Direct binding of Smad3 and Smad4 to critical TGFβ-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene

EMBO Journal

Volumn 17, Issue 11, 1998, Pages 3091-3100

  Dennler, Sylviane ^a   Itoh, Susumu ^b   Vivien, Denis ^c   Dijke, Peter Ten ^b   Huet, Stéphane ^a   Gauthier, Jean Michel ^a  

^a Laboratoire GlaxoWellcome   (France)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

^c UNIVERSITÉ DE CAEN   (France)

Author keywords

DNA binding; PAI 1; Smad; TGF ; Transcription

Indexed keywords

BONE MORPHOGENETIC PROTEIN; PLASMINOGEN ACTIVATOR INHIBITOR; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ARTICLE; GENE MUTATION; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ACTIVINS; ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL LINE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HUMANS; INHIBINS; MINK; MUTAGENESIS, SITE-DIRECTED; NUCLEAR PROTEINS; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; SMAD3 PROTEIN; SMAD4 PROTEIN; SMAD7 PROTEIN; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; TUMOR CELLS, CULTURED;

ANIMALIA;

EID: 0032101178     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.11.3091     Document Type: Article

References (59)

1. Abdollah, S., Macias-Silva, M., Tsukazaki, T., Hayashi, H., Attisano, L. and Wrana, J.L. (1997) TβRI phosphorylation of Smad2 on Ser465 and 467 is required for Smad2/Smad4 complex formation and signalling. J. Biol. Chem., 272, 27678-27685.
2. Baker, J.C. and Harland, R.M. (1996) A novel mesoderm inducer, Madr2, functions in the activin signal transduction pathway. Genes Dev., 10, 1880-1889.
3. Chen, X., Rubock, M.J. and Whitman, M. (1996) A transcriptional partner for MAD proteins in TGF-β signalling. Nature, 383, 691-696.
4. Chen, X., Weisberg, E., Fridmacher, V., Watanabe, M. and Whitman, M. (1997) Smad4 and FAST-1 in the assembly of activin-responsive factor. Nature, 389, 85-89.
5. Chen, Y., Lebrun, J.-J. and Vale, W. (1996) Regulation of transforming growth factor β and activin-induced transcription by mammalian Mad proteins. Proc. Natl Acad. Sci. USA, 93, 12992-12997.
6. Chen, Y., Bhushan, A. and Vale, W. (1997) Smad8 mediates the signaling of the receptor senne kinase. Proc. Natl Acad. Sci. USA, 94, 12938-12943.
7. Datto, M., Hu, P., Kowalik, T., Yingling, J. and Wang, X.F. (1997) The viral oncoprotein E1A blocks TGFβ-mediated induction of p21/WAF1/ Cip1 and p15/INK4B. Mol. Cell. Biol., 17, 2030-2037.
8. de Caestecker, M.P., Hemmati, P., Larisch-Bloch, S., Ajimera, R., Roberts, A.B. and Leichleider, R.J. (1997) Characterization of functional domains within Smad4/DPC4. J. Biol. Chem., 272, 13690-13696.
9. de Winter, J.P., Roelen, B.A.J., ten Dijke, P., van der Burg, B. and van den Eijnden-van Raaij, A.J.M. (1997) DPC4 (SMAD4) mediates transforming growth factor-β1 (TGF-β1) induced growth inhibition and transcriptional response in breast tumour cells. Oncogene, 14, 1891-1900.
10. Derynck, R. (1994) TGF-β-receptor-mediated signaling. Trends Biochem. Sci., 19, 548-553.
11. Elbendary, A., Berchuck, A., Davis, P., Havrilesky, L., Bast, R.C., Iglehart, J.D. and Marks, J.R. (1994) TGFβ1 can induce CIP1/WAF1 expression independent of the p53 pathway in ovarian cancer cells. Cell Growth Differ., 5, 1301-1307.
12. Eppert, K. et al. (1996) MADR2 maps to 18q21 and encodes a TGFβ-regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell, 86, 543-552.
13. Graff, J.M., Bansal, A. and Melton, D.A. (1996) Xenopus Mad proteins transduce distinct subsets of signals for the TGFβ superfamily. Cell, 85, 479-487.
14. Hata, A., Lo, R., Woton, D., Lagan, G. and Massagué, J. (1997) Mutations increasing autoinhibition inactivate tumour suppressors Smad2 and Smad4. Nature, 388, 82-87.
15. Hata, A., Lagna, G., Massagué, J. and Hemmati-Brivanlou, A. (1998) Sinado inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev., in press.
16. Hayashi, H. et al. (1997) The MAD-related protein Smad7 associates with the TGFβ receptor and functions as an antagonist of TGFβ signaling. Cell, 89, 1165-1173.
17. Heldin, C.-H., Miyazono, K. and ten Dijke, P. (1997) TGFβ signalling from cell membrane to nucleus via Smad proteins. Nature, 390, 465-471.
18. Hoodless, P.A., Haerry, T., Abdollah, S., Stapleton, M., O'Connor, M.B., Attisano, L. and Wrana, J.L. (1996) MAOR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell, 85, 489-500.
19. Imamura, T., Takase, M., Nishihara, A., Oeda, E., Hanai, J., Kawabata, M. and Miyazono, K. (1997) Smad6 inhibits signalling by the TGF-β superfamily. Nature, 389, 622-626.
20. Inagaki, Y., Truter, S. and Ramirez, F. (1994) TGFβ stimulates α2(I) collagen gene expression through a cis-acting element that contains an Sp1-binding site. J. Biol. Chem., 269, 14828-14834.
21. Keeton, M., Curriden, S., van Zonneveld, A.J. and Loskutoff, D. (1991) Identification of regulatory sequences in the type 1 plasminogen activator inhibitor gene responsive to TGFβ. J. Biol. Chem., 266, 23048-23052.
22. Kim, J., Johnson, K., Chen, H.J., Carrol, S. and Laughon, A. (1997) Drosophila Mad binds to DNA and directly mediates activation of vestigial by Decapentaplegic. Nature, 388, 304-308.
23. Kim, S.-J., Jeang, K.-T., Glick, A., Sporn, M. and Roberts, A. (1989a) Promoter sequences of the human transforming growth factor-β1 gene responsive in transforming growth factor-β1 autoinduction. J. Biol. Chem., 264, 7041-7045.
24. Kim, S.-J., Dennhez, F., Kim, K.-Y., Holt, J., Sporn, M. and Roberts, A. (1989b) Activation of the second promoter of the TGFβ1 gene by TGFβ1 and phorbol ester occurs through the same target sequence. J. Biol. Chem., 264, 19373-19378.
25. Kretzschmar, M. and Massagué, J. (1998) SMADs: mediators and regulators of TGF-β signaling. Curr. Opin. Genet. Dev., 8, 103-111.
26. Kretzschmar, M., Liu, F., Hata, A., Doody, J. and Massagué, J. (1997) The TGF-β family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev., 11, 984-995.
27. Lagna, G., Hata, A., Hemmati-Brivanlou, A. and Massagué, J. (1996) Partnership between DPC4 and SMAD proteins in TGF-β signalling pathways. Nature, 383, 832-836.
28. Li, J.-M., Nichols, M.A., Chandrasekharan, S., Xiong, Y. and Wang, X.-F. (1995) Transforming growth factor β activates the promoter of cyclin-dependent kinase inhibitor p15INK4B through an Sp1 consensus site. J. Biol. Chem., 270, 26750-26753.
29. Lin, Y.C. and Stavnezer, J. (1992) Regulation of transcription of the germ-line Igα constant region gene by an ATF element and by novel TGFβ1-responsive elements. J. Immunol., 149, 2914-2925.
30. Liu, F., Hata, A., Baker, J.C., Doody, J., Carcamo, J., Harland, R.M. and Massagué, J. (1996) A human Mad protein acting as a BMP-regulated transcriptional activator. Nature, 381, 620-623.
31. Liu, F., Pouponnot, C. and Massagué, J. (1997) Dual role of the Smad4/ DPC4 tumor suppressor in TGFβ-inducible transcriptional complexes. Genes Dev., 11, 3157-3167
32. Macias-Silva, M., Abdollah, S., Hoodless, P.A., Pirone, R., Attisano, L. and Wrana, J.L. (1996) MADR2 is a substrate of the TGFβ receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell, 87, 1215-1224.
33. Massagué, J. and Weis-Garcia, F. (1996) Serine/threonine kinase receptors: mediators of transforming growth factor β signals. Cancer Surv., 27, 41-64.
34. Meersseman, G. et al. (1997) The C-terminal domain of Mad-like signal transducers is sufficient for biological activity in the Xenopus embryo and transcriptional activation. Mech. Dev., 61, 127-140.
35. Nakao, A. et al. (1997a) Identification of Smad7, a TGFβ-inducible antagonist of TGFβ signalling. Nature, 389, 631-635.
36. Nakao, A. et al. (1997b) TGF-β receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J., 16, 5353-5362.
37. Newfeld, S.J., Chartoff, E.H., Graff, J.M., Melton, D.A. and Gelbart, W.M. (1996) Mothers against dpp encodes a conserved cytoplasmic protein required in DPP/TGF-β responsive cells. Development, 122, 2099-2108.
38. Newfeld, S.J., Mehra, A., Singer, M.A., Wrana, J.L., Attisano, L and Gelbart, W.M. (1997) Mothers against dpp participates in a DPP/TGF-β responsive serine-threonine kinase signal transduction cascade. Development, 124, 3167-3176.
39. Riccio, A., Pedone, P., Lund, L., Olesen, T., Steen Olsen, H. and Andreasen, P. (1992) TGFβ1-responsive element: closely associated binding sites for USF and CCAAT-binding transcription factor-Nuclear Factor I in the type 1 plasminogen activator inhibitor gene. Mol. Cell. Biol., 12, 1846-1855.
40. Roberts, A.B. and Sporn, M.B. (1993) Physiological actions and clinical applications of transforming growth factor-β (TGF-β). Growth Factors, 8, 1-9.
41. Sadowski, H.B. and Gilman, M.Z. (1993) Cell-free activation of a DNA-binding protein by EGF. Nature, 362, 79-83.
42. Savage, C., Das, P., Finelli, A.L., Townsend, S.R., Sun, C.-Y., Baird, S.E. and Padgett, R.W. (1996) Caenorhabditis elegans genes sma-2, sma-3, and sma-4 define a conserved family of transforming growth factor β pathway components. Proc. Natl Acad. Sci. USA, 93, 790-794.
43. Sekelsky, J.J., Newfeld, S.J., Raftery, L.A., Chartoff, E.H. and Gelbart, W.M. (1995) Genetic characterization and cloning of Mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics, 139, 1347-1358.
44. Shi, Y., Hata, A., Lo, R., Massagué, J. and Pavletich, N. (1997) A structural basis for mutational inactivation of the tumor suppressor Smad4. Nature, 388, 87-93.
45. Souchelnytskyi, S., Tamaki, K., Engström, U., Wernstedt, C., ten Dijke, P., Heldin, C.-H. (1997) Phosphorylation of Ser465 and Ser467 in the C-terminus of Smad2 mediates interaction with Smad4 and is required for TGF-β signalling. J. Biol. Chem., 272, 28107-28115.
46. Suzuki, A., Chang, C., Yingling, J.M., Wang, X.-F. and Hemmati-Brivanlou, A. (1997) Smad5 induces ventral fates in Xenopus embryo. Dev. Biol., 184, 402-405.
47. Thomsen, G.H. (1996) Xenopus mothers against decapentaplegic is an embryonic ventralizing agent that acts downstream of the BMP-2/4 receptor. Development, 122, 2359-2366.
48. Westerhausen, D., Hopkins, W. and Billadello, J. (1991) Multiple TGFβ-inducible elements regulate expression of plasminogen activator inhibitor type-1 gene in HepG2 cells. J. Biol. Chem., 266, 1092-1100.
49. Wiersdorff, V., Lecuit, T., Cohen, S.M. and Mlodzik, M. (1996) Mad acts downstream of Dpp receptors, revealing a differential requirement for dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye. Development, 122, 2153-2162.
50. Wieser, R., Wrana, J.L. and Massagué, J. (1995) GS domain mutations that constitutively activate TβR-I. the downstream signaling component in the TGF-β receptor complex. EMBO J., 14, 2199-2208.
51. Wrana, J.L., Attisano, L., Carcamo, J., Zentella, A., Doody, J., Laiho, M., Wang, X.-F. and Massagué, J. (1992) TGFβ signals through a heteromeric protein kinase receptor complex. Cell, 71, 1003-1014.
52. Wrana, J.L., Attisano, L., Wieser, R., Ventura, F. and Massagué, J. (1994) Mechanism of activation of the TGF-β receptor. Nature, 370, 341-347.
53. Wu, R.-Y., Zhang, Y., Feng, X.-H. and Derynck, R. (1997) Heteromeric and homomeric interactions correlate with signaling activity and functional cooperativity of Smad3 and Smad4/DPC4. Mol. Cell. Biol., 17, 2521-2528.
54. Yamashita, H., ten Dijke, P., Huylebroeck, D., Sampah, T.K., Andries, M., Smith, J.C., Heldin, C.-H. and Miyazono, K. (1995) Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J. Cell Biol., 130, 217-226.
55. Yingling, J.M., Das, P., Savage, C., Zhang, M., Padgett, R.W. and Wang, X.-F. (1996) Mammalian dwarfins are phosphorylated in response to transforming growth factor β and are implicated in control of cell growth. Ptoc. Natl Acad. Sci. USA, 93, 8940-8944.
56. Yingling, J.M., Datto, M.B., Wong, C., Frederick, J.P., Liberati, N.T. and Wang, X.-F. (1997) Tumor suppressor Smad4 is a transforming growth factor β-inducible DNA binding protein. Mol. Cell. Biol., 17, 7019-7028.
57. Zawel, L., Dai, J.L., Buckhaults, P., Zhou, P., Kinzler, K., Vogelstein, B. and Kern, S.E (1998) Human Smad3 and Smad4 are sequence-specific transcription activators. Mol. Cell, 1, 611-617.
58. Zhang, Y., Feng, X.-H., Wu, R.-Y. and Derynck, R. (1996) Receptor-associated Mad homologues synergize as effectors of the TGFβ response. Nature, 383, 168-172.
59. Zhang, Y., Musci, T. and Derynck, R. (1997) The tumor suppressor Smad4/ DPC4 as a central mediator of Smad function. Curr. Biol., 7, 270-276.