Regulation of bone formation by osteoclasts involves Wnt/BMP signaling and the chemokine sphingosine-1-phosphate

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 52, 2008, Pages 20764-20769

  Pederson, Larry ^a   Ruan, Ming ^a   Westendorf, Jennifer J ^a,b   Khosla, Sundeep ^a   Oursler, Merry Jo ^a,b  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

Mineralization; Osteoblast

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CHEMOKINE; DICKKOPF 1 PROTEIN; SPHINGOSINE 1 PHOSPHATE; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; MESENCHYME; MOUSE; NONHUMAN; OSTEOCLAST; PRIORITY JOURNAL;

ANIMALS; BONE MORPHOGENETIC PROTEIN 6; CALCIFICATION, PHYSIOLOGIC; CELL DIFFERENTIATION; CELL LINE; CELL MOVEMENT; CHEMOKINES; CULTURE MEDIA, CONDITIONED; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSOPHOSPHOLIPIDS; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED BALB C; OSTEOCLASTS; OSTEOGENESIS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; SPHINGOSINE; WNT PROTEINS;

EID: 58549115903     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0805133106     Document Type: Article

References (52)

1. Khosla S (2001) Minireview: The OPG/RANKL/RANK system. Endocrinology 142:5050-5055.
2. Martin TJ, Sims NA (2005) Osteoclast-derived activity in the coupling of bone formation to resorption. Trends Mol Med 11:76-81.
3. Karsdal MA, Martin TJ, Bollerslev J, Christiansen C, Henriksen K (2007) Are nonresorbing osteoclasts sources of bone anabolic activity? J Bone Miner Res 22:487-494.
4. Marzia M, et al. (2000) Decreased c-Src expression enhances osteoblast differentiation and bone formation. J Cell Biol 151:311-320.
5. Kornak U, et al. (2001) Loss of the ClC-7 chloride channel leads to osteopetrosis in mice and man. Cell 104:205-215.
6. Soriano P, Montgomery C, Geske R, Bradley A (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64:693-702.
7. Del Fattore A, et al. (2006) Clinical, genetic, and cellular analysis of 49 osteopetrotic patients: Implications for diagnosis and treatment. J Med Genet 43:315-325.
8. Cleiren E, et al. (2001) Albers-Schonberg disease (autosomal dominant osteopetrosis, type II) results from mutations in the ClCN7 chloride channel gene. Hum Mol Genet 10:2861-2867.
9. Dai XM, Zong XH, Akhter MP, Stanley ER (2004) Osteoclast deficiency results in disorganized matrix, reduced mineralization, and abnormal osteoblast behavior in developing bone. J Bone Miner Res 19:1441-1451.
10. Sakagami N, et al. (2005) Reduced osteoblastic population and defective mineralization in osteopetrotic (op/op) mice. Micron 36:688-695.
11. Tuukkanen J, et al. (2000) Mineral density and bone strength are dissociated in long bones of rat osteopetrotic mutations. J Bone Miner Res 15:1905-1911.
12. Westendorf JJ, Kahler RA, Schroeder TM (2004) Wnt signaling in osteoblasts and bone diseases. Gene 341:19-39.
13. Hens JR, et al. (2005) TOPGAL mice show that the canonical Wnt signaling pathway is active during bone development and growth and is activated by mechanical loading in vitro. J Bone Miner Res 20:1103-1113.
14. Khosla S, Westendorf JJ, Oursler MJ (2008) Building bone to reverse osteoporosis and repair fractures. J Clin Invest 118:421-428.
15. Almeida M, Han L, Bellido T, Manolagas SC, Kousteni S (2005) Wnt proteins prevent apoptosis of both uncommitted osteoblast progenitors and differentiated osteoblasts by beta-catenin-dependent and -independent signaling cascades involving Src/ERK and phosphatidylinositol 3-kinase/AKT. J Biol Chem 280:41342-41351.
16. Bodine PV, et al. (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.
17. Bodine PV, et al. (2005) The Wnt antagonist secreted frizzled-related protein-1 controls osteoblast and osteocyte apoptosis. J Cell Biochem 96:1212-1230.
18. Bennett CN, et al. (2005) Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc Natl Acad Sci USA 102:3324-3329.
19. Bennett CN, et al. (2007) Wnt10b increases postnatal bone formation by enhancing osteoblast differentiation. J Bone Miner Res 22:1924-1932.
20. van Bezooijen, et al. (2007) Wnt but not BMP signaling is involved in the inhibitory action of sclerostin on BMP-stimulated bone formation. J Bone Miner Res 22:19-28.
21. Winkler DG, et al. (2003) Osteocyte control of bone formation via sclerostin, a novel BMP antagonist. EMBO J 22:6267-6276.
22. Balemans W, et al. (2001) Increased bone density in sclerosteosis is due to the deficiency of a novel secreted protein (SOST). Hum Mol Genet 10:537-543.
23. Brunkow ME, et al. (2001) Bone dysplasia sclerosteosis results from loss of the SOST gene product, a novel cystine knot-containing protein. Am J Hum Genet 68:577-589.
24. Li X, et al. (2005) Dkk2 has a role in terminal osteoblast differentiation and mineralized matrix formation. Nat Genet 37:945-952.
25. Ellies DL, et al. (2006) Bone density ligand, Sclerostin, directly interacts with LRP5 but not LRP5G171V to modulate Wnt activity. J Bone Miner Res 21:1738-1749.
26. Rawadi G, Vayssiere B, Dunn F, Baron R, 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.
27. Mbalaviele G, et al. (2005) Beta-catenin and BMP-2 synergize to promote osteoblast differentiation and new bone formation. J Cell Biochem 94:403-418.
28. Sammons J, Ahmed N, El-Sheemy M, Hassan HT (2004) The role of BMP-6, IL-6, and BMP-4 in mesenchymal stem cell-dependent bone development: Effects on osteoblastic differentiation induced by parathyroid hormone and vitamin D(3). Stem Cells Dev 13:273-280.
29. Simic P, et al. (2006) Systemically administered bone morphogenetic protein-6 restores bone in aged ovariectomized rats by increasing bone formation and suppressing bone resorption. J Biol Chem 281:25509-25521.
30. Ryu J, et al. (2006) Sphingosine 1-phosphate as a regulator of osteoclast differentiation and osteoclast-osteoblast coupling. EMBO J 25:5840-5851.
31. Poole KE, et al. (2005) Sclerostin is a delayed secreted product of osteocytes that inhibits bone formation. FASEB J 19:1842-1844.
32. van Bezooijen RL, et al. (2004) Sclerostin is an osteocyte-expressed negative regulator of bone formation, but not a classical BMP antagonist. J Exp Med 199:805-814.
33. Bellido T, et al. (2005) Chronic elevation of parathyroid hormone in mice reduces expression of sclerostin by osteocytes: A novel mechanism for hormonal control of osteoblastogenesis. Endocrinology 146:4577-4583.
34. Robling AG, et al. (2008) Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J Biol Chem 283:5866-5875.
35. Bonewald LF (1999) Establishment and characterization of an osteocyte-like cell line, MLO-Y4. J Bone Miner Metab 17:61-65.
36. Garimella R, et al. (2008) Expression and synthesis of bone morphogenetic proteins by osteoclasts: A possible path to anabolic bone remodeling. J Histochem Cytochem 56:569-577.
37. Goetzl E, et al. (2000) Mechanisms of lysolipid phosphate effects on cellular survival and proliferation. Ann NY Acad Sci 905:177-187.
38. Mulroy T, McMahon JA, Burakoff SJ, McMahon AP, Sen J (2002) Wnt-1 and Wnt-4 regulate thymic cellularity. Eur J Immunol 32:967-971.
39. Si W, et al. (2006) CCN1/Cyr61 is regulated by the canonical Wnt signal and plays an important role in Wnt3A-induced osteoblast differentiation of mesenchymal stem cells. Mol Cell Biol 26:2955-2964.
40. Itoh K, et al. (2001) Bone morphogenetic protein 2 stimulates osteoclast differentiation and survival supported by receptor activator of nuclear factor-kappaB ligand. Endocrinology 142:3656-3662.
41. Kugimiya F, et al. (2005) Involvement of endogenous bone morphogenetic protein (BMP) 2 and BMP6 in bone formation. J Biol Chem 280:35704-35712.
42. Perry MJ, McDougall KE, Hou SC, Tobias JH (2008) Impaired growth plate function in bmp-6 null mice. Bone 42:216-225.
43. Mizugishi K, et al. (2005) Essential role for sphingosine kinases in neural and vascular development. Mol Cell Biol 25:11113-11121.
44. Delorme G, Saltel F, Bonnelye E, Jurdic P, Machuca-Gayet I (2005) Expression and function of semaphorin 7A in bone cells. Biol Cell 97:589-597.
45. Zhao C, et al. (2006) Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metab 4:111-121.
46. Grano M, et al. (1996) Hepatocyte growth factor is a coupling factor for osteoclasts and osteoblasts in vitro. Proc Natl Acad Sci USA 93:7644-7648.
47. Gingery A, Bradley E, Shaw A, Oursler MJ (2003) Phosphatidylinositol 3-kinase coordinately activates the MEK/ERK and AKT/NFkappaB pathways to maintain osteoclast survival. J Cell Biochem 89:165-179.
48. Gori F, Thomas T, Hicok KC, Spelsberg TC, Riggs BL (1999) Differentiation of human marrow stromal precursor cells: Bone morphogenetic protein-2 increases OSF2/CBFA1, enhances osteoblast commitment, and inhibits late adipocyte maturation. J Bone Miner Res 14:1522-1535.
49. Bills CE, Eisenberg H, Pallante SL (1971) Complexes of organic acids with calcium phosphate: The von Kossa stain as a clue to the composition of bone mineral. Johns Hopkins Med J 128:194-207.
50. Gilmore SK, Whitson SW, Bowers DE, Jr (1986) A simple method using alizarin red S for the detection of calcium in epoxy resin embedded tissue. Stain Technol 61:89-92.
51. Johnsen SA, Subramaniam M, Janknecht R, Spelsberg TC (2002) TGFbeta inducible early gene enhances TGFbeta/Smad-dependent transcriptional responses. Oncogene 21:5783-5790.
52. Karst M, Gorny G, Galvin RJ, Oursler MJ (2004) Roles of stromal cell RANKL, OPG, and M-CSF expression in biphasic TGF-beta regulation of osteoclast differentiation. J Cell Physiol 200:99-106.