Smad9 is a new type of transcriptional regulator in bone morphogenetic protein signaling

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Tsukamoto, S ^a   Mizuta, T ^a   Fujimoto, M ^a   Ohte, S ^a   Osawa, K ^a   Miyamoto, A ^a   Yoneyama, K ^a   Murata, E ^a   Machiya, A ^a   Jimi, E ^b   Kokabu, S ^a   Katagiri, T ^a  

^a SAITAMA MEDICAL UNIVERSITY   (Japan)

^b KYUSHU DENTAL COLLEGE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; SMAD1 PROTEIN; SMAD1 PROTEIN, MOUSE; SMAD8 PROTEIN; SMAD9 PROTEIN, MOUSE;

ANIMAL; CELL LINE; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL LINE; MICE; SIGNAL TRANSDUCTION; SMAD1 PROTEIN; SMAD8 PROTEIN; TRANSCRIPTION, GENETIC;

EID: 84939835163     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep07596     Document Type: Article

References (49)

1. Katagiri, T., Suda, T. & Miyazono, K. The bonemorphogenetic proteins. In: TGF-β Family, Derynck, R. & Miyazono, K. eds. (Cold Spring Harbor Press, 2008), pp. 121-149.
2. Miyazono, K., Kamiya, Y. & Morikawa, M. Bone morphogenetic protein receptors and signal transduction. J. Biochem. 147, 35-51 (2010).
3. Urist, M. R. Bone: formation by autoinduction. Science 150, 893-899 (1965).
4. Sampath, T. K., Muthukumaran, N. & Reddi, A. H. Isolation of osteogenin, an extracellular matrix-associated, bone-inductive protein, by heparin affinity chromatography. Proc. Natl. Acad. Sci. U. S. A. 84, 7109-7113 (1987).
5. Wozney, J. M. et al. Novel regulators of bone formation: molecular clones and activities. Science 242, 1528-1534 (1988).
6. Katagiri, T. et al. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J. Cell. Biol. 127, 1755-1766 (1994).
7. Mueller, T. D. & Nickel, J. Promiscuity and specificity in BMP receptor activation. FEBS Lett. 586, 1846-1859 (2012).
8. Katagiri, T. & Tsukamoto, S. The unique activity of bone morphogenetic proteins in bone: a critical role of the Smad signaling pathway. Biol. Chem. 394, 703-714 (2013).
9. Wieser, R., Wrana, J. L. & Massague, J. GS domain mutations that constitutively activate TβR-I, the downstream signaling component in the TGF-β receptor complex. EMBO J. 14, 2199-2208 (1995).
10. Akiyama, S. et al. Constitutively active BMP type I receptors transduce BMP-2 signals without the ligand in C2C12 myoblasts. Exp. Cell. Res. 235, 362-369 (1997).
11. Fujii, M. et al. Roles of bone morphogenetic protein type I receptors and Smad proteins in osteoblast and chondroblast differentiation. Mol. Biol. Cell. 10, 3801-3813 (1999).
12. Glaser, D. L. et al. In vivo somatic cell gene transfer of an engineered Noggin mutein prevents BMP4-induced heterotopic ossification. J. Bone. Joint. Surg. Am. 85-A, 2332-2342 (2003).
13. Katagiri, T. Recent topics in fibrodysplasia ossificans progressiva. J. Oral. Biosci 54, 119-123 (2012).
14. Shore, E. M. et al. A recurrent mutation in the BMP type I receptor ACVR1 causes inherited and sporadic fibrodysplasia ossificans progressiva. Nat. Genet. 38, 525-527 (2006).
15. Fukuda, T. et al. 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 (2008).
16. Fukuda, T. et al. Constitutively activated ALK2 and increased SMAD1/5 cooperatively induce bone morphogenetic protein signaling in fibrodysplasia ossificans progressiva. J. Biol. Chem. 284, 7149-7156 (2009).
17. Ohte, S. et al. A novel mutation of ALK2, L196P, found in the most benign case of fibrodysplasia ossificans progressiva activates BMP-specific intracellular signaling equivalent to a typical mutation, R206H. Biochem. Biophys. Res. Commun. 407, 213-218 (2011).
18. Yu, P. B. et al. BMP type I receptor inhibition reduces heterotopic ossification. Nat. Med. 14, 1363-1369 (2008).
19. Wrighton, K. H., Lin, X. & Feng, X. H. Phospho-control of TGF-β superfamily signaling. Cell. Res. 19, 8-20 (2009).
20. Massague, J. TGFβ signalling in context. Nat. Rev. Mol. Cell. Biol. 13, 616-630 (2012).
21. Wakefield, L. M. & Hill, C. S. Beyond TGFβ: roles of other TGFβ superfamily members in cancer. Nat. Rev. Cancer. 13, 328-341 (2013).
22. Moustakas, A. & Heldin, C. H. The regulation of TGFβ signal transduction. Development 136, 3699-3714 (2009).
23. Zi, Z., Chapnick, D. A. & Liu, X. Dynamics of TGF-β/Smad signaling. FEBS Lett. 586, 1921-1928 (2012).
24. Kokabu, S., Katagiri, T., Yoda, T. & Rosen, V. Role of Smad phosphatases in BMPSmad signaling axis-induced osteoblast differentiation. J. Oral. Biosci 54, 73-78 (2012).
25. Bruce, D. L. & Sapkota, G. P. Phosphatases in SMAD regulation. FEBS Lett. 586, 1897-1905 (2012).
26. Qin, B. Y. et al. Structural basis of Smad1 activation by receptor kinase phosphorylation. Mol. Cell. 8, 1303-1312 (2001).
27. Wu, M. Y. & Hill, C. S. TGF-β superfamily signaling in embryonic development and homeostasis. Dev. Cell. 16, 329-343 (2009).
28. Hayashi, H. et al. The MAD-related protein Smad7 associates with the TGFβ receptor and functions as an antagonist of TGFβ signaling. Cell 89, 1165-1173 (1997).
29. Imamura, T. et al. Smad6 inhibits signalling by the TGF-β superfamily. Nature 389, 622-626 (1997).
30. Nakao, A. et al. Identification of Smad7, a TGFβ-inducible antagonist of TGF-β signalling. Nature 389, 631-635 (1997).
31. Zhang, X. et al. Fine-tuning BMP7 signalling in adipogenesis by UBE2O/E2- 230K-mediated monoubiquitination of SMAD6. EMBO J. 32, 996-1007 (2013).
32. Itoh, S. & ten Dijke, P. Negative regulation of TGF-β receptor/Smad signal transduction. Curr Opin Cell Biol. 19, 176-184 (2007).
33. Bai, S., Shi, X., Yang, X. & Cao, X. Smad6 as a transcriptional corepressor. J. Biol. Chem. 275, 8267-8270 (2000).
34. Lin, X. et al. Smad6 recruits transcription corepressor CtBP to repress bone morphogenetic protein-induced transcription. Mol Cell Biol. 23, 9081-9093 (2003).
35. Katagiri, T. et al. Identification of a BMP-responsive element in Id1, the gene for inhibition of myogenesis. Genes. Cells. 7, 949-960 (2002).
36. 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. 277, 4883-4891 (2002).
37. Lopez-Rovira, T., Chalaux, E., Massague, J., Rosa, J. L. & 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. 277, 3176-3185 (2002).
38. Shepherd, T. G., Theriault, B. L. & Nachtigal, M. W. Autocrine BMP4 signalling regulates ID3 proto-oncogene expression in human ovarian cancer cells. Gene 414, 95-105 (2008).
39. Kurooka, H., Nakahiro, T., Mori, K., Sano, K. & Yokota, Y. BMP signaling is responsible for serum-induced Id2 expression. Biochem. Biophys. Res. Commun. 420, 281-287 (2012).
40. Shin, M. et al. Identification of a novel bone morphogenetic protein (BMP)- inducible transcript, BMP-inducible transcript-1, by utilizing the conserved BMP-responsive elements in the Id genes. J. Bone. Miner. Metab. 31, 34-43 (2013).
41. Nohe, A., Keating, E., Knaus, P. & Petersen, N. O. Signal transduction of bone morphogenetic protein receptors. Cell. Signal. 16, 291-299 (2004).
42. Nojima, J. et al. Dual roles of smad proteins in the conversion from myoblasts to osteoblastic cells by bone morphogenetic proteins. J. Biol. Chem. 285, 15577-15586 (2010).
43. Yamazaki, M. et al. Tumor necrosis factor alpha represses bone morphogenetic protein (BMP) signaling by interfering with the DNA binding of Smads through the activation of NF-kB. J. Biol Chem 284, 35987-35995 (2009).
44. Sapkota, G., Alarcon, C., Spagnoli, F. M., Brivanlou, A. H. & Massague, J. Balancing BMP signaling through integrated inputs into the Smad1 linker. Mol Cell. 25, 441-454 (2007).
45. Miyai, K. et al. ANA deficiency enhances bone morphogenetic protein-induced ectopic bone formation via transcriptional events. J. Biol Chem 284, 10593-10600 (2009).
46. Arnold, S. J., Maretto, S., Islam, A., Bikoff, E. K. & Robertson, E. J. Dose-dependent Smad1, Smad5 and Smad8 signaling in the early mouse embryo. Dev Biol 296, 104-118 (2006).
47. Goldman, L. A., Cutrone, E. C., Kotenko, S. V., Krause, C. D. & Langer, J. A. Modifications of vectors pEF-BOS, pcDNA1 and pcDNA3 result in improved convenience and expression. Biotechniques 21, 1013-1015 (1996).
48. Kodaira, K. et al. Purification and identification of a BMP-like factor from bovine serum. Biochem. Biophys. Res. Commun. 345, 1224-1231 (2006).
49. Ohte, S. et al. Identification and functional analysis of Zranb2 as a novel Smadbinding protein that suppresses BMP signaling. J. Cell. Biochem. 113, 808-814 (2012).