RANK ligand signaling modulates the matrix metalloproteinase-9 gene expression during osteoclast differentiation

Experimental Cell Research

Volumn 313, Issue 1, 2007, Pages 168-178

  Sundaram, Kumaran ^a   Nishimura, Riko ^b   Senn, Joseph ^a   Youssef, Rimon F ^a   London, Steven D ^c   Reddy, Sakamuri V ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b OSAKA UNIVERSITY   (Japan)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Matrix metalloproteinase 9 (MMP 9); NFAT; Osteoclast; RANK ligand (RANKL); TRAF6

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; GELATINASE B; LUCIFERASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; OLIGONUCLEOTIDE; OSTEOCLAST DIFFERENTIATION FACTOR; PEPTIDE; PROTEIN VIVIT; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NFAT; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; MOUSE; NONHUMAN; OSTEOCLAST; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; REPORTER GENE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; START CODON;

EID: 33845654949     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2006.10.001     Document Type: Article

References (45)

1. Reponen P., Sahlberg C., Munaut C., Thesleff I., and Tryggvason K. High expression of 92-kD type IV collagenase (gelatinase B) in the osteoclast lineage during mouse development. J. Cell Biol. 124 (1994) 1091-1102
2. Wucherpfennig A.L., Li Y.P., Stetler-Stevenson W.G., Rosenberg A.E., and Stashenko P. Expression of 92 kD type IV collagenase/gelatinase B in human osteoclasts. J. Bone Miner. Res. 9 (1994) 549-556
3. Tsai C.H., Chen Y.J., Huang F.M., Su Y.F., and Chang Y.C. The upregulation of matrix metalloproteinase-9 in inflamed human dental pulps. J. Endod. 31 (2005) 860-862
4. Kusano K., Miyaura C., Inada M., Tamura T., Ito A., Nagase H., Kamoi K., and Suda T. 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
5. Zhou M., Zhang Y., Ardans J.A., and Wahl L.M. Interferon-gamma differentially regulates monocyte matrix metalloproteinase-1 and -9 through tumor necrosis factor-alpha and caspase 8. J. Biol. Chem. 278 (2003) 45406-45413
6. Yu X., Huang Y., Collin-Osdoby P., and Osdoby P. Stromal cell-derived factor-1 (SDF-1) recruits osteoclast precursors by inducing chemotaxis, matrix metalloproteinase-9 (MMP-9) activity, and collagen transmigration. J. Bone Miner. Res. 18 (2003) 1404-1418
7. Delaisse J.M., Andersen T.L., Engsig M.T., Henriksen K., Troen T., and Blavier L. Matrix metalloproteinases (MMP) and cathepsin K contribute differently to osteoclastic activities. Microsc. Res. Tech. 61 (2003) 504-513
8. 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. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93 (1998) 411-422
9. Colnot C., Thompson Z., Miclau T., Werb Z., and Helms J.A. Altered fracture repair in the absence of MMP9. Development 130 (2003) 4123-4133
10. Ortega N., Behonick D.J., Colnot C., Cooper D.N., and Werb Z. Galectin-3 is a downstream regulator of matrix metalloproteinase-9 function during endochondral bone formation. Mol. Biol. Cell 16 (2005) 3028-3039
11. Boyle W.J., Simonet W.S., and Lacey D.L. Osteoclast differentiation and activation. Nature 423 (2003) 337-342
12. Vignery A. Osteoclasts and giant cells: macrophage-macrophage fusion mechanism. Int. J. Exp. Pathol. 81 (2000) 291-304
13. Spessotto P., Rossi F.M., Degan M., Di Francia R., Perris R., Colombatti A., and Gattei V. Hyaluronan-CD44 interaction hampers migration of osteoclast-like cells by down-regulating MMP-9. J. Cell Biol. 158 (2002) 1133-1144
14. Theoleyre S., Wittrant Y., Couillaud S., Vusio P., Berreur M., Dunstan C., Blanchard F., Redini F., and Heymann D. Cellular activity and signaling induced by osteoprotegerin in osteoclasts: involvement of receptor activator of nuclear factor kappaB ligand and MAPK. Biochim. Biophys. Acta 1644 (2004) 1-7
15. Kanazawa K., Azuma Y., Nakano H., and Kudo A. TRAF5 functions in both RANKL- and TNFalpha-induced osteoclastogenesis. J. Bone Miner. Res. 18 (2003) 443-450
16. Teitelbaum S.L., and Ross F.P. Genetic regulation of osteoclast development and function. Nat. Rev., Genet. 4 (2003) 638-649
17. Takayanagi H., Kim S., Koga T., Nishina H., Isshiki M., Yoshida H., Saiura A., Isobe M., Yokochi T., Inoue J., Wagner E.F., Mak T.W., Kodama T., and Taniguchi T. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev. Cell 3 (2002) 889-901
18. Hirotani H., Tuohy N.A., Woo J.T., Stern P.H., and Clipstone N.A. The calcineurin/nuclear factor of activated T cells signaling pathway regulates osteoclastogenesis in RAW264.7 cells. J. Biol. Chem. 279 (2004) 13984-13992
19. Roach J., Choi S.J., Schaub R.L., Leach R.J., Roodman G.D., and Reddy S.V. Further characterization of the murine collagenase (type IVB) gene promoter and analysis of mRNA expression in murine tissues. Gene 208 (1998) 117-122
20. Munaut C., Salonurmi T., Kontusaari S., Reponen P., Morita T., Foidart J.M., and Tryggvason K. Murine matrix metalloproteinase 9 gene. 5′-upstream region contains cis-acting elements for expression in osteoclasts and migrating keratinocytes in transgenic mice. J. Biol. Chem. 274 (1999) 5588-5596
21. Quesada A.R., Barbacid M.M., Mira E., Fernandez-Resa P., Marquez G., and Aracil M. Evaluation of fluorometric and zymographic methods as activity assays for stromelysins and gelatinases. Clin. Exp. Metastasis 15 (1997) 26-32
22. Srinivasan S., Ito M., Kajiya H., Key Jr. L.L., Johnson-Pais T.L., and Reddy S.V. Functional characterization of human osteoclast inhibitory peptide-1 (OIP-1/hSca) gene promoter. Gene 371 (2006) 16-24
23. Koide M., Maeda H., Roccisana J.L., Kawanabe N., and Reddy S.V. Cytokine regulation and the signaling mechanism of osteoclast inhibitory peptide-1 (OIP-1/hSca) to inhibit osteoclast formation. J. Bone Miner. Res. 18 (2003) 458-465
24. Mukhopadhyay S., Munshi H.G., Kambhampati S., Sassano A., Platanias L.C., and Stack M.S. Calcium-induced matrix metalloproteinase 9 gene expression is differentially regulated by ERK1/2 and p38 MAPK in oral keratinocytes and oral squamous cell carcinoma. J. Biol. Chem. 279 (2004) 33139-43316
25. Ikeda F., Nishimura R., Matsubara T., Tanaka S., Inoue J., Reddy S.V., Hata K., Yamashita K., Hiraga T., Watanabe T., Kukita T., Yoshioka K., Rao A., and Yoneda T. Critical roles of c-Jun signaling in regulation of NFAT family and RANKL-regulated osteoclast differentiation. J. Clin. Invest. 114 (2004) 475-484
26. Suda T., Takahashi N., Udagawa N., Jimi E., Gillespie M.T., and Martin T.J. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr. Rev. 20 (1999) 345-357
27. Hsu H., Lacey D.L., Dunstan C.R., Solovyev I., Colombero A., Timms E., Tan H.L., Elliott G., Kelley M.J., Sarosi I., Wang L., Xia X.Z., Elliott R., Chiu L., Black T., Scully S., Capparelli C., Morony S., Shimamoto G., Bass M.B., and Boyle W.J. Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 3540-3545
28. Kanazawa K., and Kudo A. TRAF2 is essential for TNF-alpha-induced osteoclastogenesis. J. Bone Miner. Res. 20 (2005) 840-847
29. Kato Y., Lambert C.A., Colige A.C., Mineur P., Noel A., Frankenne F., Foidart J.M., Baba M., Hata R., Miyazaki K., and Tsukuda M. Acidic extracellular pH induces matrix metalloproteinase-9 expression in mouse metastatic melanoma cells through the phospholipase D-mitogen-activated protein kinase signaling. J. Biol. Chem. 280 (2005) 10938-10944
30. Rao A., Luo C., and Hogan P.G. Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 15 (1997) 707-747
31. Matsumoto M., Kogawa M., Wada S., Takayanagi H., Tsujimoto M., Katayama S., Hisatake K., and Nogi Y. Essential role of p38 mitogen-activated protein kinase in cathepsin K gene expression during osteoclastogenesis through association of NFATc1 and PU.1. J. Biol. Chem. 279 (2004) 45969-45979
32. Hogan P.G., Chen L., Nardone J., and Rao A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 17 (2003) 2205-2232
33. Lee S.E., Woo K.M., Kim S.Y., Kim H.M., Kwack K., Lee Z.H., and Kim H.H. The phosphatidylinositol 3-kinase, p38, and extracellular signal-regulated kinase pathways are involved in osteoclast differentiation. Bone 30 (2002) 71-77
34. Matsumoto M., Sudo T., Saito T., Osada H., and Tsujimoto M. Involvement of p38 mitogen-activated protein kinase signaling pathway in osteoclastogenesis mediated by receptor activator of NF-kappa B ligand (RANKL). J. Biol. Chem. 275 (2000) 31155-31161
35. Li X., Udagawa N., Itoh K., Suda K., Murase Y., Nishihara T., Suda T., and Takahashi N. p38 MAPK-mediated signals are required for inducing osteoclast differentiation but not for osteoclast function. Endocrinology 143 (2002) 3105-3113
36. Li X., Udagawa N., Takami M., Sato N., Kobayashi Y., and Takahashi N. p38 Mitogen-activated protein kinase is crucially involved in osteoclast differentiation but not in cytokine production, phagocytosis, or dendritic cell differentiation of bone marrow macrophages. Endocrinology 144 (2003) 4999-5005
37. Lee Z.H., and Kim H.H. Signal transduction by receptor activator of nuclear factor kappa B in osteoclasts. Biochem. Biophys. Res. Commun. 305 (2003) 211-214
38. Yang C.R., Wang J.H., Hsieh S.L., Wang S.M., Hsu T.L., and Lin W.W. Decoy receptor 3 (DcR3) induces osteoclast formation from monocyte/macrophage lineage precursor cells. Cell Death Differ. 11 Suppl 1 (2004) S97-S107
39. Hong S., Park K.K., Magae J., Ando K., Lee T.S., Kwon T.K., Kwak J.Y., Kim C.H., and Chang Y.C. Ascochlorin inhibits matrix metalloproteinase-9 expression by suppressing activator protein-1-mediated gene expression through the ERK1/2 signaling pathway: inhibitory effects of ascochlorin on the invasion of renal carcinoma cells. J. Biol. Chem. 280 (2005) 25202-25209
40. Porter C.M., Havens M.A., and Clipstone N.A. Identification of amino acid residues and protein kinases involved in the regulation of NFATc subcellular localization. J. Biol. Chem. 275 (2000) 3543-3551
41. Komarova S.V., Pereverzev A., Shum J.W., Sims S.M., and Dixon S.J. Convergent signaling by acidosis and receptor activator of NF-kappaB ligand (RANKL) on the calcium/calcineurin/NFAT pathway in osteoclasts. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 2643-2648
42. Wittrant Y., Theoleyre S., Couillaud S., Dunstan C., Heymann D., and Redini F. Regulation of osteoclast protease expression by RANKL. Biochem. Biophys. Res. Commun. 310 (2003) 774-778
43. Matsuo K., Galson D.L., Zhao C., Peng L., Laplace C., Wang K.Z., Bachler M.A., Amano H., Aburatani H., Ishikawa H., and Wagner E.F. Nuclear factor of activated T-cells (NFAT) rescues osteoclastogenesis in precursors lacking c-Fos. J. Biol. Chem. 279 (2004) 26475-26480
44. Crotti T.N., Flannery M., Walsh N.C., Fleming J.D., Goldring S.R., and McHugh K.P. NFATc1 regulation of the human beta3 integrin promoter in osteoclast differentiation. Gene 372 (2006) 92-102
45. Asagiri M., Sato K., Usami T., Ochi S., Nishina H., Yoshida H., Morita I., Wagner E.F., Mak T.W., Serfling E., and Takayanagi H. Autoamplification of NFATc1 expression determines its essential role in bone homeostasis. J. Exp. Med. 202 (2005) 1261-1269