Cytokine & Growth Factor Reviews
Volume 22, Issue 5 , Pages 287-300 , October 2011

Few Smad proteins and many Smad-interacting proteins yield multiple functions and action modes in TGFβ/BMP signaling in vivo

  • Andrea Conidi

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Shared first authors.
    • Tel.: +32 16 373135; fax: +32 16 372581.
  • ,
  • Silvia Cazzola

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Shared first authors.
    • Tel.: +32 16 373137; fax: +32 16 372581.
  • ,
  • Karen Beets

      Affiliations

    • Laboratory of Developmental Signaling of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 10 753025; fax: +32 10 753000.
  • ,
  • Kathleen Coddens

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 373137; fax: +32 16 372581.
  • ,
  • Clara Collart

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Present address: Systems Biology, MRC National Institute for Medical Research, The Ridgeway, Mill Hill, London NW7 1AA, UK. Tel.: +44 20 8816 2272; fax: +44 20 8906 4477.
  • ,
  • Frederique Cornelis

      Affiliations

    • Laboratory of Developmental Signaling of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Present address: Division of Rheumatology, University of Leuven, Campus Gasthuisberg, Building Ond&Nav1, Herestraat 49, B-3000 Leuven, Belgium. Tel.: +32 16 346151; fax: +32 16 346200.
  • ,
  • Luk Cox

      Affiliations

    • Laboratory of Developmental Signaling of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Present address: Laboratory of Molecular Pathogenesis of Leukemia of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium. Tel.: +32 16 330119; fax: +32 16 330084.
  • ,
  • Debruyn Joke

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 10 753025; fax: +32 10 753000.
  • ,
  • Mariya P. Dobreva

      Affiliations

    • Laboratory of Developmental Signaling of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 330724; fax: +32 16 372581.
  • ,
  • Ruben Dries

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 373137; fax: +32 16 372581.
  • ,
  • Camila Esguerra

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Present address: Laboratory of Pharmaceutical Biology, University of Leuven, Campus Gasthuisberg, Building Ond&Nav2 Herestraat 49, B-3000 Leuven, Belgium. Tel.: +32 16 323439; fax: +32 16 323460.
  • ,
  • Annick Francis

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 373137; fax: +32 16 372581.
  • ,
  • Abdelilah Ibrahimi

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 495 221103; fax: +32 10 753000.
  • ,
  • Roel Kroes

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 373135; fax: +32 16 372581.
  • ,
  • Flore Lesage

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 373135; fax: +32 16 372581.
  • ,
  • Elke Maas

      Affiliations

    • Laboratory of Developmental Signaling of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 373169; fax: +32 16 372581.
  • ,
  • Ivan Moya

      Affiliations

    • Laboratory of Developmental Signaling of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 330724; fax: +32 16 372581.
  • ,
  • Paulo N.G. Pereira

      Affiliations

    • Laboratory of Developmental Signaling of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 330006; fax: +32 16 372581.
  • ,
  • Elke Stappers

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 373135; fax: +32 16 372581.
  • ,
  • Agata Stryjewska

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 373137; fax: +32 16 372581.
  • ,
  • Veronique van den Berghe

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 373135; fax: +32 16 372581.
  • ,
  • Liesbeth Vermeire

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Present address: InfraMouse, Animal facility, Campus Gasthuisberg, Herestraat 49, B-3000 Leuven, Belgium. Tel.: +32 16 330757; fax: +32 16 372581.
  • ,
  • Griet Verstappen

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 373135; fax: +32 16 372581.
  • ,
  • Eve Seuntjens

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 373135; fax: +32 16 372581.
  • ,
  • Lieve Umans

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Laboratory of Developmental Signaling of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 373137; fax: +32 16 372581.
  • ,
  • An Zwijsen

      Affiliations

    • Laboratory of Developmental Signaling of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), Campus Gasthuisberg, Building Ond&Nav4 level 06, Herestraat 49, B-3000 Leuven, Belgium
    • Tel.: +32 16 330006; fax: +32 16 372581.
  • ,
  • Danny Huylebroeck

      Affiliations

    • Laboratory of Molecular Biology (Celgen) of the Center for Human Genetics, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Department of Molecular and Developmental Genetics (VIB11), University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 level 05, Herestraat 49, B-3000 Leuven, Belgium
    • Corresponding Author InformationCorresponding author at: Laboratory of Molecular Biology (Celgen), c/o Stem Cell Institute, University of Leuven, Campus Gasthuisberg, Building Ond&Nav4 (room 05.313), Herestraat 49, B-3000 Leuven, Belgium. Tel.: +32 16 373139; fax: +32 16 372581.

References 

  1. Feng XH, Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Annu Rev Cell Dev Biol. 2005;21:659–693
  2. Schmierer B, Hill CS. TGFbeta–SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol. 2007;8:970–982
  3. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-beta family signaling. Nature. 2003;425:577–584
  4. Itoh S, ten Dijke P. Negative regulation of TGF-beta receptor/Smad signal transduction. Curr Opin Cell Biol. 2007;19:176–184
  5. Moustakas A, Heldin CH. The regulation of TGFbeta signal transduction. Development. 2009;136:3699–3714
  6. David L, Mallet C, Mazerbourg S, Feige JJ, Bailly S. Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells. Blood. 2007;109:1953–1961
  7. David L, Mallet C, Keramidas M, Lamandé N, Gasc JM, Dupuis-Girod S, et al. Bone morphogenetic protein-9 is a circulating vascular quiescence factor. Circ Res. 2008;102:914–922
  8. Goumans MJ, Liu Z, ten Dijke P. TGF-beta signaling in vascular biology and dysfunction. Cell Res. 2009;19:116–127
  9. David L, Feige JJ, Bailly S. Emerging role of bone morphogenetic proteins in angiogenesis. Cytokine Growth Factor Rev. 2009;20:203–212
  10. Pardali E, Goumans MJ, ten Dijke P. Signaling by members of the TGF-beta family in vascular morphogenesis and disease. Trends Cell Biol. 2010;20:556–567
  11. Le Roy C, Wrana JL. Clathrin- and non-clathrin-mediated endocytic regulation of cell signaling. Nat Rev Mol Cell Biol. 2005;6:112–126
  12. Hartung A, Bitton-Worms K, Rechtman MM, Wenzel V, Boergermann JH, Hassel S, et al. Different routes of bone morphogenic protein (BMP) receptor endocytosis influence BMP signaling. Mol Cell Biol. 2006;26:7791–7805
  13. Sieber C, Kopf J, Hiepen C, Knaus P. Recent advances in BMP receptor signaling. Cytokine Growth Factor Rev. 2009;20:343–355
  14. Nickel J, Sebald W, Groppe JC, Mueller TD. Intricacies of BMP receptor assembly. Cytokine Growth Factor Rev. 2009;20:367–377
  15. Zawel L, Dai JL, Buckhaults P, Zhou S, Kinzler KW, Vogelstein B, et al. Human Smad3 and Smad4 are sequence-specific transcription activators. Mol Cell. 1998;1:611–617
  16. Dennler S, Itoh S, Vivien D, ten Dijke P, Huet S, Gauthier JM. Direct binding of Smad3 and Smad4 to critical TGFbeta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J. 1998;17:3091–3100
  17. Ishida W, Hamamoto T, Kusanagi K, Yagi K, Kawabata M, Takehara K, et al. Characterization of bone morpho-genetic protein-responsive element in the mouse Smad6 promoter. J Biol Chem. 2000;275:6075–6079
  18. López-Rovira T, Chalaux E, Massagué J, Rosa JL, Ventura F. Direct binding of Smad1 and Smad4 to two distinct motifs mediates bone morphogenetic protein-specific transcriptional activation of Id1 gene. J Biol Chem. 2002;277:3176–3185
  19. Brugger SM, Merrill AE, Torres-Vazquez J, Wu N, Ting MC, Cho JY, et al. A phylogenetically conserved cis-regulatory module in the Msx2 promoter is sufficient for BMP-dependent transcription in murine and Drosophila embryos. Development. 2004;131:5153–5165
  20. Korchynskyi O, ten Dijke P. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem. 2002;277:4883–4891
  21. Nishihara A, Hanai JI, Okamoto N, Yanagisawa J, Kato S, Miyazono K, et al. Role of p300, a transcriptional coactivator, in signaling of TGF-beta. Genes Cells. 1998;3:613–623
  22. Pearson KL, Hunter T, Janknecht R. Activation of Smad1-mediated transcription by p300/CBP. Biochim Biophys Acta. 1999;1489:354–364
  23. Attisano L, Wrana JL. Smads as transcriptional co-modulators. Curr Opin Cell Biol. 2000;12:235–243
  24. Corradini E, Babitt JL, Lin HY. The RGM/DRAGON family of BMP co-receptors. Cytokine Growth Factor Rev. 2009;20:389–398
  25. Kang JS, Liu C, Derynck R. New regulatory mechanisms of TGF-beta receptor function. Trends Cell Biol. 2009;19:385–394
  26. Zakin L, De Robertis EM. Extracellular regulation of BMP signaling. Curr Biol. 2010;20:R89–R92
  27. Hill CS. Nucleocytoplasmic shuttling of Smad proteins. Cell Res. 2009;19:36–46
  28. Ishimura A, Ng JK, Taira M, Young SG, Osada S. Man1, an inner nuclear membrane protein, regulates vascular remodeling by modulating transforming growth factor beta signaling. Development. 2006;133:3919–3928
  29. Hellemans J, Preobrazhenska O, Willaert A, Debeer P, Verdonk PC, Costa T, et al. Loss-of-function mutations in LEMD3 result in osteopoikilosis, Buschke–Ollendorff syndrome and melorheostosis. Nat Genet. 2004;36:1213–1218
  30. Davis BN, Hilyard AC, Lagna G, Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature. 2008;454:56–61
  31. Zhang H, Bradley A. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development. 1996;122:2977–2986
  32. Winnier G, Blessing M, Labosky PA, Hogan BL. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 1995;9:2105–2116
  33. Lawson KA, Dunn NR, Roelen BA, Zeinstra LM, Davis AM, Wright CV, et al. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 1999;13:424–436
  34. Mishina Y, Suzuki A, Ueno N, Behringer RR. Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev. 1995;9:3027–3037
  35. Beppu H, Kawabata M, Hamamoto T, Chytil A, Minowa O, Noda T, et al. BMP type II receptor is required for gastrulation and early development of mouse embryos. Dev Biol. 2000;221:249–258
  36. Arnold SJ, Maretto S, Islam A, Bikoff EK, Robertson EJ. Dose-dependent Smad1, Smad5 and Smad8 signaling in the early mouse embryo. Dev Biol. 2006;296:104–118
  37. Chang H, Huylebroeck D, Verschueren K, Guo Q, Matzuk MM, Zwijsen A. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development. 1999;126:1631–1642
  38. Yang X, Castilla LH, Xu X, Li C, Gotay J, Weinstein M, et al. Angiogenesis defects and mesenchymal apoptosis in mice lacking SMAD5. Development. 1999;126:1571–1580
  39. Umans L, Cox L, Tjwa M, Bito V, Vermeire L, Laperre K, et al. Inactivation of Smad5 in endothelial cells and smooth muscle cells demonstrates that Smad5 is required for cardiac homeostasis. Am J Pathol. 2007;170:1460–1472
  40. Tremblay KD, Dunn NR, Robertson EJ. Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development. 2001;128:3609–3621
  41. Lechleider RJ, Ryan JL, Garrett L, Eng C, Deng C, Wynshaw-Boris A, et al. Targeted mutagenesis of Smad1 reveals an essential role in chorioallantoic fusion. Dev Biol. 2001;240:157–167
  42. Hayashi K, Kobayashi T, Umino T, Goitsuka R, Matsui Y, Kitamura D. SMAD1 signaling is critical for initial commitment of germ cell lineage from mouse epiblast. Mech Dev. 2002;118:99–109
  43. Furtado MB, Solloway MJ, Jones VJ, Costa MW, Biben C, Wolstein O, et al. BMP/SMAD1 signaling sets a threshold for the left/right pathway in lateral plate mesoderm and limits availability of SMAD4. Genes Dev. 2008;22:3037–3049
  44. Bosman EA, Lawson KA, Debruyn J, Beek L, Francis A, Schoonjans L, et al. Smad5 determines murine amnion fate through the control of bone morphogenetic protein expression and signaling levels. Development. 2006;133:3399–3409
  45. Ben-Haim N, Lu C, Guzman-Ayala M, Pescatore L, Mesnard D, Bischofberger M, et al. The nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4. Dev Cell. 2006;11:313–323
  46. Shen MM. Nodal signaling: developmental roles and regulation. Development. 2007;134:1023–1034
  47. Daly AC, Randall RA, Hill CS. Transforming growth factor beta-induced Smad1/5 phosphorylation in epithelial cells is mediated by novel receptor complexes and is essential for anchorage-independent growth. Mol Cell Biol. 2008;28:6889–6902
  48. Kaplan FS, Xu M, Seemann P, Connor JM, Glaser DL, Carroll L, et al. Classic and atypical fibrodysplasia ossificans progressiva (FOP) phenotypes are caused by mutations in the bone morphogenetic protein (BMP) type I receptor ACVR1. Hum Mutat. 2009;30:379–390
  49. Groppe JC, Wu J, Shore EM, Kaplan FS. In vitro analyses of the dysregulated R206H ALK2 kinase-FKBP12 interaction associated with heterotopic ossification in FOP. Cells Tissues Organs. 2011;194:291–295
  50. Shen Q, Little SC, Xu M, Haupt J, Ast C, Katagiri T, et al. The fibrodysplasia ossificans progressiva R206H ACVR1 mutation activates BMP-independent chondrogenesis and zebrafish embryo ventralization. J Clin Invest. 2009;119:3462–3472
  51. Kaplan FS, Pignolo RJ, Shore EM. The FOP metamorphogene encodes a novel type I receptor that dysregulates BMP signaling. Cytokine Growth Factor Rev. 2009;20:399–407
  52. Yu PB, Deng DY, Beppu H, Hong CC, Lai C, Hoyng SA, et al. Bone morphogenetic protein (BMP) type II receptor is required for BMP-mediated growth arrest and differentiation in pulmonary artery smooth muscle cells. J Biol Chem. 2008;283:3877–3888
  53. Lebrin F, Mummery CL. Endoglin-mediated vascular remodeling: mechanisms underlying hereditary hemorrhagic telangiectasia. Trends Cardiovasc Med. 2008;18:25–32
  54. Shovlin CL. Hereditary haemorrhagic telangiectasia: pathophysiology, diagnosis and treatment. Blood Rev. 2010;24:203–219
  55. Lowery JW, de Caestecker MP. BMP signaling in vascular development and disease. Cytokine Growth Factor Rev. 2010;21:287–298
  56. Cunha SI, Pietras K. ALK1 as an emerging target for antiangiogenic therapy of cancer. Blood. 2011;117:6999–7006
  57. Singh A, Morris RJ. The Yin and Yang of bone morphogenetic proteins in cancer. Cytokine Growth Factor Rev. 2010;21:299–313
  58. van Wijk B, Moorman AF, van den Hoff MJ. Role of bone morphogenetic proteins in cardiac differentiation. Cardiovasc Res. 2007;74:244–255
  59. Boström KI, Rajamannan NM, Towler DA. The regulation of valvular and vascular sclerosis by osteogenic morphogens. Circ Res. 2011;109:564–577
  60. Singh R, Kispert A. Tbx20, Smads, and the atrioventricular canal. Trends Cardiovasc Med. 2010;20:109–114
  61. Colak D, Mori T, Brill MS, Pfeifer A, Falk S, Deng C, et al. Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J Neurosci. 2008;28:434–446
  62. Mira H, Andreu Z, Suh H, Lie DC, Jessberger S, Consiglio A, et al. Signaling through BMPR-IA regulates quiescence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell. 2010;7:78–89
  63. Sabo JK, Kilpatrick TJ, Cate HS. Effects of bone morphogenic proteins on neural precursor cells and regulation during central nervous system injury. Neurosignals. 2009;17:255–264
  64. Robel S, Berninger B, Götz M. The stem cell potential of glia: lessons from reactive gliosis. Nat Rev Neurosci. 2011;12:88–104
  65. Li H, He Y, Richardson WD, Casaccia P. Two-tier transcriptional control of oligodendrocyte differentiation. Curr Opin Neurobiol. 2009;19:479–485
  66. Emery B. Regulation of oligodendrocyte differentiation and myelination. Science. 2010;330:779–782
  67. Dummula K, Vinukonda G, Chu P, Xing Y, Hu F, Mailk S, et al. Bone morphogenetic protein inhibition promotes neurological recovery after intraventricular hemorrhage. J Neurosci. 2011;31:12068–12082
  68. Ono Y, Calhabeu F, Morgan JE, Katagiri T, Amthor H, Zammit PS. BMP signaling permits population expansion by preventing premature myogenic differentiation in muscle satellite cells. Cell Death Differ. 2011;18:222–234
  69. Daughters RS, Chen Y, Slack JM. Origin of muscle satellite cells in the Xenopus embryo. Development. 2011;138:821–830
  70. Friedrichs M, Wirsdöerfer F, Flohé SB, Schneider S, Wuelling M, Vortkamp A. BMP signaling balances proliferation and differentiation of muscle satellite cell descendants. BMC Cell Biol. 2011;12:26
  71. Pangas SA, Li X, Umans L, Zwijsen A, Huylebroeck D, Gutierrez C, et al. Conditional deletion of Smad1 and Smad5 in somatic cells of male and female gonads leads to metastatic tumor development in mice. Mol Cell Biol. 2008;28:248–257
  72. Middlebrook BS, Eldin K, Li X, Shivasankaran S, Pangas SA. Smad1-Smad5 ovarian conditional knockout mice develop a disease profile similar to the juvenile form of human granulosa cell tumors. Endocrinology. 2009;150:5208–5217
  73. Nasim MT, Ogo T, Ahmed M, Randall R, Chowdhury HM, Snape KM, et al. Molecular genetic characterization of SMAD signaling molecules in pulmonary arterial hypertension. Hum Mutat. 2011;[Epub ahead of print]
  74. Burton VJ, Ciuclan LI, Holmes AM, Rodman DM, Walker C, Budd DC. Bone morphogenetic protein receptor II regulates pulmonary artery endothelial cell barrier function. Blood. 2011;117:333–341
  75. Morrell NW. Role of bone morphogenetic protein receptors in the development of pulmonary arterial hypertension. Adv Exp Med Biol. 2010;661:251–264
  76. Dunn NR, Vincent SD, Oxburgh L, Robertson EJ, Bikoff EK. Combinatorial activities of Smad2 and Smad3 regulate mesoderm formation and patterning in the mouse embryo. Development. 2004;131:1717–1728
  77. Hellström M, Phng LK, Hofmann JJ, Wallgard E, Coultas L, Lindblom P, et al. Dll4 signaling through Notch1 regulates formation of tip cells during angiogenesis. Nature. 2007;445:776–780
  78. Orvis GD, Jamin SP, Kwan KM, Mishina Y, Kaartinen VM, Huang S, et al. Functional redundancy of TGF-beta family type I receptors and receptor-Smads in mediating anti-Mullerian hormone-induced Mullerian duct regression in the mouse. Biol Reprod. 2008;78:994–1001
  79. Orvis GD, Behringer RR. Cellular mechanisms of Müllerian duct formation in the mouse. Dev Biol. 2007;306:493–504
  80. Josso N, Belville C, di Clemente N, Picard JY. AMH and AMH receptor defects in persistent Müllerian duct syndrome. Hum Reprod Update. 2005;11:351–356
  81. Behringer RR, Finegold MJ, Cate RL. Mullerian-inhibiting substance function during mammalian sexual development. Cell. 1994;79:415–425
  82. Mishina Y, Whitworth DJ, Racine C, Behringer RR. High specificity of Mullerian-inhibiting substance signaling in vivo. Endocrinology. 1999;140:2084–2088
  83. Mishina Y, Rey R, Finegold MJ, Matzuk MM, Josso N, Cate RL, et al. Genetic analysis of the Mullerian-inhibiting substance signal transduction pathway in mammalian sexual differentiation. Genes Dev. 1996;10:2577–2587
  84. Jamin SP, Arango NA, Mishina Y, Hanks MC, Behringer RR. Requirement of Bmpr1a for Mullerian duct regression during male sexual development. Nat Genet. 2002;32:408–410
  85. Gaussin V, Van de Putte T, Mishina Y, Hanks MC, Zwijsen A, Huylebroeck D, et al. Endocardial cushion and myocardial defects after cardiac myocyte-specific conditional deletion of the bone morphogenetic protein receptor ALK3. Proc Natl Acad Sci USA. 2002;99:2878–2883
  86. Schneider MD, Gaussin V, Lyons KM. Tempting fate: BMP signals for cardiac morphogenesis. Cytokine Growth Factor Rev. 2003;14:1–4
  87. Collart C, Remacle JE, Barabino S, van Grunsven LA, Nelles L, Schellens A, et al. Smicl is a novel Smad interacting protein and cleavage and polyadenylation specificity factor associated protein. Genes Cells. 2005;10:897–906
  88. Millevoi S, Vagner S. Molecular mechanisms of eukaryotic pre-mRNA 3′ end processing regulation. Nucleic Acids Res. 2010;38:2757–2774
  89. Collart C, Verschueren K, Rana A, Smith JC, Huylebroeck D. The novel Smad-interacting protein Smicl regulates Chordin expression in the Xenopus embryo. Development. 2005;132:4575–4586
  90. Collart C, Ramis JM, Down TA, Smith JC. Smicl is required for phosphorylation of RNA polymerase II and affects 3′-end processing of RNA at the midblastula transition in Xenopus. Development. 2009;136:3451–3461
  91. Pype S, Declercq W, Ibrahimi A, Michiels C, Van Rietschoten JG, Dewulf N, et al. TTRAP, a novel protein that associates with CD40, tumor necrosis factor (TNF) receptor-75 and TNF receptor-associated factors (TRAFs), and that inhibits nuclear factor-kappa B activation. J Biol Chem. 2000;275:18586–18593
  92. Esguerra CV, Nelles L, Vermeire L, Ibrahimi A, Crawford AD, Derua R, et al. Ttrap is an essential modulator of Smad3-dependent Nodal signaling during zebrafish gastrulation and left–right axis determination. Development. 2007;134:4381–4393
  93. Hofmann K, Tomiuk S, Wolff G, Stoffel W. Cloning and characterization of the mammalian brain-specific, Mg2+-dependent neutral sphingomyelinase. Proc Natl Acad Sci USA. 2000;97:5895–5900
  94. Rodrigues-Lima F, Josephs M, Katan M, Cassinat B. Sequence analysis identifies TTRAP, a protein that associates with CD40 and TNF receptor-associated factors, as a member of a superfamily of divalent cation-dependent phosphodiesterases. Biochem Biophys Res Commun. 2001;285:1274–1279
  95. Pei H, Yordy JS, Leng Q, Zhao Q, Watson DK, Li R. EAPII interacts with ETS1 and modulates its transcriptional function. Oncogene. 2003;22:2699–2709
  96. Hecker CM, Rabiller M, Haglund K, Bayer P, Dikic I. Specification of SUMO1- and SUMO2-interacting motifs. J Biol Chem. 2006;281:16117–16127
  97. Zhang JQ, Wang JJ, Li WJ, Huang L, Tian L, Xue JL, et al. Cellular protein TTRAP interacts with HIV-1 integrase to facilitate viral integration. Biochem Biophys Res Commun. 2009;387:256–260
  98. Zucchelli S, Vilotti S, Calligaris R, Lavina ZS, Biagioli M, Foti R, et al. Aggresome-forming TTRAP mediates pro-apoptotic properties of Parkinson's disease-associated DJ-1 missense mutations. Cell Death Differ. 2009;16:428–438
  99. Xu GL, Pan YK, Wang BY, Huang L, Tian L, Xue JL, et al. TTRAP is a novel PML nuclear bodies-associated protein. Biochem Biophys Res Commun. 2008;375:395–398
  100. Cortes Ledesma F, El Khamisy SF, Zuma MC, Osborn K, Caldecott KW. A human 5′-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage. Nature. 2009;461:674–678
  101. Zeng Z, Cortés-Ledesma F, El Khamisy SF, Caldecott KW. TDP2/TTRAP is the major 5′-tyrosyl DNA phosphodiesterase activity in vertebrate cells and is critical for cellular resistance to topoisomerase II-induced DNA damage. J Biol Chem. 2011;286:403–409
  102. El-Khamisy SF, Saifi GM, Weinfeld M, Johansson F, Helleday T, Lupski JR, et al. Defective DNA single-strand break repair in spinocerebellar ataxia with axonal neuropathy-1. Nature. 2005;434:108–113
  103. Hirano R, Interthal H, Huang C, Nakamura T, Deguchi K, Choi K, et al. Spinocerebellar ataxia with axonal neuropathy: consequence of a Tdp1 recessive neomorphic mutation?. EMBO J. 2007;26:4732–4743
  104. Verschueren K, Remacle JE, Collart C, Kraft H, Baker BS, Tylzanowski P, et al. SIP1, a novel zinc finger/homeodomain repressor, interacts with Smad proteins and binds to 5′-CACCT sequences in candidate target genes. J Biol Chem. 1999;274:20489–20498
  105. Remacle JE, Kraft H, Lerchner W, Wuytens G, Collart C, Verschueren K, et al. New mode of DNA binding of multi-zinc finger transcription factors: deltaEF1 family members bind with two hands to two target sites. EMBO J. 1999;18:5073–5084
  106. van Grunsven LA, Taelman V, Michiels C, Verstappen G, Souopgui J, Nichane M, et al. XSip1 neuralizing activity involves the co-repressor CtBP and occurs through BMP dependent and independent mechanisms. Dev Biol. 2007;306:34–49
  107. Verstappen G, van Grunsven LA, Michiels C, Van de Putte T, Souopgui J, Van Damme J, et al. Atypical Mowat–Wilson patient confirms the importance of the novel association between ZFHX1B/SIP1 and NuRD corepressor complex. Hum Mol Genet. 2008;17:1175–1183
  108. van Grunsven LA, Taelman V, Michiels C, Opdecamp K, Huylebroeck D, Bellefroid EJ. deltaEF1 and SIP1 are differentially expressed and have overlapping activities during Xenopus embryogenesis. Dev Dyn. 2006;235:1491–1500
  109. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF, et al. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial–mesenchymal transition. Cancer Res. 2008;68:7846–7854
  110. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 2008;22:894–907Erratum in: Genes Dev 2009;23:1378
  111. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 2008;10:593–601
  112. Christoffersen NR, Silahtaroglu A, Orom UA, Kauppinen S. Lund AH. miR-200b mediates post-transcriptional repression of ZFHX1B. RNA. 2007;13:1172–1178
  113. Wakamatsu N, Yamada Y, Yamada K, Ono T, Nomura N, Taniguchi H, et al. Mutations in SIP1, encoding Smad interacting protein-1, cause a form of Hirschsprung disease. Nat Genet. 2001;27:369–370
  114. Cacheux V, Dastot-Le Moal F, Kääriäinen H, Bondurand N, Rintala R, Boissier B, et al. Loss-of-function mutations in SIP1 Smad interacting protein 1 result in a syndromic Hirschsprung disease. Hum Mol Genet. 2001;10:1503–1510
  115. Zweier C, Thiel CT, Dufke A, Crow YJ, Meinecke P, Suri M, et al. Clinical and mutational spectrum of Mowat–Wilson syndrome. Eur J Med Genet. 2005;48:97–111
  116. Dastot-Le Moal F, Wilson M, Mowat D, Collot N, Niel F, Goossens M. ZFHX1B mutations in patients with Mowat–Wilson syndrome. Hum Mutat. 2007;28:313–321
  117. Garavelli L, Zollino M, Mainardi PC, Gurrieri F, Rivieri F, Soli F, et al. Mowat–Wilson syndrome: facial phenotype changing with age: study of 19 Italian patients and review of the literature. Am J Med Genet A. 2009;149A:417–426
  118. Saunders CJ, Zhao W, Ardinger HH. Comprehensive ZEB2 gene analysis for Mowat–Wilson syndrome in a North American cohort: a suggested approach to molecular diagnostics. Am J Med Genet A. 2009;149A:2527–2531
  119. Adam MP, Schelley S, Gallagher R, Brady AN, Barr K, Blumberg B, et al. Clinical features and management issues in Mowat–Wilson syndrome. Am J Med Genet A. 2006;140:2730–2741
  120. Van de Putte T, Maruhashi M, Francis A, Nelles L, Kondoh H, Huylebroeck D, et al. Mice lacking ZFHX1B, the gene that codes for Smad-interacting protein-1, reveal a role for multiple neural crest cell defects in the etiology of Hirschsprung disease-mental retardation syndrome. Am J Hum Genet. 2003;72:465–470
  121. Van de Putte T, Francis A, Nelles L, van Grunsven LA, Huylebroeck D. Neural crest-specific removal of Zfhx1b in mouse leads to a wide range of neurocristopathies reminiscent of Mowat–Wilson syndrome. Hum Mol Genet. 2007;16:1423–1436
  122. Maruhashi M, Van De Putte T, Huylebroeck D, Kondoh H, Higashi Y. Involvement of SIP1 in positioning of somite boundaries in the mouse embryo. Dev Dyn. 2005;234:332–338
  123. Jeub M, Emrich M, Pradier B, Taha O, Gailus-Durner V, Fuchs H, et al. The transcription factor Smad-interacting protein 1 controls pain sensitivity via modulation of DRG neuron excitability. Pain. 2011;152:2384–2398
  124. Seuntjens E, Nityanandam A, Miquelajauregui A, Debruyn J, Stryjewska A, Goebbels S, et al. Sip1 regulates sequential fate decisions by feedback signaling from postmitotic neurons to progenitors. Nat Neurosci. 2009;12:1373–1380
  125. Chng Z, Teo A, Pedersen RA, Vallier L. SIP1 mediates cell-fate decisions between neuroectoderm and mesendoderm in human pluripotent stem cells. Cell Stem Cell. 2010;6:59–70
  126. Goossens S, Janzen V, Bartunkova S, Yokomizo T, Drogat B, Crisan M, et al. The EMT regulator Zeb2/Sip1 is essential for murine embryonic haematopoietic stem/progenitor cell differentiation and mobilization. Blood. 2011;117:5620–5630
  127. Huang S, Tang B, Usoskin D, Lechleider RJ, Jamin SP, Li C, et al. Conditional knockout of the Smad1 gene. Genesis. 2002;32(2 (February)):76–79
  128. Umans L, Vermeire L, Francis A, Chang H, Huylebroeck D, Zwijsen A. Generation of a floxed allele of Smad5 for cre-mediated conditional knockout in the mouse. Genesis. 2003;37(1 (September)):5–11
  129. Hester M, Thompson JC, Mills J, Liu Y, El-Hodiri HM, Weinstein M. Smad1 and Smad8 function similarly in mammalian central nervous system development. Mol Cell Biol. 2005;25(11 (June)):4683–4692
  130. Huang J, Dattilo LK, Rajagopal R, Liu Y, Kaartinen V, Mishina Y, et al. FGF-regulated BMP signaling is required for eyelid closure and to specify conjunctival epithelial cell fate. Development. 2009;136:1741–1750
  131. Yang SM, Guo WW, Hu YY, Sun YX, Hou ZH, Sun JH, et al. Smad5 haploinsufficiency leads to hair cell and hearing loss. Dermatol Nurs. 2009;69:153–161
  132. Allaire JM, Darsigny M, Marcoux SS, Roy SA, Schmouth JF, Umans L, et al. Loss of Smad5 leads to the disassembly of the apical junctional complex and increased susceptibility to experimental colitis. Am J Physiol Gastrointest Liver Physiol. 2011;300:G586–G597
  133. Singbrant S, Karlsson G, Ehinger M, Olsson K, Jaako P, Miharada K, et al. Canonical BMP signaling is dispensable for haematopoietic stem cell function in both adult and fetal liver haematopoiesis, but essential to preserve colon architecture. Blood. 2010;115:4689–4698
  134. Rajagopal R, Dattilo LK, Kaartinen V, Deng CX, Umans L, Zwijsen A, et al. Functions of the type 1 BMP receptor Acvr1 (Alk2) in lens development: cell proliferation, terminal differentiation, and survival. Invest Ophthalmol Vis Sci. 2008;49:4953–4960
  135. Rajagopal R, Huang J, Dattilo LK, Kaartinen V, Mishina Y, Deng CX, et al. The type I BMP receptors Bmpr1a and Acvr1, activate multiple signaling pathways to regulate lens formation. Dev Biol. 2009;335:305–316
  136. Singbrant S, Moody JL, Blank U, Karlsson G, Umans L, Zwijsen A, et al. Smad5 is dispensable for adult murine haematopoiesis. Blood. 2006;108:3707–3712
  137. Xu B, Chen C, Chen H, Zheng SG, Bringas P, Xu M, et al. Smad1 and its target gene Wif1 coordinate BMP and Wnt signaling activities to regulate fetal lung development. Development. 2011;138:925–935
  138. Retting KN, Song B, Yoon BS, Lyons KM. BMP canonical Smad signaling through Smad1 and Smad5 is required for endochondral bone formation. Development. 2009;136:1093–1104
  139. Wang M, Jin H, Tang D, Huang S, Zuscik MJ, Chen D. Smad1 plays an essential role in bone development and postnatal bone formation. Osteoarthritis Cartilage. 2011;19:751–762
  140. Higashi Y, Maruhashi M, Nelles L, Van de Putte T, Verschueren K, Miyoshi T, et al. Generation of the floxed allele of the SIP1 (Smad-interacting protein 1) gene for Cre-mediated conditional knockout in the mouse. Genesis. 2002;32:82–84
  141. Stanchina L, Van de Putte T, Goossens M, Huylebroeck D, Bondurand N. Genetic interaction between Sox10 and Zfhx1b during enteric nervous system development. Dev Biol. 2010;341:416–428
  142. Miyoshi T, Maruhashi M, Van De Putte T, Kondoh H, Huylebroeck D, Higashi Y. Complementary expression pattern of Zfhx1 genes Sip1 and deltaEF1 in the mouse embryo and their genetic interaction revealed by compound mutants. Dev Dyn. 2006;235:1941–1952
  143. Yoshimoto A, Saigou Y, Higashi Y, Kondoh H. Regulation of ocular lens development by Smad-interacting protein 1 involving Foxe3 activation. Development. 2005;132:4437–4448
  144. Miquelajauregui A, Van de Putte T, Polyakov A, Nityanandam A, Boppana S, Seuntjens E, et al. Smad-interacting protein-1 (Zfhx1b) acts upstream of Wnt signaling in the mouse hippocampus and controls its formation. Proc Natl Acad Sci USA. 2007;104:12919–12924
  145. Phng LK, Gerhardt H. Angiogenesis: a team effort coordinated by Notch. Dev Cell. 2009;16:196–208
  146. Ryan K, Calvo O, Manley JL. Evidence that polyadenylation factor CPSF-73 is the mRNA 3′ processing endonuclease. RNA. 2004;10:565–573
  147. Tomecki R, Dziembowski A. Novel endoribonucleases as central players in various pathways of eukaryotic RNA metabolism. RNA. 2010;16:1692–1724
  148. Long J, Zuo D, Park M. Pc2-mediated sumoylation of Smad-interacting protein 1 attenuates transcriptional repression of E-cadherin. J Biol Chem. 2005;280:35477–35489
  149. van Grunsven LA, Michiels C, Van de Putte T, Nelles L, Wuytens G, Verschueren K, et al. Interaction between Smad-interacting protein-1 and the corepressor C-terminal binding protein is dispensable for transcriptional repression of E-cadherin. J Biol Chem. 2003;278:26135–26145
  150. Comijn J, Berx G, Vermassen P, Verschueren K, van Grunsven L, Bruyneel E, et al. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell. 2001;7:1267–1278
  151. Postigo AA, Depp JL, Taylor JJ, Kroll KL. Regulation of Smad signaling through a differential recruitment of coactivators and corepressors by ZEB proteins. EMBO J. 2003;22:2453–2462

PII: S1359-6101(11)00059-1

doi: 10.1016/j.cytogfr.2011.11.006

Cytokine & Growth Factor Reviews
Volume 22, Issue 5 , Pages 287-300 , October 2011