Wnt signalling in osteoblasts regulates expression of the receptor activator of NFκB ligand and inhibits osteoclastogenesis in vitro

Journal of Cell Science

Volumn 119, Issue 7, 2006, Pages 1283-1296

  Spencer, Gary J ^a   Utting, Jennifer C ^b   Etheridge, Sharon L ^a,c   Arnett, Timothy R ^b   Genever, Paul G ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

catenin; Osteoblast; Osteoclast; Receptor activator of NF B ligand; T cell factor; Wnt

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; BETA CATENIN; CD14 ANTIGEN; GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM CHLORIDE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; MESSENGER RNA; OSTEOCLAST DIFFERENTIATION FACTOR; WNT PROTEIN; WNT3A PROTEIN;

ANIMAL CELL; ARTICLE; BONE METABOLISM; CELL ACTIVITY; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; RAT; SIGNAL TRANSDUCTION; SPLEEN CELL; STEM CELL;

ACID PHOSPHATASE; ANIMALS; ANIMALS, NEWBORN; BETA CATENIN; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL NUCLEUS; CELLS, CULTURED; CLONE CELLS; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; CYTOSKELETAL PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; GENE EXPRESSION REGULATION; GTP-BINDING PROTEINS; HUMANS; ISOENZYMES; LDL-RECEPTOR RELATED PROTEINS; LITHIUM CHLORIDE; MALE; MEMBRANE GLYCOPROTEINS; MONOCYTES; NUCLEAR PROTEINS; OSTEOBLASTS; OSTEOCLASTS; PROMOTER REGIONS (GENETICS); RANK LIGAND; RATS; RATS, WISTAR; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; RNA, MESSENGER; SIGNAL TRANSDUCTION; SPLEEN; WNT PROTEINS;

ANIMALIA;

EID: 33646808104     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02883     Document Type: Article

References (64)

1. Arnett, T. R. and Dempster, D. W. (1986). Effect of pH on bone resorption by rat osteoclasts in vitro. Endocrinology 119, 119-124.
2. Arnett, T. R., Gibbons, D. C., Utting, J. C., Orriss, I. R., Hoebertz, A., Rosendaal, M. and Meghji, S. (2003). Hypoxia is a major stimulator of osteoclast formation and bone resorption. J. Cell Physiol. 196, 2-8.
3. Atkins, G. J., Kostakis, P., Pan, B., Farrugia, A., Gronthos, S., Evdokiou, A., Harrison, K., Findlay, D. M. and Zannettino, A. C. (2003). RANKL expression is related to the differentiation state of human osteoblasts. J. Bone Miner Res. 18, 1088-1098.
4. Babij, P., Zhao, W., Small, C., Kharode, Y., Yaworsky, P. J., Bouxsein, M. L., Reddy, P. S., Bodine, P. V., Robinson, J. A., Bhat, B. et al. (2003). High bone mass in mice expressing a mutant LRP5 gene. J. Bone Miner Res. 18, 960-974.
5. Bellows, C. G., Aubin, J. E., Heersche, J. N. and Antosz, M. E. (1986). Mineralized bone nodules formed in vitro from enzymatically released rat calvaria cell populations. Calcif. Tissue Int. 38, 143-154.
6. Beresford, J. N., Gallagher, J. A., Poser, J. W. and Russell, R. G. (1984). Production of osteocalcin by human bone cells in vitro. Effects of 1,25(OH)2D3, 24,25(OH)2D3, parathyroid hormone, and glucocorticoids. Metab. Bone Dis. Relat. Res. 5, 229-234.
7. Berridge, M. J., Downes, C. P. and Hanley, M. R. (1989). Neural and developmental actions of lithium: a unifying hypothesis. Cell 59, 411-419.
8. Bodine, P. V., Zhao, W., Kharode, Y. P., Bex, F. J., Lambert, A. J., Goad, M. B., Gaur, T., Stein, G. S., Lian, J. B. and Komm, B. S. (2004). The Wnt antagonist secreted frizzled-related protein-1 is a negative regulator of trabecular bone formation in adult mice. Mol. Endocrinol. 18, 1222-1237.
9. Boyden, L. M., Mao, J., Belsky, J., Mitzner, L., Farhi, A., Mitnick, M. A., Wu, D., Insogna, K. and Lifton, R. P. (2002). High bone density due to a mutation in LDL-receptor-related protein 5. N. Engl. J. Med. 346, 1513-1521.
10. Bradbury, J. M., Niemeyer, C. C., Dale, T. C. and Edwards, P. A. (1994). Alterations of the growth characteristics of the fibroblast cell line C3H 10T1/2 by members of the Wnt gene family. Oncogene 9, 2597-2603.
11. Brantjes, H., Roose, J., van De, W. M. and Clevers, H. (2001). All Tcf HMG box transcription factors interact with Groucho-related co-repressors. Nucleic Acids Res. 29, 1410-1419.
12. De Boer, J., Siddappa, R., Gaspar, C., Van Apeldoorn, A., Fodde, R. and Van Blitterswijk, C. (2004). Wnt signaling inhibits osteogenic differentiation of human mesenchymal stem cells. Bone 34, 818-826.
13. Deng, J., Xia, W., Miller, S. A., Wen, Y., Wang, H. Y. and Hung, M. C. (2004). Crossregulation of NF-kappaB by the APC/GSK-3beta/beta-catenin pathway. Mol. Carcinog. 39, 139-146.
14. Derksen, P. W., Tjin, E., Meijer, H. P., Klok, M. D., MacGillavry, H. D., van Oers, M. H., Lokhorst, H. M., Bloem, A. C., Clevers, H., Nusse, R. et al. (2004). Illegitimate WNT signaling promotes proliferation of multiple myeloma cells. Proc. Natl. Acad. Sci. USA 101, 6122-6127.
15. Deyama, Y., Takeyama, S., Koshikawa, M., Shirai, Y., Yoshimura, Y., Nishikata, M., Suzuki, K. and Matsumoto, A. (2000). Osteoblast maturation suppressed osteoclastogenesis in coculture with bone marrow cells. Biochem. Biophys. Res. Commun. 274, 249-254.
16. Drayer, A. L., Van der, K. J., Mayr, G. W. and Van Haastert, P. J. (1994). Role of phospholipase C in Dictyostelium: formation of inositol 1,4,5- trisphosphate and normal development in cells lacking phospholipase C activity. EMBO J. 13, 1601-1609.
17. Etheridge, S. L., Spencer, G. J., Heath, D. J. and Genever, P. G. (2004). Expression profiling and functional analysis of wnt signaling mechanisms in mesenchymal stem cells. Stem Cells 22, 849-860.
18. Glass, D. A., Bialek, P., Ahn, J. D., Starbuck, M., Patel, M. S., Clevers, H., Taketo, M. M., Long, F., McMahon, A. P., Lang, R. A. et al. (2005). Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev. Cell 8, 751-764.
19. Gong, Y., Slee, R. B., Fukai, N., Rawadi, G., Roman-Roman, S., Reginato, A. M. Wang, H., Cundy, T., Glorieux, F. H., Lev, D. et al. (2001). LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 107, 513-523.
20. Gregory, C. A., Singh, H., Perry, A. S. and Prockop, D. J. (2003). The Wnt signaling inhibitor dickkopf-1 is required for reentry into the cell cycle of human adult stem cells from bone marrow. J. Biol. Chem. 278, 28067-28078.
21. Hartmann, C. and Tabin, C. J. (2000). Dual roles of Wnt signaling during chondrogenesis in the chicken limb. Development 127, 3141-3159.
22. Hartmann, C. and Tabin, C. J. (2001). Wnt-14 plays a pivotal role in inducing synovial joint formation in the developing appendicular skeleton. Cell 104, 341-351.
23. Hausler, K. D., Horwood, N. J., Chuman, Y., Fisher, J. L., Ellis, J., Martin, T. J. Rubin, J. S. and Gillespie, M. T. (2004). Secreted frizzled-related protein-1 inhibits RANKL-dependent osteoclast formation. J. Bone Miner. Res. 19, 1873-1881.
24. Hedgepeth, C. M., Conrad, L. J., Zhang, J., Huang, H. C., Lee, V. M. and Klein, P. S. (1997). Activation of the Wnt signaling pathway: a molecular mechanism for lithium action. Dev. Biol. 185, 82-91.
25. Hoebertz, A. and Arnett, T. R. (2003). Isolated osteoclast cultures. Methods Mol. Med. 80, 53-64.
26. Holmen, S. L., Giambernardi, T. A., Zylstra, C. R., Buckner-Berghuis, B.D., Resau, J. H., Hess, J. F., Glatt, V., Bouxsein, M. L., Ai, M., Warman, M. L. et al. (2004). Decreased BMD and limb deformities in mice carrying mutations in both Lrp5 and Lrp6. J. Bone Miner Res. 19, 2033-2040.
27. Holmen, S. L., Zylstra, C. R., Mukherjee, A., Sigler, R. E., Faugere, M.C., Bouxsein, M. L., Deng, L., Clemens, T. L. and Williams, B. O. (2005). Essential role of beta-catenin in postnatal bone acquisition. J. Biol. Chem. 280, 21162-21168.
28. Ikeda, S., Kishida, S., Yamamoto, H., Murai, H., Koyama, S. and Kikuchi, A. (1998). Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin. EMBO J. 17, 1371-1384.
29. Johnson, M. L., Harnish, K., Nusse, R. and Van Hul, W. (2004). LRP5 and Wnt signaling: a union made for bone. J. Bone Miner Res. 19, 1749-1757.
30. Kahler, R. A. and Westendorf, J. J. (2003). Lymphoid enhancer factor-1 and beta-catenin inhibit Runx2-dependent transcriptional activation of the osteocalcin promoter. J. Biol. Chem. 278, 11937-11944.
31. Kao, K., Masui, Y. and Elinson, R. (1986). Lithium-induced respecification of pattern in Xenopus laevis embryos. Nature 322, 371-373.
32. Kato, M., Patel, M. S., Levasseur, R., Lobov, I., Chang, B. H., Glass, D.A., Hartmann, C., Li, L., Hwang, T. H., Brayton, C. F. et al. (2002). Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J. Cell Biol. 157, 303-314.
33. Kharode, Y., Green, P., Marzolf, J., Zhao, W., Askew, R. and Bex, F.(2003). Alteration of bone density in mice due to heterozygous inactivation of LRP6. J. Bone Miner Res. S60.
34. Kishida, S., Yamamoto, H., Ikeda, S., Kishida, M., Sakamoto, L, Koyama, S. and Kikuchi, A. (1998). Axin, a negative regulator of the wnt signaling pathway, directly interacts with adenomatous polyposis coli and regulates the stabilization of beta-catenin. J. Biol. Chem. 273, 10823-10826.
35. Kitazawa, S., Kajimoto, K., Kondo, T. and Kitazawa, R. (2003). Vitamin D3 supports osteoclastogenesis via functional vitamin D response element of human RANKL gene promoter. J. Cell Biochem. 89, 771-777.
36. Klein, P. S. and Melton, D. A. (1996). A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. USA 93, 8455-8459.
37. Little, R. D., Carulli, J. P., Del Mastro, R. G., Dupuis, J., Osborne, M., Folz, C., Manning, S. P., Swain, P. M., Zhao, S. C., Eustace, B. et al. (2002). A mutation in the LDL receptor-related protein 5 gene results in the autosomal dominant high-bone-mass trait. Am. J. Hum. Genet. 70, 11-19.
38. Mao, B., Wu, W., Li, Y., Hoppe, D., Stannek, P., Glinka, A. and Niehrs,C. (2001). LDL-receptor-related protein 6 is a receptor for Dickkopf proteins. Nature 411, 321-325.
39. Monaghan, H., Bubb, V. J., Sirimujalin, R., Millward-Sadler, S. J. and Salter, D. M. (2001). Adenomatous polyposis coli (APC), beta-catenin, and cadberin are expressed in human bone and cartilage. Histopathology 39, 611-619.
40. Moon, R. T., Brown, J. D., Yang-Snyder, J. A. and Miller, J. R. (1997). Structurally related receptors and antagonists compete for secreted Wnt ligands. Cell 88, 725-728.
41. Patel, M. S. and Karsenty, G. (2002). Regulation of bone formation and vision by LRP5. N. Engl. J. Med. 346, 1572-1574.
42. Peet, N. M., Grabowski, P. S., Laketic-Ljubojevic, I. and Skerry, T. M. (1999). The glutamate receptor antagonist MK801 modulates bone resorption in vitro by a mechanism predominantly involving osteoclast differentiation. FASEB J. 13, 2179-2185.
43. Pepersack, T., Corazza, F., Demulder, A., Guns, M., Fondu, P. and Bergmann, P. (1994a). Lithium inhibits calcitriol-stimulated formation of multinucleated cells in human long-term marrow cultures. J. Bone Miner Res. 9, 645-650.
44. Pepersack, T., Corvilain, J. and Bergmann, P. (1994b). Effects of lithium on bone resorption in cultured foetal rat long-bones. Eur. J. Clin. Invest. 24, 400-405.
45. Rawadi, G., Vayssiere, B., Dunn, F., Baron, R. and Roman-Roman, S. (2003). BMP-2 controls alkaline phosphatase expression and osteoblast mineralization by a Wnt autocrine loop. J. Bone Miner. Res. 18, 1842-1853.
46. Rodan, G. A. and Martin, T. J. (2000). Therapeutic approaches to bone diseases. Science 289, 1508-1514.
47. Rudnicki, J. A. and Brown, A. M. (1997). Inhibition of chondrogenesis by Wnt gene expression in vivo and in vitro. Dev. Biol. 185, 104-118.
48. Sadot, E., Simcha, I., Shtutman, M., Ben Ze'ev, A. and Geiger, B. (1998). Inhibition of beta-catenin-mediated transactivation by cadherin derivatives. Proc. Natl. Acad. Sci. USA 95, 15339-15344.
49. Shea, C. M., Edgar, C. M., Einhorn, T. A. and Gerstenfeld, L. C. (2003). BMP treatment of C3H10T1/2 mesenchymal stem cells induces both chondrogenesis and osteogenesis. J. Cell Biochem. 90, 1112-1127.
50. Stambolic, V., Ruel, L. and Woodgett, J. R. (1996). Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr Biol. 6, 1664-1668.
51. Suda, T., Takahashi, N., Udagawa, N., Jimi, E., Gillespie, M. T. and Martin, T. J. (1999). Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr Rev. 20, 345-357.
52. Tamai, K., Semenov, M., Kato, Y., Spokony, R., Liu, C., Katsuyama, Y., Hess, F., Saint-Jeannet, J. P. and He, X. (2000). LDL-receptor-related proteins in Wnt signal transduction. Nature 407, 530-535.
53. Tian, E., Zhan, F., Walker, R., Rasmussen, E., Ma, Y., Barlogie, B. and Shaughnessy, J. D., Jr (2003). The role of the Wnt-signaling antagonist DKK1 in the development of osteolytic lesions in multiple myeloma. N. Engl. J. Med. 349, 2483-2494.
54. Topol, L., Jiang, X., Choi, H., Garrett-Beal, L., Carolan, P. J. and Yang, Y. (2003). Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent beta-catenin degradation. J. Cell Biol. 162, 899-908.
55. Van Den Berg, D. J., Sharma, A. K., Bruno, E. and Hoffman, R. (1998). Role of members of the Wnt gene family in human hematopoiesis. Blood 92, 3189-3202.
56. Van Lookeren Campagne, M. M., Wang, M., Spek, W., Peters, D. and Schaap,P. (1988). Lithium respecifies cyclic AMP-induced cell-type specific gene expression in Dictyostelium. Dev. Genet. 9, 589-596.
57. van Noort, M., Meeldijk, J., van der, Z. R., Destree, O. and Clevers, H. (2002), Wnt signaling controls the phosphorylation status of beta-catenin. J. Biol. Chem. 277, 17901-17905.
58. Van Wesenbeeck, L., Cleiren, E., Gram, J., Beals, R. K., Benichou, O., Scopelliti, D., Key, L., Renton, T., Bartels, C., Gong, Y. et al. (2003). Six novel missense mutations in the LDL receptor-related protein 5 (LRP5) gene in different conditions with an increased bone density. Am. J. Hum. Genet. 72, 763-771.
59. Willert, J., Epping, M., Pollack, J. R., Brown, P. O. and Nusse, R. (2002). A transcriptional response to Wnt protein in human embryonic carcinoma cells. BMC. Dev. Biol. 2, 8.
60. Willert, K. and Nusse, R. (1998). Beta-catenin: a key mediator of Wnt signaling. Curr. Opin. Genet. Dev. 8, 95-102.
61. Willert, K., Brown, J. D., Danenberg, E., Duncan, A. W., Weissman, I. L., Reya T., Yates, J. R., III and Nusse, R. (2003). Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423, 448-452.
62. Yamane, T., Kunisada, T., Tsukamoto, H., Yamazaki, H., Niwa, H., Takada, S. and Hayashi, S. I. (2001). Wnt signaling regulates hemopoiesis through stromal cells. J. Immunol. 167, 765-772.
63. Zakany, J. and Duboule, D. (1993). Correlation of expression of Wnt-1 in developing limbs with abnormalities in growth and skeletal patterning. Nature 362, 546-549.
64. Zhurinsky, J., Shtutman, M. and Ben Ze'ev, A. (2000). Differential mechanisms of LEF/TCF family-dependent transcriptional activation by beta-catenin and plakoglobin. Mol. Cell. Biol. 20, 4238-4252.