Nuclear integration of positive Dpp signals, antagonistic Wg inputs and mesodermal competence factors during Drosophila visceral mesoderm induction

Development

Volumn 132, Issue 6, 2005, Pages 1429-1442

  Lee, Hsiu Hsiang ^a,b   Frasch, Manfred ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dpp; Drosophila; Wg

Indexed keywords

HOMEODOMAIN PROTEIN; SMAD PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DPP; TRANSCRIPTION FACTOR FOXG; TRANSCRIPTION FACTOR TINMAN; UNCLASSIFIED DRUG; WNT1 PROTEIN;

ARTICLE; BAGPIPE GENE; BINDING SITE; DROSOPHILA; EMBRYO DEVELOPMENT; ENHANCER REGION; ENZYME ACTIVATION; GENE CONTROL; GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC CODE; GENETIC CONSERVATION; HOMEOBOX; HYBRID CELL; MESODERM; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; TISSUE INDUCTION;

ANIMALS; BASE SEQUENCE; CONSERVED SEQUENCE; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYONIC INDUCTION; ENHANCER ELEMENTS (GENETICS); HOMEODOMAIN PROTEINS; MESODERM; MOLECULAR SEQUENCE DATA; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; TRANS-ACTIVATORS;

EID: 17244378298     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01687     Document Type: Article

References (61)

1. Andrioli, L., Vasisht, V., Theodosopoulou, E., Oberstein, A. and Small, S. (2002). Anterior repression of a Drosophila stripe enhancer requires three position-specific mechanisms. Development 129, 4931-4940.
2. Azpiazu, N. and Frasch, M. (1993). tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila. Genes Dev. 7, 1325-1340.
3. Azpiazu, N., Lawrence, P., Vincent, J.-P. and Frasch, M. (1996). Segmentation and specification of the Drosophila mesoderm. Genes Dev. 10, 3183-3194.
4. Baylies, M., Martinez Arias, A. and Bate, M. (1995). wingless is required for the formation of a subset of muscle founder cells during Drosophila embryogenesis. Development 121, 3829-3837.
5. Bodmer, R. (1993). The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118, 719-729.
6. Bodmer, R., Jan, L. Y. and Jan, Y. N. (1990). A new homeobox-containing gene, msh-2, is transiently expressed early during mesoderm formation of Drosophila. Development 110, 661-669.
7. Campos-Ortega, J. A. and Hartenstein, V. (1997). The Embryonic Development of Drosophila melanogaster. Berlin: Springer Verlag.
8. Carmena, A., Gisselbrecht, S., Harrison, J., Jimenez, F. and Michelson, A. (1998). Combinatorial signaling codes for the progressive determination of cell fates in the Drosophila embryonic mesoderm. Genes Dev. 15, 3910-3922.
9. Chen, C. and Schwartz, R. (1995). Identification of novel DNA binding targets and regulatory domains of a murine tinman homeodomain factor, nkx-2.5. J. Biol. Chem. 270, 15628-15633.
10. Cripps, R., Black, B., Zhao, B., Lien, C., Schulz, R. and Olson, E. (1998). The myogenic regulatory gene Mef2 is a direct target for transcriptional activation by Twist during Drosophila myogenesis. Genes Dev. 12, 422-434.
11. Dou, C., Lee, J., Liu, B., Liu, F., Massague, J., Xuan, S. and Lai, E. (2000). BF-1 interferes with transforming growth factor beta signaling by associating with Smad partners. Mol. Cell. Biol. 20, 6201-6211.
12. Englund, C., Loren, C. E., Grabbe, C., Varshney, G. K., Deleuil, F., Hallberg, B. and Palmer, R. H. (2003). Jeb signals through the Alk receptor tyrosine kinase to drive visceral muscle fusion. Nature 425, 512-516.
13. Feng, X. H., Zhang, Y., Wu, R. Y. and Derynck, R. (1998). The tumor suppressor Smad4/DPC4 and transcriptional adaptor CBP/p300 are coactivators for Smad3 in TGF-beta-induced transcriptional activation. Genes Dev. 12, 2153-2163.
14. Frasch, M. (1995). Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature 374, 464-467.
15. Frasch, M. and Nguyen, H. T. (1999). Genetic control of mesoderm patterning and differentiation during Drosophila embryogenesis. Adv. Dev. Biochem. 5, 1-47.
16. Frasch, M., Hoey, T., Rushlow, C., Doyle, H. J. and Levine, M. (1987). Characterization and localization of the even-skipped protein of Drosophila. EMBO J. 6, 749-759.
17. Gajewski, K., Kim, Y., Lee, Y., Olson, E. and Schulz, R. (1997). D-mef2 is a target for Tinman activation during Drosophila heart development. EMBO J. 16, 515-522.
18. Gebelein, B., McKay, D. J. and Mann, R. S. (2004). Direct integration of Hox and segmentation gene inputs during Drosophila development. Nature 431, 653-659.
19. Halfon, M., Carmena, A., Gisselbrecht, S., Sackerson, C., Jimenez, F., Baylies, M. and Michelson, A. (2000). Ras pathway specificity is determined by the integration of multiple signal-activated and tissue-restricted transcription factors. Cell 103, 63-74.
20. Han, Z., Fujioka, M., Su, M., Liu, M., Jaynes, J. B. and Bodmer, R. (2002). Transcriptional integration of competence modulated by mutual repression generates cell-type specificity within the cardiogenic mesoderm. Dev. Biol. 252, 225-240.
21. Hazelett, D. J., Bourouis, M., Walldorf, U. and Treisman, J. E. (1998). decapentaplegic and wingless are regulated by eyes absent and eyegone and interact to direct the pattern of retinal differentiation in the eye disc. Development 125, 3741-3751.
22. Jagla, T., Bidet, Y., da Ponte, J. P., Dastugue, B. and Jagla, K. (2002). Cross-repressive interactions of identity genes are essential for proper specification of cardiac and muscular fates in Drosophila. Development 129, 1037-1047.
23. Janknecht, R., Wells, N. J. and Hunter, T. (1998). TGF-beta-stimulated cooperation of Smad proteins with the coactivators CBP/p300. Genes Dev. 12, 2114-2119.
24. Jazwinska, A., Rushlow, C. and Roth, S. (1999). The role of brinker in mediating the graded response to Dpp in early Drosophila embryos. Development 126, 3323-3334.
25. Kaufmann, E., Muller, D. and Knöchel, W. (1995). DNA recognition site analysis of Xenopus winged helix proteins. J. Mol. Biol. 248, 239-254.
26. Kim, D. W., Kempf, H., Chen, R. E. and Lassar, A. B. (2003). Characterization of Nkx3.2 DNA binding specificity and its requirement for somitic chondrogenesis. J. Biol. Chem. 278, 27532-27539.
27. Kim, J., Johnson, K., Chen, H., Carroll, S. and Laughon, A. (1997). Drosophila Mad binds to DNA and directly mediates activation of vestigial by Decapentaplegic. Nature 388, 304-308.
28. Kirkpatrick, H., Johnson, K. and Laughon, A. (2001). Repression of dpp targets by binding of Brinker to Mad sites. J. Biol. Chem. 276, 18216-18222.
29. Knirr, S. and Frasch, M. (2001). Molecular integration of inductive and mesoderm-intrinsic inputs governs even-skipped enhancer activity in a subset of pericardial and dorsal muscle progenitors. Dev. Biol. 238, 13-26.
30. Kopp, A., Blackman, R. K. and Duncan, I. (1999). Wingless, Decapentaplegic and EGF receptor signaling pathways interact to specify dorso-ventral pattern in the adult abdomen of Drosophila. Development 126, 3495-3507.
31. Lee, H. and Frasch, M. (2000). Wingless effects mesoderm patterning and ectoderm segmentation events via induction of its downstream target sloppy paired. Development 127, 5497-5508.
32. Lee, H. H. and Frasch, M. (2004). A survey of fork head domain encoding genes in the Drosophila genome: Classification and expresssion patterns. Dev. Dyn. 229, 357-366.
33. Lee, H. H., Norris, A., Weiss, J. B. and Frasch, M. (2003). Jelly belly protein activates the receptor tyrosine kinase Alk to specify visceral muscle pioneers. Nature 425, 507-512.
34. 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.
35. Marty, T., Vigano, M. A., Ribeiro, C., Nussbaumer, U., Grieder, N. C. and Affolter, M. (2001). A HOX complex, a repressor element and a 50 bp sequence confer regional specificity to a DPP-responsive enhancer. Development 128, 2833-2845.
36. Michelson, A. M., Gisselbrecht, S., Zhou, Y., Baek, K. H. and Buff, E. M. (1998). Dual functions of the Heartless fibroblast growth factor receptor in development of the Drosophila embryonic mesoderm. Dev. Genet. 22, 212-229.
37. Morata, G. (2001). How Drosophila appendages develop. Nat. Rev. Mol. Cell. Biol. 2, 89-97.
38. Nishita, M., Hashimoto, M. K., Ogata, S., Laurent, M. N., Ueno, N., Shibuya, H. and Cho, K. W. (2000). Interaction between Wnt and TGF-beta signalling pathways during formation of Spemann's organizer. Nature 403, 781-785.
39. Pierrou, S., Hellqvist, M., Samuelsson, L., Enerback, S. and Carlsson, P. (1994). Cloning and characterization of seven human forkhead proteins: binding site specificity and DNA bending. EMBO J. 13, 5002-5012.
40. Pouponnot, C., Jayaraman, L. and Massague, J. (1998). Physical and functional interaction of SMADs and p300/CBP. J. Biol. Chem. 273, 22865-22868.
41. Riechmann, V., Irion, U., Wilson, R., Grosskortenhaus, A. and Leptin, M. (1997). Control of cell fates and segmentation in the Drosophila mesoderm. Development 124, 2915-2922.
42. Rushlow, C., Colosimo, P., Lin, M.-C., Xu, M. and Kirov, N. (2001). Transcriptional regulation of the Drosophila gene zen by competing Smad and Brinker inputs. Genes Dev. 15, 340-351.
43. Saller, E. and Bienz, M. (2001). Direct competition between Brinker and Drosophila Mad in Dpp target gene transcription. EMBO Rep. 2, 298-305.
44. Shi, Y. (2001). Structural insights on Smad function in TGFbeta signaling. BioEssays 23, 223-232.
45. Shi, Y., Wang, Y. F., Jayaraman, L., Yang, H., Massague, J. and Pavletich, N. P. (1998). Crystal structure of a Smad MH1 domain bound to DNA: insights on DNA binding in TGF-beta signaling. Cell 94, 585-594.
46. Sivasankaran, R., Vigano, M., Muller, B., Affolter, M. and Basler, K. (2000). Direct transcriptional control of the Dpp target omb by the DNA binding protein Brinker. EMBO J. 19, 6162-6172.
47. Staehling-Hampton, K., Hoffmann, F. M., Baylies, M. K., Rushton, E. and Bate, M. (1994). dpp induces mesodermal gene expression in Drosophila. Nature 372, 783-786.
48. Su, M., Fujioka, M., Goto, T. and Bodmer, R. (1999). The Drosophila homeobox genes zfh-1 and even-skipped are required for cardiac-specific differentiation of a numb dependent lineage decision. Development 126, 3241-3251.
49. Waltzer, L. and Bienz, M. (1999). A function of CBP as a transcriptional co-activator during Dpp signalling. EMBO J. 18 1630-1641.
50. Waltzer, L., Vandel, L. and Bienz, M. (2001). Teashirt is required for transcriptional repression mediated by high Wingless levels. EMBO J. 20, 137-145.
51. Wu, X., Golden, K. and Bodmer, R. (1995). Heart development in Drosophila requires the segment polarity gene wingless. Dev. Biol. 169, 619-628.
52. Xu, X., Yin, Z., Hudson, J., Ferguson, E. and Frasch, M. (1998). Smad proteins actin combination with synergistic and antagonistic regulators to target Dpp responses to the Drosophila mesoderm. Genes Dev. 12, 2354-2370.
53. Yao, J., Lai, E. and Stifani, S. (2001). The winged-helix protein Brain Factor 1 interacts with Groucho and Hes proteins to repress transcription. Mol. Cell. Biol. 21, 1962-1972.
54. Yin, Z. and Frasch, M. (1998). Regulation and function of tinman during dorsal mesoderm induction and heart specification in Drosophila. Dev. Genet. 22, 187-200.
55. Yin, Z., Xu, X.-L. and Frasch, M. (1997). Regulation of the Twist target gene tinman by modular cis-regulatory elements during early mesoderm development. Development 124, 4871-4982.
56. Yu, X., Riese, J., Eresh, S. and Bienz, M. (1998). Transcriptional repression due to high levels of Wingless signalling. EMBO J. 17, 7021-7032.
57. Zaffran, S. and Frasch, M. (2002). Early signals in cardiac development. Circ. Res. 91, 457-469.
58. Zaffran, S., Kachler, A., Lee, H. H. and Frasch, M. (2001). biniou (FoxF), a central component in a regulatory network controlling visceral mesoderm development and midgut morphogenesis in Drosophila. Genes Dev. 15, 2900-2915.
59. Zaffran, S., Xu, X., Lo, P. C., Lee, H. H. and Frasch, M. (2002). Cardiogenesis in the Drosophila model: control mechanisms during early induction and diversification of cardiac progenitors. Cold Spring Harbor Symp. Quant. Biol. 67, 1-12.
60. Zawel, L., Dai, J. L., Buckhaults, P., Zhou, S., Kinzler, K. W., Vogelstein, B. and Kern, S. E. (1998). Human Smad3 and Smad4 are sequence-specific transcription activators. Mol. Cell 1, 611-617.
61. Zhang, H., Levine, M. and Ashe, H. (2001). Brinker is a sequence-specific transcriptional repressor in the Drosophila embryo. Genes Dev. 15, 261-266.