The metalloproteinase MT1-MMP is required for normal development and maintenance of osteocyte processes in bone

Journal of Cell Science

Volumn 118, Issue 1, 2005, Pages 147-156

  Holmbeck, Kenn ^a   Bianco, Paolo ^b   Pidoux, Isabelle ^c   Inoue, S ^c   Billinghurst, R C ^c,d   Wu, W ^c,e   Chrysovergis, Kali ^a   Yamada, Susan ^a   Birkedal Hansen, Henning ^a   Poole, A Robin ^c  

^a NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c MCGILL UNIVERSITY   (Canada)

^d St Lawrence College   (Canada)

^e UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Bone; Collagen cleavage; Membrane type matrix metalloproteinase 1; MMP 13; Osteocytes processes

Indexed keywords

COLLAGEN TYPE 1; COLLAGENASE 3; INTERSTITIAL COLLAGENASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE GROWTH; CELL DENSITY; CELL MATURATION; CELL ULTRASTRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEFICIENCY; MOUSE; NONHUMAN; OSTEOCYTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSMISSION ELECTRON MICROSCOPY; WILD TYPE;

ANIMALS; AZURE STAINS; BONE AND BONES; COLLAGEN TYPE I; IN SITU HYBRIDIZATION; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASES, MEMBRANE-ASSOCIATED; METALLOENDOPEPTIDASES; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; OSTEOCYTES; SILVER STAINING; TIME FACTORS;

EID: 20944440742     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01581     Document Type: Article

References (48)

1. Aarden, E. M., Burger, E. H. and Nijweide, P. J. (1994). Function of osteocytes in bone. J. Cell Biochem. 55, 287-299.
2. Aarden, E. M., Wassenaar, A. M., Alblas, M. J. and Nijweide, P. J. (1996). Immunocytochemical demonstration of extracellular matrix proteins in isolated osteocytes. Histochem. Cell Biol. 106, 495-501.
3. Aimes, R. T. and Quigley, J. P. (1995). Matrix metalloproteinase-2 is an interstitial collagenase. Inhibitor-free enzyme catalyzes the cleavage of collagen fibrils and soluble native type I collagen generating the specific 3/4- and 1/4-length fragments. J. Biol. Chem. 270, 5872-5876.
4. Ajubi, N. E., Klein-Nulend, J., Nijweide, P. J., Vrijheid-Lammers, T., Alblas, M. J. and Burger, E. H. (1996). Pulsating fluid flow increases prostaglandin production by cultured chicken osteocytes - a cytoskeleton-dependent process. Biochem. Biophys. Res. Commun. 225, 62-68.
5. Balbin, M., Fueyo, A., Knauper, V., Pendas, A. M., Lopez, J. M., Jimenez, M. G., Murphy, G. and Lopez-Otin, C. (1998). Collagenase 2 (MMP-8) expression in murine tissue-remodeling processes. Analysis of its potential role in postpartum involution of the uterus. J. Biol. Chem. 273, 23959-23968.
6. Balbin, M., Fueyo, A., Knauper, V. V., Lopez, J. M., Alvarez, J., Sanchez, L. M., Quesada, V. V., Bordallo, J., Murphy, G. and Lopez-Otin, C. (2000). Identification and enzymatic characterization of two diverging murine counterparts of human interstitial collagenase (MMP-1) expressed at sites of embryo implantation. J. Biol. Chem. 12, 12.
7. Billinghurst, R. C., Dahlberg, L., Ionescu, M., Reiner, A., Bourne, R., Rorabeck, C., Mitchell, P., Hambor, J., Diekmann, O., Tschesche, H. et al. (1997). Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. J. Clin. Invest. 99, 1534-1545.
8. Blavier, L., Lazaryev, A., Groffen, J., Heisterkamp, N., DeClerck, Y. A. and Kaartinen, V. (2001). TGF-beta3-induced palatogenesis requires matrix metalloproteinases. Mol. Biol. Cell 12, 1457-1466.
9. Burger, E. H. and Klein-Nulen, J. (1999a). Responses of bone cells to biomechanical forces in vitro. Adv. Dent. Res. 13 93-98.
10. Burger, E. H. and Klein-Nulend, J. (1999b). Mechanotransduction in bone - role of the lacuno-canalicular network. FASEB J. 13, S101-S112.
11. Cowell, S., Knauper, V., Stewart, M. L., D'Ortho, M. P., Stanton, H., Hembry, R. M., Lopez-Otin, C., Reynolds, J. J. and Murphy, G. (1998). Induction of matrix metalloproteinase activation cascades based on membrane-type 1 matrix metalloproteinase: associated activation of gelatinase A, gelatinase B and collagenase 3. Biochem. J. 331 453-458.
12. d'Ortho, M. P., Stanton, H., Butler, M., Atkinson, S. J., Murphy, G. and Hembry, R. M. (1998). MT1-MMP on the cell surface causes focal degradation of gelatin films. FEBS Lett. 421, 159-164.
13. Dodge, G. R., Pidoux, I. and Poole, A. R. (1991). The degradation of type II collagen in rheumatoid arthritis: an immunoelectron microscopic study. Matrix 11, 330-338.
14. Donahue, H. J. (2000). Gap junctions and biophysical regulation of bone cell differentiation. Bone 26, 417-422.
15. Friedl, P. and Brocker, E. B. (2000). The biology of cell locomotion within three-dimensional extracellular matrix. Cell Mol. Life Sci. 57, 41-64.
16. Friedl, P., Borgmann, S. and Brocker, E. B. (2001). Amoeboid leukocyte crawling through extracellular matrix: lessons from the Dictyostelium paradigm of cell movement. J. Leukocyte Biol. 70, 491-509.
17. Hiraoka, N., Allen, E., Apel, I. J., Gyetko, M. R. and Weiss, S. J. (1998). Matrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins. Cell 95, 365-377.
18. Hollander, A. P., Pidoux, I,, Reiner, A., Rorabeck, C., Bourne, R. and Poole, A. R. (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.
19. Holmbeck, K., Bianco, P., Caterina, J., Yamada, S., Kromer, M., Kuznetsov, S. A., Mankani, M., Robey, P. G., Poole, A. R., Pidoux, I. et al. (1999). MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 99, 81-92.
20. Holmbeck, K., Bianco, P., Chrysovergis, K., Yamada, S. and Birkedal-Hansen, H. (2003). MT1-MMP-dependent, apoptotic remodeling of unmineralized cartilage: a critical process in skeletal growth. J. Cell Biol. 163, 661-671.
21. Hotary, K., Allen, E., Punturieri, A., Yana, I. and Weiss, S. J. (2000). Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. J. Cell Biol. 149, 1309-1323.
22. Hotary, K. B., Allen, E. D., Brooks, P. C., Datta, N. S., Long, M. W. and Weiss, S. J. (2003). Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 114, 33-45.
23. Kageyama, N., Kusuzaki, K., Yamashita, F., Hirasawa, Y. and Ashihara, T. (1991). Staining of bone canaliculi using decalcified bone tissues. Nippon Seikeigeka Gakkai Zasshi 65, 757-761.
24. Kamioka, H., Miki, Y., Sumitani, K., Tagami, K., Terai, K., Hosoi, K. and Kawata, T. (1995). Extracellular calcium causes the release of calcium from intracellular stores in chick osteocytes. Biochem. Biophys. Res. Commun. 212, 692-696.
25. Kamioka, H., Honjo, T. and Takano-Yamamoto, T. (2001). A three-dimensional distribution of osteocyte processes revealed by the combination of confocal laser scanning microscopy and differential interference contrast microscopy. Bone 28, 145-149.
26. Klein-Nulend, J., Semeins, C. M., Ajubi, N. E., Nijweide, P. J. and Burger, E. H. (1995a). Pulsating fluid flow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fibroblasts - correlation with prostaglandin upregulation. Biochem. Biophys. Res. Commun. 217, 640-648.
27. Klein-Nulend, J., van der Plas, A., Semeins, C. M., Ajubi, N. E., Frangos, J. A., Nijweide, P. J. and Burger, E. H. (1995b). Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J. 9, 441-445.
28. Knauper, V., Will, H., Lopez-Otin, C., Smith, B., Atkinson, S. J., Stanton, H., Hembry, R. M. and Murphy, G. (1996). Cellular mechanisms for human procollagenase-3 (MMP-13) activation. Evidence that MT1-MMP (MMP-14) and gelatinase A (MMP-2) are able to generate active enzyme. J. Biol. Chem. 271, 17124-17131.
29. Knothe-Tate, M. L., Adamson, J. R., Tami, A. E. and Bauer, T. W. (2004). The osteocyte. Int. J. Biochem. Cell Biol. 36 1-8.
30. Koshikawa, N., Giannelli, G., Cirulli, V., Miyazaki, K. and Quaranta, V. (2000). Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J. Cell Biol. 148 615-624.
31. Menton, D. N., Simmons, D. J., Chang, S. L. and Orr, B. Y. (1984). From bone lining cell to osteocyte - an SEM study. Anat. Rec. 209, 29-39.
32. Mikuni-Takagaki, Y., Kakai, Y., Satoyoshi, M., Kawano, E., Suzuki, Y., Kawase, T. and Saito, S. (1995). Matrix mineralization and the differentiation of osteocyte-like cells in culture. J. Bone Miner. Res. 10, 231-242.
33. Miyauchi, A., Notoya, K., Mikuni-Takagaki, Y., Takagi, Y., Goto, M., Miki, Y., Takano-Yamamoto, T., Jinnai, K., Takahashi, K., Kumegawa, M. et al. (2000). Parathyroid hormone-activated volume-sensitive calcium influx pathways in mechanically loaded osteocytes. J. Biol. Chem. 275, 3335-3342.
34. Mullender, M. G., van der Meer, D. D., Huiskes, R. and Lips, P. (1996). Osteocyte density changes in aging and osteoporosis. Bone 18, 109-113.
35. Ohuchi, E., Imai, K., Fujii, Y., Sato, H., Seiki, M. and Okada, Y. (1997). Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J. Biol. Chem. 272, 2446-2451.
36. Palumbo, C., Palazzini, S., Zaffe, D. and Marotti, G. (1990). Osteocyte differentiation in the tibia of newborn rabbit: an ultrastructural study of the formation of cytoplasmic processes. Acta Anat. 137, 350-358.
37. Robey, P. G. (2002). Bone matrix proteoglycans and glycoproteins. In Principles of Bone Biology, Vol. 1 (ed. J. P. Bilezikian, L. G. Raisz and G. A. Rodan), pp. 225-237. San Diego, CA: Academic Press.
38. Sasano, Y., Zhu, J. X., Kamakura, S., Kusunoki, S., Mizoguchi, I. and Kagayama, M. (2000). Expression of major bone extracellular matrix proteins during embryonic osteogenesis in rat mandibles. Anat. Embryol. 202, 31-37.
39. Seltzer, J. L. (1999). Native type I collagen is not a substrate for MMP2 (gelatinase A). J. Invest. Dermatol. 112, 993-994.
40. Shapiro, F. (1997). Variable conformation of GAP junctions linking bone cells: a transmission electron microscopic study of linear, stacked linear, curvilinear, oval, and annular junctions. Calcif. Tissue Int. 61, 285-293.
41. Sun, Y. Q., McLeod, K. J. and Rubin, C. T. (1995). Mechanically induced periosteal bone formation is paralleled by the upregulation of collagen type one mRNA in osteocytes as measured by in situ reverse transcript-polymerase chain reaction. Calcif. Tissue Int. 57, 456-462.
42. Tarlo, L. B. H. (1964). The Origin of Bone. Oxford, UK: Pergamon Press.
43. Vu, T. H., Shipley, J. M., Bergers, G., Berger, J. E., Helms, J. A., Hanahan, D., Shapiro, S. D., Senior, R. M. and Werb, Z. (1998). MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93 411-422.
44. Wu, C. W., Tchetina, E. V., Mwale, F., Hasty, K., Pidoux, I., Reiner, A., Chen, J., Van, W. and Poole, A. R. (2002). Proteolysis involving matrix metalloproteinase 13 (collagenase-3) is required for chondrocyte differentiation that is associated with matrix mineralization. J. Bone Miner. Res. 17, 639-651.
45. Yellowley, C. E., Li, Z., Zhou, Z., Jacobs, C. R. and Donahue, H. J. (2000). Functional gap junctions between osteocytic and osteoblastic cells. J. Bone Miner. Res. 15, 209-217.
46. Zhao, W., Byrne, M. H., Wang, Y. and Krane, S. M. (2000). Osteocyte and osteoblast apoptosis and excessive bone deposition accompany failure of collagenase cleavage of collagen. J. Clin. Invest. 106, 941-949.
47. Zhou, Z., Apte, S. S., Soininen, R., Cao, R., Baaklini, G. Y., Rauser, R. W., Wang, J., Cao, Y. and Tryggvason, K. (2000). Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc. Natl. Acad. Sci. USA 97, 4052-4057.
48. Zhu, J. X., Sasano, Y., Takahashi, I., Mizoguchi, I. and Kagayama, M. (2001). Temporal and spatial gene expression of major bone extracellular matrix molecules during embryonic mandibular osteogenesis in rats. Histochem. J. 33, 25-35.