Mad is required for wingless signaling in wing development and segment patterning in Drosophila

PLoS ONE

Volumn 4, Issue 8, 2009, Pages

  Eivers, Edward ^a   Fuentealba, Luis C ^a   Sander, Veronika ^a   Clemens, James C ^b   Hartnett, Lori ^c   De Robertis, E M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PURDUE UNIVERSITY   (United States)

^c NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; GLYCOGEN SYNTHASE KINASE 3; PROTEIN MAD; SMAD8 PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; WNT1 PROTEIN; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; MAD PROTEIN, DROSOPHILA; WG PROTEIN, DROSOPHILA;

ADULT ANIMAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL BIOLOGY; DROSOPHILA; EMBRYO; EMBRYO PATTERN FORMATION; FORELIMB; GENE OVEREXPRESSION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LIMB DEVELOPMENT; MICROSCOPY; MUTANT; NONHUMAN; PHENOTYPE; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA ISOLATION; SIGNAL TRANSDUCTION; UBIQUITINATION; WESTERN BLOTTING; XENOPUS; ANIMAL; GENETICS; METABOLISM; MORPHOGENESIS; MUTATION; PHYSIOLOGY; PRENATAL DEVELOPMENT;

ANIMALS; BODY PATTERNING; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; MUTATION; PHENOTYPE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; WING; WNT1 PROTEIN;

EID: 68449085657     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006543     Document Type: Article

References (57)

1. Shi Y, Massague' J (2003) Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113: 685-700.
2. Kretzschmar M, Doody J, Massagué (1997) Opposing BMP and EGF signaling pathways converge on the TGF-β family mediator Smad1. Nature 389: 618-622.
3. Pera EM, Ikeda A, Eivers E, De Robertis EM (2003) Integration of IGF, FGF and anti-BMP signals via Smad1 phosphorylation in neural induction. Genes Dev 17: 3023-3028.
4. Sapkota G, Alarcon C, Spagnoli FM, Brivanlou AH, Massagué J (2007) Balancing BMP signaling through integrated inputs into the Smad1 linker. Mol Cell 25: 441-454.
5. Fuentealba LC, Eivers E, Ikeda A, Hurtado C, Kuroda H, et al. (2007) Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131: 980-993.
6. Fuentealba LC, Eivers E, Geissert D, Taelman V, De Robertis EM (2008) Asymmetric mitosis: Unequal segregation of proteins destined for degradation. PNAS 105: 7732-7737.
7. Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Biol 20: 781-810.
8. Bilic JL, Huang YL, Davidson G, Zimmermann T, Cruciat, et al. (2007) Wnt induces LRP6 signalosomes and promotes disheveled-dependent LRP6 phosphorylation. Science 316: 1619-1622.
9. Niehrs C (2004) Regionally specific induction by the Spemann-Mangold organizer. Nat Rev Genet 6: 425-434.
10. Little SC, Mullins MC (2006) Extracellular modulation of BMP activity in patterning the dorsoventral axis. Birth Defects Res C Embryo Today 78: 224-242.
11. De Robertis EM (2008) Evo-Devo: Variations on ancestral themes. Cell 132: 185-195.
12. Eivers E, Fuentealba LC, De Robertis EM (2008) Integrating positional information at the level of Smad1/5/8. Curr Opin Genet Dev 18: 1-7.
13. 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: 1347-1358.
14. Couso JP, Bishop SA, Martinez Arias A (1994) The wingless signalling pathway and the patterning of the wing margin in Drosophila. Development 120: 621-636.
15. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-405.
16. Lecuit T, Brook WJ, Ng M, Calleja M, Sun H, et al. (1996) Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 381: 387-393.
17. Struhl G, Basler K (1993) Organizing activity of wingless protein in Drosophila. Cell 72: 527-540.
18. Gabay L, Seger R, Shilo BZ (1997) MAP kinase in situ activation atlas during Drosophila embryogenesis. Development 124: 3533-3541.
19. Lee YS, Carthew RW (2003) Making a better RNAi vector for Drosophila: use of intron spacers. Methods 30: 322-329.
20. Müller B, Hartmann B, Pyrowolakis G, Affolter M, Basler K (2003) Conversion of an extracellular Dpp/BMP morphogen gradient into an inverse transcriptional gradient. Cell 113: 221-233.
21. Baena LA, García-Bellido A (2006) Control of growth and positional information by the graded vestigial expression pattern in the wing of Drosophila melanogaster. Proc Natl Acad Sci USA 103: 13734-13739.
22. Cremazy F, Berta P, Girard F (2000) Sox neuro, a new Drosophila Sox gene expressed in the developing central nervous system. Mech Dev 93: 215-219.
23. Mizutani CM, Bier E (2008) EvoD/Vo: the origins of BMP signalling in the neuroectoderm. Nat Rev Genet 9: 663-677.
24. Rørth P (1998) Gal4 in the Drosophila female germline. Mech Dev 78: 113-118.
25. Nüsslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287: 795-801.
26. Szüts D, Freeman M, Bienz M (1997) Antagonism between EGFR and Wingless signalling in the larval cuticle of Drosophila. Development 124: 3209-3219.
27. Struhl G, Barbash DA, Lawrence PA (1997) Hedgehog acts by distinct gradient and signal relay mechanisms to organize cell type and cell polarity in the Drosophila abdomen. Development 124: 2155-2165.
28. Bejsovec A, Wieschaus E (1993) Segment polarity gene interactions modulate epidermal patterning in Drosophila embryos. Development 119: 501-517.
29. Brunner E, Peter O, Schweizer L, Basler K (1997) pangolin encodes a Lef-1 homolog that acts downstream of Armadillo to transduce the Wingless signal of Drosophila. Nature 385: 829-833.
30. Miyanga Y, Torregroza I, Evans T (2002) A maternal Smad protein regulates early embryonic apoptosis in Xenopus laevis. Mol Cell Bio 22: 1317-1328.
31. Zeng YA, Rahnama M, Wang S, Sosu-Sedzorme W, Verheyen EM (2007) Drosophila Nemo antagonizes BMP signaling by phosphorylation of Mad and inhibition of its nuclear accumulation. Development 134: 2061-2071.
32. Takaesu NT, Herbig E, Zhitomersky D, O'Connor MB, Newfeld SJ (2005) DNA-binding domain mutations in smad genes yield dominant-negative proteins or a neomorphic protein that can activate WG target genes in Drosophila. Development 132: 4883-4894.
33. O'Keefe L, Dougan ST, Gabay L, Raz E, Shilo BZ, et al. (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.
34. Affolter M, Nellen D, Nussbaumer U, Basler K (1994) Multiple requirements for the receptor serine/threonine kinase thick veins reveal novel functions of TGF beta homologs during Drosophila embryogenesis. Development 120: 3105-3117.
35. Schwyter DH, Huang JD, Dubnicoff T, Courey AJ (1995) The decapentaplegic core promoter region plays an integral role in the spatial control of transcription. Mol Cell Biol 15: 3960-3968.
36. Zeng YA, Rahnama M, Wang S, Lee W, Verheyen EM (2008) Inhibition of Drosophila Wg signaling involves competition between Mad and Armadillo/ beta-catenin for dTcf binding. PLoS ONE 3: e3893.
37. Ferguson EL, Anderson KV (1992) Localized enhancement and repression of the activity of the TGF-beta family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo. Development 114: 583-597.
38. Takaesu NT, Bulanin DS, Johnson AN, Orenic TV, Newfeld SJ (2008) A combinatorial enhancer recognized by Mad, TCF and Brinker first activates then represses dpp expression in the posterior spiracles of Drosophila. Dev Biol 313: 829-843.
39. Holley SA, Jeffrey NL, Attisano L, Wrana JL, Sasai Y, et al. (1996) The Xenopus dorsalizing factor noggin ventralizes Drosophila embryos by preventing DPP from activating its receptor. Cell 86: 607-617.
40. Kramps T, Peter O, Brunner E, Nellen D, Froesch B, et al. (2005) Wnt/ wingless signaling requires BCL9/legless-mediated recruitment of pygopus to the nuclear beta-catenin-TCF complex. Cell 109: 47-60.
41. Estella C, McKay DJ, Mann RS (2008) Molecular integration of wingless, decapentaplegic, and autoregulatory inputs into Distalless during Drosophila leg development. Dev Cell 14: 86-96.
42. Labbé E, Letamendia A, Attisano L (2000) Association of Smads with lymphoid enhancer binding factor 1/T cell-specific factor mediates cooperative signaling by the transforming growth factor-β and Wnt pathways. Proc Natl Acad Sci USA 97: 8358-8363.
43. Nishita M, Hashimoto MK, Ogata S, Laurent MN, Ueno N, et al. (2000) Interaction between Wnt and TGF-beta signalling pathways during formation of Spemann's organizer. Nature 403: 781-785.
44. Hu MC, Rosenblum ND (2005) Smad1, β-Catenin and Tcf4 associate in a molecular complex with the Myc promoter in dysplastic renal tissue and cooperate to control Myc transcription. Development 132: 215-225.
45. Pourquié O (2003) The segmentation clock: converting embryonic time into spatial pattern. Science 301: 328-330.
46. Damen WG (2007) Evolutionary conservation and divergence of the segmentation process in arthropods. Dev Dyn 236: 1379-1391.
47. Pueyo JI, Lanfear R, Couso JP (2008) Ancestral Notch-mediated segmentation revealed in the cockroach Periplaneta Americana. Proc Natl Acad Sci USA 105: 16614-16619.
48. De Robertis EM (2008) Evolutionary biology: The molecular ancestry of segmentation mechanisms. Proc Natl Acad Sci USA. 105: 16411-16412.
49. Marquez RM, Singer MA, Takaesu NT, Waldrip WR, Kraytsberg Y, et al. (2001) Transgenic analysis of the Smad family of TGF-beta signal transducers in Drosophila melanogaster suggests new roles and new interactions between family members. Genetics 157: 1639-1648.
50. Wieschaus E, Nusslein-Volhard C (2003) Looking at embryos In Drosophila, DB Roberts ed, Second Edition. Oxford, UK: Oxford University Press. pp 179-214.
51. LaLonde M, Janssens H, Yun S, Crosby J, Redina O, et al. (2006) A role for Phospholipase D in Drosophila embryonic cellularization. BMC Dev Biol 6: 60.
52. Sive HL, Grainger RM, Harland RM (2000) Early Development of Xenopus laevis: A Laboratory Manual. Cold Spring Harbor NY: Cold Spring Harbor Laboratory Press.
53. Sander V, Reversade B, De Robertis EM (2007) The opposing homeobox genes Goosecoid and Vent1/2 self-regulate Xenopus patterning. EMBO J 26: 2955-2966.
54. Kintner CR, Brockes JP (1984) Monoclonal antibodies identify blastemal cells derived from dedifferentiating limb regeneration. Nature 308: 67-69.
55. Garrity PA, Lee CH, Salecker I, Robertson HC, Desai CJ, et al. (1999) Retinal axon target selection in Drosophila is regulated by a receptor protein tyrosine phosphatase. Neuron 4: 707-717.
56. Persson U, Izumi H, Souchelnytskyi S, Itoh S, Grimsby S, et al. (1998) The L45 loop in type I receptors for TGF-beta family members is a critical determinant in specifying Smad isoform activation. FEBS Lett 434: 83-87.
57. Zecca M, Basler K, Struhl G (1995) Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 121: 2265-2278.