Balancing BMP Signaling through Integrated Inputs into the Smad1 Linker

Molecular Cell

Volumn 25, Issue 3, 2007, Pages 441-454

  Sapkota, Gopal ^a   Alarcón, Claudio ^a   Spagnoli, Francesca M ^b   Brivanlou, Ali H ^b   Massagué, Joan ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

DEVBIO; SIGNALING

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR; CARRIER PROTEIN; FIBROBLAST GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; NUCLEOPORIN; PROTEIN NUP214; RAS PROTEIN; SMAD1 PROTEIN; UBIQUITIN LIGASE SMURF1; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CATALYST; CELL NUCLEUS; CELL STRAIN HEK293; CYTOPLASM; EMBRYO; FEEDBACK SYSTEM; HELA CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OSSIFICATION; OSTEOBLAST; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; UBIQUITINATION; XENOPUS;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELLS, CULTURED; FIBROBLAST GROWTH FACTORS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; MITOGENS; NUCLEAR PORE COMPLEX PROTEINS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SMAD1 PROTEIN; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; XENOPUS;

VERTEBRATA;

EID: 33846688094     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.01.006     Document Type: Article

References (58)

1. Alexandrova E.M., and Thomsen G.H. Smurf1 regulates neural patterning and folding in Xenopus embryos by antagonizing the BMP/Smad1 pathway. Dev. Biol. 299 (2006) 398-410 10.1016/j.ydbio.2006.08.009 Published online August 10, 2006
2. Aubin J., Davy A., and Soriano P. In vivo convergence of BMP and MAPK signaling pathways: impact of differential Smad1 phosphorylation on development and homeostasis. Genes Dev. 18 (2004) 1482-1494
3. Bennett B.L., Sasaki D.T., Murray B.W., O'Leary E.C., Sakata S.T., Xu W., Leisten J.C., Motiwala A., Pierce S., Satoh Y., et al. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. USA 98 (2001) 13681-13686
4. Brivanlou A.H., and Harland R.M. Expression of an engrailed-related protein is induced in the anterior neural ectoderm of early Xenopus embryos. Development 106 (1989) 611-617
5. Chen C.R., Kang Y., Siegel P.M., and Massagué J. E2F4/5 and p107 as Smad cofactors linking the TGFbeta receptor to c-myc repression. Cell 110 (2002) 19-32
6. Chen D., Zhao M., and Mundy G.R. Bone morphogenetic proteins. Growth Factors 22 (2004) 233-241
7. Cohen P., and Frame S. The renaissance of GSK3. Nat. Rev. Mol. Cell Biol. 2 (2001) 769-776
8. Cuenda A., Rouse J., Doza Y.N., Meier R., Cohen P., Gallagher T.F., Young P.R., and Lee J.C. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 364 (1995) 229-233
9. De Robertis E.M. Spemann's organizer and self-regulation in amphibian embryos. Nat. Rev. Mol. Cell Biol. 7 (2006) 296-302
10. De Robertis E.M., and Kuroda H. Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu. Rev. Cell Dev. Biol. 20 (2004) 285-308
11. Derynck R., and Zhang Y.E. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425 (2003) 577-584
12. Duan X., Liang Y.Y., Feng X.H., and Lin X. Protein serine/threonine phosphatase PPM1A dephosphorylates Smad1 in the bone morphogenetic protein signaling pathway. J. Biol. Chem. 281 (2006) 36526-36532 10.1074/jbc.M605169200 Published online August 24, 2006
13. Ebisawa T., Fukuchi M., Murakami G., Chiba T., Tanaka K., Imamura T., and Miyazono K. Smurf1 interacts with transforming growth factor-beta type I receptor through Smad7 and induces receptor degradation. J. Biol. Chem. 276 (2001) 12477-12480
14. Favata M.F., Horiuchi K.Y., Manos E.J., Daulerio A.J., Stradley D.A., Feeser W.S., Van Dyk D.E., Pitts W.J., Earl R.A., Hobbs F., et al. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273 (1998) 18623-18632
15. Feng X.H., and Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Annu. Rev. Cell Dev. Biol. 21 (2005) 659-693
16. Gomis R.R., Alarcon C., He W., Wang Q., Seoane J., Lash A., and Massagué J. A FoxO-Smad synexpression group in human keratinocytes. Proc. Natl. Acad. Sci. USA 103 (2006) 12747-12752
17. Grimm O.H., and Gurdon J.B. Nuclear exclusion of Smad2 is a mechanism leading to loss of competence. Nat. Cell Biol. 4 (2002) 519-522
18. Harland R. Neural induction. Curr. Opin. Genet. Dev. 10 (2000) 357-362
19. Harradine K.A., and Akhurst R.J. Mutations of TGFb signaling molecules in human disease. Ann. Med. 38 (2006) 403-414
20. Hata A., Seoane J., Lagna G., Montalvo E., Hemmati-Brivanlou A., and Massagué J. OAZ uses distinct DNA- and protein-binding zinc fingers in separate BMP-Smad and Olf signaling pathways. Cell 100 (2000) 229-240
21. Ingham R.J., Gish G., and Pawson T. The Nedd4 family of E3 ubiquitin ligases: functional diversity within a common modular architecture. Oncogene 23 (2004) 1972-1984
22. Ingham R.J., Colwill K., Howard C., Dettwiler S., Lim C.S., Yu J., Hersi K., Raaijmakers J., Gish G., Mbamalu G., et al. WW domains provide a platform for the assembly of multiprotein networks. Mol. Cell. Biol. 25 (2005) 7092-7106
23. Joyner A.L., Liu A., and Millet S. Otx2, Gbx2 and Fgf8 interact to position and maintain a mid-hindbrain organizer. Curr. Opin. Cell Biol. 12 (2000) 736-741
24. Kang Y., Chen C.R., and Massagué J. A self-enabling TGFbeta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol. Cell 11 (2003) 915-926
25. Katagiri T., Yamaguchi A., Komaki M., Abe E., Takahashi N., Ikeda T., Rosen V., Wozney J.M., Fujisawa-Sehara A., and Suda T. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J. Cell Biol. 127 (1994) 1755-1766
26. Knockaert M., Sapkota G., Alarcon C., Massagué J., and Brivanlou A.H. Unique players in the BMP pathway: small C-terminal domain phosphatases dephosphorylate Smad1 to attenuate BMP signaling. Proc. Natl. Acad. Sci. USA 103 (2006) 11940-11945
27. Kretzschmar M., Doody J., and Massagué J. Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1. Nature 389 (1997) 618-622
28. Kretzschmar M., Doody J., Timokhina I., and Massagué J. A mechanism of repression of TGFbeta/Smad signaling by oncogenic Ras. Genes Dev. 13 (1999) 804-816
29. Lagna G., Hata A., Hemmati-Brivanlou A., and Massagué J. Partnership between DPC4 and SMAD proteins in TGF-beta signalling pathways. Nature 383 (1996) 832-836
30. Lehmann K., Janda E., Pierreux C.E., Rytomaa M., Schulze A., McMahon M., Hill C.S., Beug H., and Downward J. Raf induces TGFbeta production while blocking its apoptotic but not invasive responses: a mechanism leading to increased malignancy in epithelial cells. Genes Dev. 14 (2000) 2610-2622
31. Liang X., Lu Y., Wilkes M., Neubert T.A., and Resh M.D. The N-terminal SH4 region of the Src family kinase Fyn is modified by methylation and heterogeneous fatty acylation: role in membrane targeting, cell adhesion, and spreading. J. Biol. Chem. 279 (2004) 8133-8139
32. Liu A., and Joyner A.L. EN and GBX2 play essential roles downstream of FGF8 in patterning the mouse mid/hindbrain region. Development 128 (2001) 181-191
33. Massagué J., and Chen Y.G. Controlling TGF-beta signaling. Genes Dev. 14 (2000) 627-644
34. Massagué J., Blain S.W., and Lo R.S. TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 103 (2000) 295-309
35. Massagué J., Seoane J., and Wotton D. Smad transcription factors. Genes Dev. 19 (2005) 2783-2810
36. Meier R., Rouse J., Cuenda A., Nebreda A.R., and Cohen P. Cellular stresses and cytokines activate multiple mitogen-activated-protein kinase kinase homologues in PC12 and KB cells. Eur. J. Biochem. 236 (1996) 796-805
37. Neubuser A., Peters H., Balling R., and Martin G.R. Antagonistic interactions between FGF and BMP signaling pathways: a mechanism for positioning the sites of tooth formation. Cell 90 (1997) 247-255
38. Niswander L., and Martin G.R. FGF-4 and BMP-2 have opposite effects on limb growth. Nature 361 (1993) 68-71
39. Pera E.M., Ikeda A., Eivers E., and De Robertis E.M. Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural induction. Genes Dev. 17 (2003) 3023-3028
40. Sapkota G., Knockaert M., Alarcon C., Montalvo E., Brivanlou A.H., and Massagué J. 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 (2006) 40412-40419 10.1074/jbc.M610172200 Published online November 2, 2006
41. Satish L., Blair H.C., Glading A., and Wells A. Interferon-inducible protein 9 (CXCL11)-induced cell motility in keratinocytes requires calcium flux-dependent activation of mu-calpain. Mol. Cell. Biol. 25 (2005) 1922-1941
42. Schaller M.D., Hildebrand J.D., and Parsons J.T. Complex formation with focal adhesion kinase: a mechanism to regulate activity and subcellular localization of Src kinases. Mol. Biol. Cell 10 (1999) 3489-3505
43. Schier A.F., and Talbot W.S. Molecular genetics of axis formation in zebrafish. Annu. Rev. Genet. 39 (2005) 561-613
44. Schohl A., and Fagotto F. Beta-catenin, MAPK and Smad signaling during early Xenopus development. Development 129 (2002) 37-52
45. Seoane J., Le H.V., Shen L., Anderson S.A., and Massagué J. Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 117 (2004) 211-223
46. Shanmugalingam S., Houart C., Picker A., Reifers F., Macdonald R., Barth A., Griffin K., Brand M., and Wilson S.W. Ace/Fgf8 is required for forebrain commissure formation and patterning of the telencephalon. Development 127 (2000) 2549-2561
47. Shi Y., and Massagué J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113 (2003) 685-700
48. Sudol M., and Hunter T. NeW wrinkles for an old domain. Cell 103 (2000) 1001-1004
49. Tsukazaki T., Chiang T.A., Davison A.F., Attisano L., and Wrana J.L. SARA, a FYVE domain protein that recruits Smad2 to the TGFbeta receptor. Cell 95 (1998) 779-791
50. Varga A.C., and Wrana J.L. The disparate role of BMP in stem cell biology. Oncogene 24 (2005) 5713-5721
51. Wang H.R., Zhang Y., Ozdamar B., Ogunjimi A.A., Alexandrova E., Thomsen G.H., and Wrana J.L. Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 302 (2003) 1775-1779
52. Wu J.W., Hu M., Chai J., Seoane J., Huse M., Li C., Rigotti D.J., Kyin S., Muir T.W., Fairman R., et al. Crystal structure of a phosphorylated Smad2. Recognition of phosphoserine by the MH2 domain and insights on Smad function in TGF-beta signaling. Mol. Cell 8 (2001) 1277-1289
53. Xie H., Pallero M.A., Gupta K., Chang P., Ware M.F., Witke W., Kwiatkowski D.J., Lauffenburger D.A., Murphy-Ullrich J.E., and Wells A. EGF receptor regulation of cell motility: EGF induces disassembly of focal adhesions independently of the motility-associated PLCgamma signaling pathway. J. Cell Sci. 111 (1998) 615-624
54. Xu L., Kang Y., Col S., and Massagué J. Smad2 nucleocytoplasmic shuttling by nucleoporins CAN/Nup214 and Nup153 feeds TGFbeta signaling complexes in the cytoplasm and nucleus. Mol. Cell 10 (2002) 271-282
55. Xu L., Alarcon C., Col S., and Massagué J. Distinct domain utilization by Smad3 and Smad4 for nucleoporin interaction and nuclear import. J. Biol. Chem. 278 (2003) 42569-42577
56. Yamashita M., Ying S.X., Zhang G.M., Li C., Cheng S.Y., Deng C.X., and Zhang Y.E. Ubiquitin ligase Smurf1 controls osteoblast activity and bone homeostasis by targeting MEKK2 for degradation. Cell 121 (2005) 101-113
57. Zhang Z., and Cohen D.M. NaCl but not urea activates p38 and jun kinase in mIMCD3 murine inner medullary cells. Am. J. Physiol. 271 (1996) F1234-F1238
58. Zhu H., Kavsak P., Abdollah S., Wrana J.L., and Thomsen G.H. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 400 (1999) 687-693