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J Biol Chem, Vol. 273, Issue 40, 25628-25636, October 2, 1998
From the BMP7 and activin are members of the transforming
growth factor
Specific Activation of Smad1 Signaling Pathways by the BMP7
Type I Receptor, ALK2
,,
,**, and**
Program in Developmental Biology, Department of Genetics, The Hospital
for Sick Children, Toronto, Ontario M5G 1X8, Canada, and the
** Department of Medical Genetics and Microbiology, University of
Toronto, Toronto, Ontario M5S 1A8, Canada
superfamily. Here we characterize endogenous activin
and BMP7 signaling pathways in P19 embryonic carcinoma cells. We show that BMP7 and activin bind to the same type II receptors, ActRII and
IIB, but recruit distinct type I receptors into heteromeric receptor
complexes. The major BMP7 type I receptor observed was ALK2, while
activin bound exclusively to ALK4 (ActRIB). BMP7 and activin elicited
distinct biological responses and activated different Smad pathways.
BMP7 stimulated phosphorylation of endogenous Smad1 and 5, formation of
complexes with Smad4 and induced the promoter for the homeobox gene,
Tlx2. In contrast, activin induced phosphorylation of
Smad2, association with Smad4, and induction of the activin response
element from the Xenopus Mix.2
gene. Biochemical analysis revealed that constitutively active ALK2
associated with and phosphorylated Smad1 on the COOH-terminal
SSXS motif, and also regulated Smad5 and Smad8
phosphorylation. Activated ALK2 also induced the Tlx2 promoter in the absence of BMP7. Furthermore, we show that ALK1 (TSRI),
an orphan receptor that is closely related to ALK2 also mediates Smad1
signaling. Thus, ALK1 and ALK2 induce Smad1-dependent pathways and ALK2 functions to mediate BMP7 but not activin
signaling.
Copyright © 1998 by The American Society for Biochemistry and Molecular Biology, Inc.
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K. D. Tremblay, N. R. Dunn, and E. J. Robertson Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation Development, September 15, 2001; 128(18): 3609 - 3621. [Abstract] [Full Text] [PDF]
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 A. Rosendahl, D. Checchin, T. E. Fehniger, P. ten Dijke, C.-H. Heldin, and P. Sideras Activation of the TGF-beta /Activin-Smad2 Pathway during Allergic Airway Inflammation Am. J. Respir. Cell Mol. Biol., July 1, 2001; 25(1): 60 - 68. [Abstract] [Full Text] [PDF]
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 J. A. Visser, R. Olaso, M. Verhoef-Post, P. Kramer, A. P. N. Themmen, and H. A. Ingraham The Serine/Threonine Transmembrane Receptor ALK2 Mediates Mullerian Inhibiting Substance Signaling Mol. Endocrinol., June 1, 2001; 15(6): 936 - 945. [Abstract] [Full Text] [PDF]
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T. R. Clarke, Y. Hoshiya, S. E. Yi, X. Liu, K. M. Lyons, and P. K. Donahoe Mullerian Inhibiting Substance Signaling Uses a Bone Morphogenetic Protein (BMP)-Like Pathway Mediated by ALK2 and Induces Smad6 Expression Mol. Endocrinol., June 1, 2001; 15(6): 946 - 959. [Abstract] [Full Text] [PDF]
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 J. Nickel, M. K. Dreyer, T. Kirsch, and W. Sebald The Crystal Structure of the BMP-2:BMPR-IA Complex and the Generation of BMP-2 Antagonists J. Bone Joint Surg. Am., April 1, 2001; 83(90010): S7 - 14. [Abstract] [Full Text] [PDF]
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H. Dorai and T K. Sampath Bone Morphogenetic Protein-7 Modulates Genes that Maintain the Vascular Smooth Muscle Cell Phenotype in Culture J. Bone Joint Surg. Am., April 1, 2001; 83(90010): S70 - 78. [Abstract] [Full Text] [PDF]
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J. Nickel, M. K. Dreyer, T. Kirsch, and W. Sebald The Crystal Structure of the BMP-2:BMPR-IA Complex and the Generation of BMP-2 Antagonists J. Bone Joint Surg. Am., March 1, 2001; 83(1_suppl_1): S7 - S14. [Abstract] [Full Text] [PDF]
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H. Dorai and T K. Sampath Bone Morphogenetic Protein-7 Modulates Genes that Maintain the Vascular Smooth Muscle Cell Phenotype in Culture J. Bone Joint Surg. Am., March 1, 2001; 83(1_suppl_1): S70 - S78. [Abstract] [Full Text] [PDF]
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H Aoki, M Fujii, T Imamura, K Yagi, K Takehara, M Kato, and K Miyazono Synergistic effects of different bone morphogenetic protein type I receptors on alkaline phosphatase induction J. Cell Sci., January 4, 2001; 114(8): 1483 - 1489. [Abstract] [PDF]
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H Bauer, Z Lele, G. Rauch, R Geisler, and M Hammerschmidt The type I serine/threonine kinase receptor Alk8/Lost-a-fin is required for Bmp2b/7 signal transduction during dorsoventral patterning of the zebrafish embryo Development, January 3, 2001; 128(6): 849 - 858. [Abstract] [PDF]
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 M. P. de Caestecker, E. Piek, and A. B. Roberts Role of Transforming Growth Factor-{beta} Signaling in Cancer J Natl Cancer Inst, September 6, 2000; 92(17): 1388 - 1402. [Abstract] [Full Text] [PDF]
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E. Labbé, A. Letamendia, and L. Attisano Association of Smads with lymphoid enhancer binding factor 1/T cell-specific factor mediates cooperative signaling by the transforming growth factor-beta and Wnt pathways PNAS, July 5, 2000; (2000) 150152697. [Abstract] [Full Text]
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D. G. Monroe, D. F. Jin, and M. M. Sanders Estrogen Opposes the Apoptotic Effects of Bone Morphogenetic Protein 7 on Tissue Remodeling Mol. Cell. Biol., July 1, 2000; 20(13): 4626 - 4634. [Abstract] [Full Text]
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 S. A. Abdalla, N. Pece-Barbara, S. Vera, E. Tapia, E. Paez, C. Bernabeu, and M. Letarte Analysis of ALK-1 and endoglin in newborns from families with hereditary hemorrhagic telangiectasia type 2 Hum. Mol. Genet., May 1, 2000; 9(8): 1227 - 1237. [Abstract] [Full Text] [PDF]
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K. Kusanagi, H. Inoue, Y. Ishidou, H. K. Mishima, M. Kawabata, and K. Miyazono Characterization of a Bone Morphogenetic Protein-responsive Smad-binding Element Mol. Biol. Cell, February 1, 2000; 11(2): 555 - 565. [Abstract] [Full Text]
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X. Yang, X. Ji, X. Shi, and X. Cao Smad1 Domains Interacting with Hoxc-8 Induce Osteoblast Differentiation J. Biol. Chem., January 14, 2000; 275(2): 1065 - 1072. [Abstract] [Full Text] [PDF]
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S Faure, M. Lee, T Keller, P ten Dijke, and M Whitman Endogenous patterns of TGFbeta superfamily signaling during early Xenopus development Development, January 7, 2000; 127(13): 2917 - 2931. [Abstract] [PDF]
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S. Yi, A Daluiski, R Pederson, V Rosen, and K. Lyons The type I BMP receptor BMPRIB is required for chondrogenesis in the mouse limb Development, January 2, 2000; 127(3): 621 - 630. [Abstract] [PDF]
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I. Gupta, M Macias-Silva, S Kim, X Zhou, T. Piscione, C Whiteside, J. Wrana, and N. Rosenblum BMP-2/ALK3 and HGF signal in parallel to regulate renal collecting duct morphogenesis J. Cell Sci., January 1, 2000; 113(2): 269 - 278. [Abstract] [PDF]
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 E. PIEK, C.-H. HELDIN, and P. TEN DIJKE Specificity, diversity, and regulation in TGF-{beta} superfamily signaling FASEB J, December 1, 1999; 13(15): 2105 - 2124. [Abstract] [Full Text]
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M. Fujii, K. Takeda, T. Imamura, H. Aoki, T. K. Sampath, S. Enomoto, M. Kawabata, M. Kato, H. Ichijo, and K. Miyazono Roles of Bone Morphogenetic Protein Type I Receptors and Smad Proteins in Osteoblast and Chondroblast Differentiation Mol. Biol. Cell, November 1, 1999; 10(11): 3801 - 3813. [Abstract] [Full Text]
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I. R. Gupta, T. D. Piscione, S. Grisaru, T. Phan, M. Macias-Silva, X. Zhou, C. Whiteside, J. L. Wrana, and N. D. Rosenblum Protein Kinase A Is a Negative Regulator of Renal Branching Morphogenesis and Modulates Inhibitory and Stimulatory Bone Morphogenetic Proteins J. Biol. Chem., September 10, 1999; 274(37): 26305 - 26314. [Abstract] [Full Text] [PDF]
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A. Franzén, E. Piek, B. Westermark, P. ten Dijke, and N.-E. Heldin Expression of Transforming Growth Factor-{beta}1, Activin A, and Their Receptors in Thyroid Follicle Cells: Negative Regulation of Thyrocyte Growth and Function Endocrinology, September 1, 1999; 140(9): 4300 - 4310. [Abstract] [Full Text]
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 C. L Shovlin and M. Letarte Rare diseases bullet 4: Hereditary haemorrhagic telangiectasia and pulmonary arteriovenous malformations: issues in clinical management and review of pathogenic mechanisms Thorax, August 1, 1999; 54(8): 714 - 729. [Full Text]
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A. Ishisaki, K. Yamato, S. Hashimoto, A. Nakao, K. Tamaki, K. Nonaka, P. ten Dijke, H. Sugino, and T. Nishihara Differential Inhibition of Smad6 and Smad7 on Bone Morphogenetic Protein- and Activin-mediated Growth Arrest and Apoptosis in B Cells J. Biol. Chem., May 7, 1999; 274(19): 13637 - 13642. [Abstract] [Full Text] [PDF]
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S. Snyders and B. D. Kohorn TAKs, Thylakoid Membrane Protein Kinases Associated with Energy Transduction J. Biol. Chem., April 2, 1999; 274(14): 9137 - 9140. [Abstract] [Full Text] [PDF]
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Y.-G. Chen and J. Massague Smad1 Recognition and Activation by the ALK1 Group of Transforming Growth Factor-beta Family Receptors J. Biol. Chem., February 5, 1999; 274(6): 3672 - 3677. [Abstract] [Full Text] [PDF]
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E Piek, A Moustakas, A Kurisaki, C. Heldin, and P ten Dijke TGF-(beta) type I receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells J. Cell Sci., January 12, 1999; 112(24): 4557 - 4568. [Abstract] [PDF]
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A. Ramsdell and H. Yost Cardiac looping and the vertebrate left-right axis: antagonism of left-sided Vg1 activity by a right-sided ALK2-dependent BMP pathway Development, January 12, 1999; 126(23): 5195 - 5205. [Abstract] [PDF]
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T Ebisawa, K Tada, I Kitajima, K Tojo, T. Sampath, M Kawabata, K Miyazono, and T Imamura Characterization of bone morphogenetic protein-6 signaling pathways in osteoblast differentiation J. Cell Sci., January 10, 1999; 112(20): 3519 - 3527. [Abstract] [PDF]
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