High resistance of the mechanical properties of the chondrocyte pericellular matrix to proteoglycan digestion by chondroitinase, aggrecanase, or hyaluronidase

Rebecca E. Wilusz1,2, Farshid Guilak1,2
1Department of Orthopaedic Surgery, Duke University Medical Center, USA
2Department of Biomedical Engineering, Duke University, USA

Tài liệu tham khảo

Akizuki, 1986, Tensile properties of human knee joint cartilage: I. Influence of ionic conditions, weight bearing, and fibrillation on the tensile modulus, Journal of Orthopaedic Research, 4, 379, 10.1002/jor.1100040401 Alexopoulos, 2005, Osteoarthritic changes in the biphasic mechanical properties of the chondrocyte pericellular matrix in articular cartilage, Journal of Biomechanics, 38, 509, 10.1016/j.jbiomech.2004.04.012 Alexopoulos, 2009, Developmental and osteoarthritic changes in Col6a1-knockout mice: biomechanics of type VI collagen in the cartilage pericellular matrix, Arthritis and Rheumatism, 60, 771, 10.1002/art.24293 Asanbaeva, 2008, Articular cartilage tensile integrity: modulation by matrix depletion is maturation-dependent, Archives of Biochemistry and Biophysics, 474, 175, 10.1016/j.abb.2008.03.012 Athanasiou, 1995, Biomechanical properties of hip cartilage in experimental animal models, Clinical Orthopaedics and Related Research, 254, 10.1097/00003086-199507000-00035 Bader, 1994, The short-term compressive properties of adult human articular cartilage, Biomedical Materials and Engineering, 4, 245 Bartholomew, 1987, Receptor-mediated binding of leukocyte elastase by chondrocytes, Arthritis and Rheumatism, 30, 431, 10.1002/art.1780300411 Bau, 2002, Relative messenger RNA expression profiling of collagenases and aggrecanases in human articular chondrocytes in vivo and in vitro, Arthritis and Rheumatism, 46, 2648, 10.1002/art.10531 Bonnevie, 2012, Fluid load support during localized indentation of cartilage with a spherical probe, Journal of Biomechanics, 45, 1036, 10.1016/j.jbiomech.2011.12.019 Chia, 2009, Fibroblast growth factor 2 is an intrinsic chondroprotective agent that suppresses ADAMTS-5 and delays cartilage degradation in murine osteoarthritis, Arthritis and Rheumatism, 60, 2019, 10.1002/art.24654 Choi, 2007, 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, 40, 2596, 10.1016/j.jbiomech.2007.01.009 Darling, 2010, Spatial mapping of the biomechanical properties of the pericellular matrix of articular cartilage measured in situ via atomic force microscopy, Biophysical Journal, 98, 2848, 10.1016/j.bpj.2010.03.037 Durigova, 2011, Involvement of ADAMTS5 and hyaluronidase in aggrecan degradation and release from OSM-stimulated cartilage, European Cells and Materials, 21, 31, 10.22203/eCM.v021a03 Eisenberg, 1985, Swelling of articular cartilage and other connective tissues: electromechanochemical forces, Journal of Orthopaedic Research, 3, 148, 10.1002/jor.1100030204 Elsaid, 2008, Decreased lubricin concentrations and markers of joint inflammation in the synovial fluid of patients with anterior cruciate ligament injury, Arthritis and Rheumatism, 58, 1707, 10.1002/art.23495 Elsaid, 2003, 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, Osteoarthritis and Cartilage, 11, 673, 10.1016/S1063-4584(03)00151-1 Ernst, 1995, Enzymatic degradation of glycosaminoglycans, Critical Reviews in Biochemistry and Molecular Biology, 30, 387, 10.3109/10409239509083490 Flannery, 1992, Identification of a stromelysin cleavage site within the interglobular domain of human aggrecan. Evidence for proteolysis at this site in vivo in human articular cartilage, Journal of Biological Chemistry, 267, 1008, 10.1016/S0021-9258(18)48387-1 Gadher, 1988, Susceptibility of cartilage collagens type II, IX, X, and XI to human synovial collagenase and neutrophil elastase, European Journal of Biochemistry, 175, 1, 10.1111/j.1432-1033.1988.tb14158.x Gendron, 2007, Proteolytic activities of human ADAMTS-5: comparative studies with ADAMTS-4, Journal of Biological Chemistry, 282, 18294, 10.1074/jbc.M701523200 Glasson, 2005, Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis, Nature, 434, 644, 10.1038/nature03369 Guilak, 2005, Zonal uniformity in mechanical properties of the chondrocyte pericellular matrix: micropipette aspiration of canine chondrons isolated by cartilage homogenization, Annals of Biomedical Engineering, 33, 1312, 10.1007/s10439-005-4479-7 Guilak, 2006, The pericellular matrix as a transducer of biomechanical and biochemical signals in articular cartilage, Annals of the New York Academy of Sciences, 1068, 498, 10.1196/annals.1346.011 Guilak, 1999, The deformation behavior and mechanical properties of chondrocytes in articular cartilage, Osteoarthritis and Cartilage, 7, 59, 10.1053/joca.1998.0162 Guo, 2006, Packing density and structural heterogeneity of insulin amyloid fibrils measured by AFM nanoindentation, Biomacromolecules, 7, 1630, 10.1021/bm0600724 Hall, 2009, Effect of dermatan sulfate on the indentation and tensile properties of articular cartilage, Osteoarthritis and Cartilage, 17, 655, 10.1016/j.joca.2008.10.010 Hardingham, 1992, Proteoglycans: many forms and many functions, FASEB Journal, 6, 861, 10.1096/fasebj.6.3.1740236 Hedbom, 1993, Binding of fibromodulin and decorin to separate sites on fibrillar collagens, Journal of Biological Chemistry, 268, 27307, 10.1016/S0021-9258(19)74250-1 Heinegard, 2009, Proteoglycans and more—from molecules to biology, International Journal of Experimental Pathology, 90, 575, 10.1111/j.1365-2613.2009.00695.x Hu, 2006, Pathogenesis of osteoarthritis-like changes in the joints of mice deficient in type IX collagen, Arthritis and Rheumatism, 54, 2891, 10.1002/art.22040 Hunziker, 2002, Quantitative structural organization of normal adult human articular cartilage, Osteoarthritis and Cartilage, 10, 564, 10.1053/joca.2002.0814 Ishiguro, 2001, Relationships of matrix metalloproteinases and their inhibitors to cartilage proteoglycan and collagen turnover and inflammation as revealed by analyses of synovial fluids from patients with rheumatoid arthritis, Arthritis and Rheumatism, 44, 2503, 10.1002/1529-0131(200111)44:11<2503::AID-ART430>3.0.CO;2-P Janoff, 1976, Degradation of cartilage proteoglycan by human leukocyte granule neutral proteases—a model of joint injury. I. Penetration of enzyme into rabbit articular cartilage and release of 35SO4-labeled material from the tissue, Journal of Clinical Investigation, 57, 615, 10.1172/JCI108317 Jansen, 2010, Type II and VI collagen in nasal and articular cartilage and the effect of IL-1alpha on the distribution of these collagens, Journal of Molecular Histology, 41, 9, 10.1007/s10735-010-9257-7 Julkunen, 2009, Composition of the pericellular matrix modulates the deformation behaviour of chondrocytes in articular cartilage under static loading, Medical and Biological Engineering and Computing, 47, 1281, 10.1007/s11517-009-0547-8 Kavanagh, 1999, Development and aging of the articular cartilage of the rabbit knee joint: distribution of biglycan, decorin, and matrilin-1, Journal of Histochemistry and Cytochemistry, 47, 1603, 10.1177/002215549904701212 Kawabata, 1996, Impaired activity of protease inhibitors towards neutrophil elastase bound to human articular cartilage, Annals of the Rheumatic Diseases, 55, 248, 10.1136/ard.55.4.248 Kielty, 1993, Catabolism of intact type VI collagen microfibrils: susceptibility to degradation by serine proteinases, Biochemical and Biophysical Research Communications, 191, 1230, 10.1006/bbrc.1993.1349 Kielty, 1992, Type VI collagen microfibrils: evidence for a structural association with hyaluronan, Journal of Cell Biology, 118, 979, 10.1083/jcb.118.4.979 Kim, 2008, The dynamic mechanical environment of the chondrocyte: a biphasic finite element model of cell-matrix interactions under cyclic compressive loading, Journal of Biomechanical Engineering, 130, 061009, 10.1115/1.2978991 Knudson, 1993, Hyaluronan receptor-directed assembly of chondrocyte pericellular matrix, Journal of Cell Biology, 120, 825, 10.1083/jcb.120.3.825 Knudson, 2003, Hyaluronan and CD44: strategic players for cell-matrix interactions during chondrogenesis and matrix assembly, Birth Defects Research C: Embryo Today, 69, 174, 10.1002/bdrc.10013 Korhonen, 2003, Fibril reinforced poroelastic model predicts specifically mechanical behavior of normal, proteoglycan depleted and collagen degraded articular cartilage, Journal of Biomechanics, 36, 1373, 10.1016/S0021-9290(03)00069-1 Laasanen, 2003, Biomechanical properties of knee articular cartilage, Biorheology, 40, 133 Lai, 1991, A triphasic theory for the swelling and deformation behaviors of articular cartilage, Journal of Biomechanical Engineering, 113, 245, 10.1115/1.2894880 Lang, 2000, The relative importance of cysteine peptidases in osteoarthritis, Journal of Rheumatology, 27, 1970 Lark, 1997, Aggrecan degradation in human cartilage. Evidence for both matrix metalloproteinase and aggrecanase activity in normal, osteoarthritic, and rheumatoid joints, Journal of Clinical Investigation, 100, 93, 10.1172/JCI119526 LeRoux, 2000, Simultaneous changes in the mechanical properties, quantitative collagen organization, and proteoglycan concentration of articular cartilage following canine meniscectomy, Journal of Orthopaedic Research, 18, 383, 10.1002/jor.1100180309 Little, 2002, Matrix metalloproteinases are involved in C-terminal and interglobular domain processing of cartilage aggrecan in late stage cartilage degradation, Matrix Biology, 21, 271, 10.1016/S0945-053X(02)00004-5 Lyyra, 1999, Experimental validation of arthroscopic cartilage stiffness measurement using enzymatically degraded cartilage samples, Physics in Medicine & Biology, 44, 525, 10.1088/0031-9155/44/2/017 Martin, 1999, Method for quantitative analysis of glycosaminoglycan distribution in cultured natural and engineered cartilage, Annals of Biomedical Engineering, 27, 656, 10.1114/1.205 McDevitt, 1991, Interaction of intact type VI collagen with hyaluronan, FEBS Letters, 294, 167, 10.1016/0014-5793(91)80660-U Melrose, 2008, Perlecan, the “jack of all trades” proteoglycan of cartilaginous weight-bearing connective tissues, Bioessays, 30, 457, 10.1002/bies.20748 Melrose, 2006, The structure, location, and function of perlecan, a prominent pericellular proteoglycan of fetal, postnatal, and mature hyaline cartilages, Journal of Biological Chemistry, 281, 36905, 10.1074/jbc.M608462200 Menninger, 1981, Lysosomal elastase: effect on mechanical and biochemical properties of normal cartilage, inhibition by polysulfonated glycosaminoglycan, and binding to chondrocytes, Rheumatology International, 1, 73, 10.1007/BF00541157 Menzel, 1998, Hyaluronidase and its substrate hyaluronan: biochemistry, biological activities and therapeutic uses, Cancer Letters, 131, 3, 10.1016/S0304-3835(98)00195-5 Mio, 2002, Inhibitors of the hyaluronidases, Matrix Biology, 21, 31, 10.1016/S0945-053X(01)00185-8 Mok, 1992, Cleavage of proteoglycan aggregate by leucocyte elastase, Archives of Biochemistry and Biophysics, 292, 442, 10.1016/0003-9861(92)90014-N Momohara, 1997, Elastase from polymorphonuclear leukocyte in articular cartilage and synovial fluids of patients with rheumatoid arthritis, Clinical Rheumatology, 16, 133, 10.1007/BF02247841 Monfort, 2006, Degradation of small leucine-rich repeat proteoglycans by matrix metalloprotease-13: identification of a new biglycan cleavage site, Arthritis Research and Therapy, 8, R26, 10.1186/ar1873 Morgelin, 1988, Cartilage proteoglycans. Assembly with hyaluronate and link protein as studied by electron microscopy, Biochemical Journal, 253, 175, 10.1042/bj2530175 Mow, 1998, Effects of fixed charges on the stress-relaxation behavior of hydrated soft tissues in a confined compression problem, International Journal of Solids and Structures, 35, 4945, 10.1016/S0020-7683(98)00103-6 Mow, 1994, Stress, strain, pressure and flow fields in articular cartilage and chondrocytes, 345 Mow, 1992, Cartilage and diarthrodial joints as paradigms for hierarchical materials and structures, Biomaterials, 13, 67, 10.1016/0142-9612(92)90001-5 Mueller, 2011, Anabolic/catabolic balance in pathogenesis of osteoarthritis: identifying molecular targets, PM&R, 3, S3, 10.1016/j.pmrj.2011.05.009 Munteanu, 2002, Highly sulfated glycosaminoglycans inhibit aggrecanase degradation of aggrecan by bovine articular cartilage explant cultures, Matrix Biology, 21, 429, 10.1016/S0945-053X(02)00034-3 Nagel, 2010, The influence of fiber orientation on the equilibrium properties of neutral and charged biphasic tissues, Journal of Biomechanical Engineering, 132, 114506, 10.1115/1.4002589 Nakada, 1961, Studies on the enzyme chondroitinase: product structure and ion effects, Archives of Biochemistry and Biophysics, 94, 244, 10.1016/0003-9861(61)90037-6 Ohya, 1970, Novel hyaluronidase from streptomyces, Biochimica et Biophysica Acta, 198, 607, 10.1016/0005-2744(70)90139-7 Owen, 1999, The cell biology of leukocyte-mediated proteolysis, Journal of Leukocyte Biology, 65, 137, 10.1002/jlb.65.2.137 Pap, 2013, Syndecans in cartilage breakdown and synovial inflammation, Nature Reviews Rheumatology, 9, 43, 10.1038/nrrheum.2012.178 Park, 2009, Mechanical properties of bovine articular cartilage under microscale indentation loading from atomic force microscopy, Proceedings of the Institution of Mechanical Engineers [H], 223, 339, 10.1243/09544119JEIM516 Plaas, 2007, Aggrecanolysis in human osteoarthritis: confocal localization and biochemical characterization of ADAMTS5-hyaluronan complexes in articular cartilages, Osteoarthritis and Cartilage, 15, 719, 10.1016/j.joca.2006.12.008 Poole, 1982, An immunoelectron microscope study of the organization of proteoglycan monomer, link protein, and collagen in the matrix of articular cartilage, Journal of Cell Biology, 93, 921, 10.1083/jcb.93.3.921 Poole, 1988, Chondrons from articular cartilage: I. Immunolocalization of type VI collagen in the pericellular capsule of isolated canine tibial chondrons, Journal of Cell Science, 90, 635, 10.1242/jcs.90.4.635 Poole, 1984, Morphological and functional interrelationships of articular cartilage matrices, Journal of Anatomy, 138, 113 Poole, 1985, Morphology of the pericellular capsule in articular cartilage revealed by hyaluronidase digestion, Journal of Ultrastructure Research, 91, 13, 10.1016/0889-1605(85)90071-0 Poole, 1997, Immunolocalization of type IX collagen in normal and spontaneously osteoarthritic canine tibial cartilage and isolated chondrons, Osteoarthritis and Cartilage, 5, 191, 10.1016/S1063-4584(97)80014-3 Roughley, 2006, The structure and function of cartilage proteoglycans, European Cells and Materials, 12, 92, 10.22203/eCM.v012a11 Sandy, 1991, Catabolism of aggrecan in cartilage explants. Identification of a major cleavage site within the interglobular domain, Journal of Biological Chemistry, 266, 8683, 10.1016/S0021-9258(18)31499-6 Schmidt, 1990, Effects of proteoglycan extraction on the tensile behavior of articular cartilage, Journal of Orthopaedic Research, 8, 353, 10.1002/jor.1100080307 Scott, 2006, Cartilage elasticity resides in shape module decoran and aggrecan sumps of damping fluid: implications in osteoarthrosis, Journal of Physiology, 574, 643, 10.1113/jphysiol.2006.108100 Solau-Gervais, 2007, Cysteine and serine proteases of synovial tissue in rheumatoid arthritis and osteoarthritis, Scandinavian Journal of Rheumatology, 36, 373, 10.1080/03009740701340172 Song, 2007, Aggrecan degradation in human articular cartilage explants is mediated by both ADAMTS-4 and ADAMTS-5, Arthritis and Rheumatism, 56, 575, 10.1002/art.22334 Starkey, 1977, The degradation of articular collagen by neutrophil proteinases, Biochimica et Biophysica Acta, 483, 386, 10.1016/0005-2744(77)90066-3 Stolz, 2004, Dynamic elastic modulus of porcine articular cartilage determined at two different levels of tissue organization by indentation-type atomic force microscopy, Biophysical Journal, 86, 3269, 10.1016/S0006-3495(04)74375-1 Sun, 2004, The influence of the fixed negative charges on mechanical and electrical behaviors of articular cartilage under unconfined compression, Journal of Biomechanical Engineering, 126, 6, 10.1115/1.1644562 SundarRaj, 1995, Perlecan is a component of cartilage matrix and promotes chondrocyte attachment, Journal of Cell Science, 108, 2663, 10.1242/jcs.108.7.2663 Tortorella, 2001, The role of ADAM-TS4 (aggrecanase-1) and ADAM-TS5 (aggrecanase-2) in a model of cartilage degradation, Osteoarthritis and Cartilage, 9, 539, 10.1053/joca.2001.0427 Tortorella, 2000, Sites of aggrecan cleavage by recombinant human aggrecanase-1 (ADAMTS-4), Journal of Biological Chemistry, 275, 18566, 10.1074/jbc.M909383199 Vincent, 2007, FGF-2 is bound to perlecan in the pericellular matrix of articular cartilage, where it acts as a chondrocyte mechanotransducer, Osteoarthritis and Cartilage, 15, 752, 10.1016/j.joca.2007.01.021 Westling, 2002, ADAMTS4 cleaves at the aggrecanase site (Glu373–Ala374) and secondarily at the matrix metalloproteinase site (Asn341–Phe342) in the aggrecan interglobular domain, Journal of Biological Chemistry, 277, 16059, 10.1074/jbc.M108607200 Wiberg, 2001, Biglycan and decorin bind close to the n-terminal region of the collagen VI triple helix, Journal of Biological Chemistry, 276, 18947, 10.1074/jbc.M100625200 Wiberg, 2002, Biglycan organizes collagen VI into hexagonal-like networks resembling tissue structures, Journal of Biological Chemistry, 277, 49120, 10.1074/jbc.M206891200 Wiberg, 2003, Complexes of matrilin-1 and biglycan or decorin connect collagen VI microfibrils to both collagen II and aggrecan, Journal of Biological Chemistry, 278, 37698, 10.1074/jbc.M304638200 Wilusz, 2012, A biomechanical role for perlecan in the pericellular matrix of articular cartilage, Matrix Biology, 31, 320, 10.1016/j.matbio.2012.05.002 Wilusz, 2012, Immunofluorescence-guided atomic force microscopy to measure the micromechanical properties of the pericellular matrix of porcine articular cartilage, Journal of the Royal Society Interface, 9, 2997, 10.1098/rsif.2012.0314 Wu, 1992, Identification of cross-linking sites in bovine cartilage type IX collagen reveals an antiparallel type II–type IX molecular relationship and type IX to type IX bonding, Journal of Biological Chemistry, 267, 23007, 10.1016/S0021-9258(18)50048-X Yamagata, 1968, Purification and properties of bacterial chondroitinases and chondrosulfatases, Journal of Biological Chemistry, 243, 1523, 10.1016/S0021-9258(18)93574-X Youn, 2006, Zonal variations in the three-dimensional morphology of the chondron measured in situ using confocal microscopy, Osteoarthritis and Cartilage, 14, 889, 10.1016/j.joca.2006.02.017 Zhen, 2008, Characterization of metalloprotease cleavage products of human articular cartilage, Arthritis and Rheumatism, 58, 2420, 10.1002/art.23654 Zhu, 1993, Viscoelastic shear properties of articular cartilage and the effects of glycosidase treatments, Journal of Orthopaedic Research, 11, 771, 10.1002/jor.1100110602