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Wnts as morphogens? The view from the wing of Drosophila

Nature Reviews Molecular Cell Biology volume 4, pages 321–325 (2003)Cite this article

Abstract

Morphogens are diffusible signalling molecules that pattern cellular fields by setting up differential gene expression in a concentration-dependent manner. Members of the Wnt family of signalling molecules are generally considered to be classical morphogens. However, a close analysis of their activity indicates that they do not fulfil all of the critera that are associated with the classical definition.

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Figure 1: Wingless signalling in the wing primordium of a third larval instar wing disc of Drosophila melanogaster.
Figure 2: Temporal relationship between different patterns of wingless expression and the onset and modulation of gene expression during wing development.
Figure 3: Different outcomes of concentration-dependent initiation or maintenance of gene expression.

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References

  1. Wolpert, L. Positional information revisited. Development (suppl.) 107, 3–12 (1989).

    PubMed  Google Scholar 

  2. Neumann, C. & Cohen, S. M. Morphogens and pattern formation. BioEssays 19, 721–729 (1997).

    Article  CAS  PubMed  Google Scholar 

  3. Gurdon, J. B. & Bourillot, P. -Y. Morphogen gradient interpretation. Nature 413, 797–803 (2001).

    Article  CAS  PubMed  Google Scholar 

  4. Martinez Arias, A. & Stewart, A. Molecular Principles of Animal Development (Oxford Univ. Press, Oxford, 2002).

    Google Scholar 

  5. Nusse, R. & Varmus, H. Wnt genes. Cell 69, 1073–1087 (1992).

    Article  CAS  PubMed  Google Scholar 

  6. Sharma, R. P. & Chopra, V. L. Effects of the wingless (wg1) mutation on wing and haltere development in Drosophila melanogaster. Dev. Biol. 48, 461–465 (1976).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  8. Baker, N. Molecular cloning of sequences from wingless, a segment polarity gene in Drosophila: the spatial distribution of a transcript in embryos. EMBO J. 6, 1765–1774 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Gonzalez, F., Bejsovec, A., Skaer, H. & Martinez Arias, A. Secretion and movement of the wingless gene product in Drosophila embryos. Mech. Dev. 35, 43–54 (1991).

    Article  CAS  PubMed  Google Scholar 

  10. Stringini, M. & Cohen, S. M. Wingless gradient formation in the Drosophila wing. Curr. Biol. 10, 293–300 (2000).

    Article  Google Scholar 

  11. Bejsovec, A. & Martinez Arias, A. Roles of wingless in the patterning of the epidermis in Drosophila. Development 113, 471–485 (1991).

    CAS  PubMed  Google Scholar 

  12. Baylies, M. K., Martinez Arias, A. & Bate, M. wingless is required for the formation of a subset of muscle founder cells during Drosophila embryogenesis. Development 121, 3829–3837 (1995).

    CAS  PubMed  Google Scholar 

  13. Ingham, P. & Martinez Arias, A. Boundaries and fields in early embryos. Cell 68, 221–235 (1992).

    Article  CAS  PubMed  Google Scholar 

  14. Martinez Arias, A., Baker, N. & Ingham, P. The role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo. Development 103, 157–170 (1988).

    CAS  PubMed  Google Scholar 

  15. Di Nardo, S., Sher, E., Heemskerk-Jongens, J., Kassis, J. A. & O'Farrell, P. H. Two tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis. Nature 332, 604–609 (1988).

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  17. Struhl, G. & Basler, K. Organizing activity of wingless protein in Drosophila. Cell 72, 527–540 (1993).

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  19. Zecca, M., Basler, K. & Struhl, G. Direct and long range action of a wingless morphogen gradient. Cell 87, 833–844 (1996).

    Article  CAS  PubMed  Google Scholar 

  20. Klein, T. & Martinez Arias, A. Different spatial and temporal interactions between Notch, wingless and vestigial specify proximal and distal pattern elements of the wing in Drosophila. Dev. Biol. 194, 196–212 (1998).

    Article  CAS  PubMed  Google Scholar 

  21. Klein, T. & Martinez Arias, A. The Vestigial gene product provides a molecular context for the interpretation of signals during the development of the wing in Drosophila. Development 126, 913–925 (1999).

    CAS  PubMed  Google Scholar 

  22. Martinez Arias, A. The informational content of gradients of Wnt proteins. Sci. STKE 43, PE1 (2000).

    Google Scholar 

  23. Ng, M., Diaz Benjumea, F. J., Vincent, J. P., Wu, J. & Cohen, S. M. Specification of the wing primordium in Drosophila. Nature 381, 316–319 (1996).

    Article  CAS  PubMed  Google Scholar 

  24. Garcia-Garcia, M. J., Ramain, P., Simpson, P. & Modolell, J. Different contributions of pannier and wingless to the patterning of the dorsal mesothorax of Drosophila. Development 126, 3523–3532 (1999).

    CAS  PubMed  Google Scholar 

  25. Phillips, R. G, Warner, N. L. & Whittle, J. R. Wingless signaling leads to an asymmetric response to decapentaplegic-dependent signaling during sense organ patterning on the notum of Drosophila melanogaster. Dev. Biol. 207, 150–162 (1999).

    Article  CAS  PubMed  Google Scholar 

  26. Couso, J. P., Bishop, S. & Martinez Arias, A. The wingless signalling pathway and the patterning of the wing margin. Development 120, 621–636 (1994).

    CAS  PubMed  Google Scholar 

  27. Martinez Arias, A., Zecchini, V. & Brennan, K. CSL-independent Notch signalling: a checkpoint in cell fate decisions in development? Curr. Opin. Genet. Dev. 12, 524–533 (2002).

    Article  PubMed  Google Scholar 

  28. Galceran, J., Hsu, S. C. & Grosschedl, R. Rescue of a Wnt mutation by an activated form of LEF-1: regulation of maintenance but not initiation of Brachyury expression. Proc. Natl Acad. Sci. USA 98, 8668–8673 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Wheeler, J. C., VanderZwan, C., Xu, X., Swantek, D., Tracey, W. D. & Gergen J. P. Distinct in vivo requirements for establishment versus maintenance of transcriptional repression. Nature Genet. 32, 206–210 (2002).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

I would like to thank M. González Gaitán, O. Grimm and T. Klein for their very useful discussions during the gestation of this piece. My work is funded by The Wellcome Trust, UK.

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  1. the Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, UK

    Alfonso Martinez Arias

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  1. Alfonso Martinez Arias
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DATABASES

LocusLink

ac

apterous

Delta

Dll

en

eve

ftz

Hh

Notch

ovo/shaven-baby

Suppressor of Hairless

vg

wg

FURTHER INFORMATION

Alfonso Martinez Arias's laboratory

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Martinez Arias, A. Wnts as morphogens? The view from the wing of Drosophila. Nat Rev Mol Cell Biol 4, 321–325 (2003). https://doi.org/10.1038/nrm1078

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