Expression of TLE3 by bone marrow stromal cells is regulated by canonical Wnt signaling

FEBS Letters

Volumn 588, Issue 4, 2014, Pages 614-619

  Kokabu, Shoichiro ^a,b   Sato, Tsuyoshi ^a   Ohte, Satoshi ^b   Enoki, Yuichiro ^a   Okubo, Masahiko ^a   Hayashi, Naoki ^a   Nojima, Junya ^a   Tsukamoto, Sho ^a   Fukushima, Yosuke ^a   Sakata, Yasuaki ^a   Katagiri, Takenobu ^a   Rosen, Vicki ^b   Yoda, Tetsuya ^a  

^a SAITAMA MEDICAL UNIVERSITY   (Japan)

^b HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

Co repressor; Groucho; Osteoblastogenesis; Osteoporosis; Transducing like enhancer of split; Wnt

Indexed keywords

REPRESSOR PROTEIN; TRANSDUCING LIKE ENHANCER OF SPLIT 3 PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CONTROLLED STUDY; GENOMICS; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STROMA CELL;

CO-REPRESSOR; GROUCHO; OSTEOBLASTOGENESIS; OSTEOPOROSIS; TRANSDUCING-LIKE ENHANCER OF SPLIT; WNT;

ANIMALS; BASE SEQUENCE; BETA CATENIN; BINDING SITES; CELL DIFFERENTIATION; CELL LINE; CO-REPRESSOR PROTEINS; CONSERVED SEQUENCE; GENE EXPRESSION REGULATION; GENOMICS; HUMANS; MESENCHYMAL STROMAL CELLS; MICE; MOLECULAR SEQUENCE DATA; OSTEOBLASTS; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84896697309     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2013.12.031     Document Type: Article

References (60)

1. S.L. Teitelbaum Bone resorption by osteoclasts Science 289 2000 1504 1508
2. M. Owen Marrow stromal stem cells J. Cell Sci. Supplement 10 1988 63 76 (Pubitemid 19096575)
3. G. Chamberlain, J. Fox, B. Ashton, and J. Middleton Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing Stem Cells 25 2007 2739 2749 (Pubitemid 350127858)
4. C.R. Howlett, J. Cave, M. Williamson, J. Farmer, S.Y. Ali, I. Bab, and M.E. Owen Mineralization in in vitro cultures of rabbit marrow stromal cells Clin. Orthop. Relat. Res. 1986 251 263 (Pubitemid 17187828)
5. B.A. Ashton, T.D. Allen, C.R. Howlett, C.C. Eaglesom, A. Hattori, and M. Owen Formation of bone and cartilage by marrow stromal cells in diffusion chambers in vivo Clin. Orthop. Relat. Res. 1980 294 307
6. R.W. Budenz, and G.W. Bernard Osteogenesis and leukopoiesis within diffusion-chamber implants of isolated bone marrow subpopulations Am. J. Anat. 159 1980 455 474 (Pubitemid 11179252)
7. R.S. Thies, M. Bauduy, B.A. Ashton, L. Kurtzberg, J.M. Wozney, and V. Rosen Recombinant human bone morphogenetic protein-2 induces osteoblastic differentiation in W-20-17 stromal cells Endocrinology 130 1992 1318 1324
8. S. Kokabu et al. BMP3 suppresses osteoblast differentiation of bone marrow stromal cells via interaction with Acvr2b Mol. Endocrinol. 26 2012 87 94
9. P. Ducy, R. Zhang, V. Geoffroy, A.L. Ridall, and G. Karsenty Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation Cell 89 1997 747 754 (Pubitemid 27516177)
10. K. Nakashima, X. Zhou, G. Kunkel, Z. Zhang, J.M. Deng, R.R. Behringer, and B. de Crombrugghe The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation Cell 108 2002 17 29 (Pubitemid 34137009)
11. S.C. Xu, M.A. Harris, J.L. Rubenstein, G.R. Mundy, and S.E. Harris Bone morphogenetic protein-2 (BMP-2) signaling to the Col2alpha1 gene in chondroblasts requires the homeobox gene Dlx-2 DNA Cell Biol. 20 2001 359 365 (Pubitemid 32692439)
12. K. Miyama, G. Yamada, T.S. Yamamoto, C. Takagi, K. Miyado, M. Sakai, N. Ueno, and H. Shibuya A BMP-inducible gene, dlx5, regulates osteoblast differentiation and mesoderm induction Dev. Biol. 208 1999 123 133 (Pubitemid 29149452)
13. T. Komori et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts Cell 89 1997 755 764 (Pubitemid 27516178)
14. F. Otto et al. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development Cell 89 1997 765 771 (Pubitemid 27516179)
15. P. Bialek et al. A twist code determines the onset of osteoblast differentiation Dev. Cell 6 2004 423 435 (Pubitemid 38364573)
16. N. Funato, S.L. Chapman, M.D. McKee, H. Funato, J.A. Morris, J.M. Shelton, J.A. Richardson, and H. Yanagisawa Hand2 controls osteoblast differentiation in the branchial arch by inhibiting DNA binding of Runx2 Development 136 2009 615 625
17. E. Hesse et al. Zfp521 controls bone mass by HDAC3-dependent attenuation of Runx2 activity J. Cell Biol. 191 2010 1271 1283
18. S. Kim et al. Stat1 functions as a cytoplasmic attenuator of Runx2 in the transcriptional program of osteoblast differentiation Genes Dev. 17 2003 1979 1991 (Pubitemid 36999325)
19. D.C. Jones, M.N. Wein, M. Oukka, J.G. Hofstaetter, M.J. Glimcher, and L.H. Glimcher Regulation of adult bone mass by the zinc finger adapter protein Schnurri-3 Science 312 2006 1223 1227 (Pubitemid 43801150)
20. S. Ohba et al. Patched1 haploinsufficiency increases adult bone mass and modulates Gli3 repressor activity Dev. Cell 14 2008 689 699 (Pubitemid 351622616)
21. B. Kanzler, S.J. Kuschert, Y.H. Liu, and M. Mallo Hoxa-2 restricts the chondrogenic domain and inhibits bone formation during development of the branchial area Development 125 1998 2587 2597 (Pubitemid 28396157)
22. V. Garg, A.N. Muth, J.F. Ransom, M.K. Schluterman, R. Barnes, I.N. King, P.D. Grossfeld, and D. Srivastava Mutations in NOTCH1 cause aortic valve disease Nature 437 2005 270 274 (Pubitemid 41294491)
23. M.J. Hilton et al. Notch signaling maintains bone marrow mesenchymal progenitors by suppressing osteoblast differentiation Nat. Med. 14 2008 306 314 (Pubitemid 351347911)
24. B.H. Jennings, and D. Ish-Horowicz The Groucho/TLE/Grg family of transcriptional co-repressors Genome Biol. 9 2008 205
25. S. Kokabu, T. Nguyen, S. Ohte, T. Sato, T. Katagiri, T. Yoda, and V. Rosen TLE3, transducing-like enhancer of split 3, suppresses osteoblast differentiation of bone marrow stromal cells Biochem. Biophys. Res. Commun. 438 2013 205 210
26. Z. Zhang, S. Schwartz, L. Wagner, and W. Miller A greedy algorithm for aligning DNA sequences J. Comput. Biol. 7 2000 203 214 (Pubitemid 30412170)
27. I. Ovcharenko, M.A. Nobrega, G.G. Loots, and L. Stubbs ECR Browser: a tool for visualizing and accessing data from comparisons of multiple vertebrate genomes Nucleic Acids Res. 32 2004 W280 W286
28. K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods Mol. Biol. Evol. 28 2011 2731 2739
29. I. Ovcharenko, G.G. Loots, R.C. Hardison, W. Miller, and L. Stubbs ZPicture: dynamic alignment and visualization tool for analyzing conservation profiles Genome Res. 14 2004 472 477 (Pubitemid 38380402)
30. G.G. Loots, and I. Ovcharenko RVISTA 2.0: evolutionary analysis of transcription factor binding sites Nucleic Acids Res. 32 2004 W217 W221
31. T. Fukuda et al. Canonical Wnts and BMPs cooperatively induce osteoblastic differentiation through a GSK3beta-dependent and beta-catenin-independent mechanism Differentiation 80 2010 46 52
32. S. Kokabu et al. Suppression of BMP-Smad signaling axis-induced osteoblastic differentiation by small C-terminal domain phosphatase 1, a Smad phosphatase Mol. Endocrinol. 25 2011 474 481
33. L.A. Goldman, E.C. Cutrone, S.V. Kotenko, C.D. Krause, and J.A. Langer Modifications of vectors pEF-BOS, pcDNA1 and pcDNA3 result in improved convenience and expression Biotechniques 21 1996 1013 1015 (Pubitemid 26422004)
34. T. Katagiri et al. The non-osteogenic mouse pluripotent cell line, C3H10T1/2, is induced to differentiate into osteoblastic cells by recombinant human bone morphogenetic protein-2 Biochem. Biophys. Res. Commun. 172 1990 295 299 (Pubitemid 20352535)
35. S. Kokabu, J. Nojima, K. Kanomata, S. Ohte, T. Yoda, T. Fukuda, and T. Katagiri Protein phosphatase magnesium-dependent 1A-mediated inhibition of BMP signaling is independent of Smad dephosphorylation J. Bone Miner. Res. 25 2010 653 660
36. T. Sato et al. Nicotine induces cell proliferation in association with cyclin D1 up-regulation and inhibits cell differentiation in association with p53 regulation in a murine pre-osteoblastic cell line Biochem. Biophys. Res Commun. 377 2008 126 130
37. J. Nojima et al. Dual roles of smad proteins in the conversion from myoblasts to osteoblastic cells by bone morphogenetic proteins J. Biol. Chem. 285 2010 15577 15586
38. S. Ohte et al. Identification and functional analysis of Zranb2 as a novel Smad-binding protein that suppresses BMP signaling J. Cell. Biochem. 113 2012 808 814
39. K. Kanomata, S. Kokabu, J. Nojima, T. Fukuda, and T. Katagiri DRAGON, a GPI-anchored membrane protein, inhibits BMP signaling in C2C12 myoblasts Genes Cells 14 2009 695 702
40. M. Shin et al. Identification of a novel bone morphogenetic protein (BMP)-inducible transcript, BMP-inducible transcript-1, by utilizing the conserved BMP-responsive elements in the Id genes J. Bone Miner. Metab. 31 2013 34 43
41. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 25 2001 402 408 (Pubitemid 34164012)
42. J.W. Lowery, A.W. Lavigne, S. Kokabu, and V. Rosen Comparative genomics identifies the mouse Bmp3 promoter and an upstream evolutionary conserved region (ECR) in mammals PloS One 8 2013 e57840
43. S.E. Ross, N. Hemati, K.A. Longo, C.N. Bennett, P.C. Lucas, R.L. Erickson, and O.A. MacDougald Inhibition of adipogenesis by Wnt signaling Science 289 2000 950 953 (Pubitemid 30659947)
44. M. Kato et al. Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor J. Cell Biol. 157 2002 303 314 (Pubitemid 34839826)
45. E.D. Rosen, C.J. Walkey, P. Puigserver, and B.M. Spiegelman Transcriptional regulation of adipogenesis Genes Dev. 14 2000 1293 1307 (Pubitemid 30397073)
46. P. Tontonoz, E. Hu, and B.M. Spiegelman Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor Cell 79 1994 1147 1156
47. R.A. Cavallo, R.T. Cox, M.M. Moline, J. Roose, G.A. Polevoy, H. Clevers, M. Peifer, and A. Bejsovec Drosophila Tcf and Groucho interact to repress Wingless signalling activity Nature 395 1998 604 608 (Pubitemid 28475714)
48. B.K. Choudhury, J. Kim, H.F. Kung, and S.S. Li Cloning and developmental expression of Xenopus cDNAs encoding the enhancer of split groucho and related proteins Gene 195 1997 41 48 (Pubitemid 27336959)
49. H. Miyasaka, B.K. Choudhury, E.W. Hou, and S.S. Li Molecular cloning and expression of mouse and human cDNA encoding AES and ESG proteins with strong similarity to Drosophila enhancer of split groucho protein Eur. J. Biochem./FEBS 216 1993 343 352 (Pubitemid 23255205)
50. A. Pflugrad, J.Y. Meir, T.M. Barnes, and D.M. Miller 3rd. The Groucho-like transcription factor UNC-37 functions with the neural specificity gene unc-4 to govern motor neuron identity in C. elegans Development 124 1997 1699 1709 (Pubitemid 27248337)
51. F.S. Sharief, S.C. Tsoi, and S.S. Li CDNA cloning and genomic organization of enhancer of split groucho gene from nematode Caenorhabditis elegans Biochem. Mol. Biol. Int. 43 1997 327 337 (Pubitemid 28297135)
52. S. Stifani, C.M. Blaumueller, N.J. Redhead, R.E. Hill, and S. Artavanis-Tsakonas Human homologs of a Drosophila Enhancer of split gene product define a novel family of nuclear proteins Nat. Genet. 2 1992 343
53. M. Mallo, F. Franco del Amo, and T. Gridley Cloning and developmental expression of Grg, a mouse gene related to the groucho transcript of the Drosophila Enhancer of split complex Mech. Dev. 42 1993 67 76 (Pubitemid 23235180)
54. G. Chen, and A.J. Courey Groucho/TLE family proteins and transcriptional repression Gene 249 2000 1 16 (Pubitemid 30265483)
55. H. Nakayama, Y. Liu, S. Stifani, and J.C. Cross Developmental restriction of Mash-2 expression in trophoblast correlates with potential activation of the notch-2 pathway Dev. Genet. 21 1997 21 30 (Pubitemid 27381637)
56. C.J. Villanueva et al. TLE3 is a dual-function transcriptional coregulator of adipogenesis Cell Metab. 13 2011 413 427
57. C.J. Villanueva et al. Adipose subtype-selective recruitment of TLE3 or Prdm16 by PPARgamma specifies lipid storage versus thermogenic gene programs Cell Metab. 17 2013 423 435
58. J. Guo et al. Suppression of Wnt signaling by Dkk1 attenuates PTH-mediated stromal cell response and new bone formation Cell Metab. 11 2010 161 171
59. V. Rosen Harnessing the parathyroid hormone, Wnt, and bone morphogenetic protein signaling cascades for successful bone tissue engineering Tissue Eng. Part B 17 2011 475 479
60. B.A. Lenart, D.G. Lorich, and J.M. Lane Atypical fractures of the femoral diaphysis in postmenopausal women taking alendronate N. Engl. J. Med. 358 2008 1304 1306 (Pubitemid 351439247)