Cathepsins in the osteoclast

Journal of Electron Microscopy

Volumn 52, Issue 6, 2003, Pages 551-558

  Goto, Tetsuya ^a   Yamaza, Takayoshi ^b   Tanaka, Teruo ^b  

^a KYUSHU DENTAL COLLEGE   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

Bone matrix; Bone resorption; Cathepsin; Cystatin; Osteoclast; Protease

Indexed keywords

CATHEPSIN;

ANIMAL; BONE MATRIX; ENZYMOLOGY; HUMAN; METABOLISM; MOUSE; OSTEOCLAST; OSTEOLYSIS; PHYSIOLOGY; RABBIT; RAT; REVIEW;

ANIMALS; BONE MATRIX; BONE RESORPTION; CATHEPSINS; HUMANS; MICE; OSTEOCLASTS; RABBITS; RATS;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

BONE; ENZYME ACTIVITY; MAMMALS;

BONE COLLAGEN; BONE MATRIX; BONE RESORPTION; CATHEPSIN; CYSTATINS; ORGANIC COMPONENTS; ORGANICS; OSTEOCLAST; PROTEASE; PROTEOLYTIC ACTIVITIES;

AMINO ACIDS;

EID: 0347093469     PISSN: 00220744     EISSN: None     Source Type: Journal    
DOI: 10.1093/jmicro/52.6.551     Document Type: Review

References (84)

1. Hedin S G (1904) Investigations on the proteolytic enzymes of the spleen of the ox. J. Physiol. 30: 155-175.
2. Dernby K G (1918) A study on autolysis of animal tissue. J. Biol. Chem. 35: 179-219.
3. Wilstatter R and Bamann E (1928) Über die proteasen der magenschleimhaut. Erste abhandlung über die enzyme der leukocyten. Z. Physiol. Chem. 180: 127-143.
4. Sakamoto M and Sakamoto S (1984) lmmunocytochemical localization of collagenase in isolated mouse bone cells. Biomed. Res. 5: 29-38.
5. Blair H C, Kahn A J, Crouch E C, Jeffrey J J, and Teitelbum S L (1986) Isolated osteodasts resorb the organic and inorganic components of bone. J. Cell Biol. 102: 1146-1172.
6. Vase G (1968) On the mechanisms of bone resorption. The action of parathyroid hormone on the extraction and synthesis of lysosomal enzymes and on the extracellular release of acid by bone cells. J. Cell Biol. 39: 676-679.
7. Delaissé J M, Eeckhout Y, and Vaes G (1984) In vivo and in vitro evidence for the involvement of cysteine proteinases in bone resorption. Biochem. Biophys. Res. Commun. 125: 441-447.
8. Delaissé J M, Eeckhout Y, and Vaes G (1980) Inhibition of bone resorption in culture by inhibitors of thiol proteinases. Biochem. J. 192: 365-368.
9. Etherington D J and Birkedahl-Hansen H (1987) The influence of dissolved calcium salts on the degradation of hard-tissue collagens by lysosomal cathepsins. Collagen Rel. Res. 7: 185-199.
10. Scott P G and Pearson H (1981) Cathepsin D: specificity of peptide bond cleavage in type-I collagen and effects of type-III collagen and procollagen. Eur. J. Biochem. 114: 59-62.
11. Baron R, Neff L, Brown W, Courtoy P J, Louvard D, and Farquhar M G (1988) Polarized secretion of lysosomal enzymes: co-distribution of cation-independent mannose-6-phosphate receptors and lysosomal enzymes along the osteoclast exocytic pathway J. Cell Biol. 106: 1863-1872.
12. Goto T, Tsukuba T, Ayasaka N, Yamamoto K, and Tanaka T (1992) Immunocytochemical localization of cathepsin D in the rat osteoclast. Histochemistry 97: 13-18.
13. Nishimura Y, Kawabata T, Yano S, and Kato K (1990) Intracellular processing and activation of lysosomal cathepsins. Acta Histochem. Cytochem. 23: 53-64.
14. Moroi R, Yamaza T, Ayukawa Y, Kiyoshima T, Ohsaki Y, Nishimura Y, Terada Y, Himeno M, and Tanaka T (1995) The changes in the immunocytochemical localization of cathepsin L and type I collagen in rat osteoclasts treated with E-64. Acta Histochem. Cytochem. 28: 523-531.
15. Lapresle C and Webb T (1962) Purification and properties of a proteolytic enzyme, rabbit cathepsin E, and further studies on rabbit cathepsin D. Biochem. J. 83: 455-462.
16. Stefanovic J, Webb T, and Lapresle C (1962) Etude des cathespines D et E dans des preparations de polynucleaires, de macrophages et de lymphocytes de lapin. Ann. Ins. Pasteur. 103: 276-284.
17. Yoshmine Y, Tsukuba T, Isobe R, Sumi M, Akamine A, Maeda K, and Yamamoto K (1995) Specific immunocytochemical localization of cathepsin E at the ruffled border membrane at active osteoclasts. Cell Tiss. Res. 281: 85-91.
18. Karrer K M, Peiffer S L, and DiTomas M E (1993) Two distinct gene subfamilies within the family of cysteine protease genes. Proc. Natl. Acad. Sci. USA 90: 3063-3067.
19. Berti P J and Storer A C (1995) Alignment/phylogeny of the papain superfamily of cysteine proteases. J. Mol. Biol. 246: 273-283.
20. Turk B, Turk D, and Turk V (2000) Lysosomal cysteine proteases: more than scavengers. Biochim. Biophys. Acta 1477: 98-111.
21. Delaissé J M, Boyde A, Maconnachie E, Ali N N, Sear C H J, Eeckhout Y, Vaes G, and Jones S J (1987) The effects of inhibitors of cysteine-proteinases and collagenases on the resorptive activity of isolated osteoclasts. Bone 8: 3005-3013.
22. Debari K, Sasaki T, Udagawa N, and Rifkin B R (1995) An ultrastructural evaluation of the effects of cysteine-proteinase inhibitors on osteoclastic resorptive functions. Calcif. Tiss. Int. 56: 566-570.
23. Millest A J, Breen S A, Loveday B E, Clarkson P N, Simpson C A, Waterton J C, and Johnstone D (1997) Effects of an inhibitor of cathepsin L on bone resorption in thyroparathyroidectomized and ovariectomized rat. Bone 20: 465-471.
24. Everts V, Beertsen W and Schroder R (1988) Effects of the proteinase inhibitors leupeptin and E-64 on osteoclastic bone resorption. Calcif. Tiss. Int. 43: 172-178.
25. Rifkin B R, Vernillo A T, Kleckner A P, Auszmann J M, Rosenberg L R, and Zimmerman M (1991) Cathepsin B and L activities in isolated osteoclasts. Biochem. Biophys. Res. Commun. 179: 63-69.
26. Goto T, Tsukuba T, Ayasaka N, Yamamoto K, and Tanaka T (1993) Immunohistochemical localization of cathepsin B, D, and L in the rat osteoclast. Histochemistry 99: 411-414.
27. Goto T, Kiyoshima T, Moroi R, Tsukuba T, Nishimura Y, Himeno M, Yamamoto K, and Tanaka T (1994) Localization of cathepsin B, D, and L in the rat osteoclast by immuno-light and -electron microscopy. Histochemistry 101: 33-40.
28. Sasaki T and Ueno-Matsuda E (1993) Cystein-proteinase localization in osteoclasts: an immunocytochemical study. Cell Tiss. Res. 271: 177-179.
29. Kakegawa H, Nikawa T, Tagami K, Kamioka H, Sumitani K, Kawata T, Drobnic-Kosorok M, Lenarcic B, Turk V, and Katunuma N (1993) Participation of cathepsin L on bone resorption. FEBS Lett. 321: 247-250.
30. Gutman H R and Fruton J S (1948) On the proteolytic enzymes of animal tissues VIII. An intracellular enzyme related to chymotrypsin. J. Biol. Chem. 174: 851-858.
31. Brown W J, Goodhouse J, and Farquhar M G (1986) Mannose-6-phosphate receptors for lysosomal enzymes cycle between the Golgi complex and endosomes. J. Cell Biol. 103: 1235-1247.
32. Pfeffer S (1987) The endosomal concentration of a mannose-6-phosphate receptor is unchanged in the absence of ligand synthesis. J. Cell Biol. 105: 229-234.
33. Inaoka T, Bilbe G, Ishibashi O, Tezuka K, Kumegawa M, and Kokubo T (1995) Molecular cloning of human cDNA for cathepsin K: novel cystein proteinase predominantly expressed in bone. Biochem. Biophys. Res. Commun. 206: 89-96.
34. Tezuka K, Tezuka Y, Maejima A, Sato T, Nemoto K, Kamioka H, Hakeda Y, and Kumegawa M (1994) Molecular cloning of a possible cysteine proteinase predominantly expressed in osteoclasts. J. Biol. Chem. 269: 1106-1109.
35. Brömme D and Okamoto K (1995) Human cathepsin O2, a novel cysteine proteinase highly expressed in osteoclastomas and ovary molecular cloning, sequencing and tissue distribution. Biol. Chem. Hoppe-Seyler 376: 379-384.
36. Shi G-P, Chapman H A, Bhairi S M, Deleeuw C, Reddy V Y, and Weiss S J (1995) Molecular cloning of human cathepsin O, a novel endoproteinase and homologue of rabbit OC2. FEBS Lett. 357: 129-134.
37. Li Y-P, Alexander M, Wucherpfenning A L, Yelick P, Chen W, and Stashenko P (1995) Cloning and complete coding sequence of a novel human cathepsin expressed in giant cells of osteoclastomas. J. Bone Miner. Res. 10: 1197-1202.
38. Rantakoko J, Aro H T, Savontaus M, and Vuorio E (1996) Mouse cathepsin K: cDNA cloning and predominant expression of the gene in osteoclasts, and in some hypertrophying chondrocytes during mouse development. FEBS Lett. 393: 307-311.
39. Gelb B D, Shi G P, Chapman H A, and Desnick RJ (1996) Pycnodysostosis, a lysosomal disease caused by cathepsin K deficiency. Science 273: 1236-1238.
40. Saftig P, Hunziker E, Wehmeyer O, Jones S, Boyde A, Rommerskirch W, Moritz J D, Schu P, and von Figura K (1998) Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc. Natl. Acad. Sci. USA 95: 13453-13458.
41. 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 (1999) Cathepsin K knockout mice develop osteopetrosis due to a deficit in matrix degradation but not demineralization. J. Bone Miner. Res. 14: 1654-1663.
42. Inui T, Ishibashi O, Inaoka T, Origane Y, Kumegawa M, Kokubo T, and Yamamura T (1997) Cathepsin K antisense oligodeoxynucleotide inhibits osteoclastic bone resorption. J. Biol. Chem. 272: 8109-8112.
43. Drake F H, Dodds R A, James I E, Connor J R, Debouck C, Richardson S, Lee-Rykaczewski E, Coleman L, Rieman D, Barthlow R, Hastings G, and Gowen M (1996) Cathepsin K, but not cathepsins B, L, or S, is abundantly expressed in human osteoclasts. J. Biol. Chem. 271: 12511-12516.
44. Littlewood-Evans A, Kokubo T, Ishibashi O, Inaoka T, Wlodarski B, Gallagher J A, and Bilbe G (1997) Localization of cathepsin K in human osteoclasts by in situ hybridization and immunohistochemistry. Bone 20: 81-86.
45. Ishibashi O, Inui T, Mori Y, Kurokawa T, Kokubo T, and Kumegawa M (2001) Quantification of the expression levels of lysosomal cysteine proteinases in purified human osteoclastic cells by competitive RT-PCR. Calcif. Tiss. Int. 68: 109-116.
46. Yamaza T, Goto T, Kamiya T, Kobayashi Y, Sakai H, and Tanaka T (1998) Study of immunoelectron microscopic localization of cathepsin K in osteoclasts and other bone cells in the mouse femur. Bone 23: 499-509.
47. Sahara T, Itoh K, Debari K, and Sasaki T (2003) Specific biological functions of vacuolar-type H(+)-ATPase and lysosomal cysteine proteinase, cathepsin K, in osteoclasts. Anat. Rec. 270A: 152-161.
48. Sasaki T (2003) Recent advances in the ultrastructural assessment of osteodastic resorptive functions. Microsc. Res. Tech. 33: 182-191.
49. Nakase T, Kaneko M, Tomita T, Myoui A, Ariga K, Sugamoto K, Uchiyama Y, Ochi T, and Yoshikawa H (2000) Immunohistochemical detection of cathepsin D, K, and L in the process of endochondral ossification in the human. Histochem. Cell Biol. 114: 21-27.
50. Punturieri A, Filippov S, Allen E, Caras I, Murray R, Reddy V, and Weiss S J (2000) Regulation of elastinolytic cysteine proteinase activity in normal and cathepsin K-deficient human macrophages. J. Exp. Med. 192: 789-799.
51. Shi G P, Sukhova G K, Grubb A, Ducharme A, Rhode L H, Lee R T, Ridker P M, Libby P, and Chapman H A (1999) Cystatin C deficiency in human atherosclerosis and aortic aneurysms. J. Clin. Invest. 104: 1191-1197.
52. Tepel C, Brömme D, Herzog V and Brix K (2000) Cathepsin K in thyroid epithelial cells: sequence, localization and possible function in extracellular proteolysis of thyroglobulin. J. Cell Sci. 113: 4487-4498.
53. Buhling F, Gerber A, Hackel C, Kruger S, Kohnlein T, Brömme D, Reinhold D, Ansorge S, and Welte T (1999) Expression of cathepsin K in lung epithelial cells. Am. J. Respir. Cell Mol. Biol. 20: 612-619.
54. Wolters P J and Chapman H A (2000) Importance of lysosomal cysteine proteases in lung disease. Respir. Res. 1: 170-177.
55. 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 (1996) Proteolytic activity of human osteoclast cathepsin K. Expression, purification, activation, and substrate identification. J. Biol. Chem. 271: 12517-12524.
56. Brömme D, Okamoto K, Wang B B, and Biroc S (1996) Human cathepsin O2, a matrix protein-degrading cysteine protease expressed in osteoclasts. Functional expression of human cathepsin O2 in Spodoptera frugiperda and characterization of the enzyme. J. Biol. Chem. 271: 2126-2132.
57. Garnero P, Borel O, Byrjalsen I, Ferreras M, Drake F H, McQueney M S, Foged N T, Delmas P D, and Delaissé J M (1998) The collagenolytic activity of cathepsin K is unique among mammalian proteinases. J. Biol. Chem. 273: 32347-32352.
58. Kafienah W, Bromme D, Buttle D J, Croucher L J, and Hollander A P (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.
59. Turk B, Turk V, and Turk D (1997) Structural and functional aspects of papain-like cysteine proteinases and their protein inhibitors. Biol. Chem. 378: 141-150.
60. Stubbs M T, Laber B, Bode W, Huber R, Jerala R, Lenarcic B, and Turk V (1990) The refined 2.4 Å X-ray crystal structure of recombinant human stefin B in complex with the cysteine proteinase papain: a novel type of proteinase inhibitor interaction. EMBO J. 9: 1939-1947.
61. Kobori M, Ikeda Y, Nara H, Kato M, Kumegawa M, Nojima H, and Kawashima H (1998) Large scale isolation of osteoclast-specific genes by an improved method involving the preparation of a subtracted cDNA library. Genes Cells 3: 459-475.
62. Lerner U H and Grubb A (1992) Human cystatin C, a cysteine proteinase inhibitor, inhibits bone resorption in vitro stimulated by parathyroid hormone and parathyroid hormone-related peptide of malignancy. J. Bone Miner. Res. 7: 433-440.
63. Lerner U H, Johansson L, Ranjso M, Rosenquist J B, Reinholt F P, and Grubb A (1998) Cystatin C, and inhibitor of bone resorption produced by osteoblasts. Acta Physiol. Scand. 161: 81-92.
64. Yamaza T, Tsuji Y, Goto T, Kido M A, Nishijima K, Moroi R, Akamine A, and Tanaka T (2001) Comparison in localization between cystatin C and cathepsin K in osteoclasts and other cells in mouse tibia epiphysis by immunolight and immunoelectron microscopy. Bone 29: 42-53.
65. Lenarcic B, Krasovec M, Ritonja A, Olafsson I, and Turk V (1991) Inactivation of human cystatin C and kininogen by human cathepsin D. FEBS Lett. 280: 211-215.
66. Honey K and Rudensky A Y (2003) Lysosomal cysteine proteases regulate antigen presentation. Nat. Rev. Immunol. 3: 472-482.
67. Saftig P, Hetman M, Schmahl W, Weber K, Heine L, Mossmann H, Koster A, Hess B, Evers M, von Figura K, and Peters C (1995) Mice deficient for the lysosomal proteinase cathepsin D exhibit progressive atrophy of the intestinal mucosa and profound destruction of lymphoid cells. EMBO J. 14: 3599-3608.
68. Guicciardi M E, Deussing J, Miyoshi H, Bronk S F, Svingen P A, Peters C, Kaufmann S H, and Gores G J (2000) Cathepsin B contributes to TNF-alpha-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c. J. Clin. Invest. 106: 1127-1137.
69. Benavides F, Starost M F, Flores M, Gimenez-Conti I B, Guenet J L, and Conti C J (2002) Impaired hair follicle morphogenesis and cycling with abnormal epidermal differentiation in nackt mice, a cathepsin L-deficient mutation. Am. J. Pathol 161: 693-703.
70. Pham C T and Ley T J (1999) Dipeptidyl peptidase I is required for the processing and activation of granzymes A and B in vivo. Proc. Natl. Acad. Sci. USA 95: 13453-13458.
71. Toomes C, James J, Wood A J, Wu C L, McCormick D, Lench N, Hewitt C, Moynihan L, Roberts E, Woods C G, Markham A, Wong M, Widmer R, Ghaffar K A, Pemberton M, Hussein I R, Temtamy S A, Davies R, Read A P, Sloan P, Dixon M J, and Thakker N S ( 1999) Loss-of-function mutations in the cathepsin C gene result in periodontal disease and palmoplantar keratosis. Nat. Genet. 23: 421-424.
72. Shi G P, Villadangos J A, Dranoff G, Small C, Gu L, Haley K J, Riese R, Ploegh H L, and Chapman H A (1999) Cathepsin S required for normal MHC class II peptide loading and germinal center development. Immunity 10: 197-206.
73. Okaji M, Sakai H, Sakai E, Shibata M, Hashimoto F, Kobayashi Y, Yoshida N, Okamoto K, Yamamoto K, and Kato Y (2003) The regulation of bone resorption in tooth formation and eruption processes in mouse alveolar crest devoid of cathepsin K. J. Pharmacol. Sci. 91: 285-294.
74. Tran Van P, Vignery A, and Baron R (1982) An electron-microscopic study of the bone-remodeling sequence in the rat. Cell Tiss. Res. 225: 283-292.
75. Jones S J, Boyde A, and Ali N N ( 1986) The interface of cells and their matrices in mineralized tissues: a review. Scan. Electron Microsc. 4: 1555-1569.
76. Everts V, Delaissé J M, Korper W, Jansen D C, Tigchelaar-Gutter W, Saftig P, and Beertsen W (2002) The bone lining cell: its role in cleaning Howship's lacunae and initiating bone formation. J. Bone Miner. Res. 17: 77-90.
77. Delaissé J M, Andersen T L, Engsig M T, Henriksen K, Troen T, and Blavier L (2003) Matrix metalloproteinases (MMP) and cathepsin K contribute differently to osteoclastic activities. Microsc. Res. Tech. 61: 504-513.
78. Nesbitt S A and Horton M A (1997) Trafficking of matrix collagens through bone-resorbing osteoclasts. Science 276: 266-269.
79. Blair H C, Teitelbaum S L, Ghiselli R, and Gluck S (1989) Osteoclastic bone resorption by a polarized vacuolar proton pump. Science 245: 855-857.
80. Chapman H A, Riese R J, and Shi G P (1997) Emerging roles for cysteine proteases in human biology. Annu. Rev. Physiol. 59: 63-88.
81. Riese R J, Wolf P R, Brömme D, Natkin L R, Villadangos J A, Ploegh H L, and Chapman H A (1996) Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading. Immunity 4: 357-366.
82. Villadangos J A, Riese R J, Peters C, Chapman H A, and Ploegh H L (1997) Degradation of mouse invariant chain: roles of cathepsins S and D and the influence of major histocompatibility complex polymorphism. J. Exp. Med. 186: 549-560.
83. Pierre P and Mellman I (1998) Developmental regulation of invariant chain proteolysis controls MHC class II trafficking in mouse dendritic cells. Cell 93: 1135-1145.
84. 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 (1999) Impaired invariant chain degradation and antigen presentation and diminished collagen-induced arthritis in cathepsin S null mice. Immunity 10: 207-217.