Role of Cysteine Cathepsins in Extracellular Proteolysis

Biology of Extracellular Matrix

Volumn 2, Issue , 2011, Pages 23-51

  Brömme, Dieter ^a   Wilson, Susan ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Cathepsin Activity; Collagenase Activity; Cysteine Cathepsin; Human Cathepsin; Resorption Lacuna

Indexed keywords

EID: 84879769698     PISSN: 08873224     EISSN: 21911959     Source Type: Book Series    
DOI: 10.1007/978-3-642-16861-1_2     Document Type: Chapter

References (185)

1. Abrahamson M, Alvarez-Fernandez M, Nathanson CM (2003) Cystatins. Biochem Soc Symp: 179–199
2. Aoyagi T, Takeuchi T, Matsuzaki A, Kawamura K, Kondo S (1969) Leupeptins, new protease inhibitors from Actinomycetes. J Antibiot Tokyo 22:283–286
3. Atley LM, Mort JS, Lalumiere M, Eyre DR (2000) Proteolysis of human bone collagen by cathepsin K: characterization of the cleavage sites generating by cross-linked N-telopeptide neoepitope. Bone 26:241–247
4. Baumgrass R, Williamson MK, Price PA (1997) Identification of peptide fragments generated by digestion of bovine and human osteocalcin with the lysosomal proteinases cathepsin B, D, L, H and S. J Bone Miner Res 12:447–455
5. Bervar A, Zajc I, Sever N, Katunuma N, Sloane BF, Lah TT (2003) Invasiveness of transformed human breast epithelial cell lines is related to cathepsin B and inhibited by cysteine proteinase inhibitors. Biol Chem 384:447–455
6. Bossard MJ, Tomaszek TT, Thompson SK, Amegadzies BY, Hannings CR, Jones C, Kurdyla JT, McNulty DE, Drake FH, Gowen M, Levy MA (1996) Proteolytic activity of human osteoclast cathepsin K. Expression, purification, activation, and substrate identification. J Biol Chem 271:12517–12524
7. Brinckerhoff CE, Matrisian LM (2002) Matrix metalloproteinases: a tail of a frog that became a prince. Nat Rev Mol Cell Biol 3:207–214
8. Brix K, Dunkhorst A, Mayer K, Jordans S (2008) Cysteine cathepsins: cellular roadmap to different functions. Biochimie 90:194–207
9. Bromme D, Lecaille F (2009) Cathepsin K inhibitors for osteoporosis and potential off-target effects. Expert Opin Investig Drugs 18:585–600
10. 2, a novel cysteine protease highly expressed in osteoclastomas and ovary molecular cloning, sequencing and tissue distribution. Biol Chem Hoppe Seyler 376:379–384
11. Bromme D, Bonneau PR, Lachance P, Wiederanders B, Kirschke H, Peters C, Thomas DY, StorerAC, Vernet T (1993) Functional expression of human cathepsin S in Saccharomyces cerevisiae. Purification and characterization of the recombinant enzyme. J Biol Chem 268:4832–4838
12. 2 in Spodoptera frugiperda and characterization of the enzyme. J Biol Chem 271:2126–2132
13. Br€omme D, Li Z, Barnes M, Mehler E (1999) Human cathepsin V functional expression, tissue distribution, electrostatic surface potential, enzymatic characterization, and chromosomal localization. Biochemistry 38:2377–2385
14. Buck MR, Karustis DG, Day NA, Honn KV, Sloane BF (1992) Degradation of extracellularmatrix proteins by human cathepsin B from normal and tumour tissues. Biochem J 282 (Pt 1):273–278
15. Buhling F, Rocken C, Brasch F, Hartig R, Yasuda Y, Saftig P, Bromme D, Welte T (2004a) Pivotal role of cathepsin K in lung fibrosis. Am J Pathol 164:2203–2216
16. Buhling F, Waldburg N, Reisenauer A, Heimburg A, Golpon H, Welte T (2004b) Lysosomal cysteine proteases in the lung: role in protein processing and immunoregulation. Eur Respir J 23:620–628
17. Burrage PS, Mix KS, Brinckerhoff CE (2006) Matrix metalloproteinases: role in arthritis. Front Biosci 11:529–543
18. Butler GS, Overall CM (2009) Updated biological roles for matrix metalloproteinases and new “intracellular” substrates revealed by degradomics. Biochemistry 48:10830–10845
19. Buttle DJ, Saklatvala J, Tamai M, Barrett AJ (1992) Inhibition of interleukin 1-stimulated cartilage proteoglycan degradation by a lipophilic inactivator of cysteine endopeptidases. Biochem J 281:175–177
20. Buttle DJ, Handley CJ, Ilic MZ, Saklatvala J, Murata M, Barrett AJ (1993) Inhibition of cartilage proteoglycan release by a specific inactivator of cathepsin B and an inhibitor of matrix metalloproteinases. Evidence for two converging pathways of chondrocyte-mediated proteoglycan degradation. Arthritis Rheum 36:1709–1717
21. Cheng XW, Kuzuya M, Nakamura K, Di Q, Liu Z, Sasaki T, Kanda S, Jin H, Shi GP, Murohara T, Yokota M, Iguchi A (2006) Localization of cysteine protease, cathepsin S, to the surface of vascular smooth muscle cells by association with integrin alphanubeta3. Am J Pathol 168:685–694
22. Choe Y, Leonetti F, Greenbaum DC, Lecaille F, Bogyo M, Bromme D, Ellman JA, Craik CS (2006) Substrate profiling of cysteine proteases using a combinatorial peptide library identifies functionally unique specificities. J Biol Chem 281:12824–12832
23. Chung L, Shimokawa KI, Nagase H (2000) Structural requirements for collagenolytic activity of matrix metalloproteinase 1 (MMP-1). Kluwer Academic Publishers, Dordrecht, The Netherlands
24. Chung L, Dinakarpandian D, Yoshida N, Lauer-Fields JL, Fields GB, Visse R, Nagase H (2004) Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J 23:3020–3030
25. Colorado PC, Torre A, Kamphaus G, Maeshima Y, Hopfer H, Takahashi K, Volk R, Zamborsky ED, Herman S, Sarkar PK, Ericksen MB, Dhanabal M, Simons M, Post M, Kufe DW, Weichselbaum RR, Sukhatme VP, Kalluri R (2000) Anti-angiogenic cues from vascular basement membrane collagen. Cancer Res 60:2520–2526
26. Coulibaly S, Schwihla H, Abrahamson M, Albini A, Cerni C, Clark JL, Ng KM, Katunuma N, Schlappack O, Glossl J, Mach L (1999) Modulation of invasive properties of murine squamous carcinoma cells by heterologous expression of cathepsin B and cystatin C. Int J Cancer 83:526–531
27. de Nooijer R, Bot I, von der Thusen JH, Leeuwenburgh MA, Overkleeft HS, Kraaijeveld AO, Dorland R, van Santbrink PJ, van Heiningen SH, Westra MM, Kovanen PT, Jukema JW, van der Wall EE, van Berkel TJ, Shi GP, Biessen EA (2009) Leukocyte cathepsin S is a potent regulator of both cell and matrix turnover in advanced atherosclerosis. Arterioscler Thromb Vasc Biol 29:188–194
28. Deaton DN, Tavares FX (2005) Design of cathepsin K inhibitors for osteoporosis. Curr Top Med Chem 5:1639–1675
29. Dejica VM, Mort JS, Laverty S, Percival MD, Antoniou J, Zukor DJ, Poole AR (2008) Cleavage of type II collagen by cathepsin K in human osteoarthritic cartilage. Am J Pathol 173:161–169
30. Desmarais S, Black WC, Oballa R, Lamontagne S, Riendeau D, Tawa P, Duong le T, Pickarski M, Percival MD (2008) Effect of cathepsin k inhibitor basicity on in vivo off-target activities. Mol Pharmacol 73:147–156
31. Drake FH, Dodds RA, James IE, Connor JR, Debouck C, Richardson S, Lee-Rykaczewski E, Coleman L, Rieman D, Barthlow R, Hastings G, Gowen M (1996) Cathepsin K, but not cathepsins B, L, or S, is abundantly expressed in human osteoclasts. J Biol Chem 271:12511–12516
32. Engsig MT, Chen QJ, Vu TH, Pedersen AC, Therkidsen B, Lund LR, Henriksen K, Lenhard T, Foged NT, Werb Z, Delaisse JM (2000) Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones. J Cell Biol 151:879–889
33. Etherington DJ (1972) The nature of the collagenolytic cathepsin of rat liver and its distribution in other rat tissues. Biochem J 127:685–692
34. Etherington DJ, Evans PJ (1977) The action of cathepsin B and collagenolytic cathepsin in the degradation of collagen. Acta Biol Med Ger 36:1555–1563
35. Everts V, Beertsen W, Schroder R (1988) Effects of proteinase inhibitors leupeptin and E-64 on osteoclastic bone resorption. Calcif Tissue Int 43:172–178
36. Everts V, van der Zee E, Creemers L, Beertsen W (1996) Phagocytosis and intracellular digestion of collagen, its role in turnover and remodeling. Histochem J 28:229–245
37. Everts V, Korper W, Jansen DC, Steinfort J, Lammerse I, Heera S, Docherty AJ, Beertsen W (1999) Functional heterogeneity of osteoclasts: matrix metalloproteinases participate in osteoclastic resorption of calvarial bone but not in resorption of long bone. FASEB J 13:1219–1230
38. Everts V, Hou WS, Rialland X, Tigchelaar W, Saftig P, Bromme D, Gelb BD, Beertsen W (2003) Cathepsin K deficiency in pycnodysostosis results in accumulation of non-digested phagocytosed collagen in fibroblasts. Calcif Tissue Int 73:380–386
39. Falgueyret JP, Desmarais S, Oballa R, Black WC, Cromlish W, Khougaz K, Lamontagne S, Masse F, Riendeau D, Toulmond S, Percival MD (2005) Lysosomotropism of basic cathepsin K inhibitors contributes to increased cellular potencies against off-target cathepsins and reduced functional selectivity. J Med Chem 48:7535–7543
40. Felbor U, Dreier L, Bryant RA, Ploegh HL, Olsen BR, Mothes W (2000) Secreted cathepsin L generates endostatin from collagen XVIII. EMBO J 19:1187–1194
41. Fosang AJ, Neame PJ, Last K, Hardingham E, Murphy G, Hamilton JA (1992) The interglobular domain of cartilage aggrecan is cleaved by PUMP, gelatinases, and cathepsin B. J Biol Chem 267:19470–19474
42. Gal S, Willingham MC, Gottesman MM (1985) Processing and lysosomal localization of a glycoprotein whose secretion is transformation stimulated. J Cell Biol 100:535–544
43. Garnero P, Borel O, Byrjalsen I, Ferreras M, Drake FH, McQueney MS, Foged NT, Delmas PD, Delaisse JM (1998) The collagenolytic activity of cathepsin K is unique among mammalian proteinases. J Biol Chem 273:32347–32352
44. Gelb BD, Shi GP, Chapman HA, Desnick RJ (1996) Pycnodysostosis, a lysosomal disease caused by cathepsin K deficiency. Science 273:1236–1238
45. Gocheva V, Joyce JA (2007) Cysteine cathepsins and the cutting edge of cancer invasion. Cell Cycle 6:60–64
46. Gocheva V, Zeng W, Ke D, Klimstra D, Reinheckel T, Peters C, Hanahan D, Joyce JA (2006) Distinct roles for cysteine cathepsin genes in multistage tumorigenesis. Genes Dev 20:543–556
47. Godat E, Herve-Grvepinet V, Veillard F, Lecaille F, Belghazi M, Bromme D, Lalmanach G (2008) Regulation of cathepsin K activity by hydrogen peroxide. Biol Chem 389:1123–1126
48. Gravallese EM (2002) Bone destruction in arthritis. Ann Rheum Dis 61(Suppl 2):ii84–ii86
49. Guncar G, Podobnik M, Pungercar J, Strukelj B, Turk V, Turk D (1998) Crystal structure of porcine cathepsin H determined at 2.1 A resolution: location of the mini-chain C-terminal carboxyl group defines cathepsin H aminopeptidase function. Structure 6:51–61
50. Guncar G, Pungercic G, Klemencic I, Turk V, Turk D (1999) Crystal structure of MHC class IIassociated p41 Ii fragment bound to cathepsin L reveals the structural basis for differentiation between cathepsins L and S. EMBO J 18:793–803
51. Guncar G, Klemencic I, Turk B, Turk V, Karaoglanovic-Carmona A, Juliano L, Turk D (2000) Crystal structure of cathepsin X: a flip-flop of the ring of His23 allows carboxy-monopeptidase and carboxy-dipeptidase activity of the protease. Structure 8:305–313
52. Hanada K, Tamai M, Yamagish M (1978) Isolation and characterization of E-64, a new thiol protease inhibitor. Agric Biol Chem 42:523–528
53. He GA, Luo JX, Zhang TY, Wang FY, Li RF (2003) Canstatin-N fragment inhibits in vitro endothelial cell proliferation and suppresses in vivo tumor growth. Biochem Biophys Res Commun 312:801–805
54. Holliday LS, Welgus HG, Fliszar CJ, Veith GM, Jeffrey JJ, Gluck SL (1997) Initiation of osteoclast bone resorption by interstitial collagenase. J Biol Chem 272:22053–22058
55. Hou WS, Li Z, Gordon RE, Chan K, Klein MJ, Levy R, Keysser M, Keyszer G, Bromme D (2001) Cathepsin K is a critical protease in synovial fibroblast-mediated collagen degradation. Am J Pathol 159:2167–2177
56. Hou W-S, Li W, Keyszer G, Weber E, Levy R, Klein MJ, Gravallese EM, Goldring SR, Bromme D (2002) Comparison of cathepsins K and S expression within the rheumatoid and osteoarthritic synovium. Arthritis Rheum 46:663–674
57. Hou WS, Li Z, Buttner FH, Bartnik E, Bromme D (2003) Cleavage site specificity of cathepsin K toward cartilage proteoglycans and protease complex formation. Biol Chem 384:891–897
58. Isemura M, Yosizawa Z, Takahashi K, Kosaka H, Kojima N, Ono T (1981) Characterization of porcine plasma fibronectin and its fragmentation by porcine liver cathepsin B. J Biochem 90:1–9
59. Ishidoh K, Kominami E (1995) Procathepsin L degrades extracellular matrix proteins in the presence of glycosaminoglycans in vitro. Biochem Biophys Res Commun 217:624–631
60. Jedeszko C, Sloane BF (2004) Cysteine cathepsins in human cancer. Biol Chem 385:1017–1027
61. Jordans S, Jenko-Kokalj S, Kuhl NM, Tedelind S, Sendt W, Bromme D, Turk D, Brix K (2009) Monitoring compartment-specific substrate cleavage by cathepsins B, K, L, and S at physiological pH and redox conditions. BMC Biochem 10:23
62. Kafienah W, Bromme D, Buttle DJ, Croucher LJ, Hollander AP (1998) Human cathepsin K cleaves native type I and II collagens at the N-terminal end of the triple helix. Biochem J 331:727–732
63. Kamiya T, Kobayashi Y, Kanaoka K, Nakashima T, Kato Y, Mizuno A, Sakai H (1998) Fluorescence microscopic demonstration of cathepsin K activity as the major lysosomal cysteine proteinase in osteoclasts. J Biochem 123:752–759
64. Kamphaus GD, Colorado PC, Panka DJ, Hopfer H, Ramchandran R, Torre A, Maeshima Y, Mier JW, Sukhatme VP, Kalluri R (2000) Canstatin, a novel matrix-derived inhibitor of angiogenesis and tumor growth. J Biol Chem 275:1209–1215
65. Keeling WB, Armstrong PA, Stone PA, Bandyk DF, Shames ML (2005) An overview of matrix metalloproteinases in the pathogenesis and treatment of abdominal aortic aneurysms. Vasc Endovasc Surg 39:457–464
66. Kim TS, Tasker AS (2006) Non-covalent cathepsin K inhibitors for the treatment of osteoporosis. Curr Top Med Chem 6:355–360
67. Kirschke H, Schmidt I, Wiederanders B (1986) Cathepsin S. The cysteine proteinase from bovine lymphoid tissue is distinct from cathepsin L (EC 3.4.22.15). Biochem J 240:455–459
68. Kitamoto S, Sukhova GK, Sun J, Yang M, Libby P, Love V, Duramad P, Sun C, Zhang Y, Yang X, Peters C, Shi GP (2007) Cathepsin L deficiency reduces diet-induced atherosclerosis in lowdensity lipoprotein receptor-knockout mice. Circulation 115:2065–2075
69. Konttinen YT, Mandelin J, Li TF, Salo J, Lassus J, Liljestrom M, Hukkanen M, Takagi M, Virtanen I, Santavirta S (2002) Acidic cysteine endoproteinase cathepsin K in the degeneration of the superficial articular hyaline cartilage in osteoarthritis. Arthritis Rheum 46:953–960
70. Lackman RL, Jamieson AM, Griffith JM, Geuze H, Cresswell P (2007) Innate immune recognition triggers secretion of lysosomal enzymes by macrophages. Traffic 8:1179–1189
71. Lah TT, Buck MR, Honn KV, Crissman JD, Rao NC, Liotta LA, Sloan BF (1989) Degradation of laminin by human tumor cathepsin B. Clin Exp Metastasis 7:461–468
72. Lane TF, Sage EH (1994) The biology of SPARC, a protein that modulates cell-matrix interactions. FASEB J 8:163–173
73. Lecaille F, Choe Y, Brandt W, Li Z, Craik CS, Bromme D (2002a) Selective inhibition of the collagenolytic activity of human cathepsin K by altering its S2 subsite specificity. Biochemistry 41:8447–8454
74. Lecaille F, Kaleta J, Bromme D (2002b) Human and parasitic papain-like cysteine proteases: their role in physiology and pathology and recent developments in inhibitor design. Chem Rev 102:4459–4488
75. Levicar N, Strojnik T, Kos J, Dewey RA, Pilkington GJ, Lah TT (2002) Lysosomal enzymes, cathepsins in brain tumour invasion. J Neurooncol 58:21–32
76. Li Z, Hou WS, Bromme D (2000) Collagenolytic activity of cathepsin K is specifically modulated by cartilage-resident chondroitin sulfates. Biochemistry 39:529–536
77. Li Z, Hou WS, Escalante-Torres CR, Gelb BD, Bromme D (2002) Collagenase activity of cathepsin K depends on complex formation with chondroitin sulfate. J Biol Chem 277:28669–28676
78. Li Z, Yasuda Y, Li W, Bogyo M, Katz N, Gordon RE, Fields GB, Bromme D (2004) Regulation of collagenase activities of human cathepsins by glycosaminoglycans. J Biol Chem 279:5470–5479
79. Li Z, Kienetz M, Cherney MM, James MN, Bromme D (2008) The crystal and molecular structures of a cathepsin K:chondroitin sulfate complex. J Mol Biol 383:78–91
80. Lijnen HR (2003) Metalloproteinases in development and progression of vascular disease. Pathophysiol Haemost Thromb 33:275–281
81. Linnevers C, Smeekens SP, Bromme D (1997) Human cathepsin W, a putative cysteine protease predominantly expressed in CD8+ T-lymphocytes. FEBS Lett 405:253–259
82. Littlewood-Evans A, Kokubo T, Ishibashi O, Inaoka T, Wlodarski B, Gallagher JA, Bilbe G (1997) Localization of cathepsin K in human osteoclasts by in situ hybridization and immunohistochemistry. Bone 20:81–86
83. Liu J, Sukhova GK, Sun JS, Xu WH, Libby P, Shi GP (2004) Lysosomal cysteine proteases in atherosclerosis. Arterioscler Thromb Vasc Biol 24:1359–1366
84. Lutgens E, Lutgens SP, Faber BC, Heeneman S, Gijbels MM, de Winther MP, Frederik P, van der Made I, Daugherty A, Sijbers AM, Fisher A, Long CJ, Saftig P, Black D, Daemen MJ, Cleutjens KB (2006) Disruption of the cathepsin K gene reduces atherosclerosis progression and induces plaque fibrosis but accelerates macrophage foam cell formation. Circulation 113:98–107
85. Lutgens SP, Cleutjens KB, Daemen MJ, Heeneman S (2007) Cathepsin cysteine proteases in cardiovascular disease. FASEB J 21:3029–3041
86. Maciewicz RA, Etherington DJ (1988) A comparison of four cathepsins (B, L, N, and S) with collagenolytic activity from rabbit spleen. Biochem J 256:433–440
87. Maciewicz RA, Wotton SF (1991) Degradation of cartilage matrix components by the cysteine proteinases, cathepsins B and L. Biomed Biochim Acta 50:561–564
88. Maciewicz RA, Wotton SF, Etherington DJ, Duance VC (1990) Susceptibility of the cartilage collagens types II, IX and XI to degradation by the cysteine proteinases, cathepsins B and L. FEBS Lett 269:189–193
89. Mai J, Waisman DM, Sloane BF (2000) Cell surface complex of cathepsin B/annexin II tetramer in malignant progression. Biochim Biophys Acta 1477:215–230
90. Mai J, Sameni M, Mikkelsen T, Sloane BF (2002) Degradation of extracellular matrix protein tenascin-C by cathepsin B: an interaction involved in the progression of gliomas. Biol Chem 383:1407–1413
91. Mason RW (2008) Emerging functions of placental cathepsins. Placenta 29:385–390
92. Mason RW, Massey SD (1992) Surface activation of pro-cathepsin L. Biochem Biophys Res Commun 189:1659–1666
93. Mason RW, Johnson DA, Barrett AJ, Chapman HA (1986) Elastinolytic activity of human cathepsin L. Biochem J 233:925–927
94. Mason RW, Gal S, Gottesman MM (1987) The identification of the major excreted protein (MEP) from a transformed mouse fibroblast cell line as a catalytically active precursor form of cathepsin L. Biochem J 248:449–454
95. McGrath ME (1999) The lysosomal cysteine proteases. Annu Rev Biophys Biomol Struct 28:181–204
96. McGrath ME, Klaus JL, Barnes MG, Bromme D (1997) Crystal structure of human cathepsin K complexed with a potent inhibitor. Nat Struct Biol 4:105–109
97. McGrath ME, Palmer JT, Bromme D, Somoza JR (1998) Crystal structure of human cathepsin S. Protein Sci 7:1294–1302
98. McQuibban GA, Gong JH, Tam EM, McCulloch CA, Clark-Lewis I, Overall CM (2000) Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science 289:1202–1206
99. Mellor GW, Thomas EW, Topham CM, Brocklehurst K (1993) Ionization characteristics of the Cys-25/His-159 interactive system and of the modulatory group of papain: resolution of ambiguity by electronic perturbation of the quasi-2-mercaptopyridine leaving group in a new pyrimidyl disulphide reactivity probe. Biochem J 290(Pt 1):289–296
100. Miller EJ, Harris ED Jr, Chung E, Finch JE Jr, McCroskery PA, Butler WT (1976) Cleavage of Type II and III collagens with mammalian collagenase: site of cleavage and primary structure at the NH2-terminal portion of the smaller fragment released from both collagens. Biochemistry 15:787–792
101. Mohamed MM, Sloane BF (2006) Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev Cancer 6:764–775
102. Molgaard A, Arnau J, Lauritzen C, Larsen S, Petersen G, Pedersen J (2007) The crystal structure of human dipeptidyl peptidase I (cathepsin C) in complex with the inhibitor Gly-Phe-CHN2. Biochem J 401:645–650
103. Morrison CJ, Butler GS, Rodriguez D, Overall CM (2009) Matrix metalloproteinase proteomics: substrates, targets, and therapy. Curr Opin Cell Biol 21:645–653
104. Mort JS, Magny MC, Lee ER (1998) Cathepsin B: an alternative protease for the generation of an aggrecan ‘metalloproteinase’ cleavage neoepitope. Biochem J 335:491–494
105. Mudgett JS, Hutchinson NI, Chartrain NA, Forsyth AJ, McDonnell J, Singer II, Bayne EK, Flanagan J, Kawka D, Shen CF, Stevens K, Chen H, Trumbauer M, Visco DM (1998) Susceptibility of stromelysin 1-deficient mice to collagen-induced arthritis and cartilage destruction. Arthritis Rheum 41:110–121
106. Musil D, Zucic D, Turk D, Engh RA, Mayr I, Huber R, Popovic T, Turk V, Towatari T, Katunuma N, Bode W (1991) The refined 2.15 A X-ray crystal structure of human liver cathepsin B: the structural basis for its specificity. EMBO J 10:2321–2330
107. Naghavi M, John R, Naguib S, Siadaty MS, Grasu R, Kurian KC, van Winkle WB, Soller B, Litovsky S, Madjid M, Willerson JT, Casscells W (2002) pH Heterogeneity of human and rabbit atherosclerotic plaques; a new insight into detection of vulnerable plaque. Atherosclerosis 164:27–35
108. Nakagawa TY, Brissette WH, Lira PD, Griffiths RJ, Petrushova N, Stock J, McNeish JD, Eastman SE, Howard ED, Clarke SR, Rosloniec EF, Elliott EA, Rudensky AY (1999) Impaired invariant chain degradation and antigen presentation and diminished collagen-induced arthritis in cathepsin S null mice. Immunity 10:207–217
109. Newby AC (2006) Do metalloproteinases destabilize vulnerable atherosclerotic plaques? Curr Opin Lipidol 17:556–561
110. Nguyen Q, Mort JS, Roughley PJ (1990) Cartilage proteoglycan aggregate is degraded more extensively by cathepsin L than by cathepsin B. Biochem J 266:569–573
111. Nosaka AY, Kanaori K, Teno N, Togame H, Inaoka T, Takai M, Kokubo T (1999) Conformational studies on the specific cleavage site of Type I collagen (alpha-1) fragment (157–192) by cathepsins K and L by proton NMR spectroscopy. Bioorg Med Chem 7:375–379
112. Overall CM, Blobel CP (2007) In search of partners: linking extracellular proteases to substrates. Nat Rev Mol Cell Biol 8:245–257
113. Page AE, Hayman AR, Andersson LMB, Chambers TJ, Warburton MJ (1993) Degradation of bone matrix proteins by osteoclast cathepsins. Int J Biochem 25:545–550
114. Palermo C, Joyce JA (2008) Cysteine cathepsin proteases as pharmacological targets in cancer. Trends Pharmacol Sci 29:22–28
115. Parikka V, Lehenkari P, Sassi ML, Halleen J, Risteli J, Harkonen P, Vaananen HK (2001) Estrogen reduces the depth of resorption pits by disturbing the organic bone matrix degradation activity of mature osteoclasts. Endocrinology 142:5371–5378
116. Parsons SL, Watson SA, Brown PD, Collins HM, Steele RJ (1997) Matrix metalloproteinases. Br J Surg 84:160–166
117. Perdereau C, Godat E, Maurel MC, Hazouard E, Diot E, Lalmanach G (2006) Cysteine cathepsins in human silicotic bronchoalveolar lavage fluids. Biochim Biophys Acta 1762:351–356
118. Pham CT, Ley TJ (1999) Dipeptidyl peptidase I is required for the processing and activation of granzymes A and B in vivo. Proc Natl Acad Sci USA 96:8627–8632
119. Platt MO, Ankeny RF, Shi GP, Weiss D, Vega JD, Taylor WR, Jo H (2007) Expression of cathepsin K is regulated by shear stress in cultured endothelial cells and is increased in endothelium in human atherosclerosis. Am J Physiol Heart Circ Physiol 292: H1479–H1486
120. Podgorski I (2009) Future of anticathepsin K drugs: dual therapy for skeletal disease and atherosclerosis? Future Med Chem 1:21–34
121. Podgorski I, Linebaugh BE, Koblinski JE, Rudy DL, Herroon MK, Olive MB, Sloane BF (2009) Bone marrow-derived cathepsin K cleaves SPARC in bone metastasis. Am J Pathol 175:1255–1269
122. Polgar L, Halasz P (1982) Current problems in mechanistic studies of serine and cysteine proteinases. Biochem J 207:1–10
123. Premzl A, Zavasnik-Bergant V, Turk V, Kos J (2003) Intracellular and extracellular cathepsin B facilitate invasion of MCF-10A neoT cells through reconstituted extracellular matrix in vitro. Exp Cell Res 283:206–214
124. Pungercar JR, Caglic D, Sajid M, Dolinar M, Vasiljeva O, Pozgan U, Turk D, Bogyo M, Turk V, Turk B (2009) Autocatalytic processing of procathepsin B is triggered by proenzyme activity. FEBS J 276:660–668
125. Quintanilla-Dieck MJ, Codriansky K, Keady M, Bhawan J, Runger TM (2008) Cathepsin K in melanoma invasion. J Invest Dermatol 128:2281–2288
126. Reddy VY, Zhang QY, Weiss SJ (1995) Pericellular mobilization of the tissue-destructive cysteine proteinases, cathepsins B, L, and S, by human monocyte-derived macrophages. Proc Natl Acad Sci USA 92:3849–3853
127. Riese RJ, Chapman HA (2000) Cathepsins and compartmentalization in antigen presentation. Curr Opin Immunol 12:107–113
128. Riese RJ, Mitchell RN, Villadangos JA, Shi GP, Palmer JT, Karp ER, De Sanctis GT, Ploegh HL, Chapman HA (1998) Cathepsin S activity regulates antigen presentation and immunity. J Clin Invest 101:2351–2363
129. Rodan SB, Duong LT (2008) Cathepsin K-A New Molecular Target for Osteoporosis. IBMS BoneKEy 5:16–24
130. Roshy S, Sloane BF, Moin K (2003) Pericellular cathepsin B and malignant progression. Cancer Metastasis Rev 22:271–286
131. Roughley PJ, Barrett AJ (1977) The degradation of cartilage proteoglycans by tissue proteinases. Proteoglycan structure susceptibility proteolysis. Biochem J 167:629–637
132. Rozhin J, Sameni M, Ziegler G, Sloane BF (1994) Pericellular pH affects distribution and secretion of cathepsin B in malignant cells. Cancer Res 54:6517–6525
133. Runger TM, Quintanilla-Dieck MJ, Bhawan J (2007) Role of cathepsin K in the turnover of the dermal extracellular matrix during scar formation. J Invest Dermatol 127:293–297
134. Sameni M, Dosescu J, Moin K, Sloane BF (2003) Functional imaging of proteolysis: stromal and inflammatory cells increase tumor proteolysis. Mol Imaging 2:159–175
135. Samokhin AO, Wong A, Saftig P, Bromme D (2008) Role of cathepsin K in structural changes in brachiocephalic artery during progression of atherosclerosis in apoE-deficient mice. Atherosclerosis 200:58–68
136. Sato T, Foged NT, Delaisse JM (1998) The migration of purified osteoclasts through collagen is inhibited by matrix metalloproteinase inhibitors. J Bone Miner Res 13:59–66
137. Satoyoshi E (1992) Therapeutic trials on progressive muscular dystrophy. Intern Med 31:841–846
138. Schedel J, Seemayer CA, Pap T, Neidhart M, Kuchen S, Michel BA, Gay RE, Muller Ladner U, Gay S, Zacharias W (2004) Targeting cathepsin L (CL) by specific ribozymes decreases CL protein synthesis and cartilage destruction in rheumatoid arthritis. Gene Ther 11:1040–1047
139. Schonefuss A, Wendt W, Schattling B, Schulten R, Hoffmann K, Stuecker M, Tigges C, Lubbert H, Stichel C (2009) Upregulation of cathepsin S in psoriatic keratinocytes. Exp Dermatol
140. Seftor RE, Seftor EA, Koshikawa N, Meltzer PS, Gardner LM, Bilban M, Stetler-Stevenson WG, Quaranta V, Hendrix MJ (2001) Cooperative interactions of laminin 5 gamma2 chain, matrix metalloproteinase-2, and membrane type-1-matrix/metalloproteinase are required for mimicry of embryonic vasculogenesis by aggressive melanoma. Cancer Res 61:6322–6327
141. Selent J, Kaleta J, Li Z, Lalmanach G, Bromme D (2007) Selective inhibition of the collagenase activity of cathepsin K. J Biol Chem 282:16492–16501
142. Serveau-Avesque C, Martino MF, Herve-Grepinet V, Hazouard E, Gauthier F, Diot E, Lalmanach G (2006) Active cathepsins B, H, K, L and S in human inflammatory bronchoalveolar lavage fluids. Biol Cell 98:15–22
143. Shapiro SD (1994) Elastolytic metalloproteinases produced by human mononuclear phagocytes. Potential roles destructive lung disease. Am J Respir Crit Care Med 150:S160–S164
144. Shi GP, Munger JS, Meara JP, Rich DH, Chapman HA (1992) Molecular cloning and expression of human alveolar macrophage cathepsin S, an elastinolytic cysteine protease. J Biol Chem 267:7258–7262
145. Shi GP, Sukhova GK, Grubb A, Ducharme A, Rhode LH, Lee RT, Ridker PM, Libby P, Chapman HA (1999) Cystatin C deficiency in human atherosclerosis and aortic aneurysms. J Clin Invest 104:1191–1197
146. Shi GP, Bryant RA, Riese R, Verhelst S, Driessen C, Li Z, Bromme D, Ploegh HL, Chapman HA (2000) Role for cathepsin F in invariant chain processing and major histocompatibility complex class II peptide loading by macrophages. J Exp Med 191:1177–1186
147. Shi GP, Sukhova GK, Kuzuya M, Ye Q, Du J, Zhang Y, Pan JH, Lu ML, Cheng XW, Iguchi A, Perrey S, Lee AM, Chapman HA, Libby P (2003) Deficiency of the cysteine protease cathepsin S impairs microvessel growth. Circ Res 92:493–500
148. Silver IA (1975) Measurement of pH and ionic composition of pericellular sites. Philos Trans R Soc Lond B Biol Sci 271:261–272
149. Silver IA, Murrills RJ, Etherington DJ (1988) Microelectrode studies on acid microenvironment beneath adherent macrophages and osteoclasts. Exp Cell Res 175:266–276
150. Sires UI, Schmid TM, Fliszar CJ, Wang ZQ, Gluck SL, Welgus HG (1995) Complete degradation of type X collagen requires the combined action of interstitial collagenase and osteoclastderived cathepsin B. J Clin Invest 95:2089–2095
151. Somoza JR, Zhan H, Bowman KK, Yu L, Mortara KD, Palmer JT, Clark JM, McGrath ME (2000) Crystal structure of human cathepsin V. Biochemistry 39:12543–12551
152. Somoza JR, Palmer JT, Ho JD (2002) The crystal structure of human cathepsin F and its implications for the development of novel immunomodulators. J Mol Biol 322:559–568
153. Srivastava M, Steinwede K, Kiviranta R, Morko J, Hoymann HG, Langer F, Buhling F, Welte T, Maus UA (2008) Overexpression of cathepsin K in mice decreases collagen deposition and lung resistance in response to bleomycin-induced pulmonary fibrosis. Respir Res 9:54
154. Sukhova GK, Shi GP, Simon DI, Chapman HA, Libby P (1998) Expression of the elastolytic cathepsins S and K in human atheroma and regulation of their production in smooth muscle cells. J Clin Invest 102:576–583
155. Sukhova GK, Wang B, Libby P, Pan JH, Zhang Y, Grubb A, Fang K, Chapman HA, Shi GP (2005) Cystatin C deficiency increases elastic lamina degradation and aortic dilatation in apolipoprotein E-null mice. Circ Res 96:368–375
156. Svelander L, Erlandsson-Harris H, Astner L, Grabowska U, Klareskog L, Lindstrom E, Hewitt E (2009) Inhibition of cathepsin K reduces bone erosion, cartilage degradation and inflammation evoked by collagen-induced arthritis in mice. Eur J Pharmacol 613:155–162
157. Szpaderska AM, Frankfater A (2001) An intracellular form of cathepsin B contributes to invasiveness in cancer. Cancer Res 61:3493–3500
158. Tai IT, Tang MJ (2008) SPARC in cancer biology: its role in cancer progression and potential for therapy. Drug Resist Updat 11:231–246
159. Takahashi H, Ishidoh K, Muno D, Ohwada A, Nukiwa T, Kominami E, Kira S (1993) Cathepsin L activity is increased in alveolar macrophages and bronchoalveolar lavage fluid of smokers. Am Rev Respir Dis 147:1562–1568
160. Taleb S, Cancello R, Clément K, Lacasa D (2006) Cathepsin S promotes human preadipocyte differentiation: possible involvement of fibronectin degradation. Endocrinology 147:4950–4959
161. Tezuka K, Tezuka Y, Maejima A, Sato T, Nemoto K, Kamioka H, Hakeda Y, Kumegawa M (1994) Molecular cloning of a possible cysteine proteinase predominantly expressed in osteoclasts. J Biol Chem 269:1106–1109
162. Tolosa E, Li W, Yasuda Y, Wienhold W, Denzin LK, Lautwein A, Driessen C, Schnorrer P, Weber E, Stevanovic S, Kurek R, Melms A, Bromme D (2003) Cathepsin V is involved in the degradation of invariant chain in human thymus and is overexpressed in myasthenia gravis. J Clin Invest 112:517–526
163. Tortorella MD, Pratta M, Liu RQ, Austin J, Ross OH, Abbaszade I, Burn T, Arner E (2000) Sites of aggrecan cleavage by recombinant human aggrecanase-1 (ADAMTS-4). J Biol Chem 275:18566–18573
164. Turk B (2006) Targeting proteases: successes, failures and future prospects. Nat Rev Drug Discov 5:785–799
165. Turk V, Turk B, Turk D (2001) Lysosomal cysteine proteases: facts and opportunities. EMBO J 20:4629–4633
166. Umezawa H (1982) Low-molecular-weight enzyme inhibitors of microbial origin. Annu Rev Microbiol 36:75–99
167. Vasiljeva O, Dolinar M, Pungercar JR, Turk V, Turk B (2005) Recombinant human procathepsin S is capable of autocatalytic processing at neutral pH in the presence of glycosaminoglycans. FEBS Lett 579:1285–1290
168. Vasiljeva O, Reinheckel T, Peters C, Turk D, Turk V, Turk B (2007) Emerging roles of cysteine cathepsins in disease and their potential as drug targets. Curr Pharm Des 13:387–403
169. Velasco G, Ferrando AA, Puente XS, Sanchez LM, Lopez-Otin C (1994) Human cathepsin O. Molecular cloning from a breast carcinoma, production of the active enzyme in Escherichia coli, and expression analysis in human tissues. J Biol Chem 269:27136–27142
170. Vinardell T, Dejica V, Poole AR, Mort JS, Richard H, Laverty S (2008) Evidence to suggest that cathepsin K degrades articular cartilage in naturally occurring equine osteoarthritis. Osteoarthritis Cartilage 17:375–383
171. Wang B, Sun J, Kitamoto S, Yang M, Grubb A, Chapman HA, Kalluri R, Shi GP (2006) Cathepsin S controls angiogenesis and tumor growth via matrix-derived angiogenic factors. J Biol Chem 281:6020–6029
172. Watari M, Watari H, Nachamkin I, Strauss JF (2000) Lipopolysaccharide induces expression of genes encoding pro-inflammatory cytokines and the elastin-degrading enzyme, cathepsin S, in human cervical smooth-muscle cells. J Soc Gynecol Investig 7:190–198
173. Westling J, Fosang AJ, Last K, Thompson VP, Tomkinson KN, Hebert T, McDonagh T, Collins Racie LA, LaVallie ER, Morris EA, Sandy JD (2002) ADAMTS4 cleaves at the aggrecanase site (Glu373-Ala374) and secondarily at the matrix metalloproteinase site (Asn341-Phe342) in the aggrecan interglobular domain. J Biol Chem 277:16059–16066
174. Wex T, Buhling F, Wex H, Gunther D, Malfertheiner P, Weber E, Bromme D (2001) Human cathepsin W, a cysteine protease predominantly expressed in NK cells, is mainly localized in the endoplasmic reticulum. J Immunol 167:2172–2178
175. Wiederanders B, Kaulmann G, Schilling K (2003) Functions of propeptide parts in cysteine proteases. Curr Protein Pept Sci 4:309–326
176. Willstaetter R, Bamann E (1929) Ueber die Proteasen der Magenschleimhaut. Hoppe Seylers Z Physiol Chem 180:127–143
177. Wilson S, Hashamiyan S, Clarke L, Saftig P, Mort J, Dejica VM, Bromme D (2009a) Glycosaminoglycan-mediated loss of cathepsin K collagenolytic activity in MPS I contributes to osteoclast and growth plate abnormalities. Am J Pathol 175:2053–2062
178. Wilson SR, Peters C, Saftig P, Bromme D (2009b) Cathepsin K activity-dependent regulation of osteoclast actin ring formation and bone resorption. J Biol Chem 284:2584–2592
179. Xia L, Kilb J, Wex H, Lipyansky A, Breuil V, Stein L, Palmer JT, Dempster DW, Br€omme D (1999) Localization of rat cathepsin K in osteoclasts and resorption pits: Inhibition of bone resorption cathepsin K-activity by peptidyl vinyl sulfones. Biol Chem 380:679–687
180. Xin XQ, Gunesekera B, RW M (1992) The specificity and elastinolytic activities of bovine cathepsins S and H. Arch Biochem Biophys 299:334–349
181. Yamashita DS, Dodds RA (2000) Cathepsin K and the design of inhibitors of cathepsin K. Curr Pharm Des 6:1–24
182. Yasuda Y, Li Z, Greenbaum D, Bogyo M, Weber E, Bromme D (2004) Cathepsin V, a novel and potent elastolytic activity expressed in activated macrophages. J Biol Chem 279:36761–36770
183. Yasuda Y, Kaleta J, Bromme D (2005) The role of cathepsins in osteoporosis and arthritis: rationale for the design of new therapeutics. Adv Drug Deliv Rev 57:973–993
184. Zheng T, Zhu Z, Wang Z, Homer RJ, Ma B, Riese RJ Jr, Chapman HA Jr, Shapiro SD, Elias JA (2000) Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase-and cathepsin-dependent emphysema. J Clin Invest 106:1081–1093
185. Zucker S, Cao J, Chen WT (2000) Critical appraisal of the use of matrix metalloproteinase inhibitors in cancer treatment. Oncogene 19:6642–6650