ADAMTS-4 and ADAMTS-5: Key enzymes in osteoarthritis

Journal of Cellular Biochemistry

Volumn 112, Issue 12, 2011, Pages 3507-3514

  Verma, Priyanka ^a   Dalal, Krishna ^a  

^a ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

ADAMTS; Aggrecan; Aggrecanase; Aggrecanase inhibitors; Osteoarthritis

Indexed keywords

AGGRECAN; AGGRECANASE 1; AGGRECANASE 2; CHONDROITIN SULFATE; DIACEREIN; GLOBULAR PROTEIN; GLUCOSAMINE SULFATE; GLYCOSAMINOGLYCAN; HISTONE DEACETYLASE INHIBITOR; HYALURONIC ACID; PENTOSAN POLYSULFATE; TISSUE INHIBITOR OF METALLOPROTEINASE 3;

ANGIOGENESIS; ANTIINFLAMMATORY ACTIVITY; ARTICLE; DISEASE COURSE; DRUG EFFICACY; HUMAN; IMMOBILIZATION; JOINT FUNCTION; JOINT INSTABILITY; JOINT PROSTHESIS; NONHUMAN; OSTEOARTHRITIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION;

ADAM PROTEINS; AGGRECANS; ANIMALS; ENDOPEPTIDASES; HUMANS; OSTEOARTHRITIS; PROCOLLAGEN N-ENDOPEPTIDASE;

EID: 80055024288     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.23298     Document Type: Article

References (72)

1. Abbaszade I, Liu RQ, Yang F, Rosenfeld SA, Ross OH, Link JR, Ellis DM, Tortorella MD, Pratta MA, Hollis JM, Wynn R, Duke JL, George HJ, Hillman MC, Jr., Murphy K, Wiswall BH, Copeland RA, Decicco CP, Bruckner R, Nagase H, Itoh Y, Newton RC, Magolda RL, Trzaskos JM, Burn TC,. 1999. Cloning and characterization of ADAMTS11, an aggrecanase from the ADAMTS family. J Biol Chem 274: 23443-23450.
2. Apte SS,. 2004. A disintegrin-like and metalloprotease (reprolysin type) with thrombospondin type 1 motifs: The ADAMTS family. Cell Biol 36: 981-985. (Pubitemid 38501549)
3. Apte SS,. 2009. A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: Functions and mechanisms. J Biol Chem 284: 31493-31497.
4. Bondeson J, Wainwright SD, Lauder S, Amos N, Hughes CE,. 2006. The role of synovial macrophages and macrophage-produced cytokines in driving aggrecanases, matrix metalloproteinases, and other destructive and inflammatory responses in osteoarthritis. Arthritis Res Ther 8: R187.
5. Chan P-S, Caron JP, Orth MW,. 2006. Short-term gene expression changes in cartilage explants stimulated with interleukin beta plus glucosamine and chondroitin sulfate. J Rheumatol 33: 1329-1340. (Pubitemid 44025148)
6. Chan P-S, Caron JP, Orth MW,. 2007. Effects of glucosamine and chondroitin sulfate on bovine cartilage explants under long-term culture conditions. Am J Vet Res 68: 709-715. (Pubitemid 47162467)
7. Clark IM, Parker AE,. 2003. Metalloproteinases: Their role in arthritis and potential as therapeutic targets. Expert Opin Ther Targets 7: 19-34. (Pubitemid 36204586)
8. Collins-Racie LA, Flannery CR, Zeng W, Corcoran C, Annis-Freeman B, Agostino MJ, Arai M, DiBlasio-Smith E, Dorner AJ, Georgiadis KE, Jin M, Tan XY, Morris EA, LaVallie ER,. 2004. ADAMTS-8 exhibits aggrecanase activity and is expressed in human articular cartilage. Matrix Biol 23: 219-230. (Pubitemid 39013980)
9. Cooper C, Snow S, McAlindon TE, Kellingray S, Stuart B, Coggon D, Dieppe PA,. 2000. Risk factors for the incidence and progression of radiographic knee osteoarthritis. Arthritis Rheum 43: 995-1000. (Pubitemid 30368175)
10. Curtis CL, Rees SG, Little CB, Flannery CR, Hughes CE, Wilson C, Dent CM, Otterness IG, Harwood JL, Caterson B,. 2002. Pathologic indicators of degradation and inflammation in human osteoarthritic cartilage are abrogated by exposure to n-3 fatty acids. Arthritis Rheum 46: 1544-1553. (Pubitemid 34620201)
11. De Savi C, Pape A, Sawyer Y, Milne D, Davies C, Cumming JG, Ting A, Lamont S, Smith PD, Tart J, Page K, Moore P,. 2011. Orally active achiral N-hydroxyformamide inhibitors of ADAM-TS4 (aggrecanase-1) and ADAM-TS5 (aggrecanase-2) for the treatment of osteoarthritis. Bioorg Med Chem Lett 21: 3301-3306.
12. Doege KJ, Sasaki M, Kimura T, Yamada Y,. 1991. Complete coding sequence and deduced primary structure of the human cartilage large aggregating proteoglycan, aggrecan. Human-specific repeats, and additional alternatively spliced forms. J Biol Chem 266: 894-902. (Pubitemid 21907200)
13. Felson DT, Kim Y-J,. 2007. The futility of current approaches to chondroprotection. Arthritis Rheum 56: 1378-1383. (Pubitemid 46764064)
14. Flannery CR, Zeng W, Corcoran C, Collins-Racie LA, Chockalingam PS, Hebert T, McDonagh T, Crawford TK, Tomkinson KN, LaVallie ER, Morris EA,. 2002. Autocatalytic cleavage of ADAMTS-4 (Aggrecanase-1) reveals multiple glycosaminoglycan-binding sites. J Biol Chem 277: 42775-42780. (Pubitemid 35285651)
15. Fosang AJ, Rogerson FM, East CJ, Stanton H,. 2008. ADAMTS-5: The story so far. Eur Cell Mater 15: 11-26. (Pubitemid 351955729)
16. Fushimi K, Troeberg L, Nakamura H, Lim NH, Nagase H,. 2008. Functional differences of the catalytic and non-catalytic domains in human ADAMTS-4 and ADAMTS-5 in aggrecanolytic activity. J Biol Chem 283: 6706-6716.
17. Gao G, Westling J, Thompson VP, Howell TD, Gottschall PE, Sandy JD,. 2002. Activation of the proteolytic activity of ADAMTS4 (aggrecanase-1) by C-terminal truncation. J Biol Chem 277: 11034-11041. (Pubitemid 34952861)
18. Gendron C, Kashiwagi M, Lim NH, Enghild JJ, ThÃgersen IB, Hughes C, Caterson B, Nagase H,. 2007. Proteolytic activities of human ADAMTS-5: Comparative studies with ADAMTS-4. J Biol Chem 282: 18294-18306. (Pubitemid 47100219)
19. Gilbert AM, Bursavich MG, Lombardi S, Georgiadis KE, Reifenberg E, Flannery CR, Morris EA,. 2007. 5-((1H-pyrazol-4-yl)methylene)-2- thioxothiazolidin-4-one inhibitors of ADAMTS-5. Bioorg Med Chem Lett 17: 1189-1192. (Pubitemid 46240864)
20. Gilbert AM, Bursavich MG, Lombardi S, Georgiadis KE, Reifenberg E, Flannery CR, Morris EA,. 2008. N-((8-hydroxy-5-substituted-quinolin-7-yl) (phenyl)methyl)-2-phenyloxy/amino-acetamide inhibitors of ADAMTS-5 (Aggrecanase-2). Bioorg Med Chem Lett 18: 6454-6457.
21. Glasson SS, Askew R, Sheppard B, Carito BA, Blanchet T, Ma, H-L, Flannery CR, Kanki K, Wang E, Peluso D, Yang Z, Majumdar MK, Morris EA,. 2004. Characterization of and osteoarthritis susceptibility in ADAMTS-4-knockout mice. Arthritis Rheum 50: 2547-2558. (Pubitemid 39062716)
22. Glasson SS, Askew R, Sheppard B, Carito B, Blanchet T, Ma H-L, Flannery CR, Peluso D, Kanki K, Yang Z, Majumdar MK, Morris EA,. 2005. Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis. Nature 434: 644-648. (Pubitemid 40488556)
23. Hollander AP, Pidoux I, Reiner A, Rorabeck C, Bourne R, Poole AR,. 1995. Damage to type II collagen in aging and osteoarthritis starts at the articular surface, originates around chondrocytes, and extends into the cartilage with progressive degeneration. J Clin Invest 96: 2859-2869.
24. Hopper DW, Vera MD, How D, Sabatini J, Xiang JS, Ipek M, Thomason J, Hu Y, Feyfant E, Wang Q, Georgiadis KE, Reifenberg E, Sheldon RT, Keohan CC, Majumdar MK, Morris EA, Skotnicki J, Sum P-E,. 2009. Synthesis and biological evaluation of ((4-keto)-phenoxy)methyl biphenyl-4-sulfonamides: A class of potent aggrecanase-1 inhibitors. Bioorg Med Chem Lett 19: 2487-2491.
25. Hörber C, Büttner FH, Kern C, Schmiedeknecht G, Bartnik E,. 2000. Truncation of the amino-terminus of the recombinant aggrecan rAgg1mut leads to reduced cleavage at the aggrecanase site. Efficient aggrecanase catabolism may depend on multiple substrate interactions. Matrix Biol 19: 533-543.
26. Hurskainen TL, Hirohata S, Seldin MF, Apte SS,. 1999. ADAM-TS5, ADAM-TS6, and ADAM-TS7, novel members of a new family of zinc metalloproteases. General features and genomic distribution of the ADAM-TS family. J Biol Chem 274: 25555-25563.
27. Kashiwagi M, Enghild JJ, Gendron C, Hughes C, Caterson B, Itoh Y, Nagase H,. 2004. Altered proteolytic activities of ADAMTS-4 expressed by C-terminal processing. J Biol Chem 279: 10109-10119. (Pubitemid 38372615)
28. Kevorkian L, Young DA, Darrah C, Donell ST, Shepstone L, Porter S, Brockbank SMV, Edwards DR, Parker AE, Clark IM,. 2004. Expression profiling of metalloproteinases and their inhibitors in cartilage. Arthritis Rheum 50: 131-141. (Pubitemid 38084297)
29. Klimiuk PA, Sierakowski S, Domyslawska I, Chwiecko J,. 2004. Effect of repeated infliximab therapy on serum matrix metalloproteinases and tissue inhibitors of metalloproteinases in patients with rheumatoid arthritis. J Rheumatol 31: 238-242. (Pubitemid 38160743)
30. Koshy PJT, Lundy CJ, Rowan AD, Porter S, Edwards DR, Hogan A, Clark IM, Cawston TE,. 2002. The modulation of matrix metalloproteinase and ADAM gene expression in human chondrocytes by interleukin-1 and oncostatin M: A time-course study using real-time quantitative reverse transcription-polymerase chain reaction. Arthritis Rheum 46: 961-967. (Pubitemid 34303808)
31. Kuno K, Okada Y, Kawashima H, Nakamura H, Miyasaka M, Ohno H, Matsushima K,. 2000. ADAMTS-1 cleaves a cartilage proteoglycan, aggrecan. FEBS Lett 478: 241-245. (Pubitemid 30621625)
32. Kuno K, Bannai K, Hakozaki M, Matsushima K, Hirose K,. 2004. The carboxyl-terminal half region of ADAMTS-1 suppresses both tumorigenicity and experimental tumor metastatic potential. Biochem Biophys Res Commun 319: 1327-1333. (Pubitemid 38759556)
33. Little CB, Mittaz L, Belluoccio D, Rogerson FM, Campbell IK, Meeker CT, Bateman JF, Pritchard MA, Fosang AJ,. 2005. ADAMTS-1-knockout mice do not exhibit abnormalities in aggrecan turnover in vitro or in vivo. Arthritis Rheum 52: 1461-1472. (Pubitemid 40663938)
34. Liu C-J, Kong W, Ilalov K, Yu S, Xu K, Prazak L, Fajardo M, Sehgal B, Di Cesare PE,. 2006. ADAMTS-7: A metalloproteinase that directly binds to and degrades cartilage oligomeric matrix protein. FASEB J 20: 988-990.
35. Lohmander LS, Neame PJ, Sandy JD,. 1993. The structure of aggrecan fragments in human synovial fluid. Evidence that aggrecanase mediates cartilage degradation in inflammatory joint disease, joint injury, and osteoarthritis. Arthritis Rheum 36: 1214-1222. (Pubitemid 23303112)
36. Makihira S, Yan W, Murakami H, Furukawa M, Kawai T, Nikawa H, Yoshida E, Hamada T, Okada Y, Kato Y,. 2003. Thyroid hormone enhances aggrecanase-2/ADAM- TS5 expression and proteoglycan degradation in growth plate cartilage. Endocrinology 144: 2480-2488. (Pubitemid 36629900)
37. Malfait A-M, Liu R-Q, Ijiri K, Komiya S, Tortorella MD,. 2002. Inhibition of ADAM-TS4 and ADAM-TS5 prevents aggrecan degradation in osteoarthritic cartilage. J Biol Chem 277: 22201-22208. (Pubitemid 34967185)
38. Mankin HJ, Lippiello L,. 1970. Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. J Bone Joint Surg Am 52: 424-434.
39. Martel-Pelletier J, Welsch DJ, Pelletier JP,. 2001. Metalloproteases and inhibitors in arthritic diseases. Best Pract Res Clin Rheumatol 15: 805-829. (Pubitemid 34092514)
40. Massardo L, Watt I, Cushnaghan J, Dieppe P,. 1989. Osteoarthritis of the knee joint: An 8 year prospective study. Ann Rheum Dis 48: 893-897. (Pubitemid 19280910)
41. Matthews RT, Gary SC, Zerillo C, Pratta M, Solomon K, Arner EC, Hockfield S,. 2000. Brain-enriched hyaluronan binding (BEHAB)/brevican cleavage in a glioma cell line is mediated by a disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS) family member. J Biol Chem 275: 22695-22703. (Pubitemid 30648860)
42. Miwa HE, Gerken TA, Hering TM,. 2006. Effects of covalently attached chondroitin sulfate on aggrecan cleavage by ADAMTS-4 and MMP-13. Matrix Biol 25: 534-545. (Pubitemid 44751448)
43. Mosyak L, Georgiadis K, Shane T, Svenson K, Hebert T, McDonagh T, Mackie S, Olland S, Lin L, Zhong X, Kriz R, Reifenberg EL, Collins-Racie LA, Corcoran C, Freeman B, Zollner R, Marvell T, Vera M, Sum P-E, Lavallie ER, Stahl M, Somers W,. 2008. Crystal structures of the two major aggrecan degrading enzymes, ADAMTS4 and ADAMTS5. Protein Sci 17: 16-21.
44. Nagase H, Kashiwagi M,. 2003. Aggrecanases and cartilage matrix degradation. Arthritis Res Ther 5: 94-103. (Pubitemid 36849755)
45. Peng L, Duan L, Liu X, Shen M, Li Y, Yan J, Li H, Ding K,. 2011. Structure-activity study on a series of α-glutamic acid scaffold based compounds as new ADAMTS inhibitors. Bioorg Med Chem Lett 21: 4457-4461.
46. Porter S, Clark IM, Kevorkian L, Edwards DR,. 2005. The ADAMTS metalloproteinases. Biochem J 386: 15-27.
47. Powell AJ, Little CB, Hughes CE,. 2007. Low molecular weight isoforms of the aggrecanases are responsible for the cytokine-induced proteolysis of aggrecan in a porcine chondrocyte culture system. Arthritis Rheum 56: 3010-3019. (Pubitemid 47502748)
48. Pratta MA, Tortorella MD, Arner EC,. 2000. Age-related changes in aggrecan glycosylation affect cleavage by aggrecanase. J Biol Chem 275: 39096-39102. (Pubitemid 32058924)
49. Pratta MA, Scherle PA, Yang G, Liu R-Q, Newton RC,. 2003. Induction of aggrecanase 1 (ADAM-TS4) by interleukin-1 occurs through activation of constitutively produced protein. Arthritis Rheum 48: 119-133. (Pubitemid 36091656)
50. Rodríguez-Manzaneque JC, Westling J, Thai SN-M, Luque A, Knauper V, Murphy G, Sandy JD, Iruela-Arispe M,. 2002. ADAMTS1 cleaves aggrecan at multiple sites and is differentially inhibited by metalloproteinase inhibitors. Biochem Biophys Res Commun 293: 501-508. (Pubitemid 34694236)
51. Roughley PJ, Barnett J, Zuo F, Mort JS,. 2003. Variations in aggrecan structure modulate its susceptibility to aggrecanases. Biochem J 375: 183-189. (Pubitemid 37255394)
52. Salzet M,. 2002. Leech thrombin inhibitors. Curr Pharm Des 8: 493-503. (Pubitemid 34449861)
53. Sandy JD, Flannery CR, Neame PJ, Lohmander LS,. 1992. 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: 1512-1516.
54. Sandy JD, Neame PJ, Boynton RE, Flannery CR,. 1991. Catabolism of aggrecan in cartilage explants. Identification of a major cleavage site within the interglobular domain. J Biol Chem 266: 8683-8685. (Pubitemid 21906567)
55. Shiozaki M, Maeda K, Miura T, Kotoku M, Yamasaki T, Matsuda I, Aoki K, Yasue K, Imai H, Ubukata M, Suma A, Yokota M, Hotta T, Tanaka M, Hase Y, Fryer AM, Laird ER, Littmann NM, Andrews SW, Josey JA, Mimura T, Shinozaki Y, Yoshiuchi H, Inaba T,. 2011. Discovery of (1S,2R,3R)-2,3-dimethyl-2-phenyl-1- sulfamidocyclopropanecarboxylates: Novel and highly selective aggrecanase inhibitors. J Med Chem 54: 2839-2863.
56. Somerville RPT, Longpre J-M, Jungers KA, Engle JM, Ross M, Evanko S, Wight TN, Leduc R, Apte SS,. 2003. Characterization of ADAMTS-9 and ADAMTS-20 as a distinct ADAMTS subfamily related to Caenorhabditis elegans GON-1. J Biol Chem 278: 9503-9513. (Pubitemid 36800443)
57. Song R-H, Tortorella MD, Malfait A-M, Alston JT, Yang Z, Arner EC, Griggs DW,. 2007. Aggrecan degradation in human articular cartilage explants is mediated by both ADAMTS-4 and ADAMTS-5. Arthritis Rheum 56: 575-585.
58. Spector TD, Dacre JE, Harris PA, Huskisson EC,. 1992. Radiological progression of osteoarthritis: An 11 year follow up study of the knee. Ann Rheum Dis 51: 1107-1110.
59. Stanton H, Rogerson FM, East CJ, Golub SB, Lawlor KE, Meeker CT, Little CB, Last K, Farmer PJ, Campbell IK, Fourie AM, Fosang AJ,. 2005. ADAMTS5 is the major aggrecanase in mouse cartilage in vivo and in vitro. Nature 434: 648-652. (Pubitemid 40488557)
60. Sugimoto K, Takahashi M, Yamamoto Y, Shimada K, Tanzawa K,. 1999. Identification of aggrecanase activity in medium of cartilage culture. J Biochem 126: 449-455. (Pubitemid 29408218)
61. Tortorella MD, Burn TC, Pratta MA, Abbaszade I, Hollis JM, Liu R, Rosenfeld SA, Copeland RA, Decicco CP, Wynn R, Rockwell A, Yang F, Duke JL, Solomon K, George H, Bruckner R, Nagase H, Itoh Y, Ellis DM, Ross H, Wiswall BH, Murphy K, Hillman MC, Jr., Hollis GF, Newton RC, Magolda RL, Trzaskos JM, Arner EC,. 1999. Purification and cloning of aggrecanase-1: A member of the ADAMTS family of proteins. Science 284: 1664-1666. (Pubitemid 29291375)
62. Tortorella MD, Malfait AM, Deccico C, Arner E,. 2001. The role of ADAM-TS4 (aggrecanase-1) and ADAM-TS5 (aggrecanase-2) in a model of cartilage degradation. Osteoarthr Cartil 9: 539-552. (Pubitemid 32842633)
63. Tortorella MD, Pratta M, Liu RQ, Austin J, Ross OH, Abbaszade I, Burn T, Arner E,. 2000a. Sites of aggrecan cleavage by recombinant human aggrecanase-1 (ADAMTS-4). J Biol Chem 275: 18566-18573. (Pubitemid 30414819)
64. Tortorella M, Pratta M, Liu RQ, Abbaszade I, Ross H, Burn T, Arner E,. 2000b. The thrombospondin motif of aggrecanase-1 (ADAMTS-4) is critical for aggrecan substrate recognition and cleavage. J Biol Chem 275: 25791-25797.
65. Tortorella MD, Tomasselli AG, Mathis KJ, Schnute ME, Woodard SS, Munie G, Williams JM, Caspers N, Wittwer AJ, Malfait A-M, Shieh H-S,. 2009. Structural and inhibition analysis reveals the mechanism of selectivity of a series of aggrecanase inhibitors. J Biol Chem 284: 24185-24191.
66. Watanabe H, Yamada Y, Kimata K,. 1998. Roles of aggrecan, a large chondroitin sulfate proteoglycan, in cartilage structure and function. J Biochem 124: 687-693. (Pubitemid 28488144)
67. Yamaji N, Nishimura K, Abe K,. 2004. Metalloprotease having aggrecanase activity. US patent 6716613.
68. Yamanishi Y, Boyle DL, Clark M, Maki RA, Tortorella MD, Arner EC, Firestein GS,. 2002. Expression and regulation of aggrecanase in arthritis: The role of TGF-beta. J Immunol 168: 1405-1412. (Pubitemid 34094512)
69. Yao W, Wasserman ZR, Chao M, Reddy G, Shi E, Liu RQ, Covington MB, Arner EC, Pratte MA, Tortorella M, Magolda RL, Newton R, Qian M, Ribadeneira MD, Christ D, Wexler RR, Decicco CP,. 2001. Design and synthesis of a series of (2R)-N(4)-hydroxy-2-(3-hydroxybenzyl)-N(1)-[(1S,2R)-2-hydroxy-2, 3-dihydro-1H-inden-1-yl]butanediamide derivatives as potent, selective, and orally bioavailable aggrecanase inhibitors. J Med Chem 44: 3347-3350. (Pubitemid 32947900)
70. Yao W, Chao M, Wasserman ZR, Liu RQ, Covington MB, Newton R, Christ D, Wexler RR, Decicco CP,. 2002. Potent P1' biphenylmethyl substituted aggrecanase inhibitors. Bioorg Med Chem Lett 12: 101-104. (Pubitemid 34008579)
71. Young DA, Lakey RL, Pennington CJ, Jones D, Kevorkian L, Edwards DR, Cawston TE, Clark IM,. 2005. Histone deacetylase inhibitors modulate metalloproteinase gene expression in chondrocytes and block cartilage resorption. Arthritis Res Ther 7: R503-R512.
72. Zeng W, Corcoran C, Collins-Racie LA, Lavallie ER, Morris EA, Flannery CR,. 2006. Glycosaminoglycan-binding properties and aggrecanase activities of truncated ADAMTSs: Comparative analyses with ADAMTS-5, -9, -16 and -18. Biochim Biophys Acta 1760: 517-524.