Oxysterol-induced osteogenic differentiation of marrow stromal cells is regulated by Dkk-1 inhibitable and PI3-kinase mediated signaling

Journal of Cellular Biochemistry

Volumn 105, Issue 2, 2008, Pages 424-436

  Amantea, Christopher M ^a   Kim, Woo Kyun ^a   Meliton, Vicente ^a   Tetradis, Sotirios ^b   Parhami, Farhad ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Center for the Health Sciences ^*

Author keywords

Dkk 1; Hedgehog signaling; Marrow stromal cells; Osteogenic differentiation; Oxysterol; PI3 kinase; Wnt pathway

Indexed keywords

BETA CATENIN; GLYCOPROTEIN; OXYSTEROL; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN DKK 1; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; WNT1 PROTEIN; WNT3A PROTEIN;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; CELL DIFFERENTIATION; CONTROLLED STUDY; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STROMA CELL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL LINE; CHOLESTEROL; HEDGEHOG PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; OSTEOGENESIS; SIGNAL TRANSDUCTION; STROMAL CELLS; WNT PROTEINS;

ERINACEIDAE;

EID: 54849424320     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21840     Document Type: Article

References (62)

1. Almeida M, Han L, Bellido T, Manolagas SC, Kousteni S. 2005. Wnt proteins prevent apoptosis of both uncommitted osteoblast progenitors and differentiated osteoblasts by β-catenin-dependent and -independent signaling cascades involving Src/ERK and Phosphatidylinositol 3-kinase/Akt. J Biol Chem 280:41342-41351.
2. Bafico A, Liu G, Yaniv A, Gazit A, Aaronson SA. 2001. Novel mechanism of Wnt signalling inhibition mediated by Dickkopf-1 interaction with LRP6/Arrow. Nature Cell Biol 3:683-686.
3. Bennett CN, Ross SE, Longo KA, Bajnok L, Hemati N, Johnson KW, Harrison SD, MacDougald OA. 2002. Regulation of Wnt signaling during adipogenesis. J Biol Chem 277:30998-31004.
4. Bennett CN, Longo KA, Wright WS, Suva LJ, Lane TF, Hankenson KD, MacDougald OA. 2005. Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc Natl Acad Sci 102:3324-3329.
5. Bjorkhem I, Dicsfalusy U. 2002. Oxysterols: Friends, foes, or just fellow passengers? Arterioscler Thromb Vasc Biol 22:734-742.
6. Boland GM, Perkins G, Hall DJ, Tuan RS. 2004. Wnt3a promotes proliferation and suppresses osteogenic differentiation of adult human mesenchymal stem cells. J Cell Biochem 93:1210-1230.
7. Boyden LM, Mao J, Belsky J, Mitzner L, Farhi A, Mitnick MA, Wu D, Insogna K, Lifton RP. 2002. High bone density due to a mutation in LDL-receptor-related protein 5. N Engl J Med. 364:1513-1521.
8. Caplan AI. 1994. The mesengenic process. Clin Plast Surg 21:429-435.
9. Clement-Lacroix P, Ai M, Morvan F, Roman-Roman S, Vayssiere B, Belleville C, Estrera K, Warman ML, Baron R, Rawadi G. 2005. Lrp5-independent activation of Wnt signaling by lithium chloride increases bone formation and bone mass in mice. Proc Natl Acad Sci 102:17404-17411.
10. Clevers H. 2006. Wnt/β-catenin signaling in development and disease. Cell 127:469-480.
11. Cummings SR, Melton LJ. 2002. Epidemiology and outcomes of osteoporotic fractures. Lancet 359:1761-1767.
12. Day TF, Guo X, Garrett-Beal L, Yang Y. 2005. Wnt/β-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Develop Cell 8:739-750.
13. Debiais F, Lefevre G, Lemonnier J, Le Mee S, Lasmoles F, Mascarelli F, Marie PJ. 2004. Fibroblast growth factor-2 induces osteoblast survival through a phosphatidylinositol 3-kinase-dependent, -β-catenin-independent signaling pathway. Experimental Cell Res 297:235-246.
14. Dwyer JR, Sever N, Carlson M, Nelson SF, Beachy PA, Parhami F. 2007. Oxysterols are novel activators of the hedgehog signaling pathway in pluripotent mesenchymal cells. J Biol Chem 282:8959-8968.
15. Fu J, Liu W, Zhou J, Sun H, Xu H, Luo L, Zhang H, Zhou Y. 2006. Sonic hedgehog protein promotes bone marrow-derived endothelial progenitor cell proliferation, migration and VEGF production by PI 3-kinase/Akt signaling pathways. Acta Pharmacol Sinica 27:685-693.
16. Fujita T, Azuma Y, Fukuyama R, Hattori Y, Yoshida C, Koida M, Ogita K, Komori T. 2004. Runx2 induces osteoblast and chondrocyte differentiation and enhances their migration by coupling with PI3K-Akt signaling. J Cell Biol 166:85-95.
17. Gaur T, Lengner CJ, Hovhannisyan H, Bhat RA, Bodine PVN, Komm BS, Javed A, Van Wijnen AJ, Stein JL, Stein GS, Lian JB. 2005. Canonical Wnt signaling promotes osteogenesis by directly stimulating Runx2 gene expression. J Biol Chem 280:33132-33140.
18. Ghosh-Choudhury N, Abboud SL, Nishimura R, Celeste A, Mahimainathan L, Choudhurry GG. 2002. Requirement of BMP-2-induced phosphatidylinositol 3-kinase and Akt serine/threonine kinase in osteoblast differentiation and Smad-dependent BMP-2 gene transcription. J Biol Chem 277:33361-33368.
19. Ghosh-Choudhurry N, Mandal CC, Choudhurry GG. 2007. Statin-induced Ras activation integrates the phosphatidylinositol 3-kinase signal to Akt and MAPK for bone morphogenetic protein-2 expression in osteoblast differentiation. J Biol Chem 282:4983-4993.
20. Goltzman D. 2002. 1; Discoveries, drugs and skeletal disorders. Nat Rev Drug Discov 1:784-796.
21. Gong Y, Slee RB, Fukai N, Rawadi G, Roman-Roman S, Reginato AM, Wang H, Cundy T, Glorieux FH., et al. 2001. LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 107:513-523.
22. Gordon MD, Nusse R. 2006. Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem 281:22429-22433.
23. Hill TP, Spater D, Taketo MM, Birchmeier W, Hartmann C. 2005. Canonical Wnt/β-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Develop Cell 8:727-738.
24. Hu H, Hilton MJ, Tu X, Yu K, Ornitz DM, Long F. 2004. Sequential roles of Hedgehog and Wnt signaling in osteoblast development. Development 132:49-60.
25. Jho E, Zhang T, Domon C, Joo C, Freund J, Costantini F. 2002. Wnt/β-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 22:1172-1183.
26. Johnson ML, Harnish K, Nusse R, Van Hul W. 2004. LRP5 and Wnt signaling: a union made for bone. J Bone Miner Res 19:1749-1757.
27. Kanda S, Mochizuki Y, Suematsu T, Miyata Y, Nomata K, Kanetake H. 2003. Sonic hedgehog induces capillary morphogenesis by endothelial cells through phosphoinositide 3-kinase. J Biol Chem 278:8244-8249.
28. Kennell JA, MacDougald OA. 2005. Wnt signaling inhibits adipogenesis through β-catenin-dependent and -independent mechanisms. J Biol Chem 280:24004-24010.
29. Kenney AM, Widlund HR, Rowitch DH. 2003. Hedgehog and PI-3 kinase signaling converge on Nmyc1 to promote cell cycle progression in cerebellar neuronal precursors. Development 131:217-228.
30. Kha HT, Basseri B, Shouhed D, Richardson J, Tetradis S, Hahn TJ, Parhami F. 2004. Oxysterols regulate differentiation of mesenchymal stem cells: probone and anti-fat. J Bone Miner Res 19:830-840.
31. Kim WK, Meliton V, Amantea CM, Hahn TJ, Parhami F. 2007a. 20(S)-hydroxycholesterol inhibits PPARgamma expression and adipogenic differentiation of bone marrow stromal cells through a hedgehog-dependent mechanism. J Bone Miner Res 22:1711-1719.
32. Kim S, Lee W, Choi K. 2007b. The PI3 kinase-Akt pathway mediates Wnt3ainduced proliferation. Cell Signal 19:511-518.
33. Lee AY, He B, You L, Xu Z, Mazieres J, Reguart N, Mikami I, Batra S, Jablons DM. 2004. Dickkopf-1 antagonizes Wnt signaling independent of β-catenin in human mesothelioma. Biochem Biophys Res Commun 323:1246-1250.
34. Liu X, Bruxvoort KJ, Zylstra CR, Liu J, Cichowski R, Faugere MC, Bouxsein ML, Wan C, Williams BO, Clemens TL. 2007. Lifelong accumulation of bone in mice lacking Pten in osteoblasts. Proc Natl Acad Sci 104:2259-2264.
35. Majors AK, Boehm CA, Nitto H, Midura RJ, Muschler GF. 1997. Characterization of human bone marrow stromal cells with respect to osteoblastic differentiation. J Orthop Res 15:546-557.
36. Mbalaviele G, Sheikh S, Stains JP, Salazar VS, Cheng S, Chen D, Civitelli R. 2005. β-Catenin and BMP-2 synergize to promote osteoblast differentiation and new bone formation. J Cell Biochem 94:403-418.
37. Mullor JL, Dahmane N, Sun T, Altaba AR. 2001. Wnt signals are targets and mediators of Gli function. Current Biol 11:769-773.
38. Mundy GR. 2002. Directions of drug discovery in osteoporosis. Annu Rev Med 53:337-354.
39. Parhami F, Morrow AD, Balucan J, Leitinger N, Watson AD, Tintut Y, Berliner JA, Demer LL. 1997. Lipid oxidation products have opposite effects on calcifying vascular cell and bone cell differentiation. Arterioscl Thromb Vasc Biol 17:680-687.
40. Parhami F, Jackson SM, Tintut Y, Le V, Balucan JP, Territo M, Demer LL. 1999. Atherogenic diet and minimally oxidized low density lipoprotein inhibit osteogenic and promote adipogenic differentiation of marrow stromal cells. J Bone Miner Res 14:2067-2078.
41. Peng S, Miao C, Li J, Fan X, Cao Y, Duan E. 2006. Dickkopf-1 induced apoptosis in human placental choriocarcinoma is independent of canonical Wnt signaling. Biochem Biophys Res Commun 350:641-647.
42. Peng X, Xu P, Chen M, Hahn-Windgassen A, Skeen J, Jacobs J, Sundararajan D, Chen WS, Crawford SE, Coleman KG, Hay N. 2007. Dwarfism, impaired skin development, skeletal muscle atrophy, delayed bone development, and impeded adipogenesis in mice lacking Akt1 and Akt2. Genes Dev 17:1352-1365.
43. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
44. Prockop DJ. 1997. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71-74.
45. 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.
46. Reguart N, He B, Xu Z, You L, Lee AY, Mazieres J, Mikami I, Batra S, Rosell R, McCormick F, Jablons DM. 2004. Cloning and characterization of the promoter of human Wnt inhibitory factor-1. Biochem Biophys Res Commun 323:229-234.
47. Richardson JA, Amantea CM, Kianmahd B, Tetradis S, Lieberman JR, Hahn TJ, Parhami F. 2007. Oxysterol-induced osteoblastic differentiation of pluripotent mesenchymal cells is mediated through a PKC- and PKA-dependent pathway. J Cell Biochem 100:1131-1145.
48. Riggs BL, Melton LJ. 1992. The prevention and treatment of osteoporosis. N Engl J Med 327:620-627.
49. Riobo NA, Lu K, Ai X, Haines GM, Emerson CP. 2006. Phosphoinositide 3-kinase and Akt are essential for Sonic Hedgehog signaling. Proc Natl Acad Sci 103:4505-4510.
50. Rodan GA, Martin TJ. 2000. Therapeutic approaches to bone diseases. Science 289:1508-1514.
51. Rodda SJ, McMahon AP. 2006. Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation, and maintenance of osteoblast progenitors. Development 133:3231-3244.
52. Schambony A, Wedlich D. 2007. Wnt-5A/Ror2 regulate expression of XPAPC through an alternative noncanonical signaling pathway. Develop Cell 12:779-792.
53. Schroepfer GJ. 2000. Oxysterols: modulators of cholesterol metabolism and other processes. Physiol Rev 80:361-554.
54. Silva-Vargas V, Lo Celso C, Giangreco A, Ofstad T, Prowse DM, Braun KM, Watt FM. 2005. β-catenin and hedgehog signal strength can specify number and location of hair follicles in adult epidermis without recruitment of bulge stem cells. Develop Cell 9:121-131.
55. Smith E, Frenkel B. 2005. Glucocorticoids inhibit the transcriptional activity of LEF/TCF in differentiating osteoblasts in a glycogen synthase kinase-3β-dependent and -independent manner. J Biol Chem 280:2388-2394.
56. Taipale J, Beachy PA. 2001. The hedgehog and Wnt signalling pathways in cancer. Nature 411:349-354.
57. Tetsu O, McCormick F. 1999. β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398:422-426.
58. Vaananen HK. 2005. Mesenchymal stem cells. Ann Med 37:469-479.
59. Van Raay TJ, Coffey RJ, Solnica-Krezel L. 2007. Zebrafish Naked1 and Naked2 antagonize both canonical and non-canonical Wnt signaling. Develop Biol 309:151-168.
60. Westendorf JJ, Kahler RA, Schroeder TM. 2004. Wnt signaling in osteoblast and bone diseases. Gene 341:19-39.
61. Wharton KA, Zimmermann G, Rousset R, Scott MP. 2001. Vertebrate proteins related to drosophila Naked Cuticle bind Dishevelled and antagonize Wnt signaling. Develop Biol 234:93-106.
62. Willert K, Jones KA. 2006. Wnt signaling: is the party in the nucleus? Genes Dev 20:1394-1404.