The forkhead transcription factor Foxc2 promotes osteoblastogenesis via up-regulation of integrin β1 expression

Bone

Volumn 49, Issue 3, 2011, Pages 428-438

  Park, Su Jin ^a   Gadi, Jogeswar ^a   Cho, Kyoung Won ^b   Kim, Kwang Joon ^a   Kim, Se Hwa ^c   Jung, Han Sung ^b   Lim, Sung Kil ^a  

^a Yonsei University College of Medicine   (South Korea)

^b Yonsei University   (South Korea)

^c Kwandong University College of Medicine   (South Korea)

Author keywords

Bone anabolic agent; Forkhead binding element; Foxc2; Integrin 1

Indexed keywords

ALPHA5 INTEGRIN; BETA1 INTEGRIN; BONE MORPHOGENETIC PROTEIN 2; FORKHEAD TRANSCRIPTION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; PARATHYROID HORMONE[1-34]; PROTEIN KINASE B; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FOXC2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CALVARIA; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EX VIVO STUDY; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; TISSUE CULTURE; UPREGULATION;

3T3 CELLS; ANIMALS; ANTIGENS, CD29; BONE MORPHOGENETIC PROTEIN 2; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HUMANS; INTEGRIN ALPHA5; MICE; OSTEOBLASTS; PARATHYROID HORMONE; PEPTIDE FRAGMENTS; RNA, SMALL INTERFERING; SKULL; TISSUE CULTURE TECHNIQUES; UP-REGULATION;

EID: 79960575675     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2011.05.012     Document Type: Article

References (40)

1. Karsenty G., Wagner E.F. Reaching a genetic and molecular understanding of skeletal development. Dev Cell 2002, 2:389-406.
2. Komori T. Regulation of osteoblast differentiation by transcription factors. J Cell Biochem 2006, 99:1233-1239.
3. Heino T.J., Hentunen T.A. Differentiation of osteoblasts and osteocytes from mesenchymal stem cells. Curr Stem Cell Res Ther 2008, 3:131-145.
4. Nishimura R., Hata K., Ikeda F., Ichida F., Shimoyama A., Matsubara T., et al. Signal transduction and transcriptional regulation during mesenchymal cell differentiation. J Bone Miner Metab 2008, 26:203-212.
5. Carlsson P., Mahlapuu M. Forkhead transcription factors: key players in development and metabolism. Dev Biol 2002, 250:1-23.
6. Iida K., Koseki H., Kakinuma H., Kato N., Mizutani-Koseki Y., Ohuchi H., et al. Essential roles of the winged helix transcription factor MFH-1 in aortic arch patterning and skeletogenesis. Development 1997, 124:4627-4638.
7. Winnier G.E., Hargett L., Hogan B.L. The winged helix transcription factor MFH1 is required for proliferation and patterning of paraxial mesoderm in the mouse embryo. Genes Dev 1997, 11:926-940.
8. Miura N., Wanaka A., Tohyama M., Tanaka K. MFH-1, a new member of the fork head domain family, is expressed in developing mesenchyme. FEBS Lett 1993, 326:171-176.
9. Nifuji A., Miura N., Kato N., Kellermann O., Noda M. Bone morphogenetic protein regulation of forkhead/winged helix transcription factor Foxc2 (Mfh1) in a murine mesodermal cell line C1 and in skeletal precursor cells. J Bone Miner Res 2001, 16:1765-1771.
10. Hayashi H., Kume T. Forkhead transcription factors regulate expression of the chemokine receptor CXCR4 in endothelial cells and CXCL12-induced cell migration. Biochem Biophys Res Commun 2008, 367:584-589.
11. Hayashi H., Sano H., Seo S., Kume T. The Foxc2 transcription factor regulates angiogenesis via induction of integrin beta3 expression. J Biol Chem 2008, 283:23791-23800.
12. Hayashi H., Kume T. Foxc transcription factors directly regulate Dll4 and Hey2 expression by interacting with the VEGF-Notch signaling pathways in endothelial cells. PloS One 2008, 3:e2401. [e2401].
13. Xue Y., Cao R., Nilsson D., Chen S., Westergren R., Hedlund E., et al. FOXC2 controls Ang-2 expression and modulates angiogenesis, vascular patterning, remodeling, and functions in adipose tissue. Proc Natl Acad Sci U S A 2008, 105:10167-10172.
14. Kim S.H., Cho K., Choi H.S., Park S.J., Rhee Y., Jung H., et al. The forkhead transcription factor Foxc2 stimulates osteoblast differentiation. Biochem Biophys Res Commun 2009, 386:532-536.
15. Franceschi R.T. The developmental control of osteoblast-specific gene expression: role of specific transcription factors and the extracellular matrix environment. Crit Rev Oral Biol Med 1999, 10:40-57.
16. Evans N.D., Gentleman E., Chen X., Roberts C.J., Polak J.M., Stevens M. Extracellular matrix-mediated osteogenic differentiation of murine embryonic stem cells. Biomaterials 2010, 31:3244-3252.
17. Lee D., Yeh C., Chang S., Lee P., Chien S., Cheng C., et al. Integrin-mediated expression of bone formation-related genes in osteoblast-like cells in response to fluid shear stress: roles of extracellular matrix, Shc, and mitogen-activated protein kinase. J Bone Miner Res 2008, 23:1140-1149.
18. Liedert A., Kaspar D., Blakytny R., Claes L., Ignatius A. Signal transduction pathways involved in mechanotransduction in bone cells. Biochem Biophys Res Commun 2006, 349:1-5.
19. Moursi A.M., Globus R.K., Damsky C.H. Interactions between integrin receptors and fibronectin are required for calvarial osteoblast differentiation in vitro. J Cell Sci 1997, 110:2187-2196.
20. Reyes C.D., Garca A.J. Alpha2beta1 integrin-specific collagen-mimetic surfaces supporting osteoblastic differentiation. J Biomed Mater Res A 2004, 69:591-600.
21. Hynes R.O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992, 69:11-25.
22. Saito T., Albelda S.M., Brighton C.T. Identification of integrin receptors on cultured human bone cells. J Orthop Res 1994, 12:384-394.
23. Gronthos S., Stewart K., Graves S.E., Hay S., Simmons P.J. Integrin expression and function on human osteoblast-like cells. J Bone Miner Res 1997, 12:1189-1197.
24. Wang L., Zhao G., Olivares-Navarrete R., Bell B.F., Wieland M., Cochran D.L., et al. Integrin beta1 silencing in osteoblasts alters substrate-dependent responses to 1,25-dihydroxy vitamin D3. Biomaterials 2006, 27:3716-3725.
25. Olivares-Navarrete R., Raz P., Zhao G., Chen J., Wieland M., Cochran D.L., et al. Integrin alpha2beta1 plays a critical role in osteoblast response to micron-scale surface structure and surface energy of titanium substrates. Proc Natl Acad Sci U S A 2008, 105:15767-15772.
26. Schwartz Z., Bell B.F., Wang L., Zhao G., Olivares-Navarrete R., Boyan B.D. Beta-1 integrins mediate substrate dependent effects of 1alpha,25(OH)2D3 on osteoblasts. J Steroid Biochem Mol Biol 2007, 103:606-609.
27. Park S.J., Kim S.J., Rhee Y., Byun J.H., Kim S.H., Kim M.H., et al. Fidgetin-like 1 gene inhibited by basic fibroblast growth factor regulates the proliferation and differentiation of osteoblasts. J Bone Miner Res 2007, 22:889-896.
28. Taya Y., O'Kane S., Ferguson M.W. Pathogenesis of cleft palate in TGF-beta3 knockout mice. Development 1999, 126:3869-3879.
29. Park S.J., Jung S., Jogeswar G., Ryoo H., Yook J.I., Choi H.S., et al. The transcription factor snail regulates osteogenic differentiation by repressing Runx2 expression. Bone 2010, 46:1498-1507.
30. Korenjak M., Brehm A. E2F-Rb complexes regulating transcription of genes important for differentiation and development. Curr Opin Genet Dev 2005, 15:520-527.
31. Xu M., Sheppard K.A., Peng C.Y., Yee A.S., Piwnica-Worms H. Cyclin A/CDK2 binds directly to E2F-1 and inhibits the DNA-binding activity of E2F-1/DP-1 by phosphorylation. Mol Cell Biol 1994, 14:8420-8431.
32. Hader C., Marlier A., Cantley L. Mesenchymal-epithelial transition in epithelial response to injury: the role of Foxc2. Oncogene 2010, 29:1031-1040.
33. Cano A., Prez-Moreno M.A., Rodrigo I., Locascio A., Blanco M.J., del Barrio M.G., et al. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2000, 2:76-83.
34. de Frutos C.A., Dacquin R., Vega S., Jurdic P., Machuca-Gayet I., Nieto M.A. Snail1 controls bone mass by regulating Runx2 and VDR expression during osteoblast differentiation. EMBO J 2009, 28:686-696.
35. Davis K.E., Moldes M., Farmer S.R. The forkhead transcription factor FoxC2 inhibits white adipocyte differentiation. J Biol Chem 2004, 279:42453-42461.
36. Kim J.K., Kim H., Park S., Cederberg A., Westergren R., Nilsson D., et al. Adipocyte-specific overexpression of FOXC2 prevents diet-induced increases in intramuscular fatty acyl CoA and insulin resistance. Diabetes 2005, 54:1657-1663.
37. Gerin I., Bommer G.T., Lidell M.E., Cederberg A., Enerback S., Macdougald O.A. On the role of FOX transcription factors in adipocyte differentiation and insulin-stimulated glucose uptake. J Biol Chem 2009, 284:10755-10763.
38. Yerges L.M., Klei L., Cauley J.A., Roeder K., Kammerer C.M., Moffett S.P., et al. High-density association study of 383 candidate genes for volumetric BMD at the femoral neck and lumbar spine among older men. J Bone Miner Res 2009, 24:2039-2049.
39. Cederberg A., Grnning L.M., Ahrn B., Taskn K., Carlsson P., Enerbck S. FOXC2 is a winged helix gene that counteracts obesity, hypertriglyceridemia, and diet-induced insulin resistance. Cell 2001, 106:563-573.
40. Yang X., Enerbck S., Smith U. Reduced expression of FOXC2 and brown adipogenic genes in human subjects with insulin resistance. Obes Res 2003, 11:1182-1191.