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Yasuhiro Ishidou

Kagoshima University

Publishes on Orthopaedic implants and arthroplasty, Sarcoma Diagnosis and Treatment, Hip disorders and treatments. 108 papers and 2.8k citations.

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Interaction and Functional Cooperation of PEBP2/CBF with Smads
J Hanai, Lin Feng Chen, Tomohiko Kanno et al.|Journal of Biological Chemistry|1999
Cited by 449Open Access

Smads are signal transducers for members of the transforming growth factor-β (TGF-β) superfamily. Upon ligand stimulation, receptor-regulated Smads (R-Smads) are phosphorylated by serine/threonine kinase receptors, form complexes with common-partner Smad, and translocate into the nucleus, where they regulate the transcription of target genes together with other transcription factors. Polyomavirus enhancer binding protein 2/core binding factor (PEBP2/CBF) is a transcription factor complex composed of α and β subunits. The α subunits of PEBP2/CBF, which contain the highly conserved Runt domain, play essential roles in hematopoiesis and osteogenesis. Here we show that three mammalian α subunits of PEBP2/CBF form complexes with R-Smads that act in TGF-β/activin pathways as well as those acting in bone morphogenetic protein (BMP) pathways. Among them, PEBP2αC/CBFA3/AML2 forms a complex with Smad3 and stimulates transcription of the germline Ig Cα promoter in a cooperative manner, for which binding of both factors to their specific binding sites is essential. PEBP2 may thus be a nuclear target of TGF-β/BMP signaling. Smads are signal transducers for members of the transforming growth factor-β (TGF-β) superfamily. Upon ligand stimulation, receptor-regulated Smads (R-Smads) are phosphorylated by serine/threonine kinase receptors, form complexes with common-partner Smad, and translocate into the nucleus, where they regulate the transcription of target genes together with other transcription factors. Polyomavirus enhancer binding protein 2/core binding factor (PEBP2/CBF) is a transcription factor complex composed of α and β subunits. The α subunits of PEBP2/CBF, which contain the highly conserved Runt domain, play essential roles in hematopoiesis and osteogenesis. Here we show that three mammalian α subunits of PEBP2/CBF form complexes with R-Smads that act in TGF-β/activin pathways as well as those acting in bone morphogenetic protein (BMP) pathways. Among them, PEBP2αC/CBFA3/AML2 forms a complex with Smad3 and stimulates transcription of the germline Ig Cα promoter in a cooperative manner, for which binding of both factors to their specific binding sites is essential. PEBP2 may thus be a nuclear target of TGF-β/BMP signaling. transforming growth factor-β bone morphogenetic protein receptor-regulated Smad common-partner Smad polyomavirus enhancer binding protein 2 core binding factor immunoglobulin Cα TGF-β type I receptor BMP type IB receptor wild-type TGF-β-responsive element glutathione S-transferase Mad homology electrophoretic mobility shift assay activation domain Smad proteins are signal transducers for members of the transforming growth factor-β (TGF-β)1 superfamily, which includes TGF-βs, activins, and bone morphogenetic proteins (BMPs) (1Heldin C.-H. Miyazono K. ten Dijke P. Nature. 1997; 390: 465-471Crossref PubMed Scopus (3358) Google Scholar,2Massagué J. Annu. Rev. Biochem. 1998; 67: 753-791Crossref PubMed Scopus (3999) Google Scholar). Smads are classified into three subgroups, i.e.receptor-regulated Smads (R-Smads), common-partner Smads (Co-Smads), and inhibitory Smads. Smad2 and Smad3 are R-Smads that transmit TGF-β/activin signals, whereas Smad1, Smad5, and Smad8 act as R-Smads mediating BMP signals. Smad4 is the only Co-Smad identified in mammals. Upon ligand stimulation, R-Smads are phosphorylated by the serine/threonine kinase receptors, form complexes with Co-Smad, and translocate into the nucleus, where they cooperatively regulate the transcription of target genes with other transcription factors, including Xenopus FAST1 and its mammalian homologues (3Chen X. Rubock M.J. Whitman M. Nature. 1996; 383: 691-696Crossref PubMed Scopus (634) Google Scholar, 4Labbé E. Silvestri C. Hoodless P.A. Wrana J.L. Attisano L. Mol. Cell. 1998; 2: 109-120Abstract Full Text Full Text PDF PubMed Scopus (464) Google Scholar, 5Zhou S. Zawel L. Lengauer C. Kinzler K.W. Vogelstein B. Mol. Cell. 1998; 2: 121-127Abstract Full Text Full Text PDF PubMed Scopus (212) Google Scholar) and also the c-Jun/c-Fos complex (6Zhang Y. Feng X.-H. Derynck R. Nature. 1998; 394: 909-913Crossref PubMed Scopus (688) Google Scholar, 7Liberati N.T. Datto M.B. Frederick J.P. Shen X. Wong C. Rougier-Chapman E.M. Wang X.-F. Proc. Natl. Acad. Sci. U. S. A. 1999; 96: 4844-4849Crossref PubMed Scopus (275) Google Scholar). TGF-β is a potent growth inhibitor for most cell types, including hematopoietic cells and lymphocytes. In addition, TGF-β directs class switching to IgA in splenic B cells (8Coffman R.L. Lebman D.A. Shrader B. J. Exp. Med. 1989; 170: 1039-1044Crossref PubMed Scopus (483) Google Scholar, 9Sonoda E. Matsumoto R. Hitoshi Y. Ishii T. Sugimoto M. Araki S. Tominaga A. Yamaguchi N. Takatsu K. J. Exp. Med. 1989; 170: 1415-1420Crossref PubMed Scopus (348) Google Scholar). BMPs play important roles in early embryogenesis and in the induction of bone formation in vivo(10Hogan B.L. Genes & Dev. 1996; 10: 1580-1594Crossref PubMed Scopus (1725) Google Scholar). It is thus important to identify and classify transcription factors that serve as nuclear targets of TGF-β/BMP signals and regulate these biological events. Polyomavirus enhancer binding protein 2/core binding factor (PEBP2/CBF) is a transcription factor complex composed of α and β subunits (11Ito Y. Bae S.-C. Yaniv M. Ghysdael J. Oncogenes as Transcriptional Regulators. Birkäuser Verlag, Basel1997: 107-132Crossref Google Scholar,12Speck N.A. Stacy T. Crit. Rev. Eukaryotic Gene Expression. 1995; 5: 337-364Crossref PubMed Scopus (150) Google Scholar). Three mammalian α subunits have been identified, termed PEBP2αA/CBFA1/AML3 (referred to as αA in this report), PEBP2αB/CBFA2/AML1 (αB), and PEBP2αC/CBFA3/AML2 (αC), whereas only a single β subunit (PEBP2β/CBFB) with several spliced variants is present in mammals. The α subunits of PEBP2, which contain the highly conserved Runt domain, are responsible for binding to DNA and transcription activity. In contrast, the β subunit does not bind to DNA by itself, but it enhances the DNA binding activity of the α subunits by interacting via the Runt domain. PEBP2/CBF plays critical roles in growth and differentiation of cells in certain specific tissues, i.e. αA in bone formation (13Ducy P. Zhang R. Geoffroy V. Ridall A.L. Karsenty G. Cell. 1997; 89: 747-754Abstract Full Text Full Text PDF PubMed Scopus (3668) Google Scholar, 14Komori T. Yagi H. Nomura S. Yamaguchi A. Sasaki K. Deguchi K. Shimizu Y. Bronson R.T. Gao Y.H. Inada M. Sato M. Okamoto R. Kitamura Y. Yoshiki S. Kishimoto T. Cell. 1997; 89: 755-764Abstract Full Text Full Text PDF PubMed Scopus (3678) Google Scholar, 15Otto F. Thornell A.P. Crompton T. Denzel A. Gilmour K.C. Rosewell I.R. Stamp G.W. Beddington R.S. Mundlos S. Olsen B.R. Selby P.B. Owen M.J. Cell. 1997; 89: 765-771Abstract Full Text Full Text PDF PubMed Scopus (2430) Google Scholar) and αB in definitive hematopoiesis (16Okuda T. van Deursen J. Hiebert S.W. Grosveld G. Downing J.R. Cell. 1996; 84: 321-330Abstract Full Text Full Text PDF PubMed Scopus (1613) Google Scholar, 17Wang Q. Stacy T. Binder M. Marin-Padilla M. Sharpe A.H. Speck N.A. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 3444-3449Crossref PubMed Scopus (1036) Google Scholar); αC appears to be important in class switching to IgA because of its ability to activate the germline Ig Cα promoter (18Shi M.J. Stavnezer J. J. Immunol. 1998; 161: 6751-6760PubMed Google Scholar). Abnormalities of the PEBP2 genes are linked to human diseases. Mutations in one allele of the humanPEBP2αA/CBFA1 gene cause human cleidocranial dysplasia syndrome (19Mundlos S. Otto F. Mundlos C. Mulliken J.B. Aylsworth A.S. Albright S. Lindhout D. Cole W.G. Henn W. Knoll J.H. Owen M.J. Mertelsmann R. Zabel B.U. Olsen B.R. Cell. 1997; 89: 773-779Abstract Full Text Full Text PDF PubMed Scopus (1285) Google Scholar, 20Zhang Y.W. Bae S.C. Takahashi E. Ito Y. Oncogene. 1997; 15: 367-371Crossref PubMed Scopus (30) Google Scholar), whereas PEBP2αB/AML1 gene is frequently disrupted by chromosomal translocations in several types of human leukemia (11Ito Y. Bae S.-C. Yaniv M. Ghysdael J. Oncogenes as Transcriptional Regulators. Birkäuser Verlag, Basel1997: 107-132Crossref Google Scholar, 12Speck N.A. Stacy T. Crit. Rev. Eukaryotic Gene Expression. 1995; 5: 337-364Crossref PubMed Scopus (150) Google Scholar). PEBP2 has been shown to interact with several transcription factors and co-activators and support context-dependent transcription of target genes (21Wotton D. Ghysdael J. Wang S. Speck N.A. Owen M.J. Mol. Cell. Biol. 1994; 14: 840-850Crossref PubMed Scopus (199) Google Scholar, 22Kim W.-Y. Sieweke M. Ogawa E. Wee H.-J. Englmeier U. Graf T. Ito Y. EMBO J. 1999; 18: 1609-1620Crossref PubMed Scopus (197) Google Scholar, 23Yagi R. Chen L.-F. Shigesada K. Murakami Y. Ito Y. EMBO J. 1999; 18: 2551-2562Crossref PubMed Scopus (453) Google Scholar). Because BMPs and αA play critical roles in bone formation, and TGF-β and αC in transcription of germline Ig α transcripts required for IgA class switching, we examined the functional cooperation between the PEBP2α subunits and Smads. Our findings suggest that PEBP2α subunits and R-Smads cooperate to synergistically activate transcription in both the TGF-β and BMP signaling pathways, thereby regulating the function of cells in specific tissues upon activation by TGF-β-like factors. FLAG-pcDEF3 and 6Myc-pcDEF3 containing six tandem copies of the Myc-epitope tag were previously described (24Imamura T. Takase M. Nishihara A. Oeda E. Hanai J.-i. Kawabata M. Miyazono K. Nature. 1997; 389: 622-626Crossref PubMed Scopus (873) Google Scholar,25Kawabata M. Inoue H. Hanyu A. Imamura T. Miyazono K. EMBO J. 1998; 17: 4056-4065Crossref PubMed Scopus (249) Google Scholar). The constructions of constitutively active forms of TGF-β type I receptor (TβR-I(TD)) and BMP-type IB receptor (BMPR-IB(QD)), TβR-II, wild-type (WT) Smads, and Smad3(DE) were reported (24Imamura T. Takase M. Nishihara A. Oeda E. Hanai J.-i. Kawabata M. Miyazono K. Nature. 1997; 389: 622-626Crossref PubMed Scopus (873) Google Scholar, 25Kawabata M. Inoue H. Hanyu A. Imamura T. Miyazono K. EMBO J. 1998; 17: 4056-4065Crossref PubMed Scopus (249) Google Scholar, 26Goto D. Yagi K. Inoue H. Iwamoto I. Kawabata M. Miyazono K. Kato M. FEBS Lett. 1998; 430: 201-204Crossref PubMed Scopus (58) Google Scholar). The constructions of αA, αB, αC, and β2 have been described elsewhere (27Kanno T. Kanno Y. Chen L.F. Ogawa E. Kim W.Y. Ito Y. Mol. Cell. Biol. 1998; 18: 2444-2454Crossref PubMed Google Scholar, 28Bae S.-C. Takahashi E. Zhang Y.W. Ogawa E. Shigesada K. Namba Y. Satake M. Ito Y. Gene ( Amst. ). 1995; 159: 245-248Crossref PubMed Scopus (152) Google Scholar, 29Ogawa E. Maruyama M. Kagoshima H. Inuzuka M. Lu J. Satake M. Shigesada K. Ito Y. Proc. Natl. Acad. Sci. U. S. A. 1993; 90: 6859-6863Crossref PubMed Scopus (563) Google Scholar). 2Y.-W. Zhang and Y. Ito, unpublished data. Deletion constructs of αC were prepared by a polymerase chain reaction-based approach. For construction of the isolated Ig Cα/TGF-β-responsive element (TβRE) promoter reporter construct ((TβRE)3-Lux) and its mutants, three tandemly repeated TβREs (WT or mutant versions) of the Ig Cα promoter were fused to the heterologous c-Fos (30Gilman M.Z. Wilson R.N. Weinberg R.A. Mol. Cell. Biol. 1986; 6: 4305-4316Crossref PubMed Scopus (301) Google Scholar) and luciferase reporters. All of the polymerase chain reaction products were sequenced. COS7 cells were cultured in Dulbecco's modified Eagle's medium with 10% fetal bovine serum and antibiotics. A20.3 B lymphoma cells (18Shi M.J. Stavnezer J. J. Immunol. 1998; 161: 6751-6760PubMed Google Scholar, 31Xu M.Z. Stavnezer J. EMBO J. 1992; 11: 145-155Crossref PubMed Scopus (93) Google Scholar) were cultured in RPMI 1640 with 10% fetal bovine serum, 50 μm2-mercaptoethanol, 0.1 mm nonessential amino acids, 1 mm sodium pyruvate, 2 mml-glutamine, and antibiotics. P19 murine embryonal carcinoma cells were cultured in a 1:1 mixture of Dulbecco's modified Eagle's medium and Ham's F-12 supplemented with 10% fetal bovine serum and antibiotics (32Ogawa E. Inuzuka M. Maruyama M. Satake M. Naito-Fujimoto M. Ito Y. Shigesada K. Virology. 1993; 194: 314-331Crossref PubMed Scopus (443) Google Scholar, 33Bae S.-C. Ogawa E. Maruyama M. Oka H. Satake M. Shigesada K. Jenkins N.A. Gilbert D.J. Copeland N.G. Ito Y. Mol. Cell. Biol. 1994; 14: 3242-3252Crossref PubMed Google Scholar). For transient transfection, cells were transfected using FuGENE6 (Roche Molecular Biochemicals). COS7 cells were transiently transfected with expression constructs for PEBP2α subunits, Smads and constitutively active forms of type I receptors. Cells were then washed, scraped, and solubilized (25Kawabata M. Inoue H. Hanyu A. Imamura T. Miyazono K. EMBO J. 1998; 17: 4056-4065Crossref PubMed Scopus (249) Google Scholar). Immunoprecipitation and immunoblotting using an enhanced chemiluminescence detection system (Amersham Pharmacia Biotech) were performed as described (25Kawabata M. Inoue H. Hanyu A. Imamura T. Miyazono K. EMBO J. 1998; 17: 4056-4065Crossref PubMed Scopus (249) Google Scholar). A GST pull-down assay was performed as described previously (22Kim W.-Y. Sieweke M. Ogawa E. Wee H.-J. Englmeier U. Graf T. Ito Y. EMBO J. 1999; 18: 1609-1620Crossref PubMed Scopus (197) Google Scholar). GST-fusion proteins containing the full-length Smad3 or the Mad homology (MH)1 or MH2 domain of Smad3 were expressed and purified as described (32Ogawa E. Inuzuka M. Maruyama M. Satake M. Naito-Fujimoto M. Ito Y. Shigesada K. Virology. 1993; 194: 314-331Crossref PubMed Scopus (443) Google Scholar).In vitro transcription and translation of C-terminal deletion constructs of αC were done using the TNT system (Promega) in the presence of [35S]methionine. GST-Smad3 (full-length), Smad3 (MH1), Smad3 (MH2), or GST bound to glutathione-Sepharose was mixed with αC proteins in 500 μl of Tris-buffered saline, pH 7.4, containing 0.5% Nonidet P-40 for 1 h and washed vigorously three times with 1 ml of the in the they were by by A20.3 B were transfected with the germline Ig Cα promoter (18Shi M.J. Stavnezer J. J. Immunol. 1998; 161: 6751-6760PubMed Google Scholar) together with the expression constructs for αC, Smads, and P19 murine embryonal carcinoma cells were transfected with or mutant of together with αC, Smads, and and luciferase were with the luciferase assay system (Promega) using luciferase activity was with to the luciferase activity. was performed as described (27Kanno T. Kanno Y. Chen L.F. Ogawa E. Kim W.Y. Ito Y. Mol. Cell. Biol. 1998; 18: 2444-2454Crossref PubMed Google Scholar) with COS7 cells were transfected with a mixture of expression TβR-II, Smads, αC, and were mixed in vitro in as and for with a complex formation between αA and R-Smads by αA with and Smad5, which were a constitutively active form of Smad4 was with R-Smads by the receptors. αA also with Smad2 and Smad3 by an active examined the other PEBP2α subunits with Smad3 by complexes not only with αA but also with αB and αC 1 by also complexes with αA, αB, and i.e. Smad2 by and by also with three α subunits not αB and αC complexes with and Smad3 whereas αA with and with Smad3 A that three mammalian PEBP2α subunits form complexes with Because αC is by TGF-β in B and is critical for the induction of the promoter for germline Ig Cα transcripts upon TGF-β (18Shi M.J. Stavnezer J. J. Immunol. 1998; 161: 6751-6760PubMed Google Scholar), complex formation between αC and Smad3 was in The complex was in the presence and of and Smad4 with Smad3 upon by The of between αC and Smad3 was by GST pull-down using deletion constructs of these a of constructs of αC was deletion of a C-terminal 2 to a of the activation domain identified in αB (27Kanno T. Kanno Y. Chen L.F. Ogawa E. Kim W.Y. Ito Y. Mol. Cell. Biol. 1998; 18: 2444-2454Crossref PubMed Google Scholar) in a of with and by deletion of Smads have highly conserved and MH2 in their and C-terminal (1Heldin C.-H. Miyazono K. ten Dijke P. Nature. 1997; 390: 465-471Crossref PubMed Scopus (3358) Google Scholar, J. Annu. Rev. Biochem. 1998; 67: 753-791Crossref PubMed Scopus (3999) Google Scholar). A GST pull-down assay that the MH2 domain bound to αC 2 In addition, the domain with αC, but the in αC where not be because of the of the the functional of using the Ig Cα The promoter for germline Ig Cα transcripts has been shown to contain a TGF-β-responsive Stavnezer J. J. Immunol. 1992; Google Scholar), in which PEBP2α binding sites have been identified (18Shi M.J. Stavnezer J. J. Immunol. 1998; 161: 6751-6760PubMed Google Scholar). The human germline Ig Cα promoter was also shown to contain PEBP2α binding sites in its E. M. P. T. J. Immunol. 1999; PubMed Scopus Google Scholar). In addition, Smad binding L. J.L. P. S. Kinzler K.W. Vogelstein B. Mol. Cell. 1998; Full Text Full Text PDF PubMed Scopus Google Scholar, S. S. D. ten Dijke P. S. EMBO J. 1998; 17: PubMed Scopus Google Scholar, S. C.-H. ten Dijke P. W. J. Biol. 1998; Full Text Full Text PDF PubMed Scopus Google Scholar) are in the an PEBP2α binding and one Smad binding are between the and the transcription the functional of these binding were into the and a assay was performed using A20.3 B lymphocytes. previously reported (18Shi M.J. Stavnezer J. J. Immunol. 1998; 161: 6751-6760PubMed Google Scholar), TGF-β the which is enhanced by the presence of Mutations in the Smad binding in the and those in the PEBP2α binding sites in in activity A of was in the mutant with in PEBP2α and Smad binding that both of these binding are essential for A form of which the activation of both Smad2 and Smad3 by D. Yagi K. Inoue H. Iwamoto I. Kawabata M. Miyazono K. Kato M. FEBS Lett. 1998; 430: 201-204Crossref PubMed Scopus (58) Google Scholar), the transcription by and αC that transcription may be by the R-Smads by of Smad3 with αC transcription the Ig Cα promoter but not the Ig Cα promoter containing in the as shown in not Smad2 not the because Smad2 is to bind to the Smad binding L. J.L. P. S. Kinzler K.W. Vogelstein B. Mol. Cell. 1998; Full Text Full Text PDF PubMed Scopus Google Scholar, S. S. D. ten Dijke P. S. EMBO J. 1998; 17: PubMed Scopus Google Scholar, S. C.-H. ten Dijke P. W. J. Biol. 1998; Full Text Full Text PDF PubMed Scopus Google Scholar, K. D. T. S. Kato M. Miyazono K. J. Biol. 1999; Full Text Full Text PDF PubMed Scopus Google Scholar). the roles of αC and in three tandemly repeated TβREs (WT or mutant versions) of the Ig Cα promoter were fused to the heterologous c-Fos and activity was using transfected P19 embryonal carcinoma which have of PEBP2α activity (32Ogawa E. Inuzuka M. Maruyama M. Satake M. Naito-Fujimoto M. Ito Y. Shigesada K. Virology. 1993; 194: 314-331Crossref PubMed Scopus (443) Google Scholar, 33Bae S.-C. Ogawa E. Maruyama M. Oka H. Satake M. Shigesada K. Jenkins N.A. Gilbert D.J. Copeland N.G. Ito Y. Mol. Cell. Biol. 1994; 14: 3242-3252Crossref PubMed Google Scholar). to the with the Ig Cα promoter using A20.3 B activity of was by Smad3 and whereas the of and αC in cells by transcription In contrast, mutant of and which have in the PEBP2 binding sites and Smad binding not to or αC, that both of these binding are essential for activation by the the in αC critical in the activation in with Smads, a of C-terminal of αC was for transcription activity. αC containing the activation in the presence of and deletion of of the in a in of was with the the that the between Smad3 and αC may be critical for the activation 2 The formation of complexes containing αC and Smad3 the germline Cα DNA was by The β subunit of PEBP2 was in this assay to the DNA binding of Smad3 by and αC which be as complexes in 2 and and In the presence of Smad3 and a complex was both in vitro and complexes were in the presence of to the or an to the β that and Smad3 bind to DNA as a Mutations in the Smad binding or in the or of Smad3 and but the binding of the PEBP2α sites were a in but not in disrupted the of and but binding of Smad3 was The Smad binding and PEBP2α binding sites thus to be specific and for the binding of but both are required for the binding of the complex to the and for activation of the promoter by αC and The findings shown in the present that PEBP2α subunits and R-Smads specific for both TGF-β and BMP signaling pathways form complexes together with Smad4 and that the complex formation appears to be critical for activation of target including the germline Ig Cα Our findings suggest that PEBP2 may function as a nuclear target of TGF-β/BMP signaling pathways and that the biological of TGF-β/BMP may be by cooperation between Smads and Smads have been reported to interact with proteins as well as the and R. Zhang Y. Feng X.-H. Cell. 1998; Full Text Full Text PDF PubMed Scopus Google Scholar, D. R.S. S. J. Cell. 1999; Full Text Full Text PDF PubMed Scopus Google Scholar). Because members of the TGF-β have with transcription factors may be required for Smads to specific in certain cell of these interacting including and the receptor (6Zhang Y. Feng X.-H. Derynck R. Nature. 1998; 394: 909-913Crossref PubMed Scopus (688) Google Scholar, J. Y. Y. M. T. K. M. Kawabata M. Miyazono K. Kato S. 1999; PubMed Scopus Google Scholar), interact with FAST1 and murine have been shown to with Smad2 as well (3Chen X. Rubock M.J. Whitman M. Nature. 1996; 383: 691-696Crossref PubMed Scopus (634) Google Scholar, 4Labbé E. Silvestri C. Hoodless P.A. Wrana J.L. Attisano L. Mol. Cell. 1998; 2: 109-120Abstract Full Text Full Text PDF PubMed Scopus (464) Google Scholar, K. D. T. S. Kato M. Miyazono K. J. Biol. 1999; Full Text Full Text PDF PubMed Scopus Google Scholar). a transcription factor has been shown to bind to X. X. Chen D. X. J. Biol. 1999; Full Text Full Text PDF PubMed Scopus (152) Google Scholar). PEBP2 is with these factors, because three mammalian α subunits of PEBP2 interact with R-Smads in the present has been shown to interact with in to the PEBP2 α subunits, is a and with R-Smads may to of of target genes by K. C. H. P. L. G. R. D. J. Biol. 1999; Full Text Full Text PDF PubMed Scopus Google Scholar). Smad3 with αC the MH2 domain, whereas the domain to by C-terminal deletion of αC that the C-terminal including the of αC, is required for with the MH2 domain of PEBP2 is a context-dependent transcription interacting for including (21Wotton D. Ghysdael J. Wang S. Speck N.A. Owen M.J. Mol. Cell. Biol. 1994; 14: 840-850Crossref PubMed Scopus (199) Google Scholar, 22Kim W.-Y. Sieweke M. Ogawa E. Wee H.-J. Englmeier U. Graf T. Ito Y. EMBO J. 1999; 18: 1609-1620Crossref PubMed Scopus (197) Google Scholar). In the germline Ig Cα both PEBP2 and Smad binding sites are essential for In contrast, FAST1 to the gene promoter with and binding of Smads to DNA may be important in the Ig Cα promoter K. D. T. S. Kato M. Miyazono K. J. Biol. 1999; Full Text Full Text PDF PubMed Scopus Google Scholar). in certain other to which PEBP2 with a together with other transcription factors, DNA binding of Smads may not be critical for cooperative activation by PEBP2 and Smads. Our present that PEBP2α subunits interact with R-Smads by as well as with those by and that functional cooperation between αC and Smad3 is required for transcription by the germline Cα Ig α transcripts are required for IgA class switching J. Immunol. 1996; PubMed Scopus (275) Google Scholar). Because members of the TGF-β a of biological it be important to PEBP2 is in these biological as a nuclear target of Smads. are to Y. and A. Nishihara for and and to Y. Inada and Y. for

The N domain of Smad7 is essential for specific inhibition of transforming growth factor-β signaling
Aki Hanyu, Yasuhiro Ishidou, Takanori Ebisawa et al.|The Journal of Cell Biology|2001
Cited by 227Open Access

Inhibitory Smads (I-Smads) repress signaling by cytokines of the transforming growth factor-beta (TGF-beta) superfamily. I-Smads have conserved carboxy-terminal Mad homology 2 (MH2) domains, whereas the amino acid sequences of their amino-terminal regions (N domains) are highly divergent from those of other Smads. Of the two different I-Smads in mammals, Smad7 inhibited signaling by both TGF-beta and bone morphogenetic proteins (BMPs), whereas Smad6 was less effective in inhibiting TGF-beta signaling. Analyses using deletion mutants and chimeras of Smad6 and Smad7 revealed that the MH2 domains were responsible for the inhibition of both TGF-beta and BMP signaling by I-Smads, but the isolated MH2 domains of Smad6 and Smad7 were less potent than the full-length Smad7 in inhibiting TGF-beta signaling. The N domains of I-Smads determined the subcellular localization of these molecules. Chimeras containing the N domain of Smad7 interacted with the TGF-beta type I receptor (TbetaR-I) more efficiently, and were more potent in repressing TGF-beta signaling, than those containing the N domain of Smad6. The isolated N domain of Smad7 physically interacted with the MH2 domain of Smad7, and enhanced the inhibitory activity of the latter through facilitating interaction with TGF-beta receptors. The N domain of Smad7 thus plays an important role in the specific inhibition of TGF-beta signaling.

Characterization of a Bone Morphogenetic Protein-responsive Smad-binding Element
Kiyoshi Kusanagi, Hirofumi Inoue, Yasuhiro Ishidou et al.|Molecular Biology of the Cell|2000
Cited by 178Open Access

Bone morphogenetic proteins (BMPs) are pleiotropic growth and differentiation factors belonging to the transforming growth factor-beta (TGF-beta) superfamily. Signals of the TGF-beta-like ligands are propagated to the nucleus through specific interaction of transmembrane serine/threonine kinase receptors and Smad proteins. GCCGnCGC has been suggested as a consensus binding sequence for Drosophila Mad regulated by a BMP-like ligand, Decapentaplegic. Smad1 is one of the mammalian Smads activated by BMPs. Here we show that Smad1 binds to this motif upon BMP stimulation in the presence of the common Smad, Smad4. The binding affinity is likely to be relatively low, because Smad1 binds to three copies of the motif weakly, but more repeats of the motif significantly enhance the binding. Heterologous reporter genes (GCCG-Lux) with multiple repeats of the motif respond to BMP stimulation but not to TGF-beta or activin. Mutational analyses reveal several bases critical for the responsiveness. A natural BMP-responsive reporter, pTlx-Lux, is activated by BMP receptors in P19 cells but not in mink lung cells. In contrast, GCCG-Lux responds to BMP stimulation in both cells, suggesting that it is a universal reporter that directly detects Smad phosphorylation by BMP receptors.

Enhanced expression of type I receptors for bone morphogenetic proteins during bone formation
Yasuhiro Ishidou, Isao Kitajima, Hiroya Obama et al.|Journal of Bone and Mineral Research|1995
Cited by 172

Type I receptors for bone morphogenetic proteins (BMPs), i.e., BMPR-IA and BMPR-IB, are transmembrane serine/threonine kinases, that bind osteogenic protein-1 (OP-1, also termed BMP-7) and BMP-4. Using antibodies specific to BMPR-IA and -IB, we have studied the expression of BMP type I receptors in the bone formation process during embryonic development and fracture healing. In the mouse embryo, both BMPR-IA and -IB were expressed in condensing mesenchymal cells at 13.5 days post coitum (p.c.). At 15.5 days p.c., expression of BMPR-IB, but not of BMPR-IA, was observed in the cells in perichondrium of developing cartilage. At 17.5 and 19.5 days p.c., expression of both receptors was observed in chondrocytes and in osteoblasts. In normal rat adult bone, expression of BMPR-IA, but not of BMPR-IB, was observed in osteoblasts in the periosteum. Three days after the femoral fracture, expression of BMPR-IA and -IB was up-regulated in cells at the proliferating osteogenic layer of the periosteum. On day 7, both receptors were found in fibroblast-like spindle cells and chondrocytes in the endochondral ossification sites, and osteoblasts in the newly formed trabecular bone. Expression of BMPR-IA was higher than that BMPR-IB in osteogenic layer on day 3 and in osteoblasts in the trabecular bone on day 7. On day 14, expression of BMP type I receptors was observed at similar sites, albeit with lower expression levels than were observed on day 7. The present data suggest that expression of BMP type I receptors is up-regulated during bone formation, and that they may play important roles in bone morphogenesis.

Interplay of Signal Mediators of Decapentaplegic (Dpp): Molecular Characterization of Mothers against dpp, Medea, and Daughters against dpp
Hirofumi Inoue, Takeshi Imamura, Yasuhiro Ishidou et al.|Molecular Biology of the Cell|1998
Cited by 108Open Access

Decapentaplegic (Dpp) plays an essential role in Drosophila development, and analyses of the Dpp signaling pathway have contributed greatly to understanding of the actions of the TGF-beta superfamily. Intracellular signaling of the TGF-beta superfamily is mediated by Smad proteins, which are now grouped into three classes. Two Smads have been identified in Drosophila. Mothers against dpp (Mad) is a pathway-specific Smad, whereas Daughters against dpp (Dad) is an inhibitory Smad genetically shown to antagonize Dpp signaling. Here we report the identification of a common mediator Smad in Drosophila, which is closely related to human Smad4. Mad forms a heteromeric complex with Drosophila Smad4 (Medea) upon phosphorylation by Thick veins (Tkv), a type I receptor for Dpp. Dad stably associates with Tkv and thereby inhibits Tkv-induced Mad phosphorylation. Dad also blocks hetero-oligomerization and nuclear translocation of Mad. We also show that Mad exists as a monomer in the absence of Tkv stimulation. Tkv induces homo-oligomerization of Mad, and Dad inhibits this step. Finally, we propose a model for Dpp signaling by Drosophila Smad proteins.