A scrutiny of matrix metalloproteinases in osteoclasts: Evidence for heterogeneity and for the presence of MMPs synthesized by other cells

Bone

Volumn 35, Issue 5, 2004, Pages 1107-1119

  Andersen, Thomas L ^a,b   Del Carmen Ovejero, Maria ^a   Kirkegaard, Tove ^a   Lenhard, Thomas ^a   Foged, Niels T ^a   Delaissé, Jean Marie ^a,b  

^a CENTER FOR CLINICAL AND BASIC RESEARCH   (Denmark)

^b LILLEBAELT HOSPITAL   (Denmark)

Author keywords

Bone resorption; Matrix metalloproteinase; Osteoclast

Indexed keywords

COLLAGENASE 3; GELATINASE A; GELATINASE B; MATRIX METALLOPROTEINASE 14;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NONHUMAN; NORTHERN BLOTTING; OSTEOCLAST; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION;

ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; BONE RESORPTION; CELLS, CULTURED; COLLAGENASES; GENE EXPRESSION; IN SITU HYBRIDIZATION; MATRIX METALLOPROTEINASE 10; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES; METALLOENDOPEPTIDASES; METATARSAL BONES; MICE; OSTEOCLASTS; PROTEIN TRANSPORT; RABBITS; RATS; SKULL; TIBIA;

EID: 8444226323     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2004.06.019     Document Type: Article

References (78)

1. S.S. Apte, N. Fukai, D.R. Beier, and B.R. Olsen The matrix metalloproteinase-14 (MMP-14) gene is structurally distinct from other MMP genes and is co-expressed with the TIMP-2 gene during mouse embryogenesis J. Biol. Chem. 272 1997 25511 25517
2. M. Balbin, A. Fueyo, V. Knauper, J.M. Lopez, J. Alvarez, and L.M. Sanchez C. Lopez-Otin Identification and enzymatic characterization of two diverging murine counterparts of human interstitial collagenase (MMP-1) expressed at sites of embryo implantation J. Biol. Chem. 276 2001 10253 10262
3. L. Blavier, and Y.A. DeClerck Tissue inhibitor of metalloproteinases-2 is expressed in the interstitial matrix in adult mouse organs and during embryonic development Mol. Biol. Cell 8 1997 1513 1527
4. L. Blavier, and J.M. Delaisse Matrix metalloproteinases are obligatory for the migration of preosteoclasts to the developing marrow cavity of primitive long bones J. Cell Sci. 108 1995 3649 3659
5. S. Bord, A. Horner, C.A. Beeton, R.M. Hembry, and J.E. Compston Tissue inhibitor of matrix metalloproteinase-1 (TIMP-1) distribution in normal and pathological human bone Bone 24 1999 229 235
6. S. Bord, A. Horner, R.M. Hembry, and J.E. Compston Stromelysin-1 (MMP-3) and stromelysin-2 (MMP-10) expression in developing human bone: potential roles in skeletal development Bone 23 1998 7 12
7. S. Bord, A. Horner, R.M. Hembry, J.J. Reynolds, and J.E. Compston Production of collagenase by human osteoblasts and osteoclasts in vivo Bone 19 1996 35 40
8. S. Bord, A. Horner, R.M. Hembry, J.J. Reynolds, and J.E. Compston Distribution of matrix metalloproteinases and their inhibitor, TIMP-1, in developing human osteophytic bone J. Anat. 191 1997 39 48
9. J.J. Breckon, S. Papaioannou, L.W. Kon, A. Tumber, R.M. Hembry, and G. Murphy Stromelysin (MMP-3) synthesis is up-regulated in estrogen-deficient mouse osteoblasts in vivo and in vitro J. Bone Miner. Res. 14 1999 1880 1890
10. P.C. Brooks, S. Stromblad, L.C. Sanders, T.L. von Schalscha, R.T. Aimes, and W.G. Stetler-Stevenson Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3 Cell 85 1996 683 693
11. C.C. Brown, R.M. Hembry, and J.J. Reynolds Immunolocalization of metalloproteinases and their inhibitor in the rabbit growth plate J. Bone Jt. Surg. Am. 71 1989 580 593
12. G.A. Candeliere, F. Liu, and J.E. Aubin Individual osteoblasts in the developing calvaria express different gene repertoires Bone 28 2001 351 361
13. J.P. Case, H. Sano, R. Lafyatis, E.F. Remmers, G.K. Kumkumian, and R.L. Wilder Transin/stromelysin expression in the synovium of rats with experimental erosive arthritis. In situ localization and kinetics of expression of the transformation-associated metalloproteinase in euthymic and athymic Lewis rats J. Clin. Invest. 84 1989 1731 1740
14. S. Colucci, M. Grano, G. Mori, K. Scotlandi, M. Mastrogiacomo, and C. Mori Retinoic acid induces cell proliferation and modulates gelatinases activity in human osteoclast-like cell lines Biochem. Biophys. Res. Commun. 227 1996 47 52
15. S.L. Dallas, J.L. Rosser, G.R. Mundy, and L.F. Bonewald 2002 Proteolysis of latent transforming growth factor-beta (TGF-beta) -binding protein-1 by osteoclasts. A cellular mechanism for release of TGF-beta from bone matrix J. Biol. Chem. 277 2002 21352 21360
16. M. D'Angelo, P.C. Billings, M. Pacifici, P.S. Leboy, and T. Kirsch Authentic matrix vesicles contain active metalloproteases (MMP). A role for matrix vesicle-associated MMP-13 in activation of transforming growth factor-beta J. Biol. Chem. 276 2001 11347 11353
17. M.A. Davoli, L. Lamplugh, A. Beauchemin, K. Chan, S. Mordier, and J.S. Mort Enzymes active in the areas undergoing cartilage resorption during the development of the secondary ossification center in the tibiae of rats aged 0-21 days: II. Two proteinases, gelatinase B and collagenase-3, are implicated in the lysis of collagen fibrils Dev. Dyn. 222 2001 71 88
18. J.M. Delaisse, T.L. Andersen, M.T. Engsig, K. Henriksen, T. Troen, and L. Blavier Matrix metalloproteinases (MMP) and cathepsin K contribute differently to osteoclastic activities Microsc. Res. Tech. 61 2003 504 513
19. J.M. Delaisse, Y. Eeckhout, L. Neff, C. Francois-Gillet, P. Henriet, and Y. Su (Pro)collagenase (matrix metalloproteinase-1) is present in rodent osteoclasts and in the underlying bone resorbing compartment J. Cell Sci. 106 1993 1071 1082
20. J.M. Delaisse, Y. Eeckhout, and G. Vaes Bone-resorbing agents affect the production and distribution of procollagenase as well as the activity of collagenase in bone tissue Endocrinology 123 1988 264 276
21. J.M. Delaisse, and G. Vaes Mechanism of mineral solubilization and matrix degradation in osteoclastic bone resorption B.R. Rifkin C.V. Gay Biology and physiology of the osteoclast 1992 CRC Press Boca Raton 289 314
22. G. Dew, G. Murphy, H. Stanton, R. Vallon, P. Angel, and J.J. Reynolds Localisation of matrix metalloproteinases and TIMP-2 in resorbing mouse bone Cell Tissue Res. 299 2000 385 394
23. M.T. Engsig, Q.J. Chen, T.H. Vu, A.C. Pedersen, B. Therkildsen, and L.R. Lund Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones J. Cell Biol. 151 2000 879 889
24. V. Everts, J.M. Delaisse, W. Korper, and W. Beertsen Cysteine proteinases and matrix metalloproteinases play distinct roles in the subosteoclastic resorption zone J. Bone Miner. Res. 13 1998 1420 1430
25. V. Everts, J.M. Delaisse, W. Korper, D.C. Jansen, W. Tigchelaar-Gutter, and P. Saftig The bone lining cell: its role in cleaning Howship's lacunae and initiating bone formation J. Bone Miner. Res. 17 2002 77 90
26. V. Everts, W. Korper, A.J. Docherty, and W. Beertsen Matrix metalloproteinase inhibitors block osteoclastic resorption of calvarial bone but not the resorption of long bone Ann. N. Y. Acad. Sci. 878 1999 603 606
27. M. Ferreras, U. Felbor, T. Lenhard, B.R. Olsen, and J.M. Delaisse Generation and degradation of human endostatin proteins by various proteinases FEBS Lett. 486 2000 247 251
28. N. Fujimoto, N. Mouri, K. Iwata, E. Ohuchi, Y. Okada, and T. Hayakawa A one-step sandwich enzyme immunoassay for human matrix metalloproteinase 2 (72-kDa gelatinase/type IV collagenase) using monoclonal antibodies Clin. Chim. Acta 221 1993 91 103
29. K. Fuller, and T.J. Chambers Localisation of mRNA for collagenase in osteocytic, bone surface and chondrocytic cells but not osteoclasts J. Cell Sci. 108 1995 2221 2230
30. S. Gack, R. Vallon, J. Schmidt, A. Grigoriadis, J. Tuckermann, and J. Schenkel Expression of interstitial collagenase during skeletal development of the mouse is restricted to osteoblast-like cells and hypertrophic chondrocytes Cell Growth Differ. 6 1995 759 767
31. P. Garnero, M. Ferreras, M.A. Karsdal, R. NicAmhlaoibh, J. Risteli, and O. Borel The type I collagen fragments ICTP and CTX reveal distinct enzymatic pathways of bone collagen degradation J. Bone Miner. Res. 18 2003 859 867
32. C. Gillet, Y. Eeckhout, and G. Vaes Purification of procollagenase and collagenase by affinity chromatography on Sepharose-collagen FEBS Lett. 74 1977 126 128
33. A.E. Grigoriadis, Z.Q. Wang, M.G. Cecchini, W. Hofstetter, R. Felix, and H.A. Fleisch c-Fos: a key regulator of osteoclast-macrophage lineage determination and bone remodeling Science 266 1994 443 448
34. T. Hayami, N. Endo, K. Tokunaga, H. Yamagiwa, H. Hatano, and M. Uchida Spatiotemporal change of rat collagenase (MMP-13) mRNA expression in the development of the rat femoral neck J. Bone Miner. Metab. 18 2000 185 193
35. B. Heissig, K. Hattori, S. Dias, M. Friedrich, B. Ferris, and N.R. Hackett Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand Cell 109 2002 625 637
36. M.H. Helfrich, S.A. Nesbitt, and M.A. Horton Integrins on rat osteoclasts: characterization of two monoclonal antibodies (F4 and F11) to rat beta 3 J. Bone Miner. Res. 7 1992 345 351
37. P.A. Hill, G. Murphy, A.J. Docherty, R.M. Hembry, T.A. Millican, and J.J. Reynolds The effects of selective inhibitors of matrix metalloproteinases (MMPs) on bone resorption and the identification of MMPs and TIMP-1 in isolated osteoclasts J. Cell Sci. 107 1994 3055 3064
38. L.S. Holliday, H.G. Welgus, C.J. Fliszar, G.M. Veith, J.J. Jeffrey, and S.L. Gluck Initiation of osteoclast bone resorption by interstitial collagenase J. Biol. Chem. 272 1997 22053 22058
39. P. Hou, I. Byrjalsen, M. Ferreras, N.T. Foged, and J.M. Delaisse Specific cleavage of bone matrix proteins by matrix metalloproteinases of osteoclasts Bone 23 1998 s252
40. P. Hou, T. Troen, M.C. Ovejero, T. Kirkegaard, T.L. Andersen, and I. Byrjalsen Matrix metalloproteinase-12 (MMP-12) in osteoclasts: new lesson on the involvement of MMPs in bone resorption Bone 34 2004 37 47
41. M. Inada, Y. Wang, M.H. Byrne, C. Miyaura, and S.M. Krane Mice with null mutation in Collagenase-3 (matrix metalloproteinase[MMP]-13) exhibit altered bone remodeling and increased bone mass J. Bone Miner. Res. 16 2001 s149
42. R. Jemtland, K. Lee, and G.V. Segre Heterogeneity among cells that express osteoclast-associated genes in developing bone Endocrinology 139 1998 340 349
43. L.G. Jenis, B. Ongphiphadhanakul, L.E. Braverman, G.S. Stein, J.B. Lian, and R. Lew Responsiveness of gene expression markers of osteoblastic and osteoclastic activity to calcitonin in the appendicular and axial skeleton of the rat in vivo Calcif. Tissue Int. 54 1994 511 515
44. M.J. Jimenez, M. Balbin, J. Alvarez, T. Komori, P. Bianco, and K. Holmbeck A regulatory cascade involving retinoic acid, Cbfa1, and matrix metalloproteinases is coupled to the development of a process of perichondrial invasion and osteogenic differentiation during bone formation J. Cell Biol. 155 2001 1333 1344
45. N. Johansson, U. Saarialho-Kere, K. Airola, R. Herva, L. Nissinen, and J. Westermarck Collagenase-3 (MMP-13) is expressed by hypertrophic chondrocytes, periosteal cells, and osteoblasts during human fetal bone development Dev. Dyn. 208 1997 387 397
46. M.A. Karsdal, M.S. Fjording, N.T. Foged, J.M. Delaisse, and A. Lochter Transforming growth factor-beta-induced osteoblast elongation regulates osteoclastic bone resorption through a p38 mitogen-activated protein kinase- and matrix metalloproteinase-dependent pathway J. Biol. Chem. 276 2001 39350 39358
47. M.A. Karsdal, L. Larsen, M.T. Engsig, H. Lou, M. Ferreras, and A. Lochter MMP dependent activation of latent TGF-{b} controls the conversion of osteoblasts into osteocytes by blocking osteoblast apoptosis J. Biol. Chem. 277 2002 44061 44068
48. V. Knauper, S. Cowell, B. Smith, C. Lopez-Otin, M. O'Shea, and H. Morris The role of the C-terminal domain of human collagenase-3 (MMP-13) in the activation of procollagenase-3, substrate specificity, and tissue inhibitor of metalloproteinase interaction J. Biol. Chem. 272 1997 7608 7616
49. K. Kusano, C. Miyaura, M. Inada, T. Tamura, A. Ito, and H. Nagase Regulation of matrix metalloproteinases (MMP-2, -3, -9, and -13) by interleukin-1 and interleukin-6 in mouse calvaria: association of MMP induction with bone resorption Endocrinology 139 1998 1338 1345
50. E.R. Lee, G. Murphy, M. Alfy, M.A. Davoli, L. Lamplugh, and A.J. Docherty Active gelatinase B is identified by histozymography in the cartilage resorption sites of developing long bones Dev. Dyn. 215 1999 190 205
51. I.M. Margulies, M. Hoyhtya, C. Evans, M.L. Stracke, L.A. Liotta, and W.G. Stetler-Stevenson Urinary type IV collagenase: elevated levels are associated with bladder transitional cell carcinoma Cancer Epidemiol., Biomarkers Prev. 1 1992 467 474
52. H. Nagase, and J.F. Woessner Matrix metalloproteinases 2000 Oxford Univ. Press New York
53. J. Nordahl, G. Andersson, and F.P. Reinholt Chondroclasts and osteoclasts in bones of young rats: comparison of ultrastructural and functional features Calcif. Tissue Int. 63 1998 401 408
54. Y. Okada, K. Naka, K. Kawamura, T. Matsumoto, I. Nakanishi, and N. Fujimoto Localization of matrix metalloproteinase 9 (92-kilodalton gelatinase/type IV collagenase = gelatinase B) in osteoclasts: implications for bone resorption Lab. Invest. 72 1995 311 322
55. T. Okamura, H. Shimokawa, Y. Takagi, H. Ono, and S. Sasaki Detection of collagenase mRNA in odontoclasts of bovine root-resorbing tissue by in situ hybridization Calcif. Tissue Int. 52 1993 325 330
56. T. Pap, G. Pap, K.M. Hummel, J.K. Franz, E. Jeisy, and I. Sainsbury Membrane-type-1 matrix metalloproteinase is abundantly expressed in fibroblasts and osteoclasts at the bone-implant interface of aseptically loosened joint arthroplasties in situ J. Rheumatol. 26 1999 166 169
57. P. Reponen, C. Sahlberg, C. Munaut, I. Thesleff, and K. Tryggvason High expression of 92-kDa type IV collagenase (gelatinase) in the osteoclast lineage during mouse development Ann. N. Y. Acad. Sci. 732 1994 472 475
58. D.P. Rice, H.J. Kim, and I. Thesleff Detection of gelatinase B expression reveals osteoclastic bone resorption as a feature of early calvarial bone development Bone 21 1997 479 486
59. J. Rubin, X. Fan, D.M. Biskobing, W.R. Taylor, and C.T. Rubin Osteoclastogenesis is repressed by mechanical strain in an in vitro model J. Orthop. Res. 17 1999 639 645
60. D. Sakai, H.S. Tong, and C. Minkin Osteoclast molecular phenotyping by random cDNA sequencing Bone 17 1995 111 119
61. T. Sato, O.M. del Carmen, P. Hou, A.M. Heegaard, M. Kumegawa, and N.T. Foged Identification of the membrane-type matrix metalloproteinase MT1-MMP in osteoclasts J. Cell Sci. 110 1997 589 596
62. T. Sato, N.T. Foged, and J.M. Delaisse The migration of purified osteoclasts through collagen is inhibited by matrix metalloproteinase inhibitors J. Bone Miner. Res. 13 1998 59 66
63. M. Stahle-Backdahl, B. Sandstedt, K. Bruce, A. Lindahl, M.G. Jimenez, and J.A. Vega Collagenase-3 (MMP-13) is expressed during human fetal ossification and re-expressed in postnatal bone remodeling and in rheumatoid arthritis Lab. Invest. 76 1997 717 728
64. M.D. Sternlicht, and Z. Werb How matrix metalloproteinases regulate cell behavior Annu. Rev. Cell Dev. Biol. 17 2001 463 516
65. A.Y. Strongin, I. Collier, G. Bannikov, B.L. Marmer, G.A. Grant, and G.I. Goldberg Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease J. Biol. Chem. 270 1995 5331 5338
66. D.E. Tacha, and L. McKinney Casein reduces nonspecific background staining in immunolabeling techniques J. Histotechol. 15 1992 127 132
67. K. Tezuka, K. Nemoto, Y. Tezuka, T. Sato, Y. Ikeda, and M. Kobori Identification of matrix metalloproteinase 9 in rabbit osteoclasts J. Biol. Chem. 269 1994 15006 15009
68. G. Vaes Cellular biology and biochemical mechanism of bone resorption. A review of recent developments on the formation, activation, and mode of action of osteoclasts Clin. Orthop. 231 1988 239 271
69. T.H. Vu, J.M. Shipley, G. Bergers, J.E. Berger, J.A. Helms, and D. Hanahan MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes Cell 93 1998 411 422
70. D.G. Walker, C.M. Lapierre, and J. Gross A colagenolytic factor in rat bone promoted by parathyroid extract Biochem. Biophys. Res. Commun. 15 1964 397 402
71. B. Winding, R. NicAmhlaoibh, H. Misander, P. Hoegh-Andersen, T.L. Andersen, and C. Holst-Hansen Synthetic matrix metalloproteinase inhibitors inhibit growth of established breast cancer osteolytic lesions and prolong survival in mice Clin. Cancer Res. 8 2002 1932 1939
72. Y. Wittrant, S. Couillaud, S. Theoleyre, C. Dunstan, D. Heymann, and F. Redini Osteoprotegerin differentially regulates protease expression in osteoclast cultures Biochem. Biophys Res. Commun. 293 2002 38 44
73. J.P. Witty, S.A. Foster, G.P. Stricklin, L.M. Matrisian, and P.H. Stern Parathyroid hormone-induced resorption in fetal rat limb bones is associated with production of the metalloproteinases collagenase and gelatinase B J. Bone Miner. Res. 11 1996 72 78
74. A.L. Wucherpfennig, Y.P. Li, W.G. Stetler-Stevenson, A.E. Rosenberg, and P. Stashenko Expression of 92 kD type IV collagenase/gelatinase B in human osteoclasts J. Bone Miner. Res. 9 1994 549 556
75. H. Yamagiwa, K. Tokunaga, T. Hayami, H. Hatano, M. Uchida, and N. Endo Expression of metalloproteinase-13 (Collagenase-3) is induced during fracture healing in mice Bone 25 1999 197 203
76. M. Yu, H. Sato, M. Seiki, and E.W. Thompson Complex regulation of membrane-type matrix metalloproteinase expression and matrix metalloproteinase-2 activation by concanavalin A in MDA-MB-231 human breast cancer cells Cancer Res. 55 1995 3272 3277
77. Q. Yu, and I. Stamenkovic 2000 Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis Genes Dev. 14 2000 163 176
78. W. Zhao, M.H. Byrne, B.F. Boyce, and S.M. Krane Bone resorption induced by parathyroid hormone is strikingly diminished in collagenase-resistant mutant mice J. Clin. Invest. 103 1999 517 524