FGF2 stimulates osteogenic differentiation through ERK induced TAZ expression

Bone

Volumn 58, Issue , 2014, Pages 72-80

  Byun, Mi Ran ^a   Kim, A Rum ^a   Hwang, Jun Ha ^a   Kim, Kyung Min ^a   Hwang, Eun Sook ^b   Hong, Jeong Ho ^a  

^a Korea University   (South Korea)

^b Ewha Womans University   (South Korea)

Author keywords

FGF2; Osteogenesis; Runx2; TAZ

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; REGULATOR PROTEIN; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR TAZ; UNCLASSIFIED DRUG;

ARTICLE; BONE DEVELOPMENT; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; GENE INDUCTION; GENETIC TRANSCRIPTION; GROWTH INHIBITION; INTRACELLULAR SIGNALING; MARKER GENE; OSTEOBLAST; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; TRANSCRIPTION INITIATION;

ERK; EXTRACELLULAR SIGNAL-REGULATED KINASE; FGF2; FIBROBLAST GROWTH FACTOR 2; MAPK; MAPK KINASE; MEK; MITOGEN ACTIVATED PROTEIN KINASES; OSTEOGENESIS; PKC; PROTEIN KINASE C; RUNX2; TAZ; TRANSCRIPTIONAL CO-ACTIVATOR WITH PDZ BINDING DOMAIN; YAP; YES-ASSOCIATED PROTEIN;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL NUCLEUS; CORE BINDING FACTOR ALPHA 1 SUBUNIT; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; MAP KINASE SIGNALING SYSTEM; MICE; OSTEOBLASTS; OSTEOGENESIS; PROTEIN BINDING; PROTEIN TRANSPORT; RNA, MESSENGER; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84886843429     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2013.09.024     Document Type: Article

References (50)

1. Kanai F., Marignani P.A., Sarbassova D., Yagi R., Hall R.A., Donowitz M., et al. TAZ: a novel transcriptional co-activator regulated by interactions with 14-3-3 and PDZ domain proteins. Embo J 2000, 19:6778-6791.
2. Hong J.H., Hwang E.S., McManus M.T., Amsterdam A., Tian Y., Kalmukova R., et al. TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 2005, 309:1074-1078.
3. Mahoney W.M., Hong J.H., Yaffe M.B., Farrance I.K. The transcriptional co-activator TAZ interacts differentially with transcriptional enhancer factor-1 (TEF-1) family members. Biochem J 2005, 388:217-225.
4. Chan S.W., Lim C.J., Loo L.S., Chong Y.F., Huang C., Hong W. TEADs mediate nuclear retention of TAZ to promote oncogenic transformation. J Biol Chem 2009, 284:14347-14358.
5. Zhang H., Liu C.Y., Zha Z.Y., Zhao B., Yao J., Zhao S., et al. TEAD transcription factors mediate the function of TAZ in cell growth and epithelial-mesenchymal transition. J Biol Chem 2009, 284:13355-13362.
6. Park K.S., Whitsett J.A., Di Palma T., Hong J.H., Yaffe M.B., Zannini M. TAZ interacts with TTF-1 and regulates expression of surfactant protein-C. J Biol Chem 2004, 279:17384-17390.
7. Murakami M., Nakagawa M., Olson E.N., Nakagawa O. A WW domain protein TAZ is a critical coactivator for TBX5, a transcription factor implicated in Holt-Oram syndrome. Proc Natl Acad Sci U S A 2005, 102:18034-18039.
8. Murakami M., Tominaga J., Makita R., Uchijima Y., Kurihara Y., Nakagawa O., et al. Transcriptional activity of Pax3 is co-activated by TAZ. Biochem Biophys Res Commun 2006, 339:533-539.
9. Varelas X., Sakuma R., Samavarchi-Tehrani P., Peerani R., Rao B.M., Dembowy J., et al. TAZ controls Smad nucleocytoplasmic shuttling and regulates human embryonic stem-cell self-renewal. Nat Cell Biol 2008, 10:837-848.
10. Jeong H., Bae S., An S.Y., Byun M.R., Hwang J.H., Yaffe M.B., et al. TAZ as a novel enhancer of MyoD-mediated myogenic differentiation. FASEB J 2010, 24:3310-3320.
11. Liu C.Y., Zha Z.Y., Zhou X., Zhang H., Huang W., Zhao D., et al. The hippo tumor pathway promotes TAZ degradation by phosphorylating a phosphodegron and recruiting the SCF{beta}-TrCP E3 ligase. J Biol Chem 2010, 285:37159-37169.
12. Lei Q.Y., Zhang H., Zhao B., Zha Z.Y., Bai F., Pei X.H., et al. TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the hippo pathway. Mol Cell Biol 2008, 28:2426-2436.
13. Solchaga L.A., Penick K., Goldberg V.M., Caplan A.I., Welter J.F. Fibroblast growth factor-2 enhances proliferation and delays loss of chondrogenic potential in human adult bone-marrow-derived mesenchymal stem cells. Tissue Eng Part A 2010, 16:1009-1019.
14. Ahn H.J., Lee W.J., Kwack K., Kwon Y.D. FGF2 stimulates the proliferation of human mesenchymal stem cells through the transient activation of JNK signaling. FEBS Lett 2009, 583:2922-2926.
15. Bianchi G., Banfi A., Mastrogiacomo M., Notaro R., Luzzatto L., Cancedda R., et al. Ex vivo enrichment of mesenchymal cell progenitors by fibroblast growth factor 2. Exp Cell Res 2003, 287:98-105.
16. Tsutsumi S., Shimazu A., Miyazaki K., Pan H., Koike C., Yoshida E., et al. Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochem Biophys Res Commun 2001, 288:413-419.
17. Montero A., Okada Y., Tomita M., Ito M., Tsurukami H., Nakamura T., et al. Disruption of the fibroblast growth factor-2 gene results in decreased bone mass and bone formation. J Clin Invest 2000, 105:1085-1093.
18. Xiao L., Sobue T., Esliger A., Kronenberg M.S., Coffin J.D., Doetschman T., et al. Disruption of the Fgf2 gene activates the adipogenic and suppresses the osteogenic program in mesenchymal marrow stromal stem cells. Bone 2010, 47:360-370.
19. Martin I., Muraglia A., Campanile G., Cancedda R., Quarto R. Fibroblast growth factor-2 supports ex vivo expansion and maintenance of osteogenic precursors from human bone marrow. Endocrinology 1997, 138:4456-4462.
20. Pri-Chen S., Pitaru S., Lokiec F., Savion N. Basic fibroblast growth factor enhances the growth and expression of the osteogenic phenotype of dexamethasone-treated human bone marrow-derived bone-like cells in culture. Bone 1998, 23:111-117.
21. Lai W.T., Krishnappa V., Phinney D.G. Fibroblast growth factor 2 (Fgf2) inhibits differentiation of mesenchymal stem cells by inducing Twist2 and Spry4, blocking extracellular regulated kinase activation, and altering Fgf receptor expression levels. Stem cells 2011, 29:1102-1111.
22. Fei Y., Xiao L., Doetschman T., Coffin D.J., Hurley M.M. FGF2 stimulation of osteoblast differentiation and bone formation is mediated by modulation of the WNT pathway. J Biol Chem 2011, 286(47):40575-40583.
23. Lima F., Niger C., Hebert C., Stains J.P. Connexin43 potentiates osteoblast responsiveness to fibroblast growth factor 2 via a protein kinase C-delta/Runx2-dependent mechanism. Mol Biol Cell 2009, 20:2697-2708.
24. Marie P.J. Fibroblast growth factor signaling controlling bone formation: an update. Gene 2012, 498:1-4.
25. Komori T. Signaling networks in RUNX2-dependent bone development. J Cell Biochem 2011, 112:750-755.
26. Yu K., Xu J., Liu Z., Sosic D., Shao J., Olson E.N., et al. Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 2003, 130:3063-3074.
27. Eswarakumar V.P., Monsonego-Ornan E., Pines M., Antonopoulou I., Morriss-Kay G.M., Lonai P. The IIIc alternative of Fgfr2 is a positive regulator of bone formation. Development 2002, 129:3783-3793.
28. Eswarakumar V.P., Horowitz M.C., Locklin R., Morriss-Kay G.M., Lonai P. A gain-of-function mutation of Fgfr2c demonstrates the roles of this receptor variant in osteogenesis. Proc Natl Acad Sci U S A 2004, 101:12555-12560.
29. Suzuki H., Suda N., Shiga M., Kobayashi Y., Nakamura M., Iseki S., et al. Apert syndrome mutant FGFR2 and its soluble form reciprocally alter osteogenesis of primary calvarial osteoblasts. J Cell Physiol 2012, 227:3267-3277.
30. Tanimoto Y., Yokozeki M., Hiura K., Matsumoto K., Nakanishi H., Matsumoto T., et al. A soluble form of fibroblast growth factor receptor 2 (FGFR2) with S252W mutation acts as an efficient inhibitor for the enhanced osteoblastic differentiation caused by FGFR2 activation in Apert syndrome. J Biol Chem 2004, 279:45926-45934.
31. Jacob A.L., Smith C., Partanen J., Ornitz D.M. Fibroblast growth factor receptor 1 signaling in the osteo-chondrogenic cell lineage regulates sequential steps of osteoblast maturation. Dev Biol 2006, 296:315-328.
32. Hong J.H., Yaffe M.B. TAZ: a beta-catenin-like molecule that regulates mesenchymal stem cell differentiation. Cell Cycle 2006, 5:176-179.
33. Turner N., Grose R. Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer 2010, 10:116-129.
34. Xiao G., Jiang D., Gopalakrishnan R., Franceschi R.T. Fibroblast growth factor 2 induction of the osteocalcin gene requires MAPK activity and phosphorylation of the osteoblast transcription factor, Cbfa1/Runx2. J Biol Chem 2002, 277:36181-36187.
35. Kim H.J., Lee M.H., Park H.S., Park M.H., Lee S.W., Kim S.Y., et al. Erk pathway and activator protein 1 play crucial roles in FGF2-stimulated premature cranial suture closure. Dev Dyn 2003, 227:335-346.
36. Miraoui H., Oudina K., Petite H., Tanimoto Y., Moriyama K., Marie P.J. Fibroblast growth factor receptor 2 promotes osteogenic differentiation in mesenchymal cells via ERK1/2 and protein kinase C signaling. J Biol Chem 2009, 284:4897-4904.
37. de Cristofaro T., Di Palma T., Ferraro A., Corrado A., Lucci V., Franco R., et al. TAZ/WWTR1 is overexpressed in papillary thyroid carcinoma. Eur J Cancer 2011, 47:926-933.
38. Xue P., Wu X., Zhou L., Ma H., Wang Y., Liu Y., et al. IGF1 promotes osteogenic differentiation of mesenchymal stem cells derived from rat bone marrow by increasing TAZ expression. Biochem Biophys Res Commun 2013, 433:226-231.
39. Byun M.R., Kim A.R., Hwang J.H., Sung M.K., Lee Y.K., Hwang B.S., et al. Phorbaketal A stimulates osteoblast differentiation through TAZ mediated Runx2 activation. FEBS Lett 2012, 586:1086-1092.
40. Ge C., Xiao G., Jiang D., Yang Q., Hatch N.E., Roca H., et al. Identification and functional characterization of ERK/MAPK phosphorylation sites in the Runx2 transcription factor. J Biol Chem 2009, 284:32533-32543.
41. Ge C., Xiao G., Jiang D., Franceschi R.T. Critical role of the extracellular signal-regulated kinase-MAPK pathway in osteoblast differentiation and skeletal development. J Cell Biol 2007, 176:709-718.
42. Kim H.J., Kim J.H., Bae S.C., Choi J.Y., Ryoo H.M. The protein kinase C pathway plays a central role in the fibroblast growth factor-stimulated expression and transactivation activity of Runx2. J Biol Chem 2003, 278:319-326.
43. Eda H., Aoki K., Marumo K., Fujii K., Ohkawa K. FGF-2 signaling induces downregulation of TAZ protein in osteoblastic MC3T3-E1 cells. Biochem Biophys Res Commun 2008, 366:471-475.
44. Alarcon C., Zaromytidou A.I., Xi Q., Gao S., Yu J., Fujisawa S., et al. Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-beta pathways. Cell 2009, 139:757-769.
45. Lian I., Kim J., Okazawa H., Zhao J., Zhao B., Yu J., et al. The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation. Genes Dev 2010, 24:1106-1118.
46. Tamm C., Bower N., Anneren C. Regulation of mouse embryonic stem cell self-renewal by a Yes-YAP-TEAD2 signaling pathway downstream of LIF. J Cell Sci 2011, 124:1136-1144.
47. Azzolin L., Zanconato F., Bresolin S., Forcato M., Basso G., Bicciato S., et al. Role of TAZ as mediator of Wnt signaling. Cell 2012, 151:1443-1456.
48. Greber B., Lehrach H., Adjaye J. Fibroblast growth factor 2 modulates transforming growth factor beta signaling in mouse embryonic fibroblasts and human ESCs (hESCs) to support hESC self-renewal. Stem cells 2007, 25:455-464.
49. Greber B., Coulon P., Zhang M., Moritz S., Frank S., Muller-Molina A.J., et al. FGF signalling inhibits neural induction in human embryonic stem cells. EMBO J 2011, 30:4874-4884.
50. Sterneckert J., Stehling M., Bernemann C., Arauzo-Bravo M.J., Greber B., Gentile L., et al. Neural induction intermediates exhibit distinct roles of Fgf signaling. Stem cells 2010, 28:1772-1781.