A function of CBP as a transcriptional co-activator during Dpp signalling

EMBO Journal

Volumn 18, Issue 6, 1999, Pages 1630-1641

  Waltzer, Lucas ^a   Bienz, Mariann ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

CBP; Dpp; Mad; TGF ; Transcription

Indexed keywords

DNA BINDING PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DROSOPHILA; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

EID: 0033559973     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.6.1630     Document Type: Article

References (84)

1. Affolter, M., Nellen, D., Nussbaumer, U. and Basler, K. (1994) Multiple requirements for the TGF-β receptor serine/threonine kinase thick veins reveal novel functions of TGF-β homologs during Drosophila embryogenesis. Development, 120, 3105-3117.
2. Akimura, H., Chen, Y., Dai, P., Hou, D.-X., Nonaka, M., Smolik, S., Armstrong, S., Goodman, R.H. and Ishii, S. (1997a) Drosophila CBP is a co-activator of cubitus interruptus in hedgehog signalling. Nature, 386, 735-738.
3. Akimura, H., Hou, D.-X. and Ishii, S. (1997b) Drosophila CBP is required for dorsal-dependent twist gene expression. Nature Genet., 17, 211-214.
4. Arias, J., Alberts, A.S., Brindle, P., Claret, F.X., Smeal, T., Karin, M., Feramisco, J. and Montminy, M. (1994) Activation of cAMP and mitogen responsive genes relics on a common nuclear factor. Nature, 370, 226-229.
5. Bienz, M. (1997) Endoderm induction in Drosophila: the nuclear targets of the inducing signals. Curr. Opin. Genet. Dev., 7, 683-688.
6. Bienz, M. (1998) TCF: transcriptional activator or repressor? Curr. Opin. Cell Biol., 10, 366-372.
7. Borrow, J. et al. (1996) The translocation t (8;16) (p11;p13) of acute myeloid leukaemia fuses a putative acetyltransferase to the CREB-binding protein. Nature Genet., 14, 33-41.
8. Brand, A.H. and Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development, 118, 401-415.
9. D1] dominant female-sterile insertions in Drosophila and their use in generating germ-line chimeras. Development, 119, 1359-1369.
10. Clifford, R.J. and Schüpbach, T. (1989) Coordinately and differentially mutable activities of torpedo, the Drosophila melanogaster homolog of the vertebrate EGF receptor gene. Genetics, 123, 771-787.
11. Das, P., Maduzia, L.L., Wang, H., Finelli, A.L., Cho, S.-H., Smith, M.M. and Padgett, R.W. (1998) The Drosophila gene Medea demonstrates the requirement for different classes of Smads in dpp signaling. Development, 125, 1519-1528.
12. Díaz-Benjumea, F.J. and García-Bellido, A. (1990) Behaviour of cells mutant for an EGF receptor homologue of Drosophila in genetic mosaics. Proc. R. Soc. Lond. B, 242, 36-44.
13. Díaz-Benjumea, F.J. and Hafen, E. ( 1994) The sevenless signalling cassette mediates Drosophila EGF receptor function during epidermal development. Development, 120, 569-578.
14. Doctor, J.S., Jackson, P.D., Rashka, K.E., Visalli, M. and Hoffmann, F.M. (1992) Sequence, biochemical characterization and developmental expression of a new member of the TGF-β superfamily in Drosophila melanogaster. Dev. Biol., 151, 491-505.
15. Eckner, R., Ewen, M.E., Newsome, D., Gerdes, M., DeCaprio, J.A., Lawrence, J.B. and Livingston, D.M. (1994) Molecular cloning and functional analysis of the adenovirus E1A-associated 300-kD protein (p300) reveals a protein with properties of a transcriptional adaptator. Genes Dev., 7, 869-884.
16. Eckner, R., Yao, T.P., Oldread, E. and Livingston, D.M. (1996) Interaction and functional collaboration of p300/CBP and bHLH proteins in muscle and B-cell differentiation. Genes Dev., 10, 2478-2490.
17. Eresh, S., Riese, J., Jackson, D.B., Bohmann, D. and Bienz, M. (1997) A CREB binding site as target for decapentaplegic signalling during Drosophila endoderm induction. EMBO J., 16, 2014-2022.
18. Feng, X.-H., Zhang, Y., Wu, R.-Y. and Derynck, R. (1998) The tumor suppressor Smad4/DPC4 and transcriptional adaptator CBP/p300 are coactivators for Smad3 in TGF-β-induced transcriptional activation. Genes Dev., 12, 2153-2163.
19. Ferguson, E.L. and Anderson, K.V. (1992) decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell, 71, 451-461.
20. Frasch, M. (1995) Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature, 374, 464-467.
21. Goldman, P.S., Tran, V.K. and Goodman, R.H. (1997) The multifunctional role of the co-activator CBP in transcriptional regulation. Recent Prog. Horm. Res., 52, 103-119.
22. Green, J.B. and Smith, J.C. (1990) Graded changes in dose of a Xenopus activin A homologue elicit stepwise transition in embryonic cell fate. Nature, 347, 391-394.
23. Green, J.B.A., New, H.V. and Smith, J.C. (1992) Responses of embryonic Xenopus cells to activin and FGF are separated by multiple dose thresholds and correspond to distinct axes of the mesoderm. Cell, 71, 731-739.
24. Gurdon, J.B., Harger, P., Mitchell, A. and Lemaire, P. (1994) Activin signalling and response to a morphogen gradient. Nature, 371, 487-492.
25. 1 and S phase protein phosphatase that associates with Cdk2. Cell, 75, 791-803.
26. Heldin, C.-H., Miyazono, K. and ten Djike, P. (1997) TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature, 390, 465-471.
27. Hoodless, P., Haerry, T., Abdollah, S., Stapleton, M., O'Connor, M., Attisano, L. and Wran, J. (1996) MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell, 85, 489-500.
28. Hoppler, S. and Bienz, M. (1994) Specification of a single cell type by a Drosophila homeotic gene. Cell, 76, 689-702.
29. Hoppler, S. and Bienz, M. (1995) Two different thresholds of wingless signalling with distinct developmental consequences in the Drosophila midgut. EMBO J., 14, 5016-5026.
30. Hursh, D.A., Padgett, R.W. and Gelbart, W.M. (1993) Cross regulation of decapentaplegic and Ultrabithorax transcription in the embryonic visceral mesoderm of Drosophila. Development, 117, 1211-1222.
31. Ida, K., Kitabayashi, I., Taki, T., Taniwaki, M., Noro, K., Yamamoto, M., Ohki, M. and Hayashi, Y. (1997) Adenoviral E1A-associated protein p300 is involved in acute myeloid leukaemia with t (11;22). Blood, 90, 4699-4704.
32. Immerglück, K., Lawrence, P.A. and Bienz, M. (1990) Induction across germ layers in Drosophila mediated by a genetic cascade. Cell, 62, 261-268.
33. Irish, V.F. and Gelbart, W.M. (1987) The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo. Genes Dev., 1, 868-879.
34. Janknecht, R. and Hunter, T. (1996) A growing coactivator network. Nature, 383, 22-23.
35. Janknecht, R., Wells, N.J. and Hunter, T. (1998) TGF-β-stimulated cooperation of Smad proteins with the coactivators CBP/p300. Genes Dev., 12, 2114-2119.
36. Kamei, Y. et al. (1996) A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors. Cell, 85, 403-414.
37. Khalsa, O., Yoon, J.W., Torres-Schumann, S. and Wharton, K.A. (1998) TGF-β/BMP superfamily members, Gbb-60A and Dpp, cooperate to provide pattern information and establish cell identity in the Drosophila wing. Development, 125, 2723-2734.
38. Kim, J., Johnson, K., Chen, H.J., Carroll, S. and Laughon, A. (1997) MAD binds to DNA and directly mediates activation of vestigial by Dpp. Nature, 388, 304-308.
39. Kingsley, D.M. (1994) The TGF-β superfamily: new members, new receptors and new genetic tests of function in different organisms. Genes Dev., 8, 133-146.
40. Klämbt, C., Glazer, L. and Shilo, B.-Z. (1992) breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes Dev., 6, 1668-1678.
41. Kwok, R.P., Lundblad, J.R., Chrivia, J.C., Richards, J.P., Bachinger, H.P., Brennan, R.G., Roberts, S.G., Green, M.R. and Goodman, R.H. (1994) Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature, 370, 223-226.
42. Lecuit, T., Brook, W.J., Ng, M., Calleja, M., Sun., H. and Cohen, S.M. (1996) Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature, 381, 387-393.
43. 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.
44. Liu, F., Pouponnot, C. and Massagué, J. (1997) Dual role of the Smad4/ DPC4 tumor suppressor in TGF-β-inducible transcriptional complexes. Genes Dev., 11, 3157-3167.
45. Llimargas, M. and Casanova, J. (1997) ventral veinless, a POU domain transcription factor, regulates different transduction pathways required for tracheal branching in Drosophila. Development, 124, 3273-3281.
46. Massagué, J. (1998) TGF-β signal transduction. Annu. Rev. Biochem., 67, 753-791.
47. Muraoka, M., Konishi, M., Kikuchi-Yanoshita, R., Tanaka, K., Shitara, N., Chong, J.-M., Iwama, T. and Miyaki, M. (1996) p300 gene alterations in colorectal and gastric carcinomas. Oncogene, 12, 1565-1569.
48. Nellen, D., Burke, R., Struhl, G. and Basler, K. (1996) Direct and longrange action of a Dpp morphogen gradient. Cell, 85, 357-368.
49. Newfeld, S., Chartoff, E., Graff, J., Melton, D. and Gelbart, W.M. (1996) Mothers against dpp encodes a conserved cytoplasmic protein required in DPP/TGF-β responsive cells. Development, 122, 3099-2108.
50. Newfeld, S., Mehra, A., Singer, M., Wrana, J., 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.
51. Padgett, R.W., St Johnston, R.D. and Gelbart, W.M. (1987) A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-β family. Nature, 325, 81-84.
52. Panganiban, G.E.F., Reuter, R., Scott, M.P. and Hoffmann, F.M. (1990) A Drosophila growth factor homolog, decapentaplegic, regulates homeotic gene expression within and across germ layers during midgut morphogenesis. Development, 110, 1041-1050.
53. Petrij, F. et al. (1995) Rubinstein-Taybi syndrome caused by mutations in the transcriptional co-activator CBP. Nature, 376, 348-351.
54. Raftery, L.A., Twombly, V., Wharton, K. and Gelbart, W.M. (1995) Genetic screens to identify elements of the decapentaplegic pathway in Drosophila. Genetics, 139, 241-254.
55. Reuter, R., Panganiban, G.E.F., Hoffmann, F.M. and Scott, M.P. (1990) Homeotic genes regulate the expression of putative growth factors in the visceral mesoderm of Drosophila embryos. Development, 110, 1031-1040.
56. Riese, J., Tremml, G. and Bienz, M. (1997a) D-Fos, a target gene for Decapentaplegic signalling with a critical role during Drosophila endoderm induction. Development, 124, 3353-3361.
57. Riese, J., Yu, X., Munnerlyn, A., Eresh, S., Grosschedl, R. and Bienz, M. (1997b) LEF-1, a nuclear factor coordinating signaling inputs from wingless and decapentaplegic. Cell, 88, 777-787.
58. Rusch, J. and Levine, M. (1997) Regulation of a dpp target gene in the Drosophila embryo. Development, 124, 303-311.
59. Sanson, B., White, P. and Vincent, J.-P. (1996) Uncoupling cadherin-based adhesion from wingless signalling in Drosophila. Nature, 383, 627-630.
60. Segal, D. and Gelbart, W.M. (1985) Shortvein, a new component of the decapentaplegic gene complex in Drosophila melanogaster. Genetics, 109, 119-143.
61. Sekelsky, J.J., Newfeld, S.J., Raftery, L.A., Chartoff, E.H. and Padgett, R.W. (1995) Genetic characterization and cloning of Mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics, 139, 1347-1358.
62. Sobulo, O.M. et al. (1997) MLL is fused to CBP, a histone acetyltransferase, in therapy-related acute myeloid leukaemia with a t (11;16) (q23;p13.3). Proc. Natl Acad. Sci. USA, 94, 8732-8737.
63. Spencer, F.A., Hoffmann, F.M. and Gelbart, W.M. (1982) Decapentaplegic, a gene complex affecting morphogenesis in Drosophila melanogaster. Cell, 28, 451-461.
64. St Johnston, R.D., Hoffmann, F.M., Blackman, R.K., Segal, D., Grimaila, R., Padgett, R.W., Irish, H.A. and Gelbart, W.M. (1990) Molecular organization of the decapentaplegic gene in Drosophila melanogaster. Genes Dev., 4, 1114-1127.
65. Staehling-Hampton, K. and Hoffmann, F.M. (1994) Ectopic decapentaplegic in the Drosophila midgut alters the expression of five homeotic genes, dpp and wingless, causing specific morphological defects. Dev. Biol., 164, 502-512.
66. Staehling-Hampton, K., Hoffmann, F.M., Baylies, M.K., Rushton, E. and Bate, M. (1994) Dpp induces mesodermal gene expression in Drosophila. Nature, 372, 783-791.
67. Sun, B., Hursh, D.A, Jackson, D. and Beachy, P.A. (1995) Ultrabithorax protein is necessary but not sufficient for full activation of decapentaplegic expression in the visceral mesoderm. EMBO J., 14, 520-535.
68. Sutherland, D., Samakovlis, C. and Krasnow, M.A. (1996) branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell, 87, 1091-1101.
69. Szüts, D., Eresh, S. and Bienz, M. (1998) Functional intertwining of Dpp and EGFR signaling during Drosophila endoderm induction. Genes Dev., 12, 2022-2035.
70. Tatei, K., Cai, H., Ip, Y.T. and Levine, M. (1995) Race: a Drosophila homologue of the angiotensin converting enzyme. Mech. Dev., 51, 147-168.
71. Thüringer, F. and Bienz, M. (1993) Indirect autoregulation of a homeotic Drosophila gene mediated by extracellular signalling. Proc. Natl Acad. Sci. USA, 90, 3899-3903.
72. Thüringer, F., Cohen, S.M. and Bienz, M. (1993) Dissection of an indirect autoregulatory response of a homeotic Drosophila gene. EMBO J., 12, 2419-2430.
73. Topper, J.N., DiChiara, M.R., Brown, J.D., Williams, A.J., Falb, D., Collins, T. and Gimbrone, M.A.,Jr (1998) CREB binding protein is a required coactivator for Smad-dependent, transforming growth factor-β transcriptional responses in endothelial cells. Proc. Natl Acad. Sci. USA, 95, 9506-9511.
74. Twombly, V., Blackman, R.K., Jin, H., Padgett, R .W. and Gelbart W.M . (1996) The TGF-β signaling pathway is required in Drosophila oogenesis. Development, 122, 1555-1565.
75. Vincent, S., Ruberte, E., Grieder, N.C., Chen, C.-K., Haerry, T., Schuh, R. and Affolter, M. (1997) DPP controls tracheal cell migration along the dorsoventral body axis of the Drosophila embryo. Development, 124, 2741-2750.
76. Waltzer, L. and Bienz, M. (1998) Drosophila CBP represses the transcription factor TCF to antagonize Wingless signalling. Nature, 395, 521-525.
77. Wappner, P., Gabay, L. and Shilo, B.-Z. (1997) Interaction between the EGF receptor and DPP pathways establish distinc cell fates in the tracheal placodes. Development, 124, 4707-416.
78. 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 Drosophila eye. Development, 122, 2153-2162.
79. Xu, X., Yin, Z., Hudson, J.B., Fergusson, E.L. and Frasch, M. (1998) Smad proteins act in combination with synergistic and antagonistic regulators to target Dpp responses to the Drosophila mesoderm. Genes Dev., 12, 2354-2370.
80. Yao, T.-P. et al. (1998) Gene dosage-dependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell, 93, 361-372.
81. 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.
82. Yu, X., Hoppler, S., Eresh, S. and Bienz, M. (1996) Decapentaplegic, a target gene of the wingless signalling pathway in the Drosophila midgut. Development, 122, 849-858.
83. Yu, X., Riese, J., Eresh, S. and Bienz, M. (1998) Transcriptional repression due to high levels of Wingless signalling. EMBO J., 17, 7021-7032.
84. Zhang, Y., Feng, X.H. and Derynck, R. (1998) Smad3 and Smad4 cooperate with c-Jun/c-Fos to mediate TGF-β-induced transcription. Nature, 394, 909-913.