Functional intertwining of Dpp and EGFR signaling during Drosophila endoderm induction

Genes and Development

Volumn 12, Issue 13, 1998, Pages 2022-2035

  Szüts, Dávid ^a   Eresh, Salih ^a   Bienz, Mariann ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Decapentaplegic; Endoderm induction; Epidermal growth factor receptor; Mad binding sites; Vein

Indexed keywords

ACTIVIN; EPIDERMAL GROWTH FACTOR RECEPTOR; NEU DIFFERENTIATION FACTOR;

ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; CYCLIC AMP RESPONSIVE ELEMENT; DROSOPHILA; EMBRYO; ENDODERM; ENHANCER REGION; HOMEOBOX; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

DROSOPHILA;

EID: 0032128289     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.13.2022     Document Type: Article

References (90)

1. Arora, K., H. Dai, S.G. Kazuko, J. Jamal, M.B. O'Connor, A. Letsou, and R. Warrior. 1995. The Drosophila schnurri gene acts in the Dpp/TGF-β signaling pathway and encodes a transcription factor homologous to the human MBP family. Cell 81: 781-790.
2. Basler, K. and G. Struhl. 1994. Compartment boundaries and the control of Drosophila limb pattern by Hedgehog protein. Nature 368: 208-214.
3. Bienz, M. 1997. Endoderm induction in Drosophila: The nuclear targets of the inducing signals. Curr. Opin. Genet. Dev. 7: 683-688.
4. Bier, E., L.Y. Jan, and Y.N. Jan. 1990. rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes & Dev. 4: 190-203.
5. Brand, A.H. and N. Perrimon. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
6. Brook, V.J. and S. Cohen. 1996. Antagonistic interactions between Wingless and Decapentaplegic responsible for dorsal-ventral pattern in the Drosophila leg. Science 273: 1372-1377.
7. Campos-Ortega, J.A. and V. Hartenstein. 1985. The embryonic development of Drosophila melanogaster. Springer Verlag, New York, NY.
8. Capdevila, J. and I. Guerrero. 1994. Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J. 13: 4459-4468.
9. Chen, X., M.J. Rubock, and M. Whitman. 1996. A transcriptional partner for MAD proteins in TGF-β signaling. Nature 383: 691-696.
10. Chen, X., E. Weisberg, V. Fridmacher, M. Watanabe, G. Naco, and M. Whitman. 1997. Smad4 and FAST-1 in the assembly of activin-responsive factor. Nature 389: 85-89.
11. D1] dominant female-sterile insertions in Drosophila and their use in generating germ-line chimeras. Development 119: 1359-1369.
12. Clifford, R. and T. Schüpbach. 1992. The torpedo (DER) receptor tyrosine kinase is required at multiple times during Drosophila embryogenesis. Development 115: 853-872.
13. de Groot, R.P., J. den Hertog, J.R. Vandenheede, J. Goris, and P. Sassone-Corsi. 1993. Multiple and cooperative phosphorylation events regulate the CREM activator function. EMBO J. 12: 3903-3911.
14. Eresh, S., J. Riese, D.B. Jackson, D. Bohmann, and M. Bienz. 1997. A CREB binding site as a target for decapentaplegic signaling during Drosophila endoderm induction. EMBO J. 16: 2014-2022.
15. Ferguson, E.L. and K.V. Anderson. 1992. decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 71: 451-461.
16. Freeman, M. 1994. The spitz gene is required for photoreceptor determination in the Drosophila eye where it interacts with the EGF receptor. Mech. Dev. 48: 25-33.
17. _. 1996. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87: 651-660.
18. Freeman, M., C. Klämbt, C.S. Goodman, and G.M. Rubin. 1992. The argos gene encodes a diffusible factor that regulates cell fate decisions in the Drosophila eye. Cell 69: 963-975.
19. Gabay, L., R. Seger, and B.-Z. Shilo. 1997. In situ activation pattern of Drosophila EGF receptor pathway during development. Science 277: 1103-1106.
20. Ganan, Y., D. Macias, M. Duterque-Coquillaud, M.A. Ros, and J.M. Hurle. 1996. Role of TGF-βs and BMPs as signals controlling the position of the digits and the areas of interdigital cell death in the developing chick limb autopod. Development 122: 2349-2357.
21. Ginty, D.D., A. Bonni, and M.E. Greenberg. 1994. Nerve growth factor activates a Ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB. Cell 77: 713-725.
22. Glise, B. and S. Noselli. 1997. Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes & Dev. 11: 1738-1747.
23. Golembo, M., E. Raz, and B.-Z. Shilo. 1996a. The Drosophila embryonic midline is the site of Spitz processing, and induces activation of the EGF receptor in the ventral ectoderm. Development 122: 3363-3370.
24. Golembo, M., R. Schweitzer, M. Freeman, and B.-Z. Shilo. 1996b. argos transcription is induced by the Drosophila EGF receptor pathway to form an inhibitory feedback loop. Development 122: 223-230.
25. Green, J.B.A. and J.C. Smith. 1990. Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature 347: 391-394.
26. Green, J.B.A., H.V. New, and J.C. Smith. 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.
27. Grieder, N.C., D. Nellen, R. Burke, K. Basler, and M. Affolter. 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.
28. Grieder, N.C., T. Marty, H.-D. Ryoo, R.S. Mann, and M. Affolter. 1997. Synergistic activation of a Drosophila enhancer by HOM/EXD and DPP signaling. EMBO J. 16: 7402-7410.
29. Gurdon, J.B., P. Harger, A. Mitchell, and P. Lemaire. 1994. Activin signalling and response to a morphogen gradient. Nature 371: 487-492.
30. Hartenstein, V. and Y.N. Jan. 1992. Studying Drosophila embryogenesis with P-LacZ enhancer trap lines. Wilhelm Roux's Arch. Dev. Biol. 201: 194-220.
31. Hemmati-Brivanlou, A. and D.A. Melton. 1992. Truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos. Nature 359: 609-614.
32. Hoppler, S. and M. Bienz. 1994. Specification of a single cell type by a Drosophila homeotic gene. Cell 76: 689-702.
33. _. 1995. Two different thresholds of wingless signaling with distinct developmental consequences in the Drosophila midgut. EMBO J. 14: 5016-5026.
34. Hou, X.S., E.S. Goldstein, and N. Perrimon. 1997. Drosophila Jun relays the Jun amino-terminal kinase signal transduction pathway to the Decapentaplegic signal transduction pathway in regulating epithelial cell sheet movement. Genes & Dev. 11: 1728-1737.
35. Huang, H.-C., L.C. Murtaugh, P.D. Vize, and M. Whitman. 1995. Identification of a potential regulator of early transcriptional responses to mesoderm inducers in the frog embryo. EMBO J. 14: 5965-5973.
36. Hursh, D.A., R.W. Padgett, and W.M. Gelbart. 1993. Cross regulation of decapentaplegic and Ultrabithorax transcription in the embryonic visceral mesoderm of Drosophila. Development 117: 1211-1222.
37. Immerglück, K., P.A. Lawrence, and M. Bienz. 1990. Induction across germ layers in Drosophila mediated by a genetic cascade. Cell 62: 261-268.
38. Irish, V.F. and W.M. Gelbart. 1987. The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo. Genes & Dev. 1: 868-879.
39. Kessler, D. and D.A. Melton. 1995. Induction of dorsal mesoderm by soluble, mature Vg1 protein. Development 121: 2155-2164.
40. Kim, J., K. Johnson, H.J. Chen, S. Carroll, and A. Laughon. 1997. MAD binds to DNA and directly mediates activation of vestigial by DPP. Nature 388: 304-308.
41. Kretschmar, M., J. Doody, and J. Massagué. 1997. Opposing BMP and EGF signaling pathways converge on the TGF-β family mediator Smad1. Nature 389: 618-622.
42. Lawrence, P.A., B. Sanson, and J.-P. Vincent. 1996. Compartments, wingless and engrailed: Patterning the ventral epidermis of Drosophila embryos. Development 122: 4095-4103.
43. Lawrence, P.A. and G. Struhl. 1996. Morphogens, compartments, and patterns: Lessons from Drosophila? Cell 85: 951-961.
44. Lecuit, T., W.J. Brook, M. Ng, M. Calleja, H. Sun, and S.M. Cohen. 1996. Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 381: 387-393.
45. Lee, T., L. Feig, and D.J. Montell. 1996. Two distinct roles for Ras in a developmentally regulated cell migration. Development 122: 409-418.
46. Lemke, G. 1996. Neuregulins in development. Mol. Cell. Neurosci. 7: 247-262.
47. Liu, F., A. Hata, J.C. Baker, J. Doody, J. Cárcamo, R.M. Harland, and J. Massagué. 1996. A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 381:620-623.
48. Martin-Bermudo, M.D., O.M. Dunin-Borkowski, and N.H. Brown. 1997. Specificity of PS integrin function during embryogenesis resides in the α subunit extracellular domain. EMBO J. 16:4184-4193.
49. Massagué, J., A. Hata, and F. Liu. 1997. TGF-β signaling through the Smad pathway. Trends Cell Biol. 7: 187-192.
50. Mayer, U. and C. Nüsslein-Volhard. 1988. A group of genes required for pattern formation in the ventral ectoderm of the Drosophila embryo. Genes & Dev. 2: 1496-1511.
51. Meyer, D. and C. Birchmeier. 1995. Multiple essential functions of neuregulin in development. Nature 378: 386-390.
52. Montminy, M.R., K.A. Sevarino, J.A. Wagner, G. Mandel, and R.H. Goodman. 1986. Identification of a cyclic-AMP-responsive element within the rat somatostatin gene. Proc. Natl. Acad Sci. 83: 6682-6686.
53. Nellen, D., R. Burke, G. Struhl, and K. Basler. 1996. Direct and long-range action of a DPP morphogen gradient. Cell 85: 357-368.
54. Neuman-Silberberg, F. and T. Schüpbach. 1993. The Drosophila gene gurken produces a dorsally localized RNA and encodes a TGFα-like protein. Cell 75: 165-174.
55. Newfeld, S.J., E.H. Chartoff, J.M. Graff, D.A. Melton, and W.M. Gelbart. 1996. Mothers against dpp encodes a conserved cytoplasmic protein required in DPP/TGF-β responsive cells. Development 122: 2099-2108.
56. Nüsslein-Volhard, C., E. Wieschaus, and H. Kluding. 1984. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. - I. Zygotic loci on the second chromosome. Wilhelm Roux's Arch. Dev. Biol. 193: 267-282.
57. Oft, M., J. Peli, C. Rudaz, H. Schwarz, H. Beug, and E. Reichmann. 1996. TGF-β1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes & Dev. 10: 2462-2477.
58. O'Keefe, L., S.T. Dougan, L. Gabay, E. Raz, B.-Z. Shilo, and S. DiNardo. 1997. Spitz and Wingless, emanating from distinct borders, cooperate to establish cell fate across the Engrailed domain in the Drosophila epidermis. Development 124: 4837-4845.
59. Panganiban, G.E.F., R. Reuter, M.P. Scott, and F.M. Hoffmann. 1990. A Drosophila growth factor homolog, decapentaplegic, regulates homeotic gene expression within and across germ layers during midgut morphogenesis. Development 110: 1041-1050.
60. Raz, E. and B.-Z. Shilo. 1992. Dissection of the faint little ball (flb) phenotype: Determination of the development of the Drosophila central nervous system by early interactions in the ectoderm. Development 114: 113-123.
61. Reuter, R., G.E.F. Panganiban, F.M. Hoffmann, and M.P. Scott. 1990. Homeotic genes regulate the expression of putative growth factors in the visceral mesoderm of Drosophila embryos. Development 110: 1031-1040.
62. Riese, J., G. Tremml, and M. Bienz. 1997a. D-Fos, a target gene for Decapentaplegic signalling with a critical role during Drosophila endoderm induction. Development 124: 3353-3361.
63. Riese, J., X. Yu, A. Munnerlyn, S. Eresh, R. Grosschedl, and M. Bienz. 1997b. LEF-1, a nuclear factor coordinating signaling inputs from wingless and decapentaplegic. Cell 88: 777-787.
64. Riesgo-Escovar, J.R. and E. Hafen. 1997. Drosophila Jun kinase regulates expression of decapentaplegic via the ETS-domain protein Aop and the AP-1 transcription factor DJun during dorsal closure. Genes & Dev. 11: 1717-1727.
65. Rutledge, B.J., K. Zhang, E. Bier, Y.N. Jan, and N. Perrimon. 1992. The Drosophila spitz gene encodes a putative EGF-like growth factor involved in dorsal - ventral axis formation and neurogenesis. Genes & Dev. 6: 1503-1517.
66. Saari, G. and M. Bienz. 1987. The structure of the Ultrabithorax promoter of Drosophila melanogaster. EMBO J. 6: 1775-1779.
67. Schnepp, B., G. Grumbling, T. Donaldson, and A. Simcox. 1996. Vein is a novel component in the Drosophila epidermal growth factor receptor pathway with similarity to the neuregulins. Genes & Dev. 10: 2302-2313.
68. Schweitzer, R., M. Shaharabany, M. Seger, and B.-Z. Shilo. 1995a. Secreted Spitz triggers the DER signalling pathway and is a limiting component in embryonic ventral ectoderm determination. Genes & Dev. 9: 1518-1529.
69. Schweitzer, R., R. Howes, R. Smith, B.-Z. Shilo, and M. Freeman. 1995b. Inhibition of Drosophila EGF receptor activation by the secreted protein Argos. Nature 376: 699-702.
70. Sekelsky, J., S. Newfeld, L. Raftery, E. Chartoff, and W.M. Gelbart. 1995. Genetic characterization and cloning of Mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics 139: 1347-1358.
71. Simcox, A. 1997. Differential requirements for EGF-like ligands in Drosophila wing development. Mech. Dev. 62: 41-50.
72. Simcox, A.A., G. Grumbling, B. Schnepp, C. Bennington-Mathias, E. Hersperger, and A. Shearn. 1996. Molecular, phenotypic, and expression analysis of vein, a gene required for growth of the Drosophila wing disc. Dev. Biol. 177: 475-489.
73. Smith, J.C., B.M.J. Price, K. Van Nimmen, and D. Huylebroeck. 1990. Identification of a potent Xenopus mesoderm inducing factor as activin A. Nature 345: 729-731.
74. Spencer, F.A., F.M. Hoffmann, and W.M. Gelbart. 1982. Decapentaplegic: A gene complex affecting morphogenesis in Drosophila melanogaster. Cell 28: 451-461.
75. Staehling-Hampton, K. and F.M. Hoffmann. 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.
76. Sun, B., D.A. Hursh, D. Jackson, and P.A. Beachy. 1995. Ultrabithorax protein is necessary but not sufficient for full activation of decapentaplegic expression in the visceral mesoderm. EMBO J. 14: 520-535.
77. Szüts, D., M. Freeman, and M. Bienz. 1997. Antagonism between EGFR and Wingless signalling in the larval cuticle of Drosophila. Development 124: 3209-3219.
78. Thüringer, F. and M. Bienz. 1993. Indirect autoregulation of a homeotic Drosophila gene mediated by extracellular signalling. Proc. Natl. Acad. Sci. 90: 3899-3903.
79. Thüringer, F., S.M. Cohen, and M. Bienz. 1993. Dissection of an indirect autoregulatory response of a homeotic Drosophila gene. EMBO J. 12: 2419-2430.
80. Tio, M., C. Ma, and K. Moses. 1994. spitz, a Drosophila homolog of transforming growth factor-alpha, is required in the founding photoreceptor cells of the compound eye facets. Mech. Dev. 48: 13-23.
81. Tremml, G. 1991. "Interaktionen homeotischer Gene in inneren Keimblättern des Drosophila Embryos." Ph.D. thesis, University of Zürich, Switzerland.
82. Tremml, G. and M. Bienz. 1989. Homeotic gene expression in the visceral mesoderm of Drosophila embryos. EMBO J. 8: 2677-2685.
83. _. 1992. Induction of labial expression in the Drosophila endoderm: Response elements for dpp signalling and for autoregulation. Development 116: 447-456.
84. Wappner, P., L. Gabay, and B.-Z. Shilo. 1997. Interactions between the EGF receptor and DPP pathways establish distinct cell fates in the tracheal placodes. Development 124: 4707-4716.
85. White, R.A.H. and M. Wilcox. 1984. Protein products of the bithorax complex in Drosophila. Cell 39: 163-171.
86. Yarnitzky, T., L. Min, and T. Volk. 1997. The Drosophila neuregulin homolog Vein mediates inductive interactions between myotubes and their epidermal attachment cells. Genes & Dev. 11: 2691-2700.
87. Yingling, J.M., M.B. Datto, C. Wong, J.P. Frederick, N.T. Liberati, and X.-F. Wang. 1997. Tumor suppressor Smad4 is a transforming growth factor β-inducible DNA binding protein. Mol. Cell. Biol. 17: 7019-7028.
88. Yu, X., S. Hoppler, S. Eresh, and M. Bienz. 1996. decapentaplegic, a target gene of the wingless signalling pathway in the Drosophila midgut. Development 122: 849-858.
89. Zak, N.B., R.J. Wides, E.D. Schejter, E. Raz, and B.-Z. Shilo. 1990. Localization of the DER/flb protein in embryos: Implication on the faint little ball lethal phenotype. Development 109: 865-874.
90. Zecca, M., K. Basler, and G. Struhl. 1995. Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 121: 2265-2278.