Suppression of BMP-Smad signaling axis-induced osteoblastic differentiation by small C-terminal domain phosphatase 1, a Smad phosphatase

Molecular Endocrinology

Volumn 25, Issue 3, 2011, Pages 474-481

  Kokabu, Shoichiro ^a   Ohte, Satoshi ^a   Sasanuma, Hiroki ^a   Shin, Masashi ^a   Yoneyama, Katsumi ^a   Murata, Eiko ^a   Kanomata, Kazuhiro ^a   Nojima, Junya ^a   Ono, Yusuke ^b   Yoda, Tetsuya ^a   Fukuda, Toru ^a   Katagiri, Takenobu ^a  

^a SAITAMA MEDICAL UNIVERSITY   (Japan)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR; PHOSPHATASE; SMAD PROTEIN; SMAD1 PROTEIN; SMALL CARBOXY TERMINAL DOMAIN PHOSPHATASE 1; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; MOUSE; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEIN 4; CELL DIFFERENTIATION; CELLS, CULTURED; CORE BINDING FACTOR ALPHA 1 SUBUNIT; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MICE; MYOBLASTS; OSTEOBLASTS; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SMAD1 PROTEIN;

EID: 79952165234     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2010-0305     Document Type: Article

References (35)

1. Urist MR 1965 Bone: formation by autoinduction. Science 150:893-899
2. Katagiri T, Yamaguchi A, Komaki M, Abe E, Takahashi N, Ikeda T, Rosen V, Wozney JM, Fujisawa-Sehara A, Suda T 1994 Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J Cell Biol 127:1755-1766 (Pubitemid 24380911)
3. Wan M, Cao X 2005 BMP signaling in skeletal development. Biochem Biophys Res Commun 328:651-657 (Pubitemid 40208302)
4. Miyazono K, Maeda S, Imamura T 2005 BMP receptor signaling: transcriptional targets, regulation of signals, and signaling crosstalk. Cytokine Growth Factor Rev 16:251-263 (Pubitemid 40910315)
5. Katagiri T, Suda T, Miyazono K 2008 The bone morphogenetic proteins. In Derynck R, Miyazono K, eds. TGF-β family. New York: Cold Spring Harbor Press, 121-149
6. Hoodless PA, Haerry T, Abdollah S, Stapleton M, O'Connor MB, Attisano L, Wrana JL 1996 MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85:489-500 (Pubitemid 26157188)
7. Chen Y, Bhushan A, Vale W 1997 Smad8 mediates the signaling of the ALK-2 [corrected] receptor serine kinase. Proc Natl Acad Sci USA 94:12938-12943 (Pubitemid 27518455)
8. Nishimura R, Kato Y, Chen D, Harris SE, Mundy GR, Yoneda T 1998 Smad5 and DPC4 are key molecules in mediating BMP-2-induced osteoblastic differentiation of the pluripotent mesenchymal precursor cell line C2C12. J Biol Chem 273:1872-1879 (Pubitemid 28069228)
9. Nojima J, Kanomata K, Takada Y, Fukuda T, Kokabu S, Ohte S, Takada T, Tsukui T, Yamamoto TS, Sasanuma H, Yoneyama K, Ueno N, Okazaki Y, Kamijo R, Yoda T, Katagiri T 2010 Dual roles of smad proteins in the conversion from myoblasts to osteoblastic cells by bone morphogenetic proteins. J Biol Chem 285:15577-15586
10. López-Rovira T, Chalaux E, Massagué J, Rosa JL, Ventura F 2002 Direct binding of Smad1 and Smad4 to two distinct motifs mediates bone morphogenetic protein-specific transcriptional activation of Id1 gene. J Biol Chem 277:3176-3185 (Pubitemid 34953179)
11. Liu CJ, Ding B, Wang H, Lengyel P 2002 The MyoD-inducible p204 protein overcomes the inhibition of myoblast differentiation by Id proteins. Mol Cell Biol 22:2893-2905 (Pubitemid 34437449)
12. 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
13. Hollnagel A, Oehlmann V, Heymer J, Rüther U, Nordheim A 1999 Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. J Biol Chem 274:19838-19845
14. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G 1997 Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89:747-754 (Pubitemid 27516177)
15. 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 (Pubitemid 34137009)
16. Kretzschmar M, Doody J, Massagué J 1997 Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1. Nature 389:618-622 (Pubitemid 27446181)
17. Zhu H, Kavsak P, Abdollah S, Wrana JL, Thomsen GH 1999 A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 400:687-693
18. Fuentealba LC, Eivers E, Ikeda A, Hurtado C, Kuroda H, Pera EM, De Robertis EM 2007 Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131:980-993 (Pubitemid 350138081)
19. Knockaert M, Sapkota G, Alarcón C, Massagué J, Brivanlou AH 2006 Unique players in the BMP pathway: small C-terminal domain phosphatases dephosphorylate Smad1 to attenuate BMP signaling. Proc Natl Acad Sci USA 103:11940-11945 (Pubitemid 44215790)
20. Lin X, Duan X, Liang YY, Su Y, Wrighton KH, Long J, Hu M, Davis CM, Wang J, Brunicardi FC, Shi Y, Chen YG, Meng A, Feng XH 2006 PPM1A functions as a Smad phosphatase to terminate TGFβ signaling. Cell 125:915-928 (Pubitemid 43795197)
21. Yeo M, Lin PS, Dahmus ME, Gill GN 2003 A novel RNA polymerase II C-terminal domain phosphatase that preferentially dephosphorylates serine 5. J Biol Chem 278:26078-26085 (Pubitemid 36835376)
22. Yeo M, Lee SK, Lee B, Ruiz EC, Pfaff SL, Gill GN 2005 Small CTD phosphatases function in silencing neuronal gene expression. Science 307:596-600 (Pubitemid 40165685)
23. Sapkota G, Knockaert M, Alarcón C, Montalvo E, Brivanlou AH, Massagué J 2006 Dephosphorylation of the linker regions of Smad1 and Smad2/3 by small C-terminal domain phosphatases has distinct outcomes for bone morphogenetic protein and transforming growth factor-beta pathways. J Biol Chem 281:40412-40419 (Pubitemid 46041844)
24. Duan X, Liang YY, Feng XH, Lin X 2006 Protein serine/threonine phosphatase PPM1A dephosphorylates Smad1 in the bone morphogenetic protein signaling pathway. J Biol Chem 281:36526-36532 (Pubitemid 46042119)
25. Kokabu S, Nojima J, Kanomata K, Ohte S, Yoda T, Fukuda T, Katagiri T 2010 Protein phosphatase magnesium-dependent 1A-mdiated inhibition of BMP signaling is independent of Smad dephosphorylation. J Bone Miner Res 25:653-660
26. Maruyama Z, Yoshida CA, Furuichi T, Amizuka N, Ito M, Fukuyama R, Miyazaki T, Kitaura H, Nakamura K, Fujita T, Kanatani N, Moriishi T, Yamana K, Liu W, Kawaguchi H, Komori T 2007 Runx2 determines bone maturity and turnover rate in postnatal bone development and is involved in bone loss in estrogen deficiency. Dev Dyn 236:1876-1890 (Pubitemid 47076017)
27. Ducy P, Karsenty G 1995 Two distinct osteoblast-specific cis-acting elements control expression of a mouse osteocalcin gene. Mol Cell Biol 15:1858-1869
28. Goldman LA, Cutrone EC, Kotenko SV, Krause CD, Langer JA 1996 Modifications of vectors pEF-BOS, pcDNA1 and pcDNA3 result in improved convenience and expression. Biotechniques 21:1013-1015 (Pubitemid 26422004)
29. Komaki M, Katagiri T, Suda T 1996 Bone morphogenetic protein-2 does not alter the differentiation pathway of committed progenitors of osteoblasts and chondroblasts. Cell Tissue Res 284:9-17 (Pubitemid 26106892)
30. Ono Y, Boldrin L, Knopp P, Morgan JE, Zammit PS 2010 Muscle satellite cells are a functionally heterogeneous population in both somite-derived and branchiomeric muscles. Dev Biol 337:29-41
31. Kodaira K, Imada M, Goto M, Tomoyasu A, Fukuda T, Kamijo R, Suda T, Higashio K, Katagiri T 2006 Purification and identification of a BMP-like factor from bovine serum. Biochem Biophys Res Commun 345:1224-1231 (Pubitemid 43776518)
32. Lee KS, Kim HJ, Li QL, Chi XZ, Ueta C, Komori T, Wozney JM, Kim EG, Choi JY, Ryoo HM, Bae SC 2000 Runx2 is a common target of transforming growth factor beta1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12. Mol Cell Biol 20:8783-8792 (Pubitemid 32245911)
33. Fukuda T, Kohda M, Kanomata K, Nojima J, Nakamura A, Kamizono J, Noguchi Y, Iwakiri K, Kondo T, Kurose J, Endo KI, Awakura T, Fukushi J, Nakashima Y, Chiyonobu T, Kawara A, Nishida Y, Wada I, Akita M, Komori T, Nakayama K, Nanba A, Maruki Y, Yoda T, Tomoda H, Yu PB, Shore EM, Kaplan FS, Miyazono K, Matsuoka M, Ikebuchi K, Akira O, Oda H, Jimi E, Owan I, Okazaki Y, Katagiri T 2009 Constitutively activated ALK2 and increased smad1/5 cooperatively induce BMP signaling in fibrodysplasia ossificans progressiva. J Biol Chem 284:7149-7156
34. Fukuda T, Kanomata K, Nojima J, Kokabu S, Akita M, Ikebuchi K, Jimi E, Komori T, Maruki Y, Matsuoka M, Miyazono K, Nakayama K, Nanba A, Tomoda H, Okazaki Y, Ohtake A, Oda H, Owan I, Yoda T, Haga N, Furuya H, Katagiri T 2008 A unique mutation of ALK2, G356D, found in a patient with fibrodysplasia ossificans progressiva is a moderately activated BMP type I receptor. Biochem Biophys Res Commun 377:905-909
35. Shore EM, Xu M, Feldman GJ, Fenstermacher DA, Cho TJ, Choi IH, Connor JM, Delai P, Glaser DL, LeMerrer M, Morhart R, Rogers JG, Smith R, Triffitt JT, Urtizberea JA, Zasloff M, Brown MA, Kaplan FS 2006 A recurrent mutation in the BMP type I receptor ACVR1 causes inherited and sporadic fibrodysplasia ossificans progressiva. Nat Genet 38:525-527