Abstract
INTERACTION between distinctly specified cells in adjacent compartments establishes organizing centres that control growth and specify cell fate in the developing limbs of Drosophila1–5. Localized expression of the secreted Hedgehog protein (Hh) by cells in the posterior compartment6–8 induces expression of the secreted signalling molecules decapentaplegic (dpp) or wingless (wg) in nearby anterior cells2,3. wg and dpp in turn organize spatial pattern in the wing and leg imaginal discs2,4,9. The Hh signal is thought to act by antagonizing the ability of the patched (ptc) gene product to repress wg and dpp expression10–14. Here we present evidence that removing activity of the gene encoding cyclic AMP-dependent protein kinase A (pka) is functionally equivalent to removing ptc activity or to providing cells with the Hh signal. These findings suggest that cyclic AMP-dependent protein kinase A is a component of the signal transduction pathway through which Hh and Ptc direct localized expression of dpp (or wg) and establish the compartment boundary organizer.
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References
Diaz-Benjumea, F. J. & Cohen, S. M. Cell 75, 741–752 (1993).
Basler, K. & Struhl, G. Nature 368, 208–214 (1994).
Tabata, T. & Kornberg, T. Cell 76, 89–102 (1994).
Diaz-Benjumea, F. J., Cohen, B. & Cohen, S. M. Nature 372, 175–179 (1994).
Irvine, K. & Wieschaus, E. Cell 79, 595–606 (1994).
Mohler, J. & Vani, K. Development 115, 957–971 (1992).
Lee, J. J., von Kessler, D. P., Parks, S. & Beachy, P. A. Cell 71, 33–50 (1992).
Tabata, T., Eaton, S. & Kornberg, T. B. Genes Dev. 6, 2635–2645 (1992).
Capdevila, J. & Guerrero, I. EMBO J. 13, 4459–4468 (1994).
Ingham, P. W., Taylor, A. M. & Nakano, Y. Nature 353, 184–187 (1991).
Ingham, P. W. Nature 366, 560–562 (1993).
Schuske, K., Hooper, J. E. & Scott, M. P. Devl Biol. 164, 300–311 (1994).
Capdevila, J., Estrada, M. P., Sánchez-Herrero, E. & Guerrero, I. EMBO J. 13, 71–82 (1994).
Forbes, A. J., Nakano, Y., Taylor, A. M. & Ingham, P. W. Development suppl. 115–124 (1993).
Kalderon, D. & Rubin, G. Genes Dev. 2, 1539–1556 (1988).
Phillips, R. G., Roberts, I. J. H., Ingham, P. W. & Whittle, J. R. S. Development 110, 105–114 (1990).
Grau, Y. & Simpson, P. Devl Biol. 122, 186–200 (1987).
Raferty, L. A., Sanicola, M., Blackman, R. K. & Gelbart, W. M. Development 113, 27–33 (1991).
Nakano, Y., Guerrero, I., Hidalgo, A., Whittle, J. R. S. & Ingham, P. W. Nature 341, 508–513 (1989).
Hooper, J. & Scott, M. P. Cell 59, 751–765 (1989).
Watson, S. & Arkinstall, S. The G-Protein Linked Receptors (Academic, London, 1994).
Stradler, C. D., Fong, T. M., Tota, M. & Underwood, D. A. Rev. Biochem. 63, 101–132 (1994).
Devreotes, P. Neuron 12, 235–241 (1994).
Hartwell, L. Nature 371, 286 (1994).
Lane, M. E. & Kalderon, D. Genes Dev. 8, 2986–2995 (1994).
Török, T., Tick, G., Alvarado, M. & Kiss, I. Genetics 135, 71–80 (1993).
Blackman, R. K., Sanicola, M., Raftery, L. A., Gillevet, T. & Gelbart, W. M. Development 111, 657–665 (1991).
Xu, T. & Rubin, G. M. Development 117, 1223–1237 (1993).
Bejsovec, A. & Wieschaus, E. Development 119, 501–517 (1993).
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Lepage, T., Cohen, S., Diaz-Benjumea, F. et al. Signal transduction by cAMP-dependent protein kinase A in Drosophila limb patterning. Nature 373, 711–715 (1995). https://doi.org/10.1038/373711a0
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DOI: https://doi.org/10.1038/373711a0
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