICELLULAR MATRIX; SHORT SURVEY; STRESS STRAIN RELATIONSHIP; ANIMAL; HUMAN; MECHANOTRANSDUCTION; METABOLISM; OSTEOARTHRITIS; PATHOLOGY;

ANIMALS; BIOMECHANICAL PHENOMENA; CARTILAGE, ARTICULAR; COLLAGEN; EXTRACELLULAR MATRIX; HUMANS; MECHANOTRANSDUCTION, CELLULAR; OSTEOARTHRITIS;

EID: 84908253920     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2014.08.009     Document Type: Review

References (101)

1. Aigner T., Zien A., Hanisch D., Zimmer R. Gene expression in chondrocytes assessed with use of microarrays. J. Bone Joint Surg. Am. 2003, 85-A(Suppl. 2):117-123.
2. Alexopoulos L.G., Haider M.A., Vail T.P., Guilak F. Alterations in the mechanical properties of the human chondrocyte pericellular matrix with osteoarthritis. J. Biomech. Eng. 2003, 125:323-333.
3. Alexopoulos L.G., Setton L.A., Guilak F. The biomechanical role of the chondrocyte pericellular matrix in articular cartilage. Acta Biomater. 2005, 1:317-325.
4. Alexopoulos L.G., Williams G.M., Upton M.L., Setton L.A., Guilak F. Osteoarthritic changes in the biphasic mechanical properties of the chondrocyte pericellular matrix in articular cartilage. J. Biomech. 2005, 38:509-517.
5. Alexopoulos L.G., Youn I., Bonaldo P., Guilak F. Developmental and osteoarthritic changes in Col6a1-knockout mice: biomechanics of type VI collagen in the cartilage pericellular matrix. Arthritis Rheum. 2009, 60:771-779.
6. Allen D.M., Mao J.J. Heterogeneous nanostructural and nanoelastic properties of pericellular and interterritorial matrices of chondrocytes by atomic force microscopy. J. Struct. Biol. 2004, 145:196-204.
7. Arikawa-Hirasawa E., Watanabe H., Takami H., Hassell J.R., Yamada Y. Perlecan is essential for cartilage and cephalic development. Nat. Genet. 1999, 23:354-358.
8. Bekkers J.E., Tsuchida A.I., van Rijen M.H., Vonk L.A., Dhert W.J., Creemers L.B., et al. Single-stage cell-based cartilage regeneration using a combination of chondrons and mesenchymal stromal cells: comparison with microfracture. Am. J. Sports Med. 2013, 41:2158-2166.
9. Benninghoff A. Form und bau der Gelenkknorpel in ihren Beziehungen Zur Funktion. Zweiter Teil: der Aufbau des Gelenkknorpels in sienen Bezienhungen zur Funktion 1925, 2:783-862.
10. Bougault C., Cueru L., Bariller J., Malbouyres M., Paumier A., Aszodi A., et al. Alteration of cartilage mechanical properties in absence of beta1 integrins revealed by rheometry and FRAP analyses. J. Biomech. 2013, 46:1633-1640.
11. Cao L., Guilak F., Setton L.A. Three-dimensional morphology of the pericellular matrix of intervertebral disc cells in the rat. J. Anat. 2007, 211:444-452.
12. Chao P.H., West A.C., Hung C.T. Chondrocyte intracellular calcium, cytoskeletal organization, and gene expression responses to dynamic osmotic loading. Am. J. Physiol. Cell Physiol. 2006, 291:C718-C725.
13. Chen C., Tambe D.T., Deng L., Yang L. Biomechanical properties and mechanobiology of the articular chondrocyte. Am. J. Physiol. Cell Physiol. 2013, 305:C1202-C1208.
14. Choi J.B., Youn I., Cao L., Leddy H.A., Gilchrist C.L., Setton L.A., et al. Zonal changes in the three-dimensional morphology of the chondron under compression: the relationship among cellular, pericellular, and extracellular deformation in articular cartilage. J. Biomech. 2007, 40:2596-2603.
15. Christensen S.E., Coles J.M., Zelenski N.A., Furman B.D., Leddy H.A., Zauscher S., et al. Altered trabecular bone structure and delayed cartilage degeneration in the knees of collagen VI null mice. PLoS One 2012, 7:e33397.
16. Coleman J.L., Widmyer M.R., Leddy H.A., Utturkar G.M., Spritzer C.E., Moorman C.T., et al. Diurnal variations in articular cartilage thickness and strain in the human knee. J. Biomech. 2013, 46:541-547.
17. Darling E.M., Zauscher S., Guilak F. Viscoelastic properties of zonal articular chondrocytes measured by atomic force microscopy. Osteoarthr. Cartil. 2006, 14:571-579.
18. 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. Biophys. J. 2010, 98:2848-2856.
19. Elsaid K.A., Jay G.D., Chichester C.O. Detection of collagen type II and proteoglycans in the synovial fluids of patients diagnosed with non-infectious knee joint synovitis indicates early damage to the articular cartilage matrix. Osteoarthr. Cartil. 2003, 11:673-680.
20. Farnsworth N., Bensard C., Bryant S.J. The role of the PCM in reducing oxidative stress induced by radical initiated photoencapsulation of chondrocytes in poly(ethylene glycol) hydrogels. Osteoarthr. Cartil. 2012, 20:1326-1335.
21. Grodzinsky A.J., Levenston M.E., Jin M., Frank E.H. Cartilage tissue remodeling in response to mechanical forces. Annu. Rev. Biomed. Eng. 2000, 2:691-713.
22. Guilak F., Hung C.T. Physical regulation of cartilage metabolism. Basic Orthopaedic Biomechanics and Mechano-Biology 2005, 179-207. Lippincott Williams & Wilkins, Philadelphia. 3rd ed. V.C. Mow, R. Huiskes (Eds.).
23. Guilak F., Mow V.C. The mechanical environment of the chondrocyte: a biphasic finite element model of cell-matrix interactions in articular cartilage. J. Biomech. 2000, 33:1663-1673.
24. Guilak F., Jones W.R., Ting-Beall H.P., Lee G.M. The deformation behavior and mechanical properties of chondrocytes in articular cartilage. Osteoarthr. Cartil. 1999, 7:59-70.
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. Ann. Biomed. Eng. 2005, 33:1312-1318.
26. Guilak F., Alexopoulos L.G., Upton M.L., Youn I., Choi J.B., Cao L., et al. The pericellular matrix as a transducer of biomechanical and biochemical signals in articular cartilage. Ann. N. Y. Acad. Sci. 2006, 1068:498-512.
27. Hagiwara H., Schroter-Kermani C., Merker H.J. Localization of collagen type VI in articular cartilage of young and adult mice. Cell Tissue Res. 1993, 272:155-160.
28. Haider M.A., Schugart R.C., Setton L.A., Guilak F. A mechano-chemical model for the passive swelling response of an isolated chondron under osmotic loading. Biomech. Model. Mechanobiol. 2006, 5:160-171.
29. Halloran J.P., Sibole S., van Donkelaar C.C., van Turnhout M.C., Oomens C.W., Weiss J.A., et al. Multiscale mechanics of articular cartilage: potentials and challenges of coupling musculoskeletal, joint, and microscale computational models. Ann. Biomed. Eng. 2012, 40:2456-2474.
30. Hedlund H., Hedbom E., Heineg D., Mengarelli-Widholm S., Reinholt F.P., Svensson O. Association of the aggrecan keratan sulfate-rich region with collagen in bovine articular cartilage. J. Biol. Chem. 1999, 274:5777-5781.
31. Heinegard D., Oldberg A. Structure and biology of cartilage and bone matrix noncollagenous macromolecules. FASEB J. 1989, 3:2042-2051.
32. Hing W.A., Sherwin A.F., Poole C.A. The influence of the pericellular microenvironment on the chondrocyte response to osmotic challenge. Osteoarthr. Cartil. 2002, 10:297-307.
33. Hu K., Xu L., Cao L., Flahiff C.M., Brussiau J., Ho K., et al. Pathogenesis of osteoarthritis-like changes in the joints of mice deficient in type IX collagen. Arthritis Rheum. 2006, 54:2891-2900.
34. Hunziker E.B., Michel M., Studer D. Ultrastructure of adult human articular cartilage matrix after cryotechnical processing. Microsc. Res. Tech. 1997, 37:271-284.
35. Julkunen P., Wilson W., Jurvelin J.S., Korhonen R.K. Composition of the pericellular matrix modulates the deformation behaviour of chondrocytes in articular cartilage under static loading. Med. Biol. Eng. Comput. 2009, 47:1281-1290.
36. Junqueira L.C., Montes G.S. Biology of collagen-proteoglycan interaction. Arch. Histol. Jpn. 1983, 46:589-629.
37. Kavanagh E., Ashhurst D.E. Development and aging of the articular cartilage of the rabbit knee joint: distribution of biglycan, decorin, and matrilin-1. J. Histochem. Cytochem. 1999, 47:1603-1616.
38. Kim E., Guilak F., Haider M.A. An axisymmetric boundary element model for determination of articular cartilage pericellular matrix properties in situ via inverse analysis of chondron deformation. J. Biomech. Eng. 2010, 132:031011.
39. Knight M.M., Lee D.A., Bader D.L. The influence of elaborated pericellular matrix on the deformation of isolated articular chondrocytes cultured in agarose. Biochim. Biophys. Acta 1998, 1405:67-77.
40. Knight M.M., Ross J.M., Sherwin A.F., Lee D.A., Bader D.L., Poole C.A. Chondrocyte deformation within mechanically and enzymatically extracted chondrons compressed in agarose. Biochim. Biophys. Acta 2001, 1526:141-146.
41. Knudson C.B. Hyaluronan receptor-directed assembly of chondrocyte pericellular matrix. J. Cell Biol. 1993, 120:825-834.
42. 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. J. Biomech. 2008, 41:480-485.
43. Kvist A.J., Johnson A.E., Morgelin M., Gustafsson E., Bengtsson E., Lindblom K., et al. Chondroitin sulfate perlecan enhances collagen fibril formation. Implications for perlecan chondrodysplasias. J. Biol. Chem. 2006, 281:33127-33139.
44. Lai W.M., Hou J.S., Mow V.C. A triphasic theory for the swelling and deformation behaviors of articular cartilage. J. Biomech. Eng. 1991, 113:245-258.
45. Leddy H.A., Christensen S.E., Guilak F. Microscale diffusion properties of the cartilage pericellular matrix measured using 3D scanning microphotolysis. J. Biomech. Eng. 2008, 130:061002.
46. Lee G.M., Poole C.A., Kelley S.S., Chang J., Caterson B. Isolated chondrons: a viable alternative for studies of chondrocyte metabolism in vitro. Osteoarthr. Cartil. 1997, 5:261-274.
47. Lee G.M., Paul T.A., Slabaugh M., Kelley S.S. The incidence of enlarged chondrons in normal and osteoarthritic human cartilage and their relative matrix density. Osteoarthr. Cartil. 2000, 8:44-52.
48. Macri L., Silverstein D., Clark R.A. Growth factor binding to the pericellular matrix and its importance in tissue engineering. Adv. Drug Deliv. Rev. 2007, 59:1366-1381.
49. Maroudas A., Bayliss M.T., Uchitel-Kaushansky N., Schneiderman R., Gilav E. Aggrecan turnover in human articular cartilage: use of aspartic acid racemization as a marker of molecular age. Arch. Biochem. Biophys. 1998, 350:61-71.
50. McLeod M.A., Wilusz R.E., Guilak F. Depth-dependent anisotropy of the micromechanical properties of the extracellular and pericellular matrices of articular cartilage evaluated via atomic force microscopy. J. Biomech. 2013, 46:586-592.
51. Melrose J., Roughley P., Knox S., Smith S., Lord M., Whitelock J. The structure, location, and function of perlecan, a prominent pericellular proteoglycan of fetal, postnatal, and mature hyaline cartilages. J. Biol. Chem. 2006, 281:36905-36914.
52. Michalek A.J., Iatridis J.C. A numerical study to determine pericellular matrix modulus and evaluate its effects on the micromechanical environment of chondrocytes. J. Biomech. 2007, 40:1405-1409.
53. Morrison E.H., Ferguson M.W., Bayliss M.T., Archer C.W. The development of articular cartilage: I. The spatial and temporal patterns of collagen types. J. Anat. 1996, 189(Pt 1):9-22.
54. Mow V.C., Bachrach N., Setton L.A., Guilak F. Stress, strain, pressure, and flow fields in articular cartilage. Cell Mechanics and Cellular Engineering 1994, 345-379. Springer Verlag, New York. V.C. Mow, F. Guilak, R. Tran-Son-Tay, R. Hochmuth (Eds.).
55. Mow V.C., Wang C.C., Hung C.T. The extracellular matrix, interstitial fluid and ions as a mechanical signal transducer in articular cartilage. Osteoarthr. Cartil. 1999, 7:41-58.
56. Ng L., Hung H.H., Sprunt A., Chubinskaya S., Ortiz C., Grodzinsky A. Nanomechanical properties of individual chondrocytes and their developing growth factor-stimulated pericellular matrix. J. Biomech. 2007, 40:1011-1023.
57. 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 chondrocytes and chondrons under compression. Biotechnol. Lett. 2009, 31:803-809.
58. 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 modelling. J. R. Soc. Interface 2010, 7:1723-1733.
59. O'Conor C., Leddy H.A., Benefield H., Liedtke W., Guilak F. TRPV4-mediated mechanotransduction regulates the metabolic response of chondrocytes to dynamic loading. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:1316-1321.
60. Peters H.C., Otto T.J., Enders J.T., Jin W., Moed B.R., Zhang Z. The protective role of the pericellular matrix in chondrocyte apoptosis. Tissue Eng. A 2011, 17:2017-2024.
61. Plumb D.A., Ferrara L., Torbica T., Knowles L., Mironov A., Kadler K.E., et al. Collagen XXVII organises the pericellular matrix in the growth plate. PLoS One 2011, 6:e29422.
62. Poole C.A. Articular cartilage chondrons: form, function and failure. J. Anat. 1997, 191:1-13.
63. Poole A.R., Pidoux I., Reiner A., Rosenberg L. An immunoelectron microscope study of the organization of proteoglycan monomer, link protein, and collagen in the matrix of articular cartilage. J. Cell Biol. 1982, 93:921-937.
64. Poole C.A., Flint M.H., Beaumont B.W. Morphological and functional interrelationships of articular cartilage matrices. J. Anat. 1984, 138(Pt 1):113-138.
65. Poole C.A., Flint M.H., Beaumont B.W. Chondrons in cartilage: ultrastructural analysis of the pericellular microenvironment in adult human articular cartilages. J. Orthop. Res. 1987, 5:509-522.
66. Poole C.A., Ayad S., Schofield J.R. Chondrons from articular cartilage: I. Immunolocalization of type VI collagen in the pericellular capsule of isolated canine tibial chondrons. J. Cell Sci. 1988, 90(Pt 4):635-643.
67. Poole C.A., Glant T.T., Schofield J.R. Chondrons from articular cartilage. (IV). Immunolocalization of proteoglycan epitopes in isolated canine tibial chondrons. J. Histochem. Cytochem. 1991, 39:1175-1187.
68. Poole C.A., Matsuoka A., Schofield J.R. Chondrons from articular cartilage. III. Morphologic changes in the cellular microenvironment of chondrons isolated from osteoarthritic cartilage. Arthritis Rheum. 1991, 34:22-35.
69. Poole C.A., Ayad S., Gilbert R.T. Chondrons from articular cartilage. V. Immunohistochemical evaluation of type VI collagen organisation in isolated chondrons by light, confocal and electron microscopy. J. Cell Sci. 1992, 103(Pt 4):1101-1110.
70. Poole C.A., Gilbert R.T., Herbage D., Hartmann D.J. Immunolocalization of type IX collagen in normal and spontaneously osteoarthritic canine tibial cartilage and isolated chondrons. Osteoarthr. Cartil. 1997, 5:191-204.
71. Radmacher M., Tillamnn R.W., Fritz M., Gaub H.E. From molecules to cells: imaging soft samples with the atomic force microscope. Science 1992, 257:1900-1905.
72. Ruoslahti E., Yamaguchi Y. Proteoglycans as modulators of growth factor activities. Cell 1991, 64:867-869.
73. Sanchez-Adams J., Wilusz R.E., Guilak F. Atomic force microscopy reveals regional variations in the micromechanical properties of the pericellular and extracellular matrices of the meniscus. J. Orthop. Res. 2013, 31:1218-1225.
74. Schinagl R.M., Gurskis D., Chen A.C., Sah R.L. Depth-dependent confined compression modulus of full-thickness bovine articular cartilage. J. Orthop. Res. 1997, 15:499-506.
75. Scott J.E. Proteoglycan-fibrillar collagen interactions. Biochem. J. 1988, 252:313-323.
76. Sen S., Kumar S. Combining mechanical and optical approaches to dissectcellular mechanobiology. J. Biomech. 2010, 43:45-54.
77. Setton L.A., Chen J. Cell mechanics and mechanobiology in the intervertebral disc. Spine (Phila Pa 1976) 2004, 29:2710-2723.
78. Sherwin A.F., Carter D.H., Poole C.A., Hoyland J.A., Ayad S. The distribution of type VI collagen in the developing tissues of the bovine femoral head. Histochem. J. 1999, 31:623-632.
79. Sibole S.C., Erdemir A. Chondrocyte deformations as a function of tibiofemoral joint loading predicted by a generalized high-throughput pipeline of multi-scale simulations. PLoS One 2012, 7:e37538.
80. Song R.H., Tortorella M.D., Malfait A.M., Alston J.T., Yang Z., Arner E.C., et al. Aggrecan degradation in human articular cartilage explants is mediated by both ADAMTS-4 and ADAMTS-5. Arthritis Rheum. 2007, 56:575-585.
81. Steward A.J., Wagner D.R., Kelly D.J. The pericellular environment regulates cytoskeletal development and the differentiation of mesenchymal stem cells and determines their response to hydrostatic pressure. Eur. Cell Mater. 2013, 25:167-178.
82. Stockwell R.A. The interrelationship of cell density and cartilage thickness in mammalian articular cartilage. J. Anat. 1971, 109:411-421.
83. SundarRaj N., Fite D., Ledbetter S., Chakravarti S., Hassell J.R. Perlecan is a component of cartilage matrix and promotes chondrocyte attachment. J. Cell Sci. 1995, 108(Pt 7):2663-2672.
84. Szirmai J.A. Structure of cartilage. Aging of Connective and Skeletal Tissue 1968, 163-184. Nordiska Bokhandelns Forlag, Stockholm. A. Engel, T. Larsson (Eds.).
85. Upton M.L., Chen J., Guilak F., Setton L.A. Differential effects of static and dynamic compression on meniscal cell gene expression. J. Orthop. Res. 2003, 21:963-969.
86. Vanden Berg-Foels W.S., Scipioni L., Huynh C., Wen X. Helium ion microscopy for high-resolution visualization of the articular cartilage collagen network. J. Microsc. 2012, 246:168-176.
87. Vincent T., Hermansson M., Bolton M., Wait R., Saklatvala J. Basic FGF mediates an immediate response of articular cartilage to mechanical injury. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:8259-8264.
88. Vincent T.L., Hermansson M.A., Hansen U.N., Amis A.A., Saklatvala J. Basic fibroblast growth factor mediates transduction of mechanical signals when articular cartilage is loaded. Arthritis Rheum. 2004, 50:526-533.
89. Vincent T.L., McLean C.J., Full L.E., Peston D., Saklatvala J. FGF-2 is bound to perlecan in the pericellular matrix of articular cartilage, where it acts as a chondrocyte mechanotransducer. Osteoarthr. Cartil. 2007, 15:752-763.
90. Vincourt J.B., Etienne S., Grossin L., Cottet J., Bantsimba-Malanda C., Netter P., et al. Matrilin-3 switches from anti- to pro-anabolic upon integration to the extracellular matrix. Matrix Biol. 2012, 31:290-298.
91. Vonk L.A., Doulabi B.Z., Huang C., Helder M.N., Everts V., Bank R.A. Preservation of the chondrocyte's pericellular matrix improves cell-induced cartilage formation. J. Cell. Biochem. 2010, 110:260-271.
92. Vonk L.A., Doulabi B.Z., Huang C., Helder M.N., Everts V., Bank R.A. Collagen-induced expression of collagenase-3 by primary chondrocytes is mediated by integrin α1 and discoidin domain receptor 2: a protein kinase C-dependent pathway. Rheumatology (Oxford) 2011, 50:463-472.
93. Wiberg C., Klatt A.R., Wagener R., Paulsson M., Bateman J.F., Heinegard D., et al. Complexes of matrilin-1 and biglycan or decorin connect collagen VI microfibrils to both collagen II and aggrecan. J. Biol. Chem. 2003, 278:37698-37704.
94. Wilusz R.E., Guilak F. High resistance of the mechanical properties of the chondrocyte pericellular matrix to proteoglycan digestion by chondroitinase, aggrecanase, or hyaluronidase. J. Mech. Behav. Biomed. Mater. 2014, 38:183-197.
95. Wilusz R.E., Defrate L.E., Guilak F. A biomechanical role for perlecan in the pericellular matrix of articular cartilage. Matrix Biol. 2012, 31:320-327.
96. Wilusz R.E., DeFrate L.E., Guilak F. Immunofluorescence-guided atomic force microscopy to measure the micromechanical properties of the pericellular matrix of porcine articular cartilage. J. R. Soc. Interface 2012, 9:2997-3007.
97. Wilusz R.E., Zauscher S., Guilak F. Micromechanical mapping of early osteoarthritic changes in the pericellular matrix of human articular cartilage. Osteoarthr. Cartil. 2013, 21:1895-1903.
98. Wu J.Z., Herzog W. Finite element simulation of location- and time-dependent mechanical behavior of chondrocytes in unconfined compression tests. Ann. Biomed. Eng. 2000, 28:318-330.
99. Xu L., Polur I., Servais J.M., Hsieh S., Lee P.L., Goldring M.B., et al. Intact pericellular matrix of articular cartilage is required for unactivated discoidin domain receptor 2 in the mouse model. Am. J. Pathol. 2011, 179:1338-1346.
100. 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. Osteoarthr. Cartil. 2006, 14:889-897.
101. Zelenski N., Leddy H.A., Sanchez-Adams J., Bonaldo P., Liedtke W., Guilak F. Collagen VI: the link between the extracellular matrix and chondrocyte mechanotranduction. Trans. Orthop. Res. Soc. 2014, 39:192.