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Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs

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Abstract

THE appendage primordia of Drosophila are subdivided into compartments1–4 by the localized expression of transcription factors5–7. Interaction between cells in adjacent compartments establishes organizing centres responsible for generating spatial pattern and promoting cell proliferation in the developing appendages7–9. Localized expression of hedgehog (hh) in the pos-terior compartment of the leg imaginal disc directs expression of wingless (wg) in ventral–anterior cells and decapentaplegic (dpp) in dorsal–anterior cells near the anterior–posterior compartment boundary8; wg then acts to specify ventral cell fate10–12 and to organize the dorsal–ventral axis of the leg13,14. Interaction between wg-expressing ventral cells and dorsal cells near the anterior–posterior compartment boundary promotes axis formation in the leg14,15. Here we show that the combined action of wg-expressing cells in the ventral–anterior compartment and dpp-expressing cells in the dorsal–anterior compartment activates expression of Distalless, a gene required for proximal–distal axis formation in the limbs. These results demonstrate that sequential interaction between anterior–posterior and dorsal–ventral compartments establishes the proximal–distal axis of the limbs.

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References

  1. Garcia-Bellido, A., Ripoll, P. & Morata, G. Nature New Biol. 245, 251–253 (1973).

    Article  CAS  Google Scholar 

  2. Morata, G. & Lawrence, P. A. Nature 255, 614–617 (1975).

    Article  ADS  CAS  Google Scholar 

  3. Lawrence, P. A. & Morata, G. Devl Biol. 50, 321–337 (1976).

    Article  CAS  Google Scholar 

  4. Kornberg, T. Proc. natn. Acad. Sci. U.S.A. 78, 1095–1099 (1981).

    Article  ADS  CAS  Google Scholar 

  5. Kornberg, T., Siden, I., O'Farrell, P. & Simon, M. Cell 40, 45–53 (1985).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Diaz-Benjumea, F. J. & Cohen, S. M. Cell 75, 741–752 (1993).

    Article  CAS  Google Scholar 

  8. Basler, K. & Struhl, G. Nature 368, 208–214 (1994).

    Article  ADS  CAS  Google Scholar 

  9. Williams, J. A., Paddock, S. W., Vorwerk, K. & Carroll, S. B. Nature 368, 299–305 (1994).

    Article  ADS  CAS  Google Scholar 

  10. Baker, N. E. Devl Biol. 125, 96–108 (1988).

    Article  CAS  Google Scholar 

  11. Peifer, M., Rauskolb, C., Williams, M., Riggleman, B. & Wieschaus, E. Development 111, 1029–1043 (1991).

    CAS  Google Scholar 

  12. Couso, J. P., Bate, M. & Martinez-Arias, A. Science 259, 484–489 (1993).

    Article  ADS  CAS  Google Scholar 

  13. Stohl, G. & Basler, K. Cell 72, 527–540 (1993).

    Article  Google Scholar 

  14. Diaz-Benjumea, F. J. & Cohen, S. M. Development 120, 1661–1670 (1994).

    CAS  Google Scholar 

  15. Campbell, G., Weaver, T. & Tomlinson, A. Cell 74, 1113–1123 (1993).

    Article  CAS  Google Scholar 

  16. Cohen, S. M., Brönner, G., Küttner, F., Jürgens, G. & Jäckle, H. Nature 338, 432–434 (1989).

    Article  ADS  CAS  Google Scholar 

  17. Sunkel, C. E. & Whittle, J. R. S. Wilhelm Roux Arch. dev. Biol. 196, 124–132 (1987).

    Article  Google Scholar 

  18. Cohen, S. M. & Jürgens, G. EMBO J. 8, 2045–2055 (1989).

    Article  CAS  Google Scholar 

  19. Cohen, S. M. & Jürgens, G. Wilhelm Roux Arch. dev. Biol. 198, 157–169 (1989).

    Article  Google Scholar 

  20. Cohen, B., Simcox, A. A. & Cohen, S. M. Development 117, 597–608 (1993).

    CAS  Google Scholar 

  21. Schubiger, G. Wilhelm Roux Arch. EntwMech. Org. 160, 9–40 (1968).

    Article  Google Scholar 

  22. Masucci, J. D., Miltenberger, R. J. & Hoffman, F. M. Genes Dev. 4, 2011–2023 (1990).

    Article  CAS  Google Scholar 

  23. Raftery, L. A., Sanicola, M., Blackman, R. K. & Gelbart, W. M. Development 113, 27–33 (1991).

    CAS  Google Scholar 

  24. Spencer, F., Hoffman, M. & Gelbart, W. M. Cell 28, 451–461 (1982).

    Article  CAS  Google Scholar 

  25. Tabata, T. & Kornberg, T. Cell 76, 89–102 (1994).

    Article  CAS  Google Scholar 

  26. Meinhardt, H. Devl Biol. 96, 375–385 (1983).

    Article  CAS  Google Scholar 

  27. Vachon, G. et al. Cell 71, 437–450 (1992).

    Article  CAS  Google Scholar 

  28. St. Johnston, R. D. et al. Genes Dev. 4, 1114–1127 (1990).

    Article  CAS  Google Scholar 

  29. Blackman, R. K., Sanicola, M., Raftery, L. A., Gillevet, T. & Gelbart, W. M. Development 111, 657–665 (1991).

    CAS  Google Scholar 

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Authors and Affiliations

  1. Differentiation Programme, European Molecular Biology Laboratory, Postfach 10.2209, 69012, Heidelberg, Germany

    Fernando J. Diaz-Benjumea, Barbara Cohen & Stephen M. Cohen

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  1. Fernando J. Diaz-Benjumea
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  2. Barbara Cohen
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  3. Stephen M. Cohen
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Diaz-Benjumea, F., Cohen, B. & Cohen, S. Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs. Nature 372, 175–179 (1994). https://doi.org/10.1038/372175a0

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  • DOI: https://doi.org/10.1038/372175a0

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