Slug gene expression supports human osteoblast maturation

Cellular and Molecular Life Sciences

Volumn 66, Issue 22, 2009, Pages 3641-3653

  Lambertini, Elisabetta ^a   Lisignoli, Gina ^b   Torreggiani, Elena ^a   Manferdini, Cristina ^b   Gabusi, Elena ^b   Franceschetti, Tiziana ^a   Penolazzi, Letizia ^a   Gambari, Roberto ^a   Facchini, Andrea ^b,c   Piva, Roberta ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Human osteoblasts; Runx2; Slug; Sox 9; Wnt signaling

Indexed keywords

BETA CATENIN; COLLAGEN TYPE 1; OSTEOCALCIN; OSTEOPONTIN; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SOX9; WNT PROTEIN;

ARTICLE; CARTILAGE CELL; CELL MATURATION; CONTROLLED STUDY; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN TISSUE; OSTEOBLAST; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

AGED; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; CORE BINDING FACTOR ALPHA 1 SUBUNIT; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; HUMANS; MIDDLE AGED; OSTEOBLASTS; OSTEOGENESIS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SIGNAL TRANSDUCTION; SOX9 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTORS; WNT PROTEINS;

EID: 70449390675     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-009-0149-5     Document Type: Article

References (43)

1. G Karsenty EF Wagner 2002 Reaching a genetic and molecular understanding of skeletal development Dev Cell 2 389 406 10.1016/S1534-5807(02)00157-0 1:CAS:528:DC%2BD38Xjt1ersb4%3D 11970890 (Pubitemid 34436569)
2. CS Soltanoff S Yang W Chen YP Li 2009 Signaling networks that control the lineage commitment and differentiation of bone cells Crit Rev Eukaryot Gene Expr 19 1 46 1:CAS:528:DC%2BD1MXjt1Sisbw%3D 19191755
3. C Hartmann 2006 A Wnt canon orchestrating osteoblastogenesis Trends Cell Biol 16 151 158 10.1016/j.tcb.2006.01.001 1:CAS:528:DC%2BD28Xit1Chsr0%3D 16466918 (Pubitemid 43358003)
4. X Wu W Shi X Cao 2007 Multiplicity of BMP signaling in skeletal development Ann N Y Acad Sci 1116 29 49 10.1196/annals.1402.053 1:CAS:528:DC%2BD1cXitVGksQ%3D%3D 18083919 (Pubitemid 350274336)
5. M Hayashi K Nimura K Kashiwagi T Harada K Takaoka H Kato K Tamai Y Kaneda 2007 Comparative roles of Twist-1 and Id1 in transcriptional regulation by BMP signaling J Cell Sci 120 1350 1357 10.1242/jcs.000067 1:CAS:528: DC%2BD2sXlsFSjtLo%3D 17374642 (Pubitemid 46780028)
6. PJ Marie 2008 Transcription factors controlling osteoblastogenesis Arch Biochem Biophys 473 98 105 10.1016/j.abb.2008.02.030 1:CAS:528: DC%2BD1cXlsFOgurg%3D 18331818
7. JB Lian A Javed SK Zaidi C Lengner M Montecino AJ van Wijnen JL Stein GS Stein 2004 Regulatory controls for osteoblast growth and differentiation: role of Runx/Cbfa/AML factors Crit Rev Eukaryot Gene Expr 14 1 41 10.1615/CritRevEukaryotGeneExpr.v14.i12.10 1:CAS:528:DC%2BD2cXkslGisbY%3D 15104525
8. G Xiao D Jiang C Ge Z Zhao Y Lai H Boules M Phimphilai X Yang G Karsenty RT Franceschi 2005 Cooperative interactions between activating transcription factor 4 and Runx2/Cbfa1 stimulate osteoblast-specific osteocalcin gene expression J Biol Chem 280 30689 30696 10.1074/jbc.M500750200 1:CAS:528:DC%2BD2MXpsVCmsLk%3D 16000305 (Pubitemid 41291797)
9. HM Hoffmann KM Catron AJ van Wijnen LR McCabe JB Lian GS Stein JL Stein 1994 Transcriptional control of the tissue-specific, developmentally regulated osteocalcin gene requires a binding motif for the Msx family of homeodomain proteins Proc Natl Acad Sci USA 91 12887 12891 10.1073/pnas.91.26.12887 1:CAS:528:DyaK2MXivVCqs7g%3D 7809141
10. MQ Hassan A Javed MI Morasso J Karlin M Montecino AJ van Wijnen GS Stein JL Stein JB Lian 2004 Dlx3 transcriptional regulation of osteoblast differentiation: temporal recruitment of Msx2, Dlx3, and Dlx5 homeodomain proteins to chromatin of the osteocalcin gene Mol Cell Biol 24 9248 9261 10.1128/MCB.24.20.9248-9261.2004 1:CAS:528:DC%2BD2cXotl2mu7o%3D 15456894 (Pubitemid 39313925)
11. ZL Deng KA Sharff N Tang WX Song J Luo X Luo J Chen E Bennett R Reid D Manning A Xue AG Montag HH Luu RC Haydon TC He 2008 Regulation of osteogenic differentiation during skeletal development Front Biosci 13 2001 2021 10.2741/2819 1:CAS:528:DC%2BD1cXhs1Cgt7g%3D 17981687 (Pubitemid 351589231)
12. M Machwate A Jullienne M Moukhtar A Lomri PJ Marie 1995 c- fos protooncogene is involved in the mitogenic effect of transforming growth factor-beta in osteoblastic cells Mol Endocrinol 9 187 198 10.1210/me.9.2.187 1:CAS:528:DyaK2MXjvVajurg%3D 7776969
13. T Gaur CJ Lengner H Hovhannisyan RA Bhat PV Bodine BS Komm A Javed AJ van Wijnen JL Stein GS Stein JB Lian 2005 Canonical WNT signaling promotes osteogenesis by directly stimulating Runx2 gene expression J Biol Chem 280 33132 33140 10.1074/jbc.M500608200 1:CAS:528:DC%2BD2MXhtVens7bJ 16043491 (Pubitemid 41397109)
14. MA Nieto 2002 The snail superfamily of zinc-finger transcription factors Nat Rev Mol Cell Biol 3 155 166 10.1038/nrm757 1:CAS:528:DC%2BD38XitFShsL4%3D 11994736
15. M Conacci-Sorrell I Simcha T Ben-Yedidia J Blechman P Savagner A Ben-Ze'ev 2003 Autoregulation of E-cadherin expression by cadherin-cadherin interactions: the roles of beta-catenin signaling, Slug, and MAPK J Cell Biol 163 847 857 10.1083/jcb.200308162 1:CAS:528:DC%2BD3sXpsVClt7s%3D 14623871 (Pubitemid 37517891)
16. KM Hajra DY Chen ER Fearon 2002 The SLUG zinc-finger protein represses E-cadherin in breast cancer Cancer Res 62 1613 1618 1:CAS:528: DC%2BD38XisVSisL8%3D 11912130
17. A Barrallo-Gimeno MA Nieto 2005 The Snail genes as inducers of cell movement and survival: Implications in development and cancer Development 132 3151 3161 10.1242/dev.01907 1:CAS:528:DC%2BD2MXosVemu74%3D 15983400 (Pubitemid 41167144)
18. B Tonnarelli C Manferdini A Piacentini K Codeluppi N Zini S Ghisu A Facchini G Lisignoli 2008 Surface-dependent modulation of proliferation, bone matrix molecules, and inflammatory factors in human osteoblasts J Biomed Mater Res 89 687 696
19. PG Robey JD Termine 1985 Human bone cells in vitro Calcif Tissue Int 37 453 460 10.1007/BF02557826 1:STN:280:DyaL28%2Flt1yhsQ%3D%3D 2998572 (Pubitemid 15250110)
20. B Grigolo G Lisignoli A Piacentini M Fiorini P Gobbi G Mazzotti M Duca A Pavesio A Facchini 2002 Evidence for redifferentiation of human chondrocytes grown on a hyaluronan-based biomaterial (HYAff 11): molecular, immunohistochemical and ultrastructural analysis Biomaterials 23 1187 1195 10.1016/S0142-9612(01)00236-8 1:CAS:528:DC%2BD3MXos1Wqtb4%3D 11791922 (Pubitemid 33109050)
21. E Lambertini E Tavanti E Torreggiani L Penolazzi R Gambari R Piva 2008 ER alpha and AP-1 interact in vivo with a specific sequence of the F promoter of the human ER alpha gene in osteoblasts J Cell Physiol 216 101 110 10.1002/jcp.21379 1:CAS:528:DC%2BD1cXnt1eksLk%3D 18247370 (Pubitemid 351813100)
22. E Lambertini L Penolazzi E Tavanti GP Schincaglia M Zennaro R Gambari R Piva 2007 Human estrogen receptor alpha gene is a target of Runx2 transcription factor in osteoblasts Exp Cell Res 313 1548 1560 10.1016/j.yexcr.2007.02.002 1:CAS:528:DC%2BD2sXksV2ktbk%3D 17350616 (Pubitemid 46589433)
23. MK Tripathi S Misra SV Khedkar N Hamilton C Irvin-Wilson C Sharan L Sealy G Chaudhuri 2005 Regulation of BRCA2 gene expression by the SLUG repressor protein in human breast cells J Biol Chem 280 17163 17171 10.1074/jbc.M501375200 1:CAS:528:DC%2BD2MXjsFOgtLY%3D 15734731 (Pubitemid 41389182)
24. H Akiyama JP Lyons Y Mori-Akiyama X Yang R Zhang Z Zhang JM Deng MM Taketo T Nakamura RR Behringer PD McCrea B de Crombrugghe 2004 Interactions between Sox9 and beta-catenin control chondrocyte differentiation Genes Dev 18 1072 1087 10.1101/gad.1171104 1:CAS:528:DC%2BD2cXkt12gtrs%3D 15132997 (Pubitemid 38620246)
25. ED Zhu MB Demay F Gori 2008 Wdr5 is essential for osteoblast differentiation J Biol Chem 283 7361 7367 10.1074/jbc.M703304200 1:CAS:528:DC%2BD1cXjt1emtbg%3D 18201971
26. M Katoh 2008 WNT signaling in stem cell biology and regenerative medicine Curr Drug Targets 9 565 570 10.2174/138945008784911750 1:CAS:528: DC%2BD1cXnsVOqtLY%3D 18673242
27. GJ Spencer JC Utting SL Etheridge TR Arnett PG Genever 2006 Wnt signalling in osteoblasts regulates expression of the receptor activator of NFkappaB ligand and inhibits osteoclastogenesis in vitro J Cell Sci 119 1283 1296 10.1242/jcs.02883 1:CAS:528:DC%2BD28Xks1Wjtrw%3D 16522681 (Pubitemid 43756545)
28. MK Mittal JN Myers S Misra CK Bailey G Chaudhuri 2008 In vivo binding to and functional repression of the VDR gene promoter by SLUG in human breast cells Biochem Biophys Res Commun 372 30 34 10.1016/j.bbrc.2008.04.187 1:CAS:528:DC%2BD1cXmvFekurc%3D 18485278
29. K Okazaki J Li H Yu N Fukui LJ Sandell 2002 CCAAT/enhancer-binding proteins beta and delta mediate the repression of gene transcription of cartilage-derived retinoic acid-sensitive protein induced by interleukin-1 beta J Biol Chem 277 31526 31533 10.1074/jbc.M202815200 1:CAS:528: DC%2BD38XmslOqsbg%3D 12072435 (Pubitemid 34968954)
30. Komori T (2009) Regulation of bone development and extracellular matrix protein genes by RUNX2. Cell Tissue Res. doi 10.1007/s00441-009-0832-8
31. Y Guo X Zi Z Koontz A Kim J Xie R Gorlick RF Holcombe BH Hoang 2007 Blocking Wnt/LRP5 signaling by a soluble receptor modulates the epithelial to mesenchymal transition and suppresses met and metalloproteinases in osteosarcoma Saos-2 cells J Orthop Res 25 964 971 10.1002/jor.20356 1:CAS:528: DC%2BD2sXotFanur0%3D 17318900 (Pubitemid 47046444)
32. G Zhou Q Zheng F Engin E Munivez Y Chen E Sebald D Krakow B Lee 2006 Dominance of Sox9 function over Runx2 during skeletogenesis Proc Natl Acad Sci USA 103 19004 19009 10.1073/pnas.0605170103 1:CAS:528:DC%2BD28XhtlektLfM 17142326 (Pubitemid 350002818)
33. LA Davis NI Zur Nieden 2008 Mesodermal fate decisions of a stem cell: the Wnt switch Cell Mol Life Sci 65 2658 2674 10.1007/s00018-008-8042-1 1:CAS:528:DC%2BD1cXhtVKisb3F 18528633
34. L Zou X Zou H Li T Mygind Y Zeng N Lü C Bünger 2006 Molecular mechanism of osteochondroprogenitor fate determination during bone formation Adv Exp Med Biol 585 431 441 10.1007/978-0-387-34133-0-28 1:CAS:528: DC%2BD1MXhtFynsr8%3D 17120800
35. L Topol W Chen H Song TF Day Y Yang 2009 Sox9 inhibits Wnt signaling by promoting beta-catenin phosphorylation in the nucleus J Biol Chem 284 3323 3333 10.1074/jbc.M808048200 1:CAS:528:DC%2BD1MXpsV2ksw%3D%3D 19047045
36. Z Hamidouche E Haÿ P Vaudin P Charbord R Schüle PJ Marie O Fromigué 2008 FHL2 mediates dexamethasone-induced mesenchymal cell differentiation into osteoblasts by activating Wnt/beta-catenin signaling-dependent Runx2 expression FASEB J 22 3813 3822 10.1096/fj.08-106302 1:CAS:528:DC%2BD1cXhtlCgtrbJ 18653765
37. Dong YF, Soung do Y, Schwarz EM, O'Keefe RJ, Drissi H (2006) Wnt induction of chondrocyte hypertrophy through the Runx2 transcription factor. J Cell Physiol 208:77-86
38. TF Day X Guo L Garrett-Beal Y Yang 2005 Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis Dev Cell 8 739 750 10.1016/j.devcel.2005.03.016 1:CAS:528:DC%2BD2MXkslentbc%3D 15866164 (Pubitemid 40585296)
39. S Kousteni M Almeida L Han T Bellido RL Jilka SC Manolagas 2007 Induction of osteoblast differentiation by selective activation of kinase-mediated actions of the estrogen receptor Mol Cell Biol 27 1516 1530 10.1128/MCB.01550-06 1:CAS:528:DC%2BD2sXit1amsLw%3D 17158928 (Pubitemid 46239831)
40. PV Bodine BS Komm 2006 Wnt signaling and osteoblastogenesis Rev Endocr Metab Disord 7 33 39 10.1007/s11154-006-9002-4 1:CAS:528:DC%2BD2sXht12mtQ%3D%3D 16960757 (Pubitemid 46049520)
41. CA de Frutos R Dacquin S Vega P Jurdic I Machuca-Gayet MA Nieto 2009 Snail1 controls bone mass by regulating Runx2 and VDR expression during osteoblast differentiation EMBO J 28 686 696 10.1038/emboj.2009.23 19197242
42. Y Zhang MQ Hassan ZY Li JL Stein JB Lian AJ van Wijnen GS Stein 2008 Intricate gene regulatory networks of helix-loop-helix (HLH) proteins support regulation of bone-tissue related genes during osteoblast differentiation J Cell Biochem 105 487 496 10.1002/jcb.21844 1:CAS:528:DC%2BD1cXht1elu7nM 18655182
43. P Leucht S Minear D Ten Berge R Nusse JA Helms 2008 Translating insights from development into regenerative medicine: the function of Wnts in bone biology Semin Cell Dev Biol 19 434 443 10.1016/j.semcdb.2008.09.002 1:CAS:528:DC%2BD1cXht1Knt73I 18824114