Matrix metalloproteinases are obligatory for the migration of preosteoclasts to the developing marrow cavity of primitive long bones
Abstract
A key event in bone resorption is the recruitment of osteoclasts to future resorption sites. We follow here the migration of preosteoclasts from the periosteum to the developing marrow cavity of fetal mouse metatarsals in culture, and investigate the role of proteinases and demineralization in this migration. Our approach consisted in testing inhibitors of proteinases and demineralization on the migration kinetics. Migration was monitored by histomorphometry and the (pre)osteoclasts were identified by their tartrate resistant acid phosphatase (TRAP) activity. At the time of explantation, TRAP+ cells (all mononucleated) are detected only in the periosteum, and the core of the diaphysis (future marrow cavity) consists of calcified cartilage. Upon culture, TRAP+ cells (differentiating progressively into multinucleated osteoclasts) migrate through a seam of osteoid and a very thin and discontinuous layer of mineral, invade the calcified cartilage and transform it into a ‘marrow’ cavity; despite the passage of maturing osteoclasts, the osteoid develops into a bone collar. The migration of TRAP+ cells is completely prevented by matrix metalloproteinase (MMP) inhibitors, but not by a cysteine proteinase inhibitor, an inhibitor of carbonic anhydrase, or a bisphosphonate. The latter three drugs inhibit, however, the resorptive activity of mature osteoclasts at least as efficiently as do the MMP inhibitors, as assessed in cultures of calvariae and radii. Furthermore, in situ hybridizations reveal the expression of 2 MMPs, gelatinase B (MMP-9 or 92 kDa type IV collagenase) in (pre)osteoclasts, and interstitial collagenase (MMP-13) in hypertrophic chondrocytes. It is concluded that only MMPs appear obligatory for the migration of (pre)osteoclasts, and that this role is distinct from the one MMPs may play in the subosteoclastic resorption compartment. We propose that this new role of MMPs is a major component of the mechanism that determines where and when the osteoclasts will attack the bone.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
MMP inhibitor administration fully prevented osteoclast recruitment in the diaphysis core in vivo and osteoclast migration through collagen in vitro.
“MMP inhibitor administration fully prevented osteoclast recruitment in the diaphysis core in vivo145 as well as osteoclast migration through collagen in vitro.146”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [145]
Cites
c-Fos: a Key Regulator of Osteoclast-Macrophage Lineage Determination and Bone Remodeling
Grigoriadis, A. E., Wang, Z., Cecchini, M. G., Hofstetter, W., Felix, R., Fleisch, H. A., & Wagner, E. F. (1994) · Science · doi:10.1126/science.7939685 · Cited by 1,260 · see citing works
Biology and biochemistry of proteinases in tumor invasion
Mignatti, P., & Rifkin, D. B. (1993) · Physiological Reviews · doi:10.1152/physrev.1993.73.1.161 · Cited by 1,257 · see citing works
Processing of tumour necrosis factor-α precursor by metalloproteinases
Gearing, A. J. H., Beckett, P., Christodoulou, M., Churchill, M., Clements, J. M., Davidson, A. H., Drummond, A. H., GALLOWAY, W. A., Gilbert, R. J. C., Gordon, J. L., et al. (1994) · Nature · doi:10.1038/370555a0 · Cited by 1,194 · see citing works
Barrett, A. J., Kembhavi, A. A., Brown, M. A., Kirschke, H., Knight, C. G., Tamai, M., & Hanada, K. (1982) · Biochemical Journal · doi:10.1042/bj2010189 · Cited by 1,022 · see citing works
Sato, M., Grasser, W., Endo, N., Akins, R., Simmons, H., Thompson, D. D., Golub, E., & Rodan, G. A. (1991) · Journal of Clinical Investigation · doi:10.1172/jci115539 · Cited by 1,004 · see citing works
Modulation of Osteoclast Differentiation
Suda, T., Takahashi, N., & Martin, T. J. (1992) · Endocrine Reviews · doi:10.1210/edrv-13-1-66 · Cited by 996 · see citing works
Connective Tissue and Its Heritable Disorders
Heinegård, D., Aspberg, A., Franzén, A., & Lorenzo, P. (2002) · Wiley eBooks · doi:10.1002/0471221929 · Cited by 946 · see citing works
92-kD type IV collagenase mediates invasion of human cytotrophoblasts.
Librach, C. L., Werb, Z., Fitzgerald, M. L., Chiu, K., Corwin, N., Esteves, R. A., Grobelny, D. W., Galardy, R. E., Damsky, C. H., & Fisher, S. J. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.113.2.437 · Cited by 718 · see citing works
Expression of matrix metalloproteinase-2 and -9 during early human wound healing.
Salo, T. A., Mäkelä, M., Kylmäniemi, M., Autio‐Harmainen, H., & Larjava, H. (1994) · PubMed · Cited by 406 · see citing works
Fuller, K., Owens, J., Jagger, C., Wilson, A., Moss, R. F., & Chambers, T. J. (1993) · The Journal of Experimental Medicine · doi:10.1084/jem.178.5.1733 · Cited by 360 · see citing works
ON THE MECHANISMS OF BONE RESORPTION
Vaes, G. (1968) · The Journal of Cell Biology · doi:10.1083/jcb.39.3.676 · Cited by 331 · see citing works
In vitro formation of osteoclasts from long-term cultures of bone marrow mononuclear phagocytes.
Burger, E. H., van der Meer, J. W., van de Gevel, J. S., Gribnau, J. C., Thesingh, G. W., & van Furth, R. (1982) · The Journal of Experimental Medicine · doi:10.1084/jem.156.6.1604 · Cited by 327 · see citing works
Okada, Y., Naka, K., Kawamura, K., Matsumoto, T., Nakanishi, I., Fujimoto, N., Sato, H., & Seiki, M. (1995) · PubMed · Cited by 303 · see citing works
Biology and Physiology of the Osteoclast
Rifkin, B. R. (1992) · Cited by 293 · see citing works
Everts, V. E., Delaissé, J., Korper, W., Niehof, A., Vaes, G., & Beertsen, W. (1992) · Journal of Cellular Physiology · doi:10.1002/jcp.1041500202 · Cited by 286 · see citing works
Self-citationReponen, P., Sahlberg, C., Munaut, C., Thesleff, I., & Tryggvason, K. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.124.6.1091 · Cited by 279 · see citing works
Recruitment of osteoclast precursors by purified bone matrix constituents.
Malone, J. D., Teitelbaum, S. L., Griffin, G. L., Senior, R. M., & Kahn, A. J. (1982) · The Journal of Cell Biology · doi:10.1083/jcb.92.1.227 · Cited by 266 · see citing works
Mammalian collagenase predisposes bone surfaces to osteoclastic resorption
Chambers, T. J., Darby, J. A., & Fuller, K. (1985) · Cell and Tissue Research · doi:10.1007/bf00214590 · Cited by 203 · see citing works
van de Wijngaert, F. P., & Burger, E. H. (1986) · Journal of Histochemistry & Cytochemistry · doi:10.1177/34.10.3745910 · Cited by 194 · see citing works
Löwik, C. W. G. M., van der Pluijm, G., van der Wee-Pals, L. J. A., Groot, H. B. V. T.-D., & Bijvoet, O. L. M. (1988) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650030210 · Cited by 191 · see citing works
Watanabe, H., Nakanishi, I., Yamashita, K., Hayakawa, T., & Okada, Y. (1993) · Journal of Cell Science · doi:10.1242/jcs.104.4.991 · Cited by 182 · see citing works
Chemotactic activity of theγ-carboxyglutamic acid containing protein in bone
Mundy, G. R., & Poser, J. W. (1983) · Calcified Tissue International · doi:10.1007/bf02405025 · Cited by 172 · see citing works
Identification of matrix metalloproteinase 9 in rabbit osteoclasts.
Tezuka, K., Nemoto, K., Tezuka, Y., Sato, T., Ikeda, Y., Kobori, M., Kawashima, H., Eguchi, H., Hakeda, Y., & Kumegawa, M. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)36566-3 · Cited by 167 · see citing works
Hill, P. A., Murphy, G., Docherty, A., Hembry, R. M., Millican, T. A., Reynolds, J. J., & Meikle, M. C. (1994) · Journal of Cell Science · doi:10.1242/jcs.107.11.3055 · Cited by 164 · see citing works
Opdenakker, G., & Damme, J. V. (1992) · Cytokine · doi:10.1016/1043-4666(92)90064-x · Cited by 158 · see citing works
Richards, C. D., SHOYAB, M., Brown, T. J., & Gauldie, J. (1993) · The Journal of Immunology · doi:10.4049/jimmunol.150.12.5596 · Cited by 146 · see citing works
Expression of 92 kD type IV collagenase/gelatinase B in human osteoclasts
Wucherpfennig, A. L., Li, Y.-P., Stetler‐Stevenson, W. G., Rosenberg, A. E., & Stashenko, P. (1994) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650090415 · Cited by 141 · see citing works
Delaissé, J., Eeckhout, Y., Neff, L., François-Gillet, C., Henriet, P., Su, Y., Vaes, G., & Baron, R. (1993) · Journal of Cell Science · doi:10.1242/jcs.106.4.1071 · Cited by 140 · see citing works
Self-citationRoles of osteoclasts in alveolar bone remodeling
Omi, M., & Mishina, Y. M. (2022) · genesis · doi:10.1002/dvg.23490 · Cited by 139 · see citing works
Adaptations of Goldner's Masson Trichrome Stain for the Study of Undecalcified Plastic Embedded Bone
Gruber, H. E. (1992) · Biotechnic & Histochemistry · doi:10.3109/10520299209110002 · Cited by 135 · see citing works
Hofstetter, W., Wetterwald, A., Cecchini, M. C., Felix, R., Fleisch, H. A., & Mueller, C. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.20.9637 · Cited by 128 · see citing works
Immunolocalization of metalloproteinases and their inhibitor in the rabbit growth plate.
Brown, C. C., Hembry, R. M., & Reynolds, J. J. (1989) · Journal of Bone and Joint Surgery · doi:10.2106/00004623-198971040-00014 · Cited by 125 · see citing works
Henriet, P., Rousseau, G. G., & Eeckhout, Y. (1992) · FEBS Letters · doi:10.1016/0014-5793(92)81323-e · Cited by 121 · see citing works
Alini, M., Matsui, Y., Dodge, G. R., & Poole, A. R. (1992) · Calcified Tissue International · doi:10.1007/bf00301630 · Cited by 118 · see citing works
Differentiation kinetics of osteoclasts in the periosteum of embryonic bones in vivo and in vitro
Scheven, B. A. A., Haas, E. W. M. K.-D., Wassenaar, A. M., & Nijweide, P. J. (1986) · The Anatomical Record · doi:10.1002/ar.1092140413 · Cited by 112 · see citing works
Developmental expression of tissue inhibitor of metalloproteinase (TIMP) RNA
Nomura, S., Hogan, B. L. M., Wills, A. J., Heath, J. K., & Edwards, D. R. (1989) · Development · doi:10.1242/dev.105.3.575 · Cited by 112 · see citing works
A new synthetic inhibitor of mammalian tissue collagenase inhibits bone resorption in culture
Delaissé, J., Eeckhout, Y., Sear, C. H. J., Galloway, A., McCullagh, K. G., & Vaes, G. (1985) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(85)90932-5 · Cited by 98 · see citing works
Self-citationMasure, S., Nys, G., Fiten, P., Damme, J. V., & Opdenakker, G. (1993) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1993.tb18359.x · Cited by 94 · see citing works
van der Pluijm, G., Most, W., van der Wee-Pals, L. J. A., de Groot, H., Papapoulos, S. E., & Löwik, C. W. G. M. (1991) · Endocrinology · doi:10.1210/endo-129-3-1596 · Cited by 91 · see citing works
Dieudonné, S. C., Foo, P., van Zoelen, E. J. J., & Burger, E. H. (1991) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650060509 · Cited by 88 · see citing works
Inhibition of cysteine proteinases in lysosomes and whole cells
Wilcox, D., & Mason, R. W. (1992) · Biochemical Journal · doi:10.1042/bj2850495 · Cited by 85 · see citing works
Argos, P., Frishman, D., Rost, B., Jim Graham, A., Stonno, G., & Snyder, E. E. (1996) · Taylor & Francis eBooks · doi:10.1201/9781420050646.ptg4 · Cited by 84 · see citing works
Beertsen, W., Niehof, A., & Everts, V. E. (1985) · American Journal of Anatomy · doi:10.1002/aja.1001740107 · Cited by 77 · see citing works
CELLULAR AND MOLECULAR BIOLOGY OF THE OSTEOCLAST
Baron, R., Ravesloot, J., Neff, L., Chakraborty, M., Chatterjee, D., Lomri, A., & Horne, W. C. (1993) · Elsevier eBooks · doi:10.1016/b978-0-08-092500-4.50018-8 · Cited by 66 · see citing works
Okamura, T., Shimokawa, H., Takagi, Y., Ono, H., & Sasaki, S. (1993) · Calcified Tissue International · doi:10.1007/bf00296659 · Cited by 59 · see citing works
van Beek, E. R., van der Wee-Pals, L. J. A., Ruit, M. V. D., Nijweide, P. J., Papapoulos, S. E., & Löwik, C. W. G. M. (1993) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650080210 · Cited by 57 · see citing works
Expression of αv and β3 integrin subunits in rat osteoclasts in situ
SHINAR, D. M., Schmidt, A., Halperin, D., Rodan, G. A., & Weinreb, M. (1993) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650080404 · Cited by 54 · see citing works
Effects of a Potent Carbonic Anhydrase Inhibitor on Bone Resorption in Organ Culture*
Raisz, L. G., Simmons, H. A., Thompson, W. J., Shepard, K. L., ANDERSON, P. S., & Rodan, G. A. (1988) · Endocrinology · doi:10.1210/endo-122-3-1083 · Cited by 54 · see citing works
van der Pluijm, G., Mouthaan, H., Baas, C., de Groot, H., Papapoulos, S. E., & Löwik, C. W. G. M. (1994) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650090709 · Cited by 42 · see citing works
Complement and the recruitment of mononuclear osteoclasts.
Mangham, D. C., Scoones, D., & Drayson, M. T. (1993) · Journal of Clinical Pathology · doi:10.1136/jcp.46.6.517 · Cited by 33 · see citing works
Leloup, G., Delaissé, J., & Vaes, G. (1994) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650090615 · Cited by 32 · see citing works
Self-citationEffects of Bone Matrix Components on Osteoclast Differentiation
Glowacki, J., Rey, C. C., Cox, K. A., & Lian, J. B. (1989) · Connective Tissue Research · doi:10.3109/03008208909023880 · Cited by 28 · see citing works
Lelièvre, Y., Bouboutou, R., Boiziau, J., Faucher, D., Achard, D., & Cartwright, T. (1990) · Matrix · doi:10.1016/s0934-8832(11)80184-8 · Cited by 27 · see citing works
Role of mineralizing cartilage in osteoclast and osteoblast recruitment
van de Wijngaert, F. P., Schipper, C. A., Tas, M., & Burger, E. H. (1988) · Bone · doi:10.1016/8756-3282(88)90107-x · Cited by 25 · see citing works
Hoekman, K., Löwik, C. W. G. M., Ruit, M. V. D., Bijvoet, O. L. M., Verheijen, J. H., & Papapoulos, S. E. (1992) · Bone and Mineral · doi:10.1016/0169-6009(92)90706-j · Cited by 17 · see citing works
Scheven, B. A. A., Hamilton, N. J., Farquharson, C., Rucklidge, G. J., & Robins, S. P. (1988) · Bone · doi:10.1016/8756-3282(88)90123-8 · Cited by 16 · see citing works
Bagi, C. M., & Miller, S. C. (1992) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650070106 · Cited by 14 · see citing works
Flagged first, then by citations
4 of the 61 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Matrix metalloproteinases: effectors of development and normal physiologyPreprint
Vu, T. H., & Werb, Z. (2000) · Genes & Development · doi:10.1101/gad.815400 · Cited by 1,236 · see citing works
Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells
Kollet, Ó., Dar, A., Shivtiel, S., Kalinkovich, A., Lapid, K., Sztainberg, Y., Tesio, M., Samstein, R. M., Goichberg, P., Spiegel, A., et al. (2006) · Nature Medicine · doi:10.1038/nm1417 · Cited by 774 · see citing works
Vandooren, J., den Steen, P. E. V., & Opdenakker, G. (2013) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2013.770819 · Cited by 767 · see citing works
Engsig, M. T., Chen, Q.-J., Vu, T. H., Pedersen, A.-C., Therkidsen, B., Lund, L. R., Henriksen, K., Lenhard, T., Foged, N. T., Werb, Z., et al. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.4.879 · Cited by 596 · see citing works
Self-citationMatrix Metalloproteinase-9 in Lung Remodeling
Atkinson, J. J., & Senior, R. M. (2003) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2002-0166tr · Cited by 585 · see citing works
Boissier, S., Ferreras, M., Peyruchaud, O., Magnetto, S., Ebetino, F. H., Colombel, M. C., Delmas, P. D., Delaissé, J., & Clézardin, P. (2000) · PubMed · Cited by 573 · see citing works
Self-citationBone remodeling: an operational process ensuring survival and bone mechanical competence
Bolamperti, S., Villa, I., & Rubinacci, A. (2022) · Bone Research · doi:10.1038/s41413-022-00219-8 · Cited by 482 · see citing works
Garnero, P., Ferreras, M., Karsdal, M. A., NicAmhlaoibh, R., Risteli, J., Borel, O., Qvist, P., Delmas, P. D., Foged, N., & Delaissé, J. (2003) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2003.18.5.859 · Cited by 472 · see citing works
Self-citationMatrix remodeling during endochondral ossification
Ortéga, N., Behonick, D. J., & Werb, Z. (2004) · Trends in Cell Biology · doi:10.1016/j.tcb.2003.12.003 · Cited by 463 · see citing works
Maes, C., Carmeliet, P., Moermans, K., Stockmans, I., Smets, N., Collen, D., Bouillon, R., & Carmeliet, G. (2002) · Mechanisms of Development · doi:10.1016/s0925-4773(01)00601-3 · Cited by 451 · see citing works
The role of matrix metalloproteinases in the oral environment
Hannas, A. R., Pereira, J. C., Granjeiro, J. M., & Tjäderhane, L. (2006) · Acta Odontologica Scandinavica · doi:10.1080/00016350600963640 · Cited by 411 · see citing works
Proteolysis and cell migration: creating a path?
Murphy, G., & Gavrilović, J. (1999) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(99)00022-8 · Cited by 384 · see citing works
Matrix metalloproteinases (MMP) and cathepsin K contribute differently to osteoclastic activities
Delaissé, J., Andersen, T. L., Engsig, M. T., Henriksen, K., Troen, T., & Blavier, L. (2003) · Microscopy Research and Technique · doi:10.1002/jemt.10374 · Cited by 341 · see citing works
Self-citationJiménez, M. J. G., Balbı́n, M., López, J. M., Álvarez, J., Komori, T., & López-Otı́n, C. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.6.4431 · Cited by 294 · see citing works
Yoneda, T., Sasaki, A., Dunstan, C. R., Williams, P. J., Bauss, F., DeClerck, Y. A., & Mundy, G. R. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119435 · Cited by 247 · see citing works
Yu, X., Huang, Y., Collin‐Osdoby, P., & Osdoby, P. (2003) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2003.18.8.1404 · Cited by 241 · see citing works
Matrix Metalloproteinases in Bone Resorption, Remodeling, and Repair
Paiva, K. B. S., & Granjeiro, J. M. (2017) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2017.05.001 · Cited by 237 · see citing works
Henriksen, K., Bollerslev, J., Everts, V. E., & Karsdal, M. A. (2011) · Endocrine Reviews · doi:10.1210/er.2010-0006 · Cited by 230 · see citing works
Proteinases in bone resorption: obvious and less obvious roles
Delaissé, J.-M., Engsig, M. T., Everts, V., del Carmen Ovejero, M., Ferreras, M., Lund, L., Vu, T. H., Werb, Z., Winding, B., Lochter, A., et al. (2000) · Clinica Chimica Acta · doi:10.1016/s0009-8981(99)00230-2 · Cited by 227 · see citing works
Self-citationZelzer, E., & Olsen, B. R. (2004) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(04)65006-x · Cited by 223 · see citing works
Arai, F., Ohneda, O., Miyamoto, T. K., Zhang, X., & Suda, T. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20011700 · Cited by 223 · see citing works
Nemeth, J. A. (2002) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/94.1.17 · Cited by 220 · see citing works
Identification of the membrane-type matrix metalloproteinase MT1-MMP in osteoclasts
Sato, T., Ovejero, M. D. C., Hou, P., Heegaard, A.-M., Kumegawa, M., Tækker Foged, N., & Delaissé, J.-M. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.5.589 · Cited by 214 · see citing works
Self-citationBehonick, D. J., Xing, Z., Lieu, S., Buckley, J. M., Lotz, J. C., Marcucio, R. S., Werb, Z., Miclau, T., & Colnot, C. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001150 · Cited by 189 · see citing works
Osteoclasts are important for bone angiogenesis
Cackowski, F. C., Anderson, J. L., Patrene, K. D., Choksi, R. J., Shapiro, S. D., Windle, J. J., Blair, H. C., & Roodman, G. D. (2010) · Blood · doi:10.1182/blood-2009-08-237628 · Cited by 188 · see citing works
Sawant, A., Deshane, J. S., Jules, J., Lee, C. M., Harris, B. A., Feng, X., & Ponnazhagan, S. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-2202 · Cited by 182 · see citing works
Yahara, Y., Barrientos, T., Tang, Y. J., Puviindran, V., Nadesan, P., Zhang, H., Gibson, J., Gregory, S. G., Diao, Y., Xiang, Y., et al. (2020) · Nature Cell Biology · doi:10.1038/s41556-019-0437-8 · Cited by 180 · see citing works
Everts, V. E., Korper, W., Jansen, D. C., Steinfort, J., Lammerse, I., Heera, S., Docherty, A. J. P., & Beertsen, W. (1999) · The FASEB Journal · doi:10.1096/fasebj.13.10.1219 · Cited by 174 · see citing works
Gelatinase B: Structure, Regulation, and Function
Vu, T. H., & Werb, Z. (1998) · Elsevier eBooks · doi:10.1016/b978-012545090-4/50006-9 · Cited by 174 · see citing works
A molecular analysis of matrix remodeling and angiogenesis during long bone development
Colnot, C., & Helms, J. A. (2001) · Mechanisms of Development · doi:10.1016/s0925-4773(00)00532-3 · Cited by 169 · see citing works
Podosomes in osteoclast-like cells
Pfaff, M., & Jurdic, P. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.15.2775 · Cited by 169 · see citing works
High d(+)glucose concentration inhibits RANKL-induced osteoclastogenesis
Wittrant, Y., Gorin, Y. C., Woodruff, K., Horn, D., Abboud, H. E., Mohan, S., & Abboud‐Werner, S. L. (2008) · Bone · doi:10.1016/j.bone.2008.02.006 · Cited by 164 · see citing works
Giant cell tumor of bone: A basic science perspective
Cowan, R. W., & Singh, G. (2012) · Bone · doi:10.1016/j.bone.2012.10.002 · Cited by 159 · see citing works
Henriksen, K., Karsdal, M. A., Delaissé, J., & Engsig, M. T. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m309193200 · Cited by 157 · see citing works
Self-citationTea Polyphenols Inhibit Rat Osteoclast Formation and Differentiation
Oka, Y., Iwai, S., Amano, H., Irie, Y., Yatomi, K., Ryu, K., Yamada, S., Inagaki, K., & Oguchi, K. (2011) · Journal of Pharmacological Sciences · doi:10.1254/jphs.11082fp · Cited by 153 · see citing works
Ljusberg, J., Wang, Y., Lång, P., Norgård, M., Dodds, R. A., Hultenby, K. R., Ek‐Rylander, B., & Andersson, G. N. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m502469200 · Cited by 151 · see citing works
Schaller, S., Henriksen, K., Sveigaard, C., Heegaard, A., Hélix, N., Stahlhut, M., Ovejero, M. D. C., Johansen, J. V., Solberg, H., Andersen, T. L., et al. (2004) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.040302 · Cited by 147 · see citing works
Self-citationAndersen, T. L., del Carmen Ovejero, M., Kirkegaard, T., Lenhard, T., Foged, N. T., & Delaissé, J.-M. (2004) · Bone · doi:10.1016/j.bone.2004.06.019 · Cited by 145 · see citing works
Self-citationEverts, V. E., Delaissé, J., Korper, W., & Beertsen, W. (1998) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1998.13.9.1420 · Cited by 134 · see citing works
Self-citationOblander, S. A., Zhou, Z., Gálvez, B. G., STARCHER, B. C., Shannon, J. M., Durbeej, M., Arroyo, A. G., Tryggvason, K., & Apte, S. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.09.033 · Cited by 125 · see citing works
Wang, K., Yamamoto, H., Chin, J. R., Werb, Z., & Vu, T. H. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m403114200 · Cited by 118 · see citing works
The Significance of Matrix Metalloproteinases during Early Stages of Tumor Progressiona
Lochter, A., Sternlicht, M. D., Werb, Z., & Bissell, M. J. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb10116.x · Cited by 119 · see citing works
Nyman, J. S., Lynch, C. C., Perrien, D. S., Thiolloy, S., O’Quinn, E. C., Patil, C. A., Bi, X., Pharr, G. M., Mahadevan-Jansen, A. M., & Mundy, G. R. (2010) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.326 · Cited by 111 · see citing works
Osteoclast formation and resorption
Lerner, U. H. (2000) · Matrix Biology · doi:10.1016/s0945-053x(00)00052-4 · Cited by 114 · see citing works
Lewis, M. P., Tippett, H. L., Sinanan, A., Morgan, M. J., & Hunt, N. P. (2000) · Journal of Muscle Research and Cell Motility · doi:10.1023/a:1005670507906 · Cited by 113 · see citing works
Bord, S., Horner, A. M., Hembry, R. M., & Compston, J. E. (1998) · Bone · doi:10.1016/s8756-3282(98)00064-7 · Cited by 113 · see citing works
Expression of VEGF and MMP-9 in giant cell tumor of bone and other osteolytic lesions
Kumta, S. M., Huang, L., Cheng, Y. Y., Chow, L. T. C., Lee, K., & Zheng, M. (2003) · Life Sciences · doi:10.1016/s0024-3205(03)00434-x · Cited by 113 · see citing works
Dong, Z., Bonfil, R. D., Chinni, S. R., Deng, X., Filho, J. C. T., Bernardo, M. M., Vaishampayan, U. N., Che, M., Sloane, B. F., Sheng, S., et al. (2005) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)62337-1 · Cited by 111 · see citing works
Schaller, S., Henriksen, K., Høegh-Andersen, P., Søndergaard, B. C., Sumer, E. U., Tankó, L. B., Qvist, P., & Karsdal, M. A. (2005) · Assay and Drug Development Technologies · doi:10.1089/adt.2005.3.553 · Cited by 112 · see citing works
Interleukin 17 synergises with tumour necrosis factor α to induce cartilage destruction in vitro
van Bezooijen, R. L., van der Wee-Pals, L., Papapoulos, S. E., & Löwik, C. W. G. M. (2002) · Annals of the Rheumatic Diseases · doi:10.1136/ard.61.10.870 · Cited by 108 · see citing works
Peng, H., Troen, T., Ovejero, M. D. C., Kirkegaard, T., Andersen, T. L., Byrjalsen, I., Ferreras, M., Sato, T., Shapiro, S. D., Foged, N. T., et al. (2003) · Bone · doi:10.1016/j.bone.2003.08.011 · Cited by 107 · see citing works
Self-citationCranberry Proanthocyanidins Inhibit MMP Production and Activity
La, V. D., Howell, A. B., & Grenier, D. (2009) · Journal of Dental Research · doi:10.1177/0022034509339487 · Cited by 107 · see citing works
Lineage-committed osteoclast precursors circulate in blood and settle down into bone
Muto, A., Mizoguchi, T., Udagawa, N., Ito, S., Kawahara, I., Abiko, Y., Arai, A., Harada, S., Kobayashi, Y., Nakamichi, Y., et al. (2011) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.490 · Cited by 105 · see citing works
Newberry, E. P., Willis, D., Latifi, T. N., Boudreaux, J. M., & Towler, D. A. (1997) · Molecular Endocrinology · doi:10.1210/mend.11.8.9958 · Cited by 104 · see citing works
The origins and roles of osteoclasts in bone development, homeostasis and repair
Yahara, Y., Nguyen, T., Ishikawa, K., Kamei, K., & Alman, B. A. (2022) · Development · doi:10.1242/dev.199908 · Cited by 107 · see citing works
Stage-Specific Secretion of HMGB1 in Cartilage Regulates Endochondral Ossification
Taniguchi, N., Yoshida, K., Ito, T., Tsuda, M., Mishima, Y., Furumatsu, T., Ronfani, L., Abeyama, K., Kawahara, K.-I., Komiya, S., et al. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00130-07 · Cited by 101 · see citing works
Sato, T., Foged, N. T., & Delaissé, J.-M. (1998) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1998.13.1.59 · Cited by 98 · see citing works
Self-citationExpression of metalloproteinase-13 (collagenase-3) is induced during fracture healing in mice
Yamagiwa, H., Tokunaga, K., Hayami, T., Hatano, K., Uchida, M., Endo, N., & Takahashi, H. (1999) · Bone · doi:10.1016/s8756-3282(99)00157-x · Cited by 98 · see citing works
Hillegass, J., Villano, C. M., Cooper, K. R., & White, L. A. (2007) · Toxicological Sciences · doi:10.1093/toxsci/kfm192 · Cited by 96 · see citing works
MMP9 protects against LPS-induced inflammation in osteoblasts
Zhang, H., Liu, L., Jiang, C., Pan, K., Deng, J., & Wan, C. (2019) · Innate Immunity · doi:10.1177/1753425919887236 · Cited by 97 · see citing works
Hyaluronan–CD44 interaction hampers migration of osteoclast-like cells by down-regulating MMP-9
Spessotto, P., Rossi, F. M., Degan, M., Francia, R. D., Perris, R., Colombatti, A., & Gattei, V. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200202120 · Cited by 95 · see citing works
Ortéga, N., Behonick, D. J., Colnot, C., Cooper, D. N. W., & Werb, Z. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-12-1119 · Cited by 96 · see citing works
Kananen, K., Volin, L., Laitinen, K., Alfthan, H. V., Ruutu, T., & Välimäki, M. J. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-2161 · Cited by 89 · see citing works
Deckers, M. M. L., van Beek, E. R., van der Pluijm, G., Wetterwald, A., van der Wee-Pals, L. J. A., Cecchini, M. G., Papapoulos, S. E., & Löwik, C. W. G. M. (2002) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2002.17.6.998 · Cited by 86 · see citing works
Hand2 Regulates Extracellular Matrix Remodeling Essential for Gut-Looping Morphogenesis in Zebrafish
Yin, C., Kikuchi, K., Hochgreb, T., Poss, K. D., & Stainier, D. Y. R. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.05.009 · Cited by 87 · see citing works
Destroy to Rebuild: The Connection Between Bone Tissue Remodeling and Matrix Metalloproteinases
Hardy, E., & Fernández-Patrón, C. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00047 · Cited by 85 · see citing works
Llavaneras, A., Ramamurthy, N. S., Heikkilä, P., Teronen, O. P., Salo, T. A., Rifkin, B. R., RYAN, M. E., Golub, L. M., & Sorsa, T. A. (2001) · Journal of Periodontology · doi:10.1902/jop.2001.72.8.1069 · Cited by 80 · see citing works
Morgan, H., Tumber, A., & Hill, P. A. (2004) · International Journal of Cancer · doi:10.1002/ijc.20056 · Cited by 77 · see citing works
Bone degradation machinery of osteoclasts: An HIV-1 target that contributes to bone loss
Raynaud-Messina, B., Bracq, L., Dupont, M., Souriant, S., Usmani, S. M., Proag, A., Pingris, K., Soldan, V., Thibault, C., Capilla, F., et al. (2018) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1713370115 · Cited by 69 · see citing works
Immunolocalization of matrix metalloproteinase-13 on bone surface under osteoclasts in rat tibia
Nakamura, H., Sato, G., Hirata, A., & Yamamoto, T. (2003) · Bone · doi:10.1016/j.bone.2003.09.001 · Cited by 77 · see citing works
MMP-2 and MMP-9 and Their Tissue Inhibitors in the Plasma of Preterm and Term Neonates
Schulz, C., Sawicki, G., Lemke, R. P., Roeten, B., Schulz, R., & Cheung, P. (2004) · Pediatric Research · doi:10.1203/01.pdr.0000120683.68630.fb · Cited by 74 · see citing works
Lochter, A., & Bissell, M. J. (1999) · Apmis · doi:10.1111/j.1699-0463.1999.tb01535.x · Cited by 73 · see citing works
Rice, D. P. C., Kim, H.-J., & Thesleff, I. (1997) · Bone · doi:10.1016/s8756-3282(97)00182-8 · Cited by 73 · see citing works
Actin polymerization modulates CD44 surface expression, MMP‐9 activation, and osteoclast function
Samanna, V., Ma, T., Mak, T. W., Rogers, M. J., & Chellaiah, M. A. (2007) · Journal of Cellular Physiology · doi:10.1002/jcp.21137 · Cited by 71 · see citing works
The Cellular Actions of Interleukin-11 on Bone Resorption in Vitro
Hill, P. A., Tumber, A., Papaioannou, S., & Meikle, M. C. (1998) · Endocrinology · doi:10.1210/en.139.4.1564 · Cited by 71 · see citing works
Rantakokko, J., Uusitalo‐Järvinen, H., Jämsä, T. J., Tuukkanen, J., Aro, H. T., & VUORIO, E. I. (1999) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1999.14.11.1934 · Cited by 70 · see citing works
Gene Expression Analyses of Subchondral Bone in Early Experimental Osteoarthritis by Microarray
Zhang, R., Fang, H., Chen, Y., Shen, J., Lu, H., Zeng, C., Ren, J., Zeng, H., Li, Z., Chen, S., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032356 · Cited by 68 · see citing works
Stromal cell-derived factor-1 (CXCL12) and its role in bone and muscle biology
Gilbert, W. B., Bragg, R., Elmansi, A. M., McGee‐Lawrence, M. E., Isales, C. M., Hamrick, M. W., Hill, W., & Fulzele, S. (2019) · Cytokine · doi:10.1016/j.cyto.2019.154783 · Cited by 66 · see citing works
Winding, B., NicAmhlaoibh, R., Misander, H., Høegh-Andersen, P., Andersen, T. L., Holst‐Hansen, C., Heegaard, A., Foged, N. T., Brünner, N., & Delaissé, J. (2002) · PubMed · Cited by 67 · see citing works
Self-citationFranco, G. C. N., Kajiya, M., Nakanishi, T., Ohta, K., Rosalen, P. L., Groppo, F. C., Ernst, C. W. O., Boyesen, J. L., Bartlett, J. D., Stashenko, P., et al. (2011) · Experimental Cell Research · doi:10.1016/j.yexcr.2011.03.014 · Cited by 61 · see citing works
Cbfa-1 mediates nitric oxide regulation of MMP-13 in osteoblasts
Zaragoza, C., López-Rivera, E., García‐Rama, C., Saura, M., Martı́nez-Ruiz, A., Lizarbe, T. R., Martín-de-Lara, F., & Lamas, S. (2006) · Journal of Cell Science · doi:10.1242/jcs.02895 · Cited by 61 · see citing works
Tissue Inhibitor of Metalloproteinase-3 (TIMP-3) Regulates Hematopoiesis and Bone Formation In Vivo
Shen, Y., Winkler, I. G., Barbier, V., Sims, N. A., Hendy, J., & Lévesque, J.-P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013086 · Cited by 60 · see citing works
Matrix Metalloproteinases in Multiple Myeloma
Kelly, T. J., Børset, M., Abe, E., Gaddy-Kurten, D., & Sanderson, R. D. (2000) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428190009089428 · Cited by 60 · see citing works
Cathepsin K mRNA Detection Is Restricted to Osteoclasts During Fetal Mouse Development
Dodds, R. A., Connor, J. R., Drake, F. H., Feild, J. A., & Gowen, M. (1998) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1998.13.4.673 · Cited by 60 · see citing works
Shastri, V. P. (2009) · Advanced Materials · doi:10.1002/adma.200900608 · Cited by 59 · see citing works
Matrix Metalloproteinases in Cerebrovascular Diseases
Fatar, M., Stroick, M., Griebe, M., & Hennerici, M. G. (2005) · Cerebrovascular Diseases · doi:10.1159/000087197 · Cited by 58 · see citing works
Localisation of matrix metalloproteinases and TIMP-2 in resorbing mouse bone
Dew, G., Murphy, G., Stanton, H., Vallon, R., Angel, P. E., Reynolds, J. J., & Hembry, R. M. (2000) · Cell and Tissue Research · doi:10.1007/s004419900166 · Cited by 57 · see citing works
Blavier, L., & DeClerck, Y. A. (1997) · Molecular Biology of the Cell · doi:10.1091/mbc.8.8.1513 · Cited by 56 · see citing works
Self-citationWoodward, J. K. L., Holen, I., Coleman, R. E., & Buttle, D. J. (2007) · Bone · doi:10.1016/j.bone.2007.07.024 · Cited by 55 · see citing works
Integrin α1β1 mediates collagen induction of MMP-13 expression in MC615 chondrocytes
Ronzière, M., Aubert‐Foucher, E., Gouttenoire, J., Bernaud, J., Herbage, D., & Mallein‐Gérin, F. (2005) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2005.08.003 · Cited by 54 · see citing works
The “love–hate” relationship between osteoclasts and bone matrix
Rucci, N., & Teti, A. M. (2016) · Matrix Biology · doi:10.1016/j.matbio.2016.02.009 · Cited by 51 · see citing works
Lee, E. R., Lamplugh, L., Davoli, M. A., Beauchemin, A., Chan, K., Mort, J. S., & Leblond, C. P. (2001) · Developmental Dynamics · doi:10.1002/dvdy.1168 · Cited by 50 · see citing works
Søe, K., Delaisse, J.-M., & Borggaard, X. G. (2021) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2020.05.016 · Cited by 49 · see citing works
Self-citationSteering the osteoclast through the demineralization–collagenolysis balance
Søe, K., Merrild, D. M. H., & Delaissé, J. (2013) · Bone · doi:10.1016/j.bone.2013.06.007 · Cited by 49 · see citing works
Self-citationWang, K., Vishwanath, P., Eichler, G. S., Al-Sebaei, M. O., Edgar, C. M., Einhorn, T. A., Smith, T. F., & Gerstenfeld, L. C. (2006) · Matrix Biology · doi:10.1016/j.matbio.2006.02.001 · Cited by 49 · see citing works
Syggelos, S. A., Aletras, A. J., Smirlaki, I., & Skandalis, S. S. (2013) · BioMed Research International · doi:10.1155/2013/230805 · Cited by 48 · see citing works
Rubino, M. T., Agamennone, M., Campestre, C., Campiglia, P., Cremasco, V., Faccio, R., Laghezza, A., Loiodice, F., Maggi, D., Panza, E., et al. (2011) · ChemMedChem · doi:10.1002/cmdc.201000540 · Cited by 48 · see citing works
Hydroxyapatite Induces Autolytic Degradation and Inactivation of Matrix Metalloproteinase-1 and -3
Kremer, E. A., Chen, Y., Suzuki, K., Nagase, H., & Gorski, J. P. (1998) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1998.13.12.1890 · Cited by 46 · see citing works
Ling, Z., Yang, C. H., Tan, J., Dou, C., & Chen, Y. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03966-9 · Cited by 43 · see citing works
Singh, A., Nelson-Moon, Z. L., Thomas, G. J., Hunt, N. P., & Lewis, M. P. (2000) · Archives of Oral Biology · doi:10.1016/s0003-9969(00)00020-0 · Cited by 43 · see citing works
- Authors
- Blavier, L., & Delaissé, J. M.
- Affiliations
- UCLouvain (BE)
- ORCID
- Delaissé, J. M.
- Venue
- Journal of Cell Science
- Publisher
- The Company of Biologists
- Published
- 1995-12-01
- Volume
- 108
- Issue
- 12
- Pages
- 3649-3659
- ISSN
- 0021-9533 (ISSN-L)
- 1477-9137
- OpenAlex
- W1953148896
- Cited by
- 221
- References
- 61
- Citations by year
- 2025: 1 · 2023: 2 · 2022: 4 · 2021: 5 · 2020: 8 · 2019: 9 · 2018: 8 · 2017: 3 · 2016: 3 · 2015: 3 · 2014: 4 · 2013: 8 · 2012: 6
- FWCI
- 2.34
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Cell Science (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Libraries (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Health Sciences › Medicine › Rheumatology › Bone and Dental Protein Studies
- Keywords
- matrix metalloproteinases, osteoclast recruitment, demineralization, MMP-9, MMP-13, bone resorption, osteoid, calcified cartilage, bisphosphonates, carbonic anhydrase inhibitors, cysteine protease inhibitors, hypertrophic chondrocytes, tartrate-resistant acid phosphatase
- MeSH terms
- Tartrate-Resistant Acid Phosphatase, Acid Phosphatase, Animals, Bone Marrow, Bone Marrow Cells, Bone Matrix, Bone Resorption, Cell Movement, Enzyme Inhibitors, Embryonic and Fetal Development, Isoenzymes, Kinetics, Metalloendopeptidases, Osteoclasts, Stem Cells, In Situ Hybridization, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review