46
Views
62
CrossRef citations to date
0
Altmetric
Article

Direct Transcriptional Repression of Zfp423 by Zfp521 Mediates a Bone Morphogenic Protein-Dependent Osteoblast versus Adipocyte Lineage Commitment Switch

, , , , , & show all
Pages 3076-3085 | Received 10 Feb 2014, Accepted 27 May 2014, Published online: 20 Mar 2023

REFERENCES

  • Verma S, Rajaratnam JH, Denton J, Hoyland JA, Byers RJ. 2002. Adipocytic proportion of bone marrow is inversely related to bone formation in osteoporosis. J. Clin. Pathol. 55:693–698. http://dx.doi.org/10.1136/jcp.55.9.693.
  • Kaplan FS, Shore EM. 2000. Progressive osseous heteroplasia. J. Bone Miner. Res. 15:2084–2094. http://dx.doi.org/10.1359/jbmr.2000.15.11.2084.
  • Urist MR. 1965. Bone: formation by autoinduction. Science 150:893–899. http://dx.doi.org/10.1126/science.150.3698.893.
  • Lowery JW, Pazin D, Intini G, Kokabu S, Chappuis V, Capelo LP, Rosen V. 2011. The role of BMP2 signaling in the skeleton. Crit. Rev. Eukaryot. Gene Expr. 21:177–185. http://dx.doi.org/10.1615/CritRevEukarGeneExpr.v21.i2.60.
  • Yamaguchi A, Katagiri T, Ikeda T, Wozney JM, Rosen V, Wang EA, Kahn AJ, Suda T, Yoshiki S. 1991. Recombinant human bone morphogenetic protein-2 stimulates osteoblastic maturation and inhibits myogenic differentiation in vitro. J. Cell Biol. 113:681–687. http://dx.doi.org/10.1083/jcb.113.3.681.
  • Gimble JM, Morgan C, Kelly K, Wu X, Dandapani V, Wang CS, Rosen V. 1995. Bone morphogenetic proteins inhibit adipocyte differentiation by bone marrow stromal cells. J. Cell. Biochem. 58:393–402. http://dx.doi.org/10.1002/jcb.240580312.
  • Hata K, Nishimura R, Ikeda F, Yamashita K, Matsubara T, Nokubi T, Yoneda T. 2003. Differential roles of Smad1 and p38 kinase in regulation of peroxisome proliferator-activating receptor gamma during bone morphogenetic protein 2-induced adipogenesis. Mol. Biol. Cell 14:545–555. http://dx.doi.org/10.1091/mbc.E02-06-0356.
  • Huang H, Song TJ, Li X, Hu L, He Q, Liu M, Lane MD, Tang QQ. 2009. BMP signaling pathway is required for commitment of C3H10T1/2 pluripotent stem cells to the adipocyte lineage. Proc. Natl. Acad. Sci. U. S. A. 106:12670–12675. http://dx.doi.org/10.1073/pnas.0906266106.
  • Jin W, Takagi T, Kanesashi SN, Kurahashi T, Nomura T, Harada J, Ishii S. 2006. Schnurri-2 controls BMP-dependent adipogenesis via interaction with Smad proteins. Dev. Cell 10:461–471. http://dx.doi.org/10.1016/j.devcel.2006.02.016.
  • Tseng YH, Kokkotou E, Schulz TJ, Huang TL, Winnay JN, Taniguchi CM, Tran TT, Suzuki R, Espinoza DO, Yamamoto Y, Ahrens MJ, Dudley AT, Norris AW, Kulkarni RN, Kahn CR. 2008. New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 454:1000–1004. http://dx.doi.org/10.1038/nature07221.
  • Acampora D, Merlo GR, Paleari L, Zerega B, Postiglione MP, Mantero S, Bober E, Barbieri O, Simeone A, Levi G. 1999. Craniofacial, vestibular and bone defects in mice lacking the Distal-less-related gene Dlx5. Development 126:3795–3809.
  • Ichida F, Nishimura R, Hata K, Matsubara T, Ikeda F, Hisada K, Yatani H, Cao X, Komori T, Yamaguchi A, Yoneda T. 2004. Reciprocal roles of MSX2 in regulation of osteoblast and adipocyte differentiation. J. Biol. Chem. 279:34015–34022. http://dx.doi.org/10.1074/jbc.M403621200.
  • Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G. 1997. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89:747–754. http://dx.doi.org/10.1016/S0092-8674(00)80257-3.
  • Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR, de Crombrugghe B. 2002. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 108:17–29. http://dx.doi.org/10.1016/S0092-8674(01)00622-5.
  • Lee MH, Kim YJ, Kim HJ, Park HD, Kang AR, Kyung HM, Sung JH, Wozney JM, Ryoo HM. 2003. BMP-2-induced Runx2 expression is mediated by Dlx5, and TGF-beta 1 opposes the BMP-2-induced osteoblast differentiation by suppression of Dlx5 expression. J. Biol. Chem. 278:34387–34394. http://dx.doi.org/10.1074/jbc.M211386200.
  • Ryoo HM, Lee MH, Kim YJ. 2006. Critical molecular switches involved in BMP-2-induced osteogenic differentiation of mesenchymal cells. Gene 366:51–57. http://dx.doi.org/10.1016/j.gene.2005.10.011.
  • Gupta RK, Arany Z, Seale P, Mepani RJ, Ye L, Conroe HM, Roby YA, Kulaga H, Reed RR, Spiegelman BM. 2010. Transcriptional control of preadipocyte determination by Zfp423. Nature 464:619–623. http://dx.doi.org/10.1038/nature08816.
  • Gupta RK, Mepani RJ, Kleiner S, Lo JC, Khandekar MJ, Cohen P, Frontini A, Bhowmick DC, Ye L, Cinti S, Spiegelman BM. 2012. Zfp423 expression identifies committed preadipocytes and localizes to adipose endothelial and perivascular cells. Cell Metab. 15:230–239. http://dx.doi.org/10.1016/j.cmet.2012.01.010.
  • Bond HM, Mesuraca M, Amodio N, Mega T, Agosti V, Fanello D, Pelaggi D, Bullinger L, Grieco M, Moore MA, Venuta S, Morrone G. 2008. Early hematopoietic zinc finger protein-zinc finger protein 521: a candidate regulator of diverse immature cells. Int. J. Biochem. Cell Biol. 40:848–854. http://dx.doi.org/10.1016/j.biocel.2007.04.006.
  • Wu M, Hesse E, Morvan F, Zhang JP, Correa D, Rowe GC, Kiviranta R, Neff L, Philbrick WM, Horne WC, Baron R. 2009. Zfp521 antagonizes Runx2, delays osteoblast differentiation in vitro, and promotes bone formation in vivo. Bone 44:528–536. http://dx.doi.org/10.1016/j.bone.2008.11.011.
  • Kamiya D, Banno S, Sasai N, Ohgushi M, Inomata H, Watanabe K, Kawada M, Yakura R, Kiyonari H, Nakao K, Jakt LM, Nishikawa S, Sasai Y. 2011. Intrinsic transition of embryonic stem-cell differentiation into neural progenitors. Nature 470:503–509. http://dx.doi.org/10.1038/nature09726.
  • Kiviranta R, Yamana K, Saito H, Ho DK, Laine J, Tarkkonen K, Nieminen-Pihala V, Hesse E, Correa D, Maatta J, Tessarollo L, Rosen ED, Horne WC, Jenkins NA, Copeland NG, Warming S, Baron R. 2013. Coordinated transcriptional regulation of bone homeostasis by Ebf1 and Zfp521 in both mesenchymal and hematopoietic lineages. J. Exp. Med. 210:969–985. http://dx.doi.org/10.1084/jem.20121187.
  • Correa D, Hesse E, Seriwatanachai D, Kiviranta R, Saito H, Yamana K, Neff L, Atfi A, Coillard L, Sitara D, Maeda Y, Warming S, Jenkins NA, Copeland NG, Horne WC, Lanske B, Baron R. 2010. Zfp521 is a target gene and key effector of parathyroid hormone-related peptide signaling in growth plate chondrocytes. Dev. Cell 19:533–546. http://dx.doi.org/10.1016/j.devcel.2010.09.008.
  • Hesse E, Saito H, Kiviranta R, Correa D, Yamana K, Neff L, Toben D, Duda G, Atfi A, Geoffroy V, Horne WC, Baron R. 2010. Zfp521 controls bone mass by HDAC3-dependent attenuation of Runx2 activity. J. Cell Biol. 191:1271–1283. http://dx.doi.org/10.1083/jcb.201009107.
  • Kang S, Akerblad P, Kiviranta R, Gupta RK, Kajimura S, Griffin MJ, Min J, Baron R, Rosen ED. 2012. Regulation of early adipose commitment by Zfp521. PLoS Biol. 10:e1001433. http://dx.doi.org/10.1371/journal.pbio.1001433.
  • Yu K, Xu J, Liu Z, Sosic D, Shao J, Olson EN, Towler DA, Ornitz DM. 2003. Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 130:3063–3074. http://dx.doi.org/10.1242/dev.00491.
  • Mundy G, Garrett R, Harris S, Chan J, Chen D, Rossini G, Boyce B, Zhao M, Gutierrez G. 1999. Stimulation of bone formation in vitro and in rodents by statins. Science 286:1946–1949. http://dx.doi.org/10.1126/science.286.5446.1946.
  • Thies RS, Bauduy M, Ashton BA, Kurtzberg L, Wozney JM, Rosen V. 1992. Recombinant human bone morphogenetic protein-2 induces osteoblastic differentiation in W-20-17 stromal cells. Endocrinology 130:1318–1324.
  • Deng W-G, Zhu Y, Montero A, Wu KK. 2003. Quantitative analysis of binding of transcription factor complex to biotinylated DNA probe by a streptavidin-agarose pulldown assay. Anal. Biochem. 323:12–18. http://dx.doi.org/10.1016/j.ab.2003.08.007.
  • Katagiri T, Imada M, Yanai T, Suda T, Takahashi N, Kamijo R. 2002. Identification of a BMP-responsive element in Id1, the gene for inhibition of myogenesis. Genes Cells 7:949–960. http://dx.doi.org/10.1046/j.1365-2443.2002.00573.x.
  • Cho YW, Hong CJ, Hou A, Gent PM, Zhang K, Won KJ, Hamilton BA. 2013. Zfp423 binds autoregulatory sites in p19 cell culture model. PLoS One 8:e66514. http://dx.doi.org/10.1371/journal.pone.0066514.
  • Sabatakos G, Rowe GC, Kveiborg M, Wu M, Neff L, Chiusaroli R, Philbrick WM, Baron R. 2008. Doubly truncated FosB isoform (Δ2ΔFosB) induces osteosclerosis in transgenic mice and modulates expression and phosphorylation of Smads in osteoblasts independent of intrinsic AP-1 activity. J. Bone Miner. Res. 23:584–595. http://dx.doi.org/10.1359/jbmr.080110.
  • Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. 2007. A global double-fluorescent Cre reporter mouse. Genesis 45:593–605. http://dx.doi.org/10.1002/dvg.20335.
  • Yang Q-Y, Liang J-F, Rogers CJ, Zhao J-X, Zhu M-J, Du M. 2013. Maternal obesity induces epigenetic modifications to facilitate Zfp423 expression and enhance adipogenic differentiation in fetal mice. Diabetes 62:3727–3735. http://dx.doi.org/10.2337/db13-0433.
  • Wang L, Xu S, Lee JE, Baldridge A, Grullon S, Peng W, Ge K. 2013. Histone H3K9 methyltransferase G9a represses PPARgamma expression and adipogenesis. EMBO J. 32:45–59. http://dx.doi.org/10.1038/emboj.2012.306.
  • Ye L, Fan Z, Yu B, Chang J, Al Hezaimi K, Zhou X, Park NH, Wang CY. 2012. Histone demethylases KDM4B and KDM6B promotes osteogenic differentiation of human MSCs. Cell Stem Cell 11:50–61. http://dx.doi.org/10.1016/j.stem.2012.04.009.
  • Bond HM, Mesuraca M, Carbone E, Bonelli P, Agosti V, Amodio N, De Rosa G, Di Nicola M, Gianni AM, Moore MA, Hata A, Grieco M, Morrone G, Venuta S. 2004. Early hematopoietic zinc finger protein (EHZF), the human homolog to mouse Evi3, is highly expressed in primitive human hematopoietic cells. Blood 103:2062–2070. http://dx.doi.org/10.1182/blood-2003-07-2388.
  • Hata A, Seoane J, Lagna G, Montalvo E, Hemmati-Brivanlou A, Massague J. 2000. OAZ uses distinct DNA- and protein-binding zinc fingers in separate BMP-Smad and Olf signaling pathways. Cell 100:229–240. http://dx.doi.org/10.1016/S0092-8674(00)81561-5.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.