A combinatorial enhancer recognized by Mad, TCF and Brinker first activates then represses dpp expression in the posterior spiracles of Drosophila

Developmental Biology

Volumn 313, Issue 2, 2008, Pages 829-843

  Takaesu, Norma T ^a   Bulanin, Denis S ^b   Johnson, Aaron N ^a   Orenic, Teresa V ^b   Newfeld, Stuart J ^a,c  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Brinker; Combinatorial signaling; Dpp; Drosophila; Gene regulation; Mad; Posterior spiracle enhancer; TCF

Indexed keywords

DECAPENTAPLEGIC PROTEIN; DROSOPHILA PROTEIN; PROTEIN BRINKER; PROTEIN MAD; T CELL FACTOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DROSOPHILA; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; REPORTER GENE;

MAMMALIA;

EID: 37849027117     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2007.10.021     Document Type: Article

References (52)

1. Ashe H., Mannervik M., and Levine M. Dpp signaling thresholds in the dorsal ectoderm of the Drosophila embryo. Development 127 (2000) 3305-3312
2. Brown S., Hu N., and Hombria J. Novel level of signaling control in the Jak/Stat pathway revealed by in situ visualization of protein-protein interaction during Drosophila development. Development 130 (2003) 3077-3084
3. Campbell G., and Tomlinson A. Transducing the Dpp morphogen gradient in the wing of Drosophila: regulation of Dpp targets by brinker. Cell 96 (1999) 553-562
4. Cordero J., Jassim O., Bao S., and Cagan R. A role for wingless in a pupal cell death event that contributes to patterning the Drosophila eye. Mech. Dev. 121 (2004) 1523-1530
5. Cripps R., and Olson E. Control of cardiac development by an evolutionarily conserved transcriptional network. Dev. Biol. 246 (2002) 14-28
6. de Celis J., Barrio R., and Kafatos F. A gene complex acting downstream of Dpp in Drosophila wing morphogenesis. Nature 381 (1996) 421-424
7. Eblaghie M., Reedy M., Oliver T., Mishina Y., and Hogan B. Evidence that autocrine signaling through BMPR1a regulates the proliferation, survival and morphogenetic behavior of distal lung epithelial cells. Dev. Biol. 291 (2006) 67-82
8. Flores G., Duan H., Yan H., Nagaraj R., Fu W., Zou Y., Noll M., and Banerjee U. Combinatorial signaling in the specification of unique cell fates. Cell 103 (2000) 75-85
9. Flybase, 2007.http://flybase.bio.indiana.edu/.
10. Halfon M., Carmena A., Gisselbrecht S., Sackerson C., Jimenez F., Baylies M., and Michelson A. Ras pathway specificity is determined by the integration of multiple signal-activated and tissue-restricted transcription factors. Cell 103 (2000) 63-74
11. Hatini V., Green R., Lengyel J., Bray S., and Dinardo S. The Drumstick/Lines/Bowl regulatory pathway links antagonistic Hedgehog and Wingless signaling inputs to epidermal cell differentiation. Genes Dev. 19 (2005) 709-718
12. Hoffmann F., and Goodman W. Identification in transgenic animals of the Drosophila dpp sequences required for embryonic dorsal pattern formation. Genes Dev. 1 (1987) 615-625
13. Horn C., Offen N., Nystedt S., Hacker U., and Wimmer E. piggyBac-based insertional mutagenesis and enhancer detection as a tool for functional insect genomics. Genetics 163 (2003) 647-661
14. Hu N., and Castelli-Gair J. Study of the posterior spiracles of Drosophila as a model to understand the genetic and cellular mechanisms controlling morphogenesis. Dev. Biol. 214 (1999) 197-210
15. Jack J., Dorsett D., Delotto Y., and Liu S. Expression of the cut locus in the Drosophila wing margin is required for cell type specification and is regulated by a distant enhancer. Development 113 (1991) 735-747
16. Jazwinska A., Rushlow C., and Roth S. The role of Brinker in mediating the graded response to Dpp in early Drosophila embryos. Development 126 (1999) 3323-3334
17. Johnson A., Bergman C., Kreitman M., and Newfeld S. Embryonic enhancers in the dpp disk region regulate a second round of Dpp signaling from the dorsal ectoderm to the mesoderm that represses Zfh-1 expression in a subset of pericardial cells. Dev. Biol. 262 (2003) 137-151
18. Johnson A., Burnett L., Sellin J., Paululat A., and Newfeld S. Defective Decapentaplegic signaling results in heart overgrowth and reduced cardiac output in Drosophila. Genetics 176 (2007) 1609-1624
19. Jurgens G. Segmental organization of the tail region in the embryo of Drosophila. A blastoderm fate map of cuticle structures of the larval tail. Roux's Arch. Dev. Biol. 196 (1987) 141-157
20. Kim J., Johnson K., Chen H., Carroll S., and Laughon A. Drosophila Mad binds to DNA and directly mediates activation of vestigial by Dpp. Nature 388 (1997) 304-308
21. Kosman D., Mizutani C., Lemons D., Cox W., McGinnis W., and Bier E. Multiplex detection of RNA Expression in Drosophila embryos. Science 305 (2004) 846
22. Kuhnlein R., Frommer G., Friedrich M., Gonzalez-Gaitan M., Weber A., Wagner-Bernholz J., Gehring W., Jackle H., and Schuh R. Spalt encodes an evolutionarily conserved zinc finger protein of novel structure which provides homeotic gene function in the head and tail region of the Drosophila embryo. EMBO J. 13 (1994) 168-179
23. Lammel U., Meadows L., and Saumweber H. Analysis of Drosophila salivary gland, epidermis and CNS development suggests an additional function of brinker in anterior-posterior cell fate specification. Mech. Dev. 92 (2000) 179-191
24. Manning G., and Krasnow M. Development of the Drosophila tracheal system. In: Bate, and Martinez-Arias (Eds). The Development of Drosophila melanogaster (1993), CSHL Press, Cold Spring Harbor, NY 609-685
25. Marquez R., Singer M., Takaesu N., Waldrip W., Kraytsberg Y., and Newfeld S. Transgenic analysis of the Smad family of TGF-β signal transducers in Drosophila suggests new roles and new interactions between family members. Genetics 157 (2001) 1639-1648
26. Martinez-Arias A., and Lawrence P. Parasegments and compartments in the Drosophila embryo. Nature 313 (1985) 639-642
27. Massagué J., Seoane J., and Wotton D. Smad transcription factors. Genes Dev. 19 (2005) 2783-2810
28. Merabet S., Hombria J., Hu N., Pradel J., and Graba Y. Hox-controlled reorganisation of intrasegmental patterning cues underlies Drosophila posterior spiracle organogenesis. Development 132 (2005) 3093-3102
29. Minami M., Kinoshita N., Kamoshida Y., Tanimoto H., and Tabata T. Brinker is a target of Dpp in Drosophila that negatively regulates Dpp-dependent genes. Nature 398 (1999) 242-246
30. Newfeld S., and Takaesu N. An analysis using the hobo genetic system reveals that combinatorial signaling by the Dpp and Wg pathways regulates dpp expression in leading edge cells of the dorsal ectoderm in Drosophila. Genetics 161 (2002) 685-692
31. Newfeld S., Wisotzkey R., and Kumar S. Molecular evolution of a developmental pathway: phylogenetic analyses of TGF-β family ligands, receptors and Smad signal transducers. Genetics 152 (1999) 783-795
32. Padgett R., Wozney J., and Gelbart W. Human BMP sequences confer normal dorsal-ventral patterning in the Drosophila embryo. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 2905-2909
33. Persson U., Izumi H., Souchelnytskyi S., Itoh S., Grimsby S., Engstrom U., Heldin C., Funa J., and ten Dijke P. The L45 loop in type I receptors for TGF-β family members is critical in specifying Smad isoform activation. FEBS Lett. 434 (1998) 83-87
34. Rushlow C., Colosimo P., Lin M., Xu M., and Kirov N. Transcriptional regulation of Drosophila gene zen by competing Smad and Brinker inputs. Genes Dev. 15 (2001) 340-351
35. Saller E., Kelley A., and Bienz M. The transcriptional repressor Brinker antagonizes Wingless signaling. Genes Dev. 16 (2002) 1828-1838
36. Shu W., Guttentag S., Wang Z., Andl T., Ballard P., Lu M., Piccolo S., Birchmeier W., Whitsett J., Millar S., and Morrisey E. Wnt/β-catenin signaling acts upstream of N-myc, BMP4, and FGF signaling to regulate proximal-distal patterning in the lung. Dev. Biol. 283 (2005) 226-239
37. Simões S., Denholm B., Azevedo D., Sotillos S., Martin P., Skaer H., Castelli-Gair J., and Jacinto A. Compartmentalisation of Rho regulators directs cell invagination during tissue morphogenesis. Development 133 (2006) 4257-4267
38. Sivasankaran R., Vigano M., Muller B., Affolter M., and Basler K. Direct control of the Dpp target omb by the DNA binding protein Brinker. EMBO J. 19 (2000) 6162-6172
39. St. Johnston R., Hoffmann F., Blackman R., Segal D., Grimaila R., Padgett R., Irick H., and Gelbart W. Molecular organization of the decapentaplegic gene in Drosophila. Genes Dev. 4 (1990) 1114-1127
40. Staehling-Hampton K., and Hoffmann F. Ectopic Dpp in the Drosophila midgut alters the expression of five homeotic genes dpp and wg causing specific morphological defects. Dev. Biol. 164 (1994) 502-512
41. Tetsu O., and McCormick F. β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398 (1999) 422-426
42. Takaesu N., Sultani O., Johnson A., and Newfeld S. Combinatorial signaling by an unconventional Wg pathway and the Dpp pathway requires Nejire (CBP/p300) to regulate dpp expression in posterior tracheal branches. Dev. Biol. 247 (2002) 225-236
43. Takaesu N., Johnson A., and Newfeld S. Posterior spiracle specific GAL4 lines: new reagents for developmental biology and respiratory physiology. Genesis 34 (2002) 16-18
44. van de Wetering M., Cavallo R., Dooijes D., van Beest M., van Es J., Loureiro J., Ypma A., Hursh D., Jones T., Bejsovec A., Peifer M., Mortin M., and Clevers H. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene TCF. Cell 88 (1997) 789-799
45. van den Heuvel M., Nusse R., Johnston P., and Lawrence P. Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication. Cell 59 (1989) 739-749
46. Waltzer L., and Bienz M. A function of CBP as a transcriptional co-activator during Dpp signaling. EMBO J. 18 (1999) 1630-1641
47. Wharton K., Ray R., and Gelbart W. An activity gradient of dpp is necessary for the specification of dorsal pattern elements in the Drosophila embryo. Development 117 (1993) 807-822
48. Whiteley M., Noguchi P., Sensabaugh S., Odenwald W., and Kassis J. The Drosophila gene escargot encodes a zinc finger motif found in snail-related genes. Mech. Dev. 36 (1992) 117-127
49. Willert K., and Jones K. Wnt signaling: is the party in the nucleus?. Genes Dev. 20 (2006) 1394-1404
50. Xu X., Yin Z., Hudson J., Ferguson E., and Frasch M. Smad proteins act in combination with synergistic and antagonistic regulators to target Dpp responses to the Drosophila mesoderm. Genes Dev. 12 (1998) 2354-2370
51. Xu C., Kauffmann R., Zhang J., Kladny S., and Carthew R. Overlapping activators and repressors delimit transcriptional response to receptor tyrosine kinase signals in the Drosophila eye. Cell 103 (2000) 87-97
52. Yang X., van Beest M., Clevers H., Jones T., Hursh D., and Mortin M. dpp is a direct target of TCF repression in the Drosophila visceral mesoderm. Development 127 (2000) 3695-3702