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Function of the Wingless Signaling Pathway in Drosophila

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Wnt Signaling

Part of the book series: Methods in Molecular Biology ((MIMB,volume 469))

Abstract

Signaling by the wingless pathway has been shown to govern numerous developmental processes. Much of our current understanding of wingless signaling mechanisms comes from studies conducted in Drosophila melanogaster, which offers superior experimental tractability for genetic and developmental studies. Wingless signaling is highly consequential during normal development and patterning of Drosophila. Its earliest identifiable role during development of Drosophila is in the embryonic segmentation cascade, wherein wingless functions as a segment polarity gene and serves to pattern each individual segment along the antero-posterior axis of the developing embryo. Subsequent developmental roles fulfilled by wingless include patterning the developing wings, legs, eyes, CNS, heart, and muscles. Each of these developmental contexts offers excellent systems to query mechanisms regulating different aspects of wingless signal transduction such as synthesis, secretion, reception, and transcription. This chapter presents a brief overview on the functions of wingless signaling during development of Drosophila melanogaster.

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References

  1. Nusslein-Volhard, C., Wieschaus, E. (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287, 795 – 801.

    Article  PubMed  CAS  Google Scholar 

  2. Peri, F., Bokel, C., Roth, S. (1999) Local Gurken signaling and dynamic MAPK activation during Drosophila oogenesis. Mech Dev 81, 75 – 88.

    Article  PubMed  CAS  Google Scholar 

  3. Peri, F., Roth, S. (2000) Combined activities of Gurken and decapentaplegic specify dorsal chorion structures of the Drosophila egg. Development 127, 841 – 850.

    PubMed  CAS  Google Scholar 

  4. Riechmann, V., Ephrussi, A. (2001) Axis formation during Drosophila oogenesis. Curr Opin Genet Dev 11, 374 – 383.

    Article  PubMed  CAS  Google Scholar 

  5. Gerhart, J. (1999) 1998 Warkany lecture: signaling pathways in development. Teratology 60, 226 – 239.

    Article  PubMed  CAS  Google Scholar 

  6. Affolter, M., Mann, R. (2001) Development. Legs, eyes, or wings – selectors and signals make the difference. Science 292, 1080 – 1081.

    Article  PubMed  CAS  Google Scholar 

  7. Wodarz, A., Nusse, R. (1998) Mechanisms of Wnt signaling in development. Annu Rev Cell Dev Biol 14, 59 – 88.

    Article  PubMed  CAS  Google Scholar 

  8. Hulskamp, M., Pfeifle, C., Tautz, D. (1990) A morphogenetic gradient of hunchback protein organizes the expression of the gap genes Kruppel and knirps in the early Drosophila embryo. Nature 346, 577 – 580.

    Article  PubMed  CAS  Google Scholar 

  9. Irish, V., Lehmann, R., Akam, M. (1989) The Drosophila posterior-group gene nanos functions by repressing hunchback activity. Nature 338, 646 – 648.

    Article  PubMed  CAS  Google Scholar 

  10. Sanson, B. (2001) Generating patterns from fields of cells. Examples from Drosophila segmentation. EMBO Rep 2, 1083 – 1088.

    Article  PubMed  CAS  Google Scholar 

  11. DiNardo, S., Sher, E., Heemskerk-Jongens, J., et al. (1988) Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis. Nature 332, 604 – 609.

    Article  PubMed  CAS  Google Scholar 

  12. Lee, J. J., von Kessler, D.P., Parks, S., et al. (1992) Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell 71, 33 – 50.

    Article  PubMed  CAS  Google Scholar 

  13. Muller, H., Samanta, R., Wieschaus, E. (1999) Wingless signaling in the Drosophila embryo: zygotic requirements and the role of the frizzled genes. Development 126, 577 – 586.

    PubMed  CAS  Google Scholar 

  14. Lessing, D., Nusse, R. (1998) Expression of wingless in the Drosophila embryo: a conserved cis-acting element lacking conserved Ci-binding sites is required for patched-mediated repression. Development 125, 1469 – 1476.

    PubMed  CAS  Google Scholar 

  15. DiNardo, S., Heemskerk, J., Dougan, S., et al. (1994) The making of a maggot: patterning the Drosophila embryonic epidermis. Curr Opin Genet Dev 4, 529 – 534.

    Article  PubMed  CAS  Google Scholar 

  16. van den Heuvel, M., Nusse, R., Johnston, P., et al. (1989) Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication. Cell 59, 739 – 749.

    Article  PubMed  CAS  Google Scholar 

  17. Ingham, P.W., Hidalgo, A. (1993) Regulation of wingless transcription in the Drosophila embryo. Development 117, 283 – 291.

    PubMed  CAS  Google Scholar 

  18. Li, X., Noll, M. (1993) Role of the gooseberry gene in Drosophila embryos: maintenance of wingless expression by a wingless – gooseberry autoregulatory loop. Embo J 12, 4499 – 4509.

    PubMed  CAS  Google Scholar 

  19. Alexandre, C., Lecourtois, M., Vincent, J. (1999) Wingless and Hedgehog pattern Drosophila denticle belts by regulating the production of short-range signals. Development 126, 5689 – 5698.

    PubMed  CAS  Google Scholar 

  20. Lawrence, P. A., Sanson, B., Vincent, J. P. (1996) Compartments, wingless and engrailed: patterning the ventral epidermis of Drosophila embryos. Development 122, 4095 – 4103.

    PubMed  CAS  Google Scholar 

  21. Sampedro, J., Johnston, P., Lawrence, P. A. (1993) A role for wingless in the segmental gradient of Drosophila? Development 117, 677 – 687.

    PubMed  CAS  Google Scholar 

  22. Sanson, B., Alexandre, C., Fascetti, N., et al. (1999) Engrailed and hedgehog make the range of Wingless asymmetric in Drosophila embryos. Cell 98, 207 – 216.

    Article  PubMed  CAS  Google Scholar 

  23. Payre, F., A. Vincent, and S. Carreno, (1999) ovo/svb integrates Wingless and DER pathways to control epidermis differentiation. Nature 400, 271 – 275.

    Article  PubMed  CAS  Google Scholar 

  24. Howes, R., Bray, S. (2000) Pattern formation: Wingless on the move. Curr Biol 10, R222 – R226.

    Article  PubMed  CAS  Google Scholar 

  25. Ganguly, A., Jiang, J., Ip, Y. T. (2005) Dro-sophila WntD is a target and an inhibitor of the Dorsal/Twist/Snail network in the gastrulating embryo. Development 132, 3419 – 3429.

    Article  PubMed  CAS  Google Scholar 

  26. Gordon, M. D., Dionne, M. S., Schneider, D. S., et al. (2005) WntD is a feedback inhibitor of Dorsal/NF-kappaB in Dro-sophila development and immunity. Nature 437, 746 – 749.

    Article  PubMed  CAS  Google Scholar 

  27. Ng, M., Diaz-Benjumea, F. J., Cohen, S. M. (1995) Nubbin encodes a POU-domain protein required for proximal-distal patterning in the Drosophila wing. Development 121, 589 – 599.

    PubMed  CAS  Google Scholar 

  28. Rodriguez Ddel, A., Terriente, J., Galindo, M. I., et al. (2002) Different mechanisms initiate and maintain wingless expression in the Drosophila wing hinge. Development 129, 3995 – 4004.

    Google Scholar 

  29. Couso, J. P., Bate, M., Martinez-Arias, A. (1993) A wingless-dependent polar coordinate system in Drosophila imaginal discs. Science 259, 484 – 489.

    Article  PubMed  CAS  Google Scholar 

  30. Han, C., Yan, D., Belenkaya, T. Y., et al. (2005) Drosophila glypicans Dally and Dally-like shape the extracellular Wingless morphogen gradient in the wing disc. Development 132, 667 – 679.

    Article  PubMed  CAS  Google Scholar 

  31. Belenkaya, T. Y., Han, C., Yan, D., et al. (2004) Drosophila Dpp morphogen movement is independent of dynamin-mediated endocytosis but regulated by the glypican members of heparan sulfate proteoglycans. Cell 119, 231 – 244.

    Article  PubMed  CAS  Google Scholar 

  32. Diaz-Benjumea, F.J., Cohen, S. M. (1995) Serrate signals through Notch to establish a Wingless-dependent organizer at the dorsal/ventral compartment boundary of the Drosophila wing. Development 121, 4215 – 4225.

    PubMed  CAS  Google Scholar 

  33. O'Brochta, D. A., Bryant, P. J. (1985) A zone of non-proliferating cells at a lineage restriction boundary in Drosophila. Nature 313, 138 – 141.

    Article  PubMed  Google Scholar 

  34. Johnston, L. A., Edgar, B. A. (1998) Wingless and Notch regulate cell-cycle arrest in the developing Drosophila wing. Nature 394, 82 – 84.

    Article  PubMed  CAS  Google Scholar 

  35. Duronio, R. J., O'Farrell, P. H., Xie, J. E., et al. (1995) The transcription factor E2F is required for S phase during Drosophila embryogenesis. Genes Dev 9, 1445 – 1455.

    Article  PubMed  CAS  Google Scholar 

  36. Neumann, C. J., Cohen, S. M. (1996) A hierarchy of cross-regulation involving Notch, wingless, vestigial and cut organizes the dorsal/ventral axis of the Drosophila wing. Development 122, 3477 – 3485.

    PubMed  CAS  Google Scholar 

  37. Jaiswal, M., Agrawal, N., Sinha, P. (2006) Fat and Wingless signaling oppositely regulate epithelial cell-cell adhesion and distal wing development in Drosophila. Development 133, 925 – 935.

    Article  PubMed  CAS  Google Scholar 

  38. Fanto, M. McNeill, H. (2004) Planar polarity from flies to vertebrates. J Cell Sci 117, 527 – 533.

    Article  PubMed  CAS  Google Scholar 

  39. Colosimo, P. F., Tolwinski, N. S. (2006) Wnt, Hedgehog and junctional Armadillo/ beta-catenin establish planar polarity in the Drosophila embryo. PLoS ONE 1, e9.

    Article  PubMed  Google Scholar 

  40. Voas, M. G., Rebay, I. (2004) Signal integration during development: insights from the Drosophila eye. Dev Dyn 229, 162 – 175.

    Article  PubMed  CAS  Google Scholar 

  41. Haynie, J. L., Bryant, P. J. (1986) Development of the eye-antenna imaginal disc and morphogenesis of the adult head in Drosophila melanogaster. J Exp Zool 237, 293 – 308.

    Article  PubMed  CAS  Google Scholar 

  42. Curtiss, J., Mlodzik, M. (2000) Morphoge-netic furrow initiation and progression during eye development in Drosophila: the roles of decapentaplegic, hedgehog and eyes absent. Development 127, 1325 – 1336.

    PubMed  CAS  Google Scholar 

  43. Halder, G., Callaerts, P., Flister, S., et al. (1998) Eyeless initiates the expression of both sine oculis and eyes absent during Drosophila compound eye development. Development125, 2181 – 2191.

    PubMed  CAS  Google Scholar 

  44. Halder, G., Callaerts, P., Gehring, W. J. (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267, 1788 – 1792.

    Article  PubMed  CAS  Google Scholar 

  45. Pignoni, F., Zipursky, S. L. (1997) Induction of Drosophila eye development by decapen-taplegic. Development 124, 271 – 278.

    PubMed  CAS  Google Scholar 

  46. Lee, J. D., Treisman, J. E. (2001) The role of Wingless signaling in establishing the anteroposterior and dorsoventral axes of the eye disc. Development 128, 1519 – 1529.

    PubMed  CAS  Google Scholar 

  47. Baonza, A., Freeman, M. (2002) Control of Drosophila eye specification by Wingless signalling. Development 129, 5313 – 5322.

    Article  PubMed  CAS  Google Scholar 

  48. Treisman, J. E., Rubin, G. M. (1995) wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121, 3519 – 3527.

    PubMed  CAS  Google Scholar 

  49. Heberlein, U., Borod, E. R., Chanut, F. A. (1998) Dorsoventral patterning in the Drosophila retina by wingless. Development 125, 567 – 577.

    PubMed  CAS  Google Scholar 

  50. Maurel-Zaffran, C., Treisman, J. E. (2000) pannier acts upstream of wingless to direct dorsal eye disc development in Drosophila. Development 127, 1007 – 1016.

    PubMed  CAS  Google Scholar 

  51. Cavodeassi, F., Diez Del Corral, R., Campuzano, S., et al. (1999) Compartments and organising boundaries in the Drosophila eye: the role of the homeodomain Iroquois proteins. Development 126, 4933 – 4942.

    PubMed  CAS  Google Scholar 

  52. Zeidler, M. P., Perrimon, N. Strutt, D. I. (1999) Polarity determination in the Drosophila eye: a novel role for unpaired and JAK/STAT signaling. Genes Dev 13, 1342 – 1353.

    Article  PubMed  CAS  Google Scholar 

  53. Yang, C. H., Simon, M. A., McNeill, H. (1999) mirror controls planar polarity and equator formation through repression of fringe expression and through control of cell affinities. Development 126, 5857 – 5866.

    PubMed  CAS  Google Scholar 

  54. Ekas, L. A., Baeg, G. H., Flaherty, M. S., et al. (2006) JAK/STAT signaling promotes regional specification by negatively regulating wingless expression in Drosophila. Development 133, 4721 – 4729.

    Article  PubMed  CAS  Google Scholar 

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Gonsalves, F.C., DasGupta, R. (2008). Function of the Wingless Signaling Pathway in Drosophila . In: Vincan, E. (eds) Wnt Signaling. Methods in Molecular Biology, vol 469. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-60327-469-2_10

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  • DOI: https://doi.org/10.1007/978-1-60327-469-2_10

  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-60327-468-5

  • Online ISBN: 978-1-60327-469-2

  • eBook Packages: Springer Protocols

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