Aggrecanolysis in human osteoarthritis: confocal localization and biochemical characterization of ADAMTS5-hyaluronan complexes in articular cartilages

Osteoarthritis and Cartilage

Volumn 15, Issue 7, 2007, Pages 719-734

  Plaas, A ^a,b   Osborn, B ^a   Yoshihara, Y ^a,d   Bai, Y ^a   Bloom, T ^c   Nelson, F ^c   Mikecz, K ^e   Sandy, J D ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c HENRY FORD HOSPITAL   (United States)

^d NATIONAL DEFENSE MEDICAL COLLEGE   (Japan)

^e RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

ADAMTS5; Aggrecanase; Cartilage; Confocal microscopy; Hyaluronan; Immunohistochemistry; Osteoarthritis

Indexed keywords

AGGRECAN; AGGRECANASE; BINDING PROTEIN; DISINTEGRIN; EDETIC ACID; ENZYME ANTIBODY; EPITOPE; FORMALDEHYDE; HYALURONIC ACID; HYALURONIDASE; METALLOPROTEINASE; N ACETYLGALACTOSAMINE 4 SULFATASE; PROTEIN ADAMTS1; PROTEIN ADAMTS15; PROTEIN ADAMTS4; PROTEIN ADAMTS5; PROTEIN ADAMTS8; PROTEIN ADAMTS9; PROTEINASE; UNCLASSIFIED DRUG;

AGED; ARTICLE; ARTICULAR CARTILAGE; BIOCHEMISTRY; CASE REPORT; CHROMATOGRAPHY; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; MALE; MOLECULAR WEIGHT; OSTEOARTHRITIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION; PROTEIN LOCALIZATION; TIBIA; WESTERN BLOTTING;

ADAM PROTEINS; AGED; AGGRECANS; CARTILAGE, ARTICULAR; CHONDROCYTES; ENDOPEPTIDASES; FEMALE; HUMANS; HYALURONIC ACID; MALE; MICROSCOPY, CONFOCAL; MIDDLE AGED; OSTEOARTHRITIS;

EID: 34249999133     PISSN: 10634584     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.joca.2006.12.008     Document Type: Article

References (76)

1. Sale J.E., Gignac M., and Hawker G. How "bad" does the pain have to be? A qualitative study examining adherence to pain medication in older adults with osteoarthritis. Arthritis Rheum 55 (2006) 272-278
2. Buckland-Wright J.C., Ward R.J., Peterfy C., Mojcik C.F., and Leff R.L. Reproducibility of the semiflexed (metatarsophalangeal) radiographic knee position and automated measurements of medial tibiofemoral joint space width in a multicenter clinical trial of knee osteoarthritis. J Rheumatol 31 (2004) 1588-1597
3. Roos E.M., and Dahlberg L. Positive effects of moderate exercise on glycosaminoglycan content in knee cartilage: a four-month, randomized, controlled trial in patients at risk of osteoarthritis. Arthritis Rheum 52 (2005) 3507-3514
4. Plaas A.H., West L.A., Wong-Palms S., and Nelson F.R. Glycosaminoglycan sulfation in human osteoarthritis. Disease-related alterations at the non-reducing termini of chondroitin and dermatan sulfate. J Biol Chem 273 (1998) 12642-12649
5. Sandy J.D., and Verscharen C. Analysis of aggrecan in human knee cartilage and synovial fluid indicates that aggrecanase (ADAMTS) activity is responsible for the catabolic turnover and loss of whole aggrecan whereas other protease activity is required for C-terminal processing in vivo. Biochem J 358 (2001) 615-626
6. Cs-Szabo G., Roughley P.J., Plaas A.H., and Glant T.T. Large and small proteoglycans of osteoarthritic and rheumatoid articular cartilage. Arthritis Rheum 38 (1995) 660-668
7. Kleemann R.U., Krocker D., Cedraro A., Tuischer J., and Duda G.N. Altered cartilage mechanics and histology in knee osteoarthritis: relation to clinical assessment (ICRS Grade). Osteoarthritis Cartilage 13 (2005) 958-963
8. Franz T., Hasler E.M., Hagg R., Weiler C., Jakob R.P., and Mainil-Varlet P. In situ compressive stiffness, biochemical composition, and structural integrity of articular cartilage of the human knee joint. Osteoarthritis Cartilage 9 (2001) 582-592
9. Pritzker K.P., Gay S., Jimenez S.A., Ostergaard K., Pelletier J.P., Revell P.A., et al. Osteoarthritis cartilage histopathology: grading and staging. Osteoarthritis Cartilage 14 (2006) 13-29
10. Nakamura Y., Nawata M., and Wakitani S. Expression profiles and functional analyses of Wnt-related genes in human joint disorders. Am J Pathol 167 (2005) 97-105
11. Bramlage C.P., Haupl T., Kaps C., Ungethum U., Krenn V., Pruss A., et al. Decrease in expression of bone morphogenetic proteins 4 and 5 in synovial tissue of patients with osteoarthritis and rheumatoid arthritis. Arthritis Res Ther 8 (2006) R58
12. Iwanaga H., Matsumoto T., Enomoto H., Okano K., Hishikawa Y., Shindo H., et al. Enhanced expression of insulin-like growth factor-binding proteins in human osteoarthritic cartilage detected by immunohistochemistry and in situ hybridization. Osteoarthritis Cartilage 13 (2005) 439-448
13. Loeser R.F., Yammani R.R., Carlson C.S., Chen H., Cole A., Im H.J., et al. Articular chondrocytes express the receptor for advanced glycation end products: potential role in osteoarthritis. Arthritis Rheum 52 (2005) 2376-2385
14. Wang X., Manner P.A., Horner A., Shum L., Tuan R.S., and Nuckolls G.H. Regulation of MMP-13 expression by RUNX2 and FGF2 in osteoarthritic cartilage. Osteoarthritis Cartilage 12 (2004) 963-973
15. Veje K., Hyllested-Winge J.L., and Ostergaard K. Topographic and zonal distribution of tenascin in human articular cartilage from femoral heads: normal versus mild and severe osteoarthritis. Osteoarthritis Cartilage 11 (2003) 217-227
16. White A.H., Watson R.E., Newman B., Freemont A.J., and Wallis G.A. Annexin VIII is differentially expressed by chondrocytes in the mammalian growth plate during endochondral ossification and in osteoarthritic cartilage. J Bone Miner Res 17 (2002) 1851-1858
17. Matsuo M., Nishida K., Yoshida A., Murakami T., and Inoue H. Expression of caspase-3 and -9 relevant to cartilage destruction and chondrocyte apoptosis in human osteoarthritic cartilage. Acta Med Okayama 55 (2001) 333-340
18. Yudoh K., Nguyen T., Nakamura H., Hongo-Masuko K., Kato T., and Nishioka K. Potential involvement of oxidative stress in cartilage senescence and development of osteoarthritis: oxidative stress induces chondrocyte telomere instability and downregulation of chondrocyte function. Arthritis Res Ther 7 (2005) R380-R391
19. Yagi R., McBurney D., Laverty D., Weiner S., and Horton Jr. W.E. Intrajoint comparisons of gene expression patterns in human osteoarthritis suggest a change in chondrocyte phenotype. J Orthop Res 23 (2005) 1128-1138
20. Tchetina E.V., Squires G., and Poole A.R. Increased type II collagen degradation and very early focal cartilage degeneration is associated with upregulation of chondrocyte differentiation related genes in early human articular cartilage lesions. J Rheumatol 32 (2005) 876-886
21. Blanco F.J., Guitian R., Vazquez-Martul E., de Toro F.J., and Galdo F. Osteoarthritis chondrocytes die by apoptosis. A possible pathway for osteoarthritis pathology. Arthritis Rheum 41 (1998) 284-289
22. Sandy J. Proteolytic Degradation of Normal and Osteoarthritic Cartilage Matrix (2003), Oxford University Press, Oxford 82-92
23. Sandy J.D., Flannery C.R., Neame P.J., and Lohmander L.S. The structure of aggrecan fragments in human synovial fluid. Evidence for the involvement in osteoarthritis of a novel proteinase which cleaves the Glu 373-Ala 374 bond of the interglobular domain. J Clin Invest 89 (1992) 1512-1516
24. Thirunavukkarasu K., Pei Y., Moore T.L., Wang H., Yu X.P., Geiser A.G., et al. Regulation of the human ADAMTS-4 promoter by transcription factors and cytokines. Biochem Biophys Res Commun 345 (2006) 197-204
25. Tortorella M.D., Arner E.C., Hills R., Gormley J., Fok K., Pegg L., et al. ADAMTS-4 (aggrecanase-1): N-terminal activation mechanisms. Arch Biochem Biophys 444 (2005) 34-44
26. Gao G., Plaas A., Thompson V.P., Jin S., Zuo F., and Sandy J.D. ADAMTS4 (aggrecanase-1) activation on the cell surface involves C-terminal cleavage by glycosylphosphatidyl inositol-anchored membrane type 4-matrix metalloproteinase and binding of the activated proteinase to chondroitin sulfate and heparan sulfate on syndecan-1. J Biol Chem 279 (2004) 10042-10051
27. Yu W.H., Yu S., Meng Q., Brew K., and Woessner Jr. J.F. TIMP-3 binds to sulfated glycosaminoglycans of the extracellular matrix. J Biol Chem 275 (2000) 31226-31232
28. Gao G., Westling J., Thompson V.P., Howell T.D., Gottschall P.E., and Sandy J.D. Activation of the proteolytic activity of ADAMTS4 (aggrecanase-1) by C-terminal truncation. J Biol Chem 277 (2002) 11034-11041
29. Flannery C.R., Zeng W., Corcoran C., Collins-Racie L.A., Chockalingam P.S., Hebert T., et al. Autocatalytic cleavage of ADAMTS-4 (aggrecanase-1) reveals multiple glycosaminoglycan-binding sites. J Biol Chem 277 (2003) 42775-42780
30. Stewart M.C., Fosang A.J., Bai Y., Osborn B., Plaas A., and Sandy J.D. ADAMTS5-mediated aggrecanolysis in murine epiphyseal chondrocyte cultures. Osteoarthritis Cartilage 3 (2006) 3
31. Lemire JM, Patis C, Gordon L, Sandy JD, Toole BP, Weiss AS. Aggrecan expression is substantially and abnormally upregulated in Hutchinson-Gilford Progeria Syndrome dermal fibroblasts. Mech Ageing Dev, in press.
32. Mort J.S., Magny M.C., and Lee E.R. Cathepsin B: an alternative protease for the generation of an aggrecan 'metalloproteinase' cleavage neoepitope. Biochem J 335 Pt 3 (1998) 491-494
33. Lemons M.L., Sandy J.D., Anderson D.K., and Howland D.R. Intact aggrecan and fragments generated by both aggrecanase and metalloproteinase-like activities are present in the developing and adult rat spinal cord and their relative abundance is altered by injury. J Neurosci 21 (2001) 4772-4781
34. Oshita H., Sandy J.D., Suzuki K., Akaike A., Bai Y., Sasaki T., et al. Mature bovine articular cartilage contains abundant aggrecan that is C-terminally truncated at Ala719-Ala720, a site which is readily cleaved by m-calpain. Biochem J 382 (2004) 253-259
35. Sandy J.D. A contentious issue finds some clarity: on the independent and complementary roles of aggrecanase activity and MMP activity in human joint aggrecanolysis. Osteoarthritis Cartilage (2005)
36. Lark M.W., Gordy J.T., Weidner J.R., Ayala J., Kimura J.H., Williams H.R., et al. Cell-mediated catabolism of aggrecan. Evidence that cleavage at the "aggrecanase" site (Glu373-Ala374) is a primary event in proteolysis of the interglobular domain. J Biol Chem 270 (1995) 2550-2556
37. Richards J.S., Hernandez-Gonzalez I., Gonzalez-Robayna I., Teuling E., Lo Y., Boerboom D., et al. Regulated expression of ADAMTS family members in follicles and cumulus oocyte complexes: evidence for specific and redundant patterns during ovulation. Biol Reprod 72 (2005) 1241-1255
38. Tortorella M.D., Pratta M., Liu R.Q., Austin J., Ross O.H., Abbaszade I., et al. Sites of aggrecan cleavage by recombinant human aggrecanase-1 (ADAMTS-4). J Biol Chem 275 (2000) 18566-18573
39. Nelson F., Billinghurst R.C., Pidoux I., Reiner A., Langworthy M., McDermott M., et al. Early post-traumatic osteoarthritis-like changes in human articular cartilage following rupture of the anterior cruciate ligament. Osteoarthritis Cartilage 14 (2006) 114-119
40. Quinn T.M., Hunziker E.B., and Hauselmann H.J. Variation of cell and matrix morphologies in articular cartilage among locations in the adult human knee. Osteoarthritis Cartilage 13 (2005) 672-678
41. Sandy J, Westling J, Kenagy RD, Iruela-Arispe ML, Verscharen C, Rodriguez-Mazaneque JC, et al. Versican V1 proteolysis in human aorta in vivo occurs at the Glu441-Ala442 bond, a site which is cleaved by recombinant ADAMTS-1 and ADAMTS-4. J Biol Chem, in press.
42. Westling J., Gottschall P.E., Thompson V.P., Cockburn A., Perides G., Zimmermann D.R., et al. ADAMTS4 (aggrecanase-1) cleaves human brain versican V2 at Glu405-Gln406 to generate glial hyaluronate binding protein. Biochem J 377 (2004) 787-795
43. Sandy J.D., Westling J., Kenagy R.D., Iruela-Arispe M.L., Verscharen C., Rodriguez-Mazaneque J.C., et al. Versican V1 proteolysis in human aorta in vivo occurs at the Glu441-Ala442 bond, a site that is cleaved by recombinant ADAMTS-1 and ADAMTS-4. J Biol Chem 276 (2001) 13372-13378
44. Ripellino J.A., Bailo M., Margolis R.U., and Margolis R.K. Light and electron microscopic studies on the localization of hyaluronic acid in developing rat cerebellum. J Cell Biol 106 (1988) 845-855
45. Riccio M., Dembic M., Cinti C., and Santi S. Multifluorescence labeling and colocalization analyses. Methods Mol Biol 285 (2004) 171-177
46. Isogai Z., Ono R.N., Ushiro S., Keene D.R., Chen Y., Mazzieri R., et al. Latent transforming growth factor beta-binding protein 1 interacts with fibrillin and is a microfibril-associated protein. J Biol Chem 278 (2003) 2750-2757
47. Kang T., Nagase H., and Pei D. Activation of membrane-type matrix metalloproteinase 3 zymogen by the proprotein convertase furin in the trans-Golgi network. Cancer Res 62 (2002) 675-681
48. Lorenzo P., Bayliss M.T., and Heinegard D. Altered patterns and synthesis of extracellular matrix macromolecules in early osteoarthritis. Matrix Biol 23 (2004) 381-391
49. Bayliss M.T., Hutton S., Hayward J., and Maciewicz R.A. Distribution of aggrecanase (ADAMts 4/5) cleavage products in normal and osteoarthritic human articular cartilage: the influence of age, topography and zone of tissue. Osteoarthritis Cartilage 9 (2001) 553-560
50. Dai S.M., Shan Z.Z., Nakamura H., Masuko-Hongo K., Kato T., Nishioka K., et al. Catabolic stress induces features of chondrocyte senescence through overexpression of caveolin 1: possible involvement of caveolin 1-induced down-regulation of articular chondrocytes in the pathogenesis of osteoarthritis. Arthritis Rheum 54 (2006) 818-831
51. Holloway I., Kayser M., Lee D.A., Bader D.L., Bentley G., and Knight M.M. Increased presence of cells with multiple elongated processes in osteoarthritic femoral head cartilage. Osteoarthritis Cartilage 12 (2004) 17-24
52. Burrage P.S., Mix K.S., and Brinckerhoff C.E. Matrix metalloproteinases: role in arthritis. Front Biosci 11 (2006) 529-543
53. Zeng W., Corcoran C., Collins-Racie L.A., Lavallie E.R., Morris E.A., and Flannery C.R. Glycosaminoglycan-binding properties and aggrecanase activities of truncated ADAMTSs: comparative analyses with ADAMTS-5, -9, -16 and -18. Biochim Biophys Acta 1760 (2006) 517-524
54. Zhuo L., Hascall V.C., and Kimata K. Inter-alpha-trypsin inhibitor, a covalent protein-glycosaminoglycan-protein complex. J Biol Chem 279 (2004) 38079-38082
55. Yingsung W., Zhuo L., Morgelin M., Yoneda M., Kida D., Watanabe H., et al. Molecular heterogeneity of the SHAP-hyaluronan complex. Isolation and characterization of the complex in synovial fluid from patients with rheumatoid arthritis. J Biol Chem 278 (2003) 32710-32718
56. Yang B., Yang B.L., Savani R.C., and Turley E.A. Identification of a common hyaluronan binding motif in the hyaluronan binding proteins RHAMM, CD44 and link protein. EMBO J 13 (1994) 286-296
57. Cardin A.D., and Weintraub H.J. Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 9 (1989) 21-32
58. Kashiwagi M., Tortorella M., Nagase H., and Brew K. Timp-3 is a potent inhibitor of aggrecanase 1 (adam-ts4) and aggrecanase 2 (adam-ts5). J Biol Chem 276 (2001) 12501-12504
59. de la Motte C.A., Hascall V.C., Drazba J., Bandyopadhyay S.K., and Strong S.A. Mononuclear leukocytes bind to specific hyaluronan structures on colon mucosal smooth muscle cells treated with polyinosinic acid:polycytidylic acid: inter-alpha-trypsin inhibitor is crucial to structure and function. Am J Pathol 163 (2003) 121-133
60. Majors A.K., Austin R.C., de la Motte C.A., Pyeritz R.E., Hascall V.C., Kessler S.P., et al. Endoplasmic reticulum stress induces hyaluronan deposition and leukocyte adhesion. J Biol Chem 278 (2003) 47223-47231
61. Wang A., and Hascall V.C. Hyaluronan structures synthesized by rat mesangial cells in response to hyperglycemia induce monocyte adhesion. J Biol Chem 279 (2004) 10279-10285
62. Rugg M.S., Willis A.C., Mukhopadhyay D., Hascall V.C., Fries E., Fulop C., et al. Characterization of complexes formed between TSG-6 and inter-alpha-inhibitor that act as intermediates in the covalent transfer of heavy chains onto hyaluronan. J Biol Chem 280 (2005) 25674-25686
63. Glant T.T., Kamath R.V., Bardos T., Gal I., Szanto S., Murad Y.M., et al. Cartilage-specific constitutive expression of TSG-6 protein (product of tumor necrosis factor alpha-stimulated gene 6) provides a chondroprotective, but not antiinflammatory, effect in antigen-induced arthritis. Arthritis Rheum 46 (2002) 2207-2218
64. Forteza R., Lieb T., Aoki T., Savani R.C., Conner G.E., and Salathe M. Hyaluronan serves a novel role in airway mucosal host defense. Faseb J 15 (2001) 2179-2186
65. Stern R., and Jedrzejas M.J. Hyaluronidases: their genomics, structures, and mechanisms of action. Chem Rev 106 (2006) 818-839
66. Sztrolovics R., Recklies A.D., Roughley P.J., and Mort J.S. Hyaluronate degradation as an alternative mechanism for proteoglycan release from cartilage during interleukin-1beta-stimulated catabolism. Biochem J 362 (2002) 473-479
67. Glasson S.S., Askew R., Sheppard B., Carito B., Blanchet T., Ma H.L., et al. Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis. Nature 434 (2005) 644-648
68. Wachsmuth L., Bau B., Fan Z., Pecht A., Gerwin N., and Aigner T. ADAMTS-1, a gene product of articular chondrocytes in vivo and in vitro, is downregulated by interleukin 1beta. J Rheumatol 31 (2004) 315-320
69. Malfait A.M., Liu R.Q., Ijiri K., Komiya S., and Tortorella M.D. Inhibition of ADAM-TS4 and ADAM-TS5 prevents aggrecan degradation in osteoarthritic cartilage. J Biol Chem 277 (2002) 22201-22208
70. Demircan K., Hirohata S., Nishida K., Hatipoglu O.F., Oohashi T., Yonezawa T., et al. ADAMTS-9 is synergistically induced by interleukin-1beta and tumor necrosis factor alpha in OUMS-27 chondrosarcoma cells and in human chondrocytes. Arthritis Rheum 52 (2005) 1451-1460
71. Dickinson S.C., Vankemmelbeke M.N., Buttle D.J., Rosenberg K., Heinegard D., and Hollander A.P. Cleavage of cartilage oligomeric matrix protein (thrombospondin-5) by matrix metalloproteinases and a disintegrin and metalloproteinase with thrombospondin motifs. Matrix Biol 22 (2003) 267-278
72. Tortorella M.D., Arner E.C., Hills R., Easton A., Korte-Sarfaty J., Fok K., et al. Alpha2-macroglobulin is a novel substrate for ADAMTS-4 and ADAMTS-5 and represents an endogenous inhibitor of these enzymes. J Biol Chem 279 (2004) 17554-17561
73. Wang P., Tortorella M., England K., Malfait A.M., Thomas G., Arner E.C., et al. Proprotein convertase furin interacts with and cleaves pro-ADAMTS4 (aggrecanase-1) in the trans-Golgi network. J Biol Chem 279 (2004) 15434-15440
74. Koo B.H., Longpre J.M., Somerville R.P., Alexander J.P., Leduc R., and Apte S.S. Cell-surface processing of pro-ADAMTS9 by furin. J Biol Chem 281 (2006) 12485-12494
75. Morales T.I., and Hascall V.C. Correlated metabolism of proteoglycans and hyaluronic acid in bovine cartilage organ cultures. J Biol Chem 263 (1988) 3632-3638
76. Sandy JD, Bai Y, Shepard S, Masuda K. Human and bovine articular cartilages contain abundant aggrecan that is truncated in vivo by proteolysis at specific m-calpain-sensitive sites near the C-terminal end of the CS-1 domain. Osteoarthritis and Cartilage, submitted for publication.