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.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Hedgehog mediated degradation of Ihog adhesion proteins modulates cell segregation in Drosophila wing imaginal discs
Nature Communications Open Access 02 November 2017
-
Proximal–distal axis formation in the Drosophila leg
Nature Open Access 10 July 1997
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
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).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/373711a0
This article is cited by
-
Control of the Hedgehog pathway by compartmentalized PKA in the primary cilium
Science China Life Sciences (2022)
-
Hedgehog mediated degradation of Ihog adhesion proteins modulates cell segregation in Drosophila wing imaginal discs
Nature Communications (2017)
-
Protein kinase-X interacts with Pin-1 and Polycystin-1 during mouse kidney development
Kidney International (2009)
-
Hedgehog signalling activity of Smoothened requires phosphorylation by protein kinase A and casein kinase I
Nature (2004)
-
Proximal–distal axis formation in the Drosophila leg
Nature (1997)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.