Dpp-induced Egfr signaling triggers postembryonic wing development in Drosophila

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 13, 2013, Pages 5058-5063

  Paul, Litty ^a   Wang, Shu Huei ^a   Manivannan, Sathiya N ^a   Bonanno, Liana ^a   Lewis, Sarah ^a   Austin, Christina L ^a   Simcox, Amanda ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Apterous; Iroquois Complex; Wingless

Indexed keywords

DECAPENTAPLEGIC PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; PNTP2 PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; DROSOPHILA; FORELIMB; GENE EXPRESSION REGULATION; GENE TARGETING; INSECT DEVELOPMENT; INTRACELLULAR SIGNALING; NONHUMAN; PARACRINE SIGNALING; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPATIOTEMPORAL ANALYSIS;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; NEUREGULINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, INVERTEBRATE PEPTIDE; SIGNAL TRANSDUCTION; WING;

DROSOPHILA MELANOGASTER; HEXAPODA;

EID: 84875485359     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1217538110     Document Type: Article

References (64)

1. Cohen B, Simcox AA, Cohen SM (1993) Allocation of the thoracic imaginal primordia in the Drosophila embryo. Development 117(2):597-608.
2. Bate M, Arias AM (1991) The embryonic origin of imaginal discs in Drosophila. Development 112(3):755-761.
3. Wieschaus E, Gehring W (1976) Clonal analysis of primordial disc cells in the early embryo of Drosophila melanogaster. Dev Biol 50(2):249-263.
4. Kubota K, Goto S, Eto K, Hayashi S (2000) EGF receptor attenuates Dpp signaling and helps to distinguish the wing and leg cell fates in Drosophila. Development 127(17): 3769-3776.
5. Goto S, Hayashi S (1997) Specification of the embryonic limb primordium by graded activity of Decapentaplegic. Development 124(1):125-132.
6. Couso JP, Bate M, Martínez-Arias A (1993) A wingless-dependent polar coordinate system in Drosophila imaginal discs. Science 259(5094):484-489.
7. Williams JA, Paddock SW, Carroll SB (1993) Pattern formation in a secondary field: A hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions. Development 117(2):571-584.
8. Ng M, Diaz-Benjumea FJ, Vincent JP, Wu J, Cohen SM (1996) Specification of the wing by localized expression of wingless protein. Nature 381(6580):316-318.
9. Whitworth AJ, Russell S (2003) Temporally dynamic response to Wingless directs the sequential elaboration of the proximodistal axis of the Drosophila wing. Dev Biol 254(2):277-288.
10. Zecca M, Struhl G (2007) Recruitment of cells into the Drosophila wing primordium by a feed-forward circuit of vestigial autoregulation. Development 134(16):3001-3010.
11. Baena-López LA, García-Bellido A (2003) Genetic requirements of vestigial in the regulation of Drosophila wing development. Development 130(1):197-208.
12. Wang SH, Simcox A, Campbell G (2000) Dual role for Drosophila epidermal growth factor receptor signaling in early wing disc development. Genes Dev 14(18):2271-2276.
13. Zecca M, Struhl G (2002) Subdivision of the Drosophila wing imaginal disc by EGFRmediated signaling. Development 129(6):1357-1368.
14. Letizia A, Barrio R, Campuzano S (2007) Antagonistic and cooperative actions of the EGFR and Dpp pathways on the iroquois genes regulate Drosophila mesothorax specification and patterning. Development 134(7):1337-1346.
15. Sharma RP, Chopra VL (1976) Effect of the Wingless (wg1) mutation on wing and haltere development in Drosophila melanogaster. Dev Biol 48(2):461-465.
16. Simcox AA, et al. (1996) Molecular, phenotypic, and expression analysis of vein, a gene required for growth of the Drosophila wing disc. Dev Biol 177(2):475-489.
17. Schnepp B, Grumbling G, Donaldson T, Simcox A (1996) Vein is a novel component in the Drosophila epidermal growth factor receptor pathway with similarity to the neuregulins. Genes Dev 10(18):2302-2313.
18. Erives A, Levine M (2004) Coordinate enhancers share common organizational features in the Drosophila genome. Proc Natl Acad Sci USA 101(11):3851-3856.
19. Zinzen RP, Senger K, Levine M, Papatsenko D (2006) Computational models for neurogenic gene expression in the Drosophila embryo. Curr Biol 16(13):1358-1365.
20. Golembo M, Yarnitzky T, Volk T, Shilo BZ (1999) Vein expression is induced by the EGF receptor pathway to provide a positive feedback loop in patterning the Drosophila embryonic ventral ectoderm. Genes Dev 13(2):158-162.
21. Wessells RJ, Grumbling G, Donaldson T, Wang SH, Simcox A (1999) Tissue-specific regulation of vein/EGF receptor signaling in Drosophila. Dev Biol 216(1):243-259.
22. Simcox A (1997) Differential requirement for EGF-like ligands in Drosophila wing development. Mech Dev 62(1):41-50.
23. Butchar JP, et al. (2012) New negative feedback regulators of Egfr signaling in Drosophila. Genetics 191(4):1213-1226.
24. Rafel N, Milán M (2008) Notch signalling coordinates tissue growth and wing fate specification in Drosophila. Development 135(24):3995-4001.
25. Grimm S, Pflugfelder GO (1996) Control of the gene optomotor-blind in Drosophila wing development by decapentaplegic and wingless. Science 271(5255):1601-1604.
26. Gibson MC, Lehman DA, Schubiger G (2002) Lumenal transmission of decapentaplegic in Drosophila imaginal discs. Dev Cell 3(3):451-460.
27. Sekelsky JJ, Newfeld SJ, Raftery LA, Chartoff EH, Gelbart WM (1995) Genetic characterization and cloning of mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics 139(3):1347-1358.
28. McClure KD, Schubiger G (2005) Developmental analysis and squamous morphogenesis of the peripodial epithelium in Drosophila imaginal discs. Development 132(22):5033-5042.
29. Weiss A, et al. (2010) A conserved activation element in BMP signaling during Drosophila development. Nat Struct Mol Biol 17(1):69-76.
30. Minami M, Kinoshita N, Kamoshida Y, Tanimoto H, Tabata T (1999) brinker is a target of Dpp in Drosophila that negatively regulates Dpp-dependent genes. Nature 398(6724):242-246.
31. Campbell G, Tomlinson A (1999) Transducing the Dpp morphogen gradient in the wing of Drosophila: Regulation of Dpp targets by brinker. Cell 96(4):553-562.
32. Jaźwińska A, Kirov N, Wieschaus E, Roth S, Rushlow C (1999) The Drosophila gene brinker reveals a novel mechanism of Dpp target gene regulation. Cell 96(4):563-573.
33. Tsuneizumi K, et al. (1997) Daughters against dpp modulates dpp organizing activity in Drosophila wing development. Nature 389(6651):627-631.
34. Pyrowolakis G, Hartmann B, Müller B, Basler K, Affolter M (2004) A simple molecular complex mediates widespread BMP-induced repression during Drosophila development. Dev Cell 7(2):229-240.
35. Klämbt C (1993) The Drosophila gene pointed encodes two ETS-like proteins which are involved in the development of the midline glial cells. Development 117(1):163-176.
36. Brunner D, et al. (1994) The ETS domain protein pointed-P2 is a target of MAP kinase in the sevenless signal transduction pathway. Nature 370(6488):386-389.
37. Scholz H, Deatrick J, Klaes A, Klämbt C (1993) Genetic dissection of pointed, a Drosophila gene encoding two ETS-related proteins. Genetics 135(2):455-468.
38. Qiao F, et al. (2006) Mae inhibits Pointed-P2 transcriptional activity by blocking its MAPK docking site. EMBO J 25(1):70-79.
39. Rogers EM, et al. (2005) Pointed regulates an eye-specific transcriptional enhancer in the Drosophila hedgehog gene, which is required for the movement of the morphogenetic furrow. Development 132(21):4833-4843.
40. Halfon MS, et al. (2000) Ras pathway specificity is determined by the integration of multiple signal-activated and tissue-restricted transcription factors. Cell 103(1):63-74.
41. Levine M, Davidson EH (2005) Gene regulatory networks for development. Proc Natl Acad Sci USA 102(14):4936-4942.
42. Peter IS, Davidson EH (2011) A gene regulatory network controlling the embryonic specification of endoderm. Nature 474(7353):635-639.
43. Klein T (2001) Wing disc development in the fly: The early stages. Curr Opin Genet Dev 11(4):470-475.
44. Baena-López LA, Pastor-Pareja JC, Resino J (2003) Wg and Egfr signalling antagonise the development of the peripodial epithelium in Drosophila wing discs. Development 130(26):6497-6506.
45. Cho KO, Chern J, Izaddoost S, Choi KW (2000) Novel signaling from the peripodial membrane is essential for eye disc patterning in Drosophila. Cell 103(2):331-342.
46. Standley HJ, Gurdon JB (2002) Uncommitted Xenopus blastula cells can be directed to uniform muscle gene expression by gradient interpretation and a community effect. Int J Dev Biol 46(8):993-998.
47. Gurdon JB (1988) A community effect in animal development. Nature 336(6201): 772-774.
48. Bolouri H, Davidson EH (2010) The gene regulatory network basis of the "community effect," and analysis of a sea urchin embryo example. Dev Biol 340(2):170-178.
49. Davidson EH, Levine MS (2008) Properties of developmental gene regulatory networks. Proc Natl Acad Sci USA 105(51):20063-20066.
50. Li Q, Ahmed S, Loeb JA (2004) Development of an autocrine neuregulin signaling loop with malignant transformation of human breast epithelial cells. Cancer Res 64(19):7078-7085.
51. Sheng Q, et al. (2010) An activated ErbB3/NRG1 autocrine loop supports in vivo proliferation in ovarian cancer cells. Cancer Cell 17(3):298-310.
52. Wilson TR, Lee DY, Berry L, Shames DS, Settleman J (2011) Neuregulin-1-mediated autocrine signaling underlies sensitivity to HER2 kinase inhibitors in a subset of human cancers. Cancer Cell 20(2):158-172.
53. Jockusch EL, Ober KA (2004) Hypothesis testing in evolutionary developmental biology: A case study from insect wings. J Hered 95(5):382-396.
54. Niwa N, et al. (2010) Evolutionary origin of the insect wing via integration of two developmental modules. Evol Dev 12(2):168-176.
55. Sepp KJ, Auld VJ (1999) Conversion of lacZ enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. Genetics 151(3):1093-1101.
56. Thummel CS, Boulet AM, Lipshitz HD (1988) Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene 74(2):445-456.
57. Foronda D, Pérez-Garijo A, Martín FA (2009) Dpp of posterior origin patterns the proximal region of the wing. Mech Dev 126(3-4):99-106.
58. Yan H, Chin ML, Horvath EA, Kane EA, Pfleger CM (2009) Impairment of ubiquitylation by mutation in Drosophila E1 promotes both cell-autonomous and non-cellautonomous Ras-ERK activation in vivo. J Cell Sci 122(Pt 9):1461-1470.
59. Kadam S, McMahon A, Tzou P, Stathopoulos A (2009) FGF ligands in Drosophila have distinct activities required to support cell migration and differentiation. Development 136(5):739-747.
60. Butler MJ, et al. (2003) Discovery of genes with highly restricted expression patterns in the Drosophila wing disc using DNA oligonucleotide microarrays. Development 130(4):659-670.
61. Xu C, Kauffmann RC, Zhang J, Kladny S, Carthew RW (2000) Overlapping activators and repressors delimit transcriptional response to receptor tyrosine kinase signals in the Drosophila eye. Cell 103(1):87-97.
62. Rushlow C, Colosimo PF, Lin MC, Xu M, Kirov N (2001) Transcriptional regulation of the Drosophila gene zen by competing Smad and Brinker inputs. Genes Dev 15(3): 340-351.
63. Saller E, Kelley A, Bienz M (2002) The transcriptional repressor Brinker antagonizes Wingless signaling. Genes Dev 16(14):1828-1838.
64. Sosinsky A, Bonin CP, Mann RS, Honig B (2003) Target Explorer: An automated tool for the identification of new target genes for a specified set of transcription factors. Nucleic Acids Res 31(13):3589-3592.