A CREB-binding site as a target for decapentaplegic signalling during Drosophila endoderm induction

EMBO Journal

Volumn 16, Issue 8, 1997, Pages 2014-2022

  Eresh, Salih ^a   Riese, Jens ^a   Jackson, David B ^b   Bohmann, Dirk ^b   Bienz, Mariann ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

CREB; Dpp signalling pathway; Drosophila; Midgut; Transcription

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; BINDING SITE; CELL NUCLEUS; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; ENHANCER REGION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HOMEOBOX; MESODERM; NONHUMAN; PRIORITY JOURNAL; REPORTER GENE; SIGNAL TRANSDUCTION;

ACTIVATING TRANSCRIPTION FACTOR 1; ANIMALS; BINDING SITES; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DIGESTIVE SYSTEM; DNA FOOTPRINTING; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYONIC INDUCTION; ENDODERM; ENHANCER ELEMENTS (GENETICS); HOMEODOMAIN PROTEINS; INSECT PROTEINS; MESODERM; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTORS;

EID: 0030897846     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.8.2014     Document Type: Article

References (75)

1. Abel, T., Bhatt, R. and Maniatis, T. (1992) A Drosophila CREB/ATF transcriptional activator binds to both fat body- and liver-specific regulatory elements. Genes Dev., 6, 466-480.
2. Andrew, D.J., Horner, M.A., Petitt, M.G., Smolik, S.M. and Scott, M.P. (1994) Setting limits on homeotic gene function: restraint of Sex combs reduced activity by teashirt and other homeotic genes. EMBO J., 13, 1132-1144.
3. Arora, K., Dai, H., Kazuko, S.G., Jamal, J., O'Connor, M.B., Letsou, A. and Warrior, R. (1995) The Drosophila schnurri gene acts in the Dpp/TGFβ signaling pathway and encodes a transcription factor homologous to the human MBP family. Cell, 81, 781-790.
4. Bienz, M. (1994) Homeotic genes and positional signalling in the Drosophila viscera. Trends Genet., 10, 22-26.
5. Biggin, M.D. and Tjian, R. (1988) Transcription factors that activate the Ultrabithorax promoter in developmentally staged extracts. Cell, 53, 699-711.
6. Bohmann, D., Ellis, M.C., Staszewski, L.M. and Mlodzik, M. (1994) Drosophila Jun mediates Ras-dependent photoreceptor determination. Cell, 78, 973-986.
7. 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.
8. Brand, A.H., Manoukian, A. and Perrimon, N. (1994) Ectopic expression in Drosophila. In Goldstein, L. and Fyrberg, E. (eds), Drosophila melanogaster: Practical Uses in Cell Biology. Academic Press, San Diego, CA, Vol. 44, pp. 635-654.
9. Busturia, A. and Bienz, M. (1993) Silencers in the Drosophila homeotic gene Abdominal-B. EMBO J., 12, 1415-1425.
10. Carlsson, R. Waterman, M.L. and Jones, K.A. (1993) The hLEF/TCF-1α HMG protein contains a context-dependent transcriptional activation domain that induces the TCRα enhancer in T cells. Genes Dev., 7, 2418-2430.
11. Cavener, D.R. (1987) Comparison of the consensus sequence flanking the translational start sites in Drosophila and vertebrates Nucleic Acids Res., 15, 1353-1361.
12. Chrivia, J.C., Kwok, R.P., Lamb, N., Hagiwara, M., Montminy, M.R. and Goodman, R.H. (1993) Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature, 365, 855-859.
13. de Groot, R.P., den Hertog, J., Vandenheede, J.R., Goris, J. and Sassone-Corsi, P. (1993) Multiple and cooperative phosphorylation events regulate the CREM activator function. EMBO J., 12, 3903-3911.
14. 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.
15. Foulkes, N.S., Borrelli, E. and Sassone-Corsi, P. (1991) CREM gene: use of alternative DNA-binding domains generates multiple antagonists of cAMP-induced transcription. Cell, 64, 739-749.
16. Frasch, M. (1995) Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature, 374, 464-467.
17. Giese, K. and Grosschedl, R. (1993) LEF-1 contains an activation domain that stimulates transcription only in a specific context of factor-binding sites. EMBO J., 12, 4667-4676.
18. Ginty, D.D., Bonni, A. and Greenberg, M.E. (1994) Nerve growth factor activates a Ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB. Cell, 77, 713-725.
19. Gonzales, G.A. and Montminy, M.R. (1989) Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell, 59, 675-680.
20. Green, J.B.A. and Smith, J.C. (1990) Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature, 347, 391-394.
21. 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.
22. Grieder, N.C., Nellen, D., Burke, R., Basler, K. and Affolter, M. (1995) Schnurri is required for Drosophila Dpp signaling and encodes a zinc finger protein similar to the mammalian transcription factor PRDII-BF1. Cell, 81, 791-800.
23. Gurdon, J.B., Harger, P., Mitchell, A. and Lemaire, P. (1994) Activin signalling and response to a morphogen gradient. Nature, 371, 487-492.
24. Hai, T. and Curran, T. (1991) Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc. Natl Acad. Sci. USA, 88, 3720-3724.
25. Hai, T., Liu, F., Coukos, W.J. and Green, M.R. (1989) Transcription factor ATF cDNA clones: an extensive family of leucine zipper proteins able to selectively form DNA-binding heterodimers. Genes Dev., 3, 2083-2090.
26. Hemmati-Brivanlou, A. and Melton, D.A. (1992) Truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos. Nature, 359, 609-614.
27. Hoeffler, J.P, Meyer, T.E., Yun, Y., Jameson, J.L. and Habener, J.F. (1988) Cyclic AMP-responsive DNA-binding protein: structure based on a cloned placental cDNA. Science, 242, 1430-1433.
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. Immerglück, K., Lawrence, P.A. and Bienz, M. (1990) Induction across germ layers in Drosophila mediated by a genetic cascade. Cell, 62, 261-268.
32. 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.
33. Jessel, T.J. and Melton, D.A. (1992) Diffusible factors in vertebrate embryonic induction. Cell, 68, 257-270.
34. Jiang, J. and Struhl, G. (1995) Protein kinase A and hedgehog signaling in Drosophila limb development. Cell, 80, 563-572.
35. Kramer, I.M., Koornneef, I., de Laat, S.W. and van den Eijnden-van Raaij, A.J.M. (1991) TGF-β1 induces phosphorylation of the cyclic AMP responsive element binding protein in ML-CCI64 cells. EMBO J., 10, 1083-1089.
36. Lalli, E. and Sassone-Corsi, P. (1994) Signal transduction and gene regulation: the nuclear response to cAMP. J. Biol. Chem., 269, 17359-17362.
37. Lawrence, P.A. and Struhl, G. (1996) Morphogens, compartments, and patterns: lessons from Drosophila? Cell, 85, 951-961.
38. 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.
39. Lee, C.Q., Yun, Y.D., Hoeffler, J.P. and Habener, J.F. (1990) Cyclic-AMP-responsive transcriptional activation of CREB-327 involves interdependent phosphorylated subdomains. EMBO J., 9, 4455-4465.
40. Li, W., Ohlmeyer, J.T., Lane, M.E. and Kalderon, D. (1995) Function of protein kinase A in hedgehog signal transduction and Drosophila imaginai disc development. Cell, 80, 553-562.
41. Lloyd, A., Yancheva, N. and Wasylyk, B. (1991) Transformation suppressor activity of a jun transcription factor lacking its activation domain Nature, 352, 635-638.
42. Masquilier, D. and Sassone-Corsi, P. (1992) Transcriptional cross-talk: nuclear factors CREM and CREB bind to AP-1 sites and inhibit activation by Jun. J. Biol. Chem., 267, 22460-22466.
43. Massagué, J. (1996) TGF-β signaling: receptors, transducers and Mad proteins. Cell, 85, 947-950.
44. Montminy, M.R., Sevarino, K.A., Wagner, J.A., Mandel, G. and Goodman, R.H. (1986) Identification of a cyclic-AMP-responsive element within the rat somatostatin gene. Proc. Natl Acad. Sci. USA, 83, 6682-6686.
45. Nellen, D., Burke, R., Struhl, G. and Basler, K. (1996) Direct and long-range action of a DPP morphogen gradient. Cell, 85, 357-368.
46. 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.
47. Niswander, L., Jeffrey, S., Martin, G.R. and Tickle, C. (1994) A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature, 371, 609-612.
48. Noordermeer, J., Johnston, P., Rijsewijk, F., Nusse, R. and Lawrence, P.A. (1992) The consequences of ubiquitous expression of the wingless gene in the Drosophila embryo. Development, 116, 711-719.
49. 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.
50. 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.
51. Perkins, K.K., Admon, A., Patel, N. and Tijan, R. (1990) The Drosophila Fos-related AP-1 protein is a developmentally regulated transcription factor. Genes Dev., 4, 822-834.
52. Peverali, F.A., Isaksson, A., Papavassiliou, A.G., Staszewski, L.M., Mlodzik, M. and Bohmann, D. (1996) Phosphorylation of Drosophila Jun by the MAP kinase Rolled during R7 photoreceptor differentiation EMBO J., 15, 3943-3950.
53. Ptashne, M. (1986) A Genetic Switch. Cell Press & Blackwell Scientific Publications.
54. 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.
55. Riese, J., Yu, X., Munnerlyn, A., Eresh, S., Hsu, S.-C., Grosschedl, R. and Bienz, M. (1997) LEF-1, a nuclear factor coordinating signalling inputs from wingless and decapentaplegic. Cell, in press.
56. Saari, G. and Bienz, M. (1987) The structure of the Ultrabithorax promoter of Drosophila melanogaster. EMBO J., 6, 1775-1779.
57. Small, S., Kraut, R., Hoey, T. Warrior, R. and Levine, M. (1991) Transcriptional regulation of a pair-rule stripe in Drosophila. Genes Dev., 5, 827-839.
58. Smith, J.C. (1994) Mesoderm-inducing factors in early vertebrate development. EMBO J., 12, 4463-1470.
59. Smith, J.C., Price, B.M.J., Van Nimmen, K. and Huylebroeck, D. (1990) Identification of a potent Xenopus mesoderm inducing factor as activin A. Nature, 345, 729-731.
60. Smolik, S.M., Rose, R.E. and Goodman, R.H. (1992) A cyclic AMP-responsive element-binding transcriptional activator in Drosophila melanogaster, dCREB-A, is a member of the leucine zipper family. Mol. Cell. Biol., 12, 4123-1131.
61. Staehling-Hampton, K. and Hoffmann, F.M. (1994) Ectopic decapentaplegic in the Drosophila midgut alters the expression of live homeotic genes, dpp, and wingless, causing specific morphological defects. Dev. Biol., 164, 502-512.
62. 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.
63. St Johnston, R.D. and Gelbart, W.M. (1987) Decapentaplegic transcripts are localised along the dorsal-ventral axis of the Drosophila embryo. EMBO J., 6, 2785-2791.
64. Studier, F.W., Rosenberg, A.H., Dunn, J.J. and Dubendorff, J.W. (1990) Use of T7 polymerase to direct expression of cloned genes. Methods Enzymol., 185, 60-89.
65. 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.
66. 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.
67. 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.
68. Tremml, G. (1991) Interaktionen homeotischer Gene in inneren Keimblättern des Drosophila Embryos. Ph.D. Thesis, University of Zürich.
69. Tremml, G. and Bienz, M. (1992) Induction of labial expression in the Drosophila endoderm: response elements for dpp signalling and for autoregulation. Development, 116, 447-456.
70. Usui, T., Smolik, S.H. and Goodman, R.H. (1993) Isolation of Drosophila CREB-B: a novel CRE-binding protein. DNA Cell. Biol., 12, 589-595.
71. van Dam, H., Duyndam, M., Rottier, R., Bosch, A., de Vries-Smits, L., Herrlich, P., Zantema, A., Angel, P. and van der Eb, A.J. (1993) Heterodimer formation of cJun and ATF-2 is responsible for induction of c-jun by the 243 aminoacid adenovirus E1A protein. EMBO J., 12, 479-487.
72. van den Heuvel, M., Nusse, R., Johnston, P. and Lawrence, P.A. (1989) Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication. Cell, 59, 739-749.
73. Yin, J.C.P., Wallah, J.S., Wilder, E.L., Klingensmith, J., Dang, D., Perrimon, N., Zhou, H., Tully, T. and Quinn, W.G. (1995) A Drosophila CREB/CREM homolog encodes multiple isoforms, including a cyclic AMP-dependent kinase-responsive transcriptional activator and antagonist. Mol. Cell. Biol., 15, 5123-5130.
74. 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.
75. Zecca, M., Basler, K. and Struhl, G. (1995) Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development, 121, 2265-2278.