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Localized hedgehog activity controls spatial limits of wingless transcription in the Drosophila embryo

Abstract

CELL patterning in the body segments of the Drosophila embryo requires activity of the segment polarity genes, a molecularly heterogeneous group defined by a generic mutant phenotype1. Two of these genes, wingless (wg) and hedgehog (hh), encode proteins that enter the secretory pathway2–4, implicating them as signals that instruct the fates of neighbouring cells5. Genetic analysis has identified wg transcription as one of the targets of hh activity6,7 and it has been suggested that the spatial control of wg expression depends on the limited range of the hh signal and the differential competence of responding cells8.I have tested this model by driving ubiquitous expression of the hh gene using the HspTO promoter. Here I report that, as predicted, this causes the ectopic activation of wg in only a subset of the cells of each parasegment. Using another target of hh activity as a probe, I demonstrate that the competence of cells to express wg is independent of their ability to receive the hh signal. Finally, I show that wg activation requires the function of the segment polarity gene fused, suggesting that the putative hh signal is transduced by the serine/threonine kinase that fused encodes.

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References

  1. Nüsslein-Volhard, C. & Wieschaus, E. Nature 287, 795–801 (1980).

    Article  ADS  Google Scholar 

  2. van den Heuvel, M., Nusse, R., Johnston, P. & Lawrence, P. A. Cell 59, 739–749 (1989).

    Article  CAS  Google Scholar 

  3. Gonzalez, F., Swales, L., Bejsovec, A., Skaer, H. & Martinez-Arías, A. Mech. Dev. 35, 43–54 (1991).

    Article  CAS  Google Scholar 

  4. Lee, J. J., von Kessler, D. P., Parks, S. & Beachy, P. A. Cell 71, 33–50 (1992).

    Article  CAS  Google Scholar 

  5. Ingham, P. W. & Martinez-Arías, A. Cell 68, 221–235 (1992).

    Article  CAS  Google Scholar 

  6. Hidalgo, A. & Ingham, P. Development 110, 291–301 (1990).

    CAS  PubMed  Google Scholar 

  7. Ingham, P. W. & Hidalgo, A. Development 117, 283–291 (1993).

    CAS  Google Scholar 

  8. Ingham, P. W., Taylor, A. M. & Nakano, Y. Nature 353, 184–187 (1991).

    Article  ADS  CAS  Google Scholar 

  9. Martinez-Arías, A. & Lawrence, P. A. Nature 313, 639–642 (1985).

    Article  ADS  Google Scholar 

  10. Baker, N. E. EMBO J. 6, 1765–1773 (1987).

    Article  CAS  Google Scholar 

  11. Mohler, J. & Vani, K. Development 115, 957–971 (1992).

    CAS  Google Scholar 

  12. Tabata, T., Eaton, S. & Kornberg, T. B. Genes Dev. 6, 2635–2645 (1992).

    Article  CAS  Google Scholar 

  13. Tashiro, S. et al. Gene 124, 183–189 (1993).

    Article  CAS  Google Scholar 

  14. Rijsewijk, F. et al. Cell 50, 649–657 (1987).

    Article  CAS  Google Scholar 

  15. Taylor, A. M., Nakano, Y., Mohler, J. & Ingham, P. W. Mech. Dev. 43, 89–96 (1993).

    Article  Google Scholar 

  16. Hooper, J. & Scott, M. P. Cell 59, 751–765 (1989).

    Article  CAS  Google Scholar 

  17. Nakano, Y. et al. Nature 341, 508–513 (1989).

    Article  ADS  CAS  Google Scholar 

  18. Martinez-Arías, A., Baker, N. & Ingham, P. W. Development 103, 157–170 (1988).

    PubMed  Google Scholar 

  19. Martinez-Arías, A., J. Embryol. exp. Morph. 87, 99–114 (1985).

    PubMed  Google Scholar 

  20. Preat, T. et al. Nature 347, 87–89 (1990).

    Article  ADS  CAS  Google Scholar 

  21. Limbourg-Bouchon, B., Busson, D. & Lamour-Isnard, C. Development 112, 417–429 (1991).

    CAS  PubMed  Google Scholar 

  22. DiNardo, S., Sher, E., Heemskerk-Jongens, J., Kassis, J. & O'Farrell, P. H. Nature 332, 604–609 (1988).

    Article  ADS  CAS  Google Scholar 

  23. Noordermeer, J., Johnston, P., Rijsewijk, F., Nusse, R. & Lawrence, P. A. Development 116, 711–719 (1992).

    CAS  PubMed  Google Scholar 

  24. Dougan, S. & DiNardo, S. Nature 360, 347–350 (1992).

    Article  ADS  CAS  Google Scholar 

  25. Bejsovec, A. & Martinez-Arías, M. Development 113, 471–485 (1991).

    CAS  Google Scholar 

  26. Thummel, C. S., Boulet, A. M. & Lipshitz, H. D. Gene 74, 445–456 (1988).

    Article  CAS  Google Scholar 

  27. Roberts, D. B. in Drosophila: a Practical Approach (ed. Roberts, D. B.) 1–38 (IRL, Oxford, 1986).

    Google Scholar 

  28. DiNardo, S., Kuner, J. M., Theis, J. & O'Farrell, P. J. Cell 43, 59–69 (1985).

    Article  CAS  Google Scholar 

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Ingham, P. Localized hedgehog activity controls spatial limits of wingless transcription in the Drosophila embryo. Nature 366, 560–562 (1993). https://doi.org/10.1038/366560a0

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