BMP-2 modulates β-catenin signaling through stimulation of Lrp5 expression and inhibition of β-TrCP expression in osteoblasts

Journal of Cellular Biochemistry

Volumn 108, Issue 4, 2009, Pages 896-905

  Zhang, Ming ^a   Yan, Ying ^a   Lim, Yong Bin ^a   Tang, Dezhi ^a,b   Xie, Rong ^a   Chen, Ann ^a   Tai, Peter ^a   Harris, Stephen E ^c   Xing, Lianping ^a   Qin, Yi Xian ^d   Chen, Di ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^d St Francis Hospital The Heart Center   (United States)

Author keywords

catenin; TrCP; BMP 2; LRP5; Osteoblast differentiation

Indexed keywords

BETA CATENIN; BETA TRCP; BONE MORPHOGENETIC PROTEIN 2; LIGASE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; UNCLASSIFIED DRUG; WNT1 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL;

3T3 CELLS; ANIMALS; BETA CATENIN; BETA-TRANSDUCIN REPEAT-CONTAINING PROTEINS; BONE MORPHOGENETIC PROTEIN 2; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; LDL-RECEPTOR RELATED PROTEINS; LIGANDS; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; OSTEOBLASTS; SIGNAL TRANSDUCTION;

EID: 70350511769     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22319     Document Type: Article

References (36)

1. Aberle H, Bauer A, Stappert J, Kispert A, Kemler R. 1997. beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J 16:3797-3804.
2. Bain G, Muller T, Wang X, Papkoff J. 2003. Activated beta-catenin induces osteoblast differentiation of C3H10T1/2 cells and participates in BMP2 mediated signal transduction. Biochem Biophys Res Commun 301:84-91. (Pubitemid 36268851)
3. Behrens J, Jerchow BA, Würtele M, Grimm J, Asbrand C, Wirtz R, Kühl M, Wedlich D, Birchmeier W. 1998. Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta. Science 280:596-599. (Pubitemid 28227764)
4. Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch DH, McMahon AP, Sommer L, Boussadia O, Kemler R. 2001. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128:1253-1264. (Pubitemid 32409648)
5. Chen D, Harris MA, Rossini G, Dunstan CR, Dallas SL, Feng JQ, Mundy GR, Harris SE. 1997. Bone morphogenetic protein 2 (BMP-2) enhances BMP-3, BMP-4, and bone cell differentiation marker gene expression during the induction of mineralized bone matrix formation in cultures of fetal tar calvarial isteoblasts. Calcif Tissue Int 60:283-290. (Pubitemid 27106254)
6. Chen D, Ji X, Harris MA, Feng JQ, Celeste AJ, Rosen V, Mundy GR, Harris SE. 1998. Differential roles for BMP receptor type IB and IA in differentiation and specification of mesenchyma precursor cells to osteoblast and adipocyte lineages. J Cell Biol 142:295-305. (Pubitemid 28341159)
7. Chen M, Zhu M, Awad H, Li TF, Sheu TJ, Boyce BF, Chen D, O'Keefe RJ. 2008. Inhibition of β-catenin signaling causes defects in postnatal cartilage development. J Cell Sci 121:1455-1465. (Pubitemid 351936310)
8. Day TF, Guo X, Garrett-Beal L, Yang Y. 2005. Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev Cell 8:739-750. (Pubitemid 40585296)
9. Devlin RD, Du Z, Pereira RC, Kimble RB, Economides N, Jorgetti V, Canalis E. 2003. Skeletal over-expression of noggin results in osteopenia and reduced bone formation. Endocrinology 144:1972-1978. (Pubitemid 36543336)
10. Fischer L, Boland G, Tuan RS. 2002a. Wnt-3A enhances bone morphogenetic protein-2-mediated chondrogenesis of murine C3H10T1/2 mesenchymal cells. J Biol Chem 277:30870-30878. (Pubitemid 34970787)
11. Fischer L, Boland G, Tuan RS. 2002b. Wnt signaling during BMP-2 stimulation of mesenchymal chondrogenesis. J Cell Biochem 84:816-831. (Pubitemid 34113120)
12. Ghosh-Choudhury N, Windle JJ, Koop BA, Harris MA, Guerrero DL, Wozney JM, Mundy GR, Harris SE. 1996. Immortalized murine osteoblasts derived from BMP 2-T-antigen expressing transgenic mice. Endocrinology 137:331-339.
13. Gong Y, Slee RB, Fukai N, et al. 2001. LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 107:513-523. (Pubitemid 33152786)
14. Hart M, Concordet JP, Lassot I, Albert I, del los Santos R, Durand H, Perret C, Rubinfeld B, Margottin F, Benarous R, Polakis P. 1999. The F-box protein beta-TrCP associates with phosphorylated beta-catenin and regulates its activity in the cell. Curr Biol 9:207-210.
15. Huelsken J, Birchmeier W. 2001. New aspects of Wnt signaling pathways in higher vertebrates. Curr Opin Genet Dev 11:547-553. (Pubitemid 32800729)
16. Jiang J, Struhl G. 1998. Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature 391:493-496. (Pubitemid 28086550)
17. Kato M, Patel MS, Levasseur R, Lobov I, Chang BH, Glass DA II, Hartmann C, Li L, Hwang TH, Brayton CF, Lang RA, Karsenty G, Chan L. 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. (Pubitemid 34839826)
18. Mao J, Wang J, Liu B, Pan W, Farr GH III, Flynn C, Yuan H, Takada S, Kimelman D, Li L, Wu D. 2001. Low-density lipoprotein receptor-related protein-5 binds to Axin and regulates the canonical Wnt signaling pathway. Mol Cell 7:801-809. (Pubitemid 32436440)
19. Mbalaviele G, Sheikh S, Stains JP, Salazar VS, Cheng SL, 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. (Pubitemid 41420317)
20. Moon RT. 2004. Teaching resource. Beta-catenin signaling and axis specification. Sci STKE 2004:tr6.
21. Moon RT, Bowerman B, Boutros M, Perrimon N. 2002. The promise and perils of Wnt signaling through β-catenin. Science 296:1644-1646. Review. (Pubitemid 34579151)
22. 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. (Pubitemid 37322562)
23. Shtutman M, Zhurinsky J, Simcha I, Albanese C, D'Amico M, Pestell R, Ben-Ze'ev A. 1999. The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc Natl Acad Sci USA 96:5522-5527.
24. Soshnikova N, Zechner D, Huelsken J, Mishina Y, Behringer RR, Taketo MM, Crenshaw EB III, Birchmeier W. 2003. Genetic interaction between Wnt/β-catenin and BMP receptor signaling during formation of the AER and the dorsal-ventral axis in the limb. Genes Dev 17:1963-1968. (Pubitemid 36999323)
25. Staal FJ, Clevers H. 2000. TCF/LEF transcription factors during T-cell development: Unique and overlapping functions. Hematol J 1:3-6.
26. Tetsu O, McCormick F. 1999. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398:422-426. (Pubitemid 29180374)
27. Westendorf JJ, Kahler RA, Schroeder TW. 2004. Wnt signaling in osteoblasts and bone diseases. Gene 341:19-39. Review.
28. Winkler DG, Sutherland MK, Geoghegan JC, Yu C, Hayes T, Skonier JE, Shpektor D, Jonas M, Kovacevich BR, Staehling-Hampton K, Appleby M, Brunkow ME, Latham JA. 2003. Osteocyte control of bone formation via sclerostin, a novel BMP antagonist. EMBO J 22:6267-6276. (Pubitemid 37522584)
29. Winkler DG, Sutherland MS, Ojala E, Turcott E, Geoghegan JC, Shpektor D, Skonier JE, Yu C, Latham JA. 2005. Sclerostin inhibition of Wnt-3a-induced C3H10T1/2 cell differentiation is indirect and mediated by bone morphogenetic proteins. J Biol Chem 280:2498-2502. (Pubitemid 40189350)
30. Wozney JM, Rosen V. 1988. Bone morphogenetic protein and bone morphogenetic protein gene family in bone formation and repair. Clin Orthop 346:26-37. Review.
31. Wu G, Xu G, Schulman BA, Jeffrey PD, Harper JW, Pavletich NP. 2003a. Structure of a beta-TrCP1-Skp1-beta-catenin complex: Destruction motif binding and lysine specificity of the SCF(beta-TrCP1) ubiquitin ligase. Mol Cell 11:1445-1456. (Pubitemid 36776532)
32. Wu XB, Li Y, Schneider A, Yu W, Rajendren G, Iqbal J, Yamamoto M, Alam M, Brunet LJ, Blair HC, Zaidi M, Abe E. 2003b. lmpaired osteoblastic differentiation, reduced bone formation, and severe osteoporosis in noggin-overexpressing mice. J Clin lnvest 112:924-934. (Pubitemid 38063750)
33. Yadav VK, Ryu JH, Suda N, Tanaka KF, Gingrich JA, Schütz G, Glorieux FH, Chiang CY, Zajac JD, Insogna KL, Mann JJ, Hen R, Ducy P, Karsenty G. 2008. Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum. Cell 135:825-837.
34. Yoshida Y, Tanaka S, Umemori H, Minowa O, Usui M, lkematsu N, Hosoda E, lmamura T, Kuno J, Yamashita T, Miyazono K, Noda M, Noda T, Yamamoto T. 2000. Negative regulation of BMP/Smad signaling by Tob in osteoblasts. Cell 103:1085-1097.
35. Zhao M, Harris SE, Horn D, Geng Z, Nishimura R, Mundy GR, Chen D. 2002. Bone morphogenetic protein receptor signaling is necessary for normal murine postnatal bone formation. J Cell Biol 157:1049-1060. (Pubitemid 34839779)
36. Zhu M, Tang D, Wu Q, Hao S, Chen M, Xie C, Rosier RN, O'Keefe RJ, Zuscik M, Chen D. 2009. Activation of β-catenin signaling in articular chondrocytes leads to osteoarthritis-like phenotype in adult β-catenin conditional activation mice. J Bone Miner Res 24:12-21