Inhibition of cathepsin K reduces bone erosion, cartilage degradation and inflammation evoked by collagen-induced arthritis in mice

European Journal of Pharmacology

Volumn 613, Issue 1-3, 2009, Pages 155-162

  Svelander, Lena ^a   Erlandsson Harris, Helena ^a   Astner, Leif ^b   Grabowska, Urszula ^b   Klareskog, Lars ^a   Lindstrom, Erik ^b   Hewitt, Ellen ^b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b MEDIVIR AB   (Sweden)

Author keywords

Bone; Cartilage; Cathepsin K; Collagen induced arthritis; Inflammation; Rheumatoid arthritis

Indexed keywords

BIOLOGICAL MARKER; CARBOXY TERMINAL TELOPEPTIDE; CARTILAGE OLIGOMERIC MATRIX PROTEIN; CATHEPSIN K; CATHEPSIN K INHIBITOR; CATHEPSIN S; COLLAGEN; CRA 013788; DEOXYPYRIDINOLINE; L 006235; N [1 [[(CYANOMETHYL)AMINO]CARBONYL]CYCLOHEXYL] 4 [2(4 METHYLPIPERAZIN 1 YL) 1,3 THIAZOL 4 YL]BENZAMIDE; PROTEIN P10; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BONE DEFECT; BONE EROSION; CARTILAGE DEGENERATION; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME INHIBITION; FEMALE; HISTOPATHOLOGY; IC 50; INFLAMMATION; MOUSE; NONHUMAN; OSTEOCLAST; PRIORITY JOURNAL; PROTEIN ANALYSIS; RHEUMATOID ARTHRITIS; SPLEEN;

ANIMALS; ARTHRITIS, EXPERIMENTAL; BENZAMIDES; BIOLOGICAL MARKERS; BONE AND BONES; BONE RESORPTION; CARTILAGE; CATHEPSINS; COLLAGEN; FEMALE; HUMANS; INFLAMMATION; MICE; PROTEASE INHIBITORS; THIAZOLES;

EID: 65749098196     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2009.03.074     Document Type: Article

References (58)

1. Ahmed M., Bjurholm A., Srinivasan G.R., Lundeberg T., Theodorsson E., Schultzberg M., and Kreicbergs A. Capsaicin effects on substance P and CGRP in rat adjuvant arthritis. Regul. Pept. 55 (1995) 85-102
2. Andersson M., and Holmdahl R. Analysis of type II collagen-reactive T cells in the mouse. I. Different regulation of autoreactive vs. non-autoreactive anti-type II collagen T cells in the DBA/1 mouse. Eur. J. Immunol. 20 (1990) 1061-1066
3. Asagiri M., Hirai T., Kunigami T., Kamano S., Gober H.J., Okamoto K., Nishikawa K., Latz E., Golenbock D.T., Aoki K., Ohya K., Imai Y., Morishita Y., Miyazono K., Kato S., Saftig P., and Takayanagi H. Cathepsin K-dependent toll-like receptor 9 signaling revealed in experimental arthritis. Science 319 (2008) 624-627
4. Black W.C., and Percival M.D. The consequences of lysosomotropism on the design of selective cathepsin K inhibitors. Chembiochem 7 (2006) 1525-1535
5. Bossard M.J., Tomaszek T.A., Thompson S.K., Amegadzie B.Y., Hanning C.R., Jones C., Kurdyla J.T., McNulty D.E., Drake F.H., Gowen M., and Levy M.A. Proteolytic activity of human osteoclast cathepsin K. Expression, purification, activation, and substrate identification. J. Biol. Chem. 271 (1996) 12517-12524
6. Bromme D., Klaus J.L., Okamoto K., Rasnick D., and Palmer J.T. Peptidyl vinyl sulphones: a new class of potent and selective cysteine protease inhibitors: S2P2 specificity of human cathepsin O2 in comparison with cathepsins S and L. Biochem. J. 315 Pt 1 (1996) 85-89
7. Bugatti S., Codullo V., Caporali R., and Montecucco C. B cells in rheumatoid arthritis. Autoimmun. Rev. 7 (2007) 137-142
8. Cohen S.B., Dore R.K., Lane N.E., Ory P.A., Peterfy C.G., Sharp J.T., van der Heijde D., Zhou L., Tsuji W., and Newmark R. Denosumab treatment effects on structural damage, bone mineral density, and bone turnover in rheumatoid arthritis: a twelve-month, multicenter, randomized, double-blind, placebo-controlled, phase II clinical trial. Arthritis Rheum. 58 (2008) 1299-1309
9. Cope A.P., Schulze-Koops H., and Aringer M. The central role of T cells in rheumatoid arthritis. Clin. Exp. Rheumatol. 25 (2007) S4-11
10. Desmarais S., Black W.C., Oballa R., Lamontagne S., Riendeau D., Tawa P., Duong le T., Pickarski M., and Percival M.D. Effect of cathepsin k inhibitor basicity on in vivo off-target activities. Mol. Pharmacol. 73 (2008) 147-156
11. Falgueyret J.P., Desmarais S., Oballa R., Black W.C., Cromlish W., Khougaz K., Lamontagne S., Masse F., Riendeau D., Toulmond S., and Percival M.D. Lysosomotropism of basic cathepsin K inhibitors contributes to increased cellular potencies against off-target cathepsins and reduced functional selectivity. J. Med. Chem. 48 (2005) 7535-7543
12. Garnero P., Ferreras M., Karsdal M.A., Nicamhlaoibh R., Risteli J., Borel O., Qvist P., Delmas P.D., Foged N.T., and Delaisse J.M. The type I collagen fragments ICTP and CTX reveal distinct enzymatic pathways of bone collagen degradation. J. Bone Miner. Res. 18 (2003) 859-867
13. Gauthier J.Y., Chauret N., Cromlish W., Desmarais S., Duong le T., Falgueyret J.P., Kimmel D.B., Lamontagne S., Leger S., LeRiche T., Li C.S., Masse F., McKay D.J., Nicoll-Griffith D.A., Oballa R.M., Palmer J.T., Percival M.D., Riendeau D., Robichaud J., Rodan G.A., Rodan S.B., Seto C., Therien M., Truong V.L., Venuti M.C., Wesolowski G., Young R.N., Zamboni R., and Black W.C. The discovery of odanacatib (MK-0822), a selective inhibitor of cathepsin K. Bioorg. Med. Chem. Lett. 18 (2008) 923-928
14. Gelb B.D., Shi G.P., Chapman H.A., and Desnick R.J. Pycnodysostosis, a lysosomal disease caused by cathepsin K deficiency. Science 273 (1996) 1236-1238
15. Gowen M., Lazner F., Dodds R., Kapadia R., Feild J., Tavaria M., Bertoncello I., Drake F., Zavarselk S., Tellis I., Hertzog P., Debouck C., and Kola I. Cathepsin K knockout mice develop osteopetrosis due to a deficit in matrix degradation but not demineralization. J. Bone Miner. Res. 14 (1999) 1654-1663
16. Gravallese E.M. Bone destruction in arthritis. Ann. Rheum. Dis. 61 Suppl 2 (2002) ii84-86
17. Herrak P., Gortz B., Hayer S., Redlich K., Reiter E., Gasser J., Bergmeister H., Kollias G., Smolen J.S., and Schett G. Zoledronic acid protects against local and systemic bone loss in tumor necrosis factor-mediated arthritis. Arthritis Rheum. 50 (2004) 2327-2337
18. Hou W.S., Li Z., Gordon R.E., Chan K., Klein M.J., Levy R., Keysser M., Keyszer G., and Bromme D. Cathepsin k is a critical protease in synovial fibroblast-mediated collagen degradation. Am. J. Pathol. 159 (2001) 2167-2177
19. Hou W.S., Li W., Keyszer G., Weber E., Levy R., Klein M.J., Gravallese E.M., Goldring S.R., and Bromme D. Comparison of cathepsins K and S expression within the rheumatoid and osteoarthritic synovium. Arthritis Rheum. 46 (2002) 663-674
20. Hou W.S., Li Z., Buttner F.H., Bartnik E., and Bromme D. Cleavage site specificity of cathepsin K toward cartilage proteoglycans and protease complex formation. Biol. Chem. 384 (2003) 891-897
21. Hummel K.M., Petrow P.K., Franz J.K., Muller-Ladner U., Aicher W.K., Gay R.E., Bromme D., and Gay S. Cysteine proteinase cathepsin K mRNA is expressed in synovium of patients with rheumatoid arthritis and is detected at sites of synovial bone destruction. J. Rheumatol. 25 (1998) 1887-1894
22. Ibrahim S.M., Koczan D., and Thiesen H.J. Gene-expression profile of collagen-induced arthritis. J. Autoimmun. 18 (2002) 159-167
23. Jones G.C., Riley G.P., and Buttle D.J. The role of proteases in pathologies of the synovial joint. Int. J. Biochem. Cell Biol. 40 (2008) 1199-1218
24. Kirstein B., Grabowska U., Samuelsson B., Shiroo M., Chambers T.J., and Fuller K. A novel assay for analysis of the regulation of the function of human osteoclasts. J. Transl. Med. 4 (2006) 45
25. Kiviranta R., Morko J., Uusitalo H., Aro H.T., Vuorio E., and Rantakokko J. Accelerated turnover of metaphyseal trabecular bone in mice overexpressing cathepsin K. J. Bone Miner. Res. 16 (2001) 1444-1452
26. Kiviranta R., Morko J., Alatalo S.L., NicAmhlaoibh R., Risteli J., Laitala-Leinonen T., and Vuorio E. Impaired bone resorption in cathepsin K-deficient mice is partially compensated for by enhanced osteoclastogenesis and increased expression of other proteases via an increased RANKL/OPG ratio. Bone 36 (2005) 159-172
27. Kumar S., Dare L., Vasko-Moser J.A., James I.E., Blake S.M., Rickard D.J., Hwang S.M., Tomaszek T., Yamashita D.S., Marquis R.W., Oh H., Jeong J.U., Veber D.F., Gowen M., Lark M.W., and Stroup G. A highly potent inhibitor of cathepsin K (relacatib) reduces biomarkers of bone resorption both in vitro and in an acute model of elevated bone turnover in vivo in monkeys. Bone 40 (2007) 122-131
28. Larsson E., Erlandsson Harris H., Larsson A., Mansson B., Saxne T., and Klareskog L. Corticosteroid treatment of experimental arthritis retards cartilage destruction as determined by histology and serum COMP. Rheumatology (Oxford) 43 (2004) 428-434
29. Lubberts E., Oppers-Walgreen B., Pettit A.R., Van Den Bersselaar L., Joosten L.A., Goldring S.R., Gravallese E.M., and Van Den Berg W.B. Increase in expression of receptor activator of nuclear factor kappaB at sites of bone erosion correlates with progression of inflammation in evolving collagen-induced arthritis. Arthritis Rheum. 46 (2002) 3055-3064
30. Moreland L. Unmet needs in rheumatoid arthritis. Arthritis Res. Ther. 7 Suppl 3 (2005) S2-8
31. Morko J., Kiviranta R., Joronen K., Saamanen A.M., Vuorio E., and Salminen-Mankonen H. Spontaneous development of synovitis and cartilage degeneration in transgenic mice overexpressing cathepsin K. Arthritis Rheum. 52 (2005) 3713-3717
32. Nakagawa T.Y., Brissette W.H., Lira P.D., Griffiths R.J., Petrushova N., Stock J., McNeish J.D., Eastman S.E., Howard E.D., Clarke S.R., Rosloniec E.F., Elliott E.A., and Rudensky A.Y. Impaired invariant chain degradation and antigen presentation and diminished collagen-induced arthritis in cathepsin S null mice. Immunity 10 (1999) 207-217
33. Palmer J.T., Rasnick D., Klaus J.L., and Bromme D. Vinyl sulfones as mechanism-based cysteine protease inhibitors. J. Med. Chem. 38 (1995) 3193-3196
34. Pap T., Muller-Ladner U., Gay R.E., and Gay S. Fibroblast biology. Role of synovial fibroblasts in the pathogenesis of rheumatoid arthritis. Arthritis Res. 2 (2000) 361-367
35. Pettit A.R., Ji H., von Stechow D., Muller R., Goldring S.R., Choi Y., Benoist C., and Gravallese E.M. TRANCE/RANKL knockout mice are protected from bone erosion in a serum transfer model of arthritis. Am. J. Pathol. 159 (2001) 1689-1699
36. Podolin P.L., Bolognese B.J., Carpenter D.C., Davis T.G., Johanson R.A., Fox J.H., Long III E., Dong X., Marquis R.W., Locastro S.M., Terfloth G.J., Kurali E., Peterson J.J., Smith B.R., McQueney M.S., Yamashita D.S., and Capper-Spudich E.A. Inhibition of invariant chain processing, antigen-induced proliferative responses, and the development of collagen-induced arthritis and experimental autoimmune encephalomyelitis by a small molecule cysteine protease inhibitor. J. Immunol. 180 (2008) 7989-8003
37. Quibell M., and Taylor S. Preparation of furanone amino acid derivatives as inhibitors of cathepsin S. PCT Int. Appl. (2000) WO 2000069855
38. Riese R.J., Wolf P.R., Bromme D., Natkin L.R., Villadangos J.A., Ploegh H.L., and Chapman H.A. Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading. Immunity 4 (1996) 357-366
39. Riese R.J., Mitchell R.N., Villadangos J.A., Shi G.P., Palmer J.T., Karp E.R., De Sanctis G.T., Ploegh H.L., and Chapman H.A. Cathepsin S activity regulates antigen presentation and immunity. J. Clin. Invest. 101 (1998) 2351-2363
40. Romas E., Sims N.A., Hards D.K., Lindsay M., Quinn J.W., Ryan P.F., Dunstan C.R., Martin T.J., and Gillespie M.T. Osteoprotegerin reduces osteoclast numbers and prevents bone erosion in collagen-induced arthritis. Am. J. Pathol. 161 (2002) 1419-1427
41. Saftig P., Hunziker E., Wehmeyer O., Jones S., Boyde A., Rommerskirch W., Moritz J.D., Schu P., and von Figura K. Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc. Natl. Acad. Sci. U S A 95 (1998) 13453-13458
42. Saidenberg-Kermanac'h N., Corrado A., Lemeiter D., deVernejoul M.C., Boissier M.C., and Cohen-Solal M.E. TNF-alpha antibodies and osteoprotegerin decrease systemic bone loss associated with inflammation through distinct mechanisms in collagen-induced arthritis. Bone 35 (2004) 1200-1207
43. Salminen-Mankonen H.J., Morko J., and Vuorio E. Role of cathepsin K in normal joints and in the development of arthritis. Current Drug Targets 8 (2007) 315-323
44. Schett G. Review: Immune cells and mediators of inflammatory arthritis. Autoimmunity 41 (2008) 224-229
45. Schurigt U., Hummel K.M., Petrow P.K., Gajda M., Stockigt R., Middel P., Zwerina J., Janik T., Bernhardt R., Schuler S., Scharnweber D., Beckmann F., Saftig P., Kollias G., Schett G., Wiederanders B., and Brauer R. Cathepsin K deficiency partially inhibits, but does not prevent, bone destruction in human tumor necrosis factor-transgenic mice. Arthritis Rheum. 58 (2008) 422-434
46. Schwarz E.M., Looney R.J., Drissi M.H., O'Keefe R.J., Boyce B.F., Xing L., and Ritchlin C.T. Autoimmunity and bone. Ann N Y Acad Sci 1068 (2006) 275-283
47. Sims N.A., Green J.R., Glatt M., Schlict S., Martin T.J., Gillespie M.T., and Romas E. Targeting osteoclasts with zoledronic acid prevents bone destruction in collagen-induced arthritis. Arthritis Rheum. 50 (2004) 2338-2346
48. Skoumal M., Haberhauer G., Kolarz G., Hawa G., Woloszczuk W., and Klingler A. Serum cathepsin K levels of patients with longstanding rheumatoid arthritis: correlation with radiological destruction. Arthritis Res. Ther. 7 (2005) R65-70
49. Smith B.D., Martin G.R., Miller E.J., Dorfman A., and Swarm R. Nature of the collagen synthesized by a transplanted chondrosarcoma. Arch. Biochem. Biophys. 166 (1975) 181-186
50. Trentham D.E., Townes A.S., and Kang A.H. Autoimmunity to type II collagen an experimental model of arthritis. J. Exp. Med. 146 (1977) 857-868
51. van Lent P.L., Grevers L., Lubberts E., de Vries T.J., Nabbe K.C., Verbeek S., Oppers B., Sloetjes A., Blom A.B., and van den Berg W.B. Fcgamma receptors directly mediate cartilage, but not bone, destruction in murine antigen-induced arthritis: uncoupling of cartilage damage from bone erosion and joint inflammation. Arthritis Rheum. 54 (2006) 3868-3877
52. Vasiljeva O., Reinheckel T., Peters C., Turk D., Turk V., and Turk B. Emerging roles of cysteine cathepsins in disease and their potential as drug targets. Curr. Pharm. Des. 13 (2007) 387-403
53. Villadangos J.A., Bryant R.A., Deussing J., Driessen C., Lennon-Dumenil A.M., Riese R.J., Roth W., Saftig P., Shi G.P., Chapman H.A., Peters C., and Ploegh H.L. Proteases involved in MHC class II antigen presentation. Immunol. Rev. 172 (1999) 109-120
54. Votta B.J., Levy M.A., Badger A., Bradbeer J., Dodds R.A., James I.E., Thompson S., Bossard M.J., Carr T., Connor J.R., Tomaszek T.A., Szewczuk L., Drake F.H., Veber D.F., and Gowen M. Peptide aldehyde inhibitors of cathepsin K inhibit bone resorption both in vitro and in vivo. J. Bone Miner. Res. 12 (1997) 1396-1406
55. Weidauer E., Yasuda Y., Biswal B.K., Cherny M., James M.N., and Bromme D. Effects of disease-modifying anti-rheumatic drugs (DMARDs) on the activities of rheumatoid arthritis-associated cathepsins K and S. Biol. Chem. 388 (2007) 331-336
56. Yamane I., Hagino H., Okano T., Enokida M., Yamasaki D., and Teshima R. Effect of minodronic acid (ONO-5920) on bone mineral density and arthritis in adult rats with collagen-induced arthritis. Arthritis Rheum. 48 (2003) 1732-1741
57. Yasuda Y., Kaleta J., and Bromme D. The role of cathepsins in osteoporosis and arthritis: rationale for the design of new therapeutics. Adv. Drug Deliv. Rev. 57 (2005) 973-993
58. Yasuda Y., Tsukuba T., Okamoto K., Kadowaki T., and Yamamoto K. The role of the cathepsin E propeptide in correct folding, maturation and sorting to the endosome. J. Biochem. (Tokyo) 138 (2005) 621-630