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Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic


The anterior/posterior (A/P) and dorsal/ventral (D/V) compartment borders that subdivide the wing imaginal discs of Drosophila third instar larvae are each associated with a developmental organizer. Decapentaplegic (Dpp), a member of the transforming growth factor-β (TGF-β) superfamily, embodies the activity of the A/P organizer. It is produced at the A/P organizer and distributes in a gradient of decreasing concentration to regulate target genes, functioning non-autonomously to regulate growth and patterning of both the anterior and posterior compartments1,2,3. Wingless (Wg) is produced at the D/V organizer and embodies its activity4,5. The mechanisms that distribute Dpp and Wg are not known, but proposed mechanisms include extracellular diffusion6, successive transfers between neighbouring cells7,8, vesicle-mediated movement9, and direct transfer via cytonemes10. Cytonemes are actin-based filopodial extensions that have been found to orient towards the A/P organizer from outlying cells. Here we show that in the wing disc, cytonemes orient towards both the A/P and D/V organizers, and that their presence and orientation correlates with Dpp signalling. We also show that the Dpp receptor, Thickveins (Tkv), is present in punctae that move along cytonemes. These observations are consistent with a role for cytonemes in signal transduction.

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Figure 1: Cytoneme profile.
Figure 2: Dpp maintains A/P cytoneme orientation.
Figure 3: Dpp overexpression induces cytoneme extensions.
Figure 4: Cytonemes contain motile Tkv punctae.
Figure 5: Distinct apical and basal cytonemes in the wing disc.


  1. Basler, K. & Struhl, G. Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208–214 (1994)

    ADS  CAS  Article  Google Scholar 

  2. Tabata, T. & Kornberg, T. B. Hedgehog is a signalling protein with a key role in patterning Drosophila imaginal discs. Cell 76, 89–102 (1994)

    CAS  Article  Google Scholar 

  3. Tabata, T. & Takei, Y. Morphogens, their identification and regulation. Development 131, 703–712 (2004)

    CAS  Article  Google Scholar 

  4. 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 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  7. Kerszberg, M. & Wolpert, L. Mechanisms for positional signalling by morphogen transport: a theoretical study. J. Theor. Biol. 191, 103–114 (1998)

    CAS  Article  Google Scholar 

  8. Entchev, E. V., Schwabedissen, A. & Gonzalez-Gaitan, M. Gradient formation of the TGF-β homolog Dpp. Cell 103, 981–991 (2000)

    CAS  Article  Google Scholar 

  9. Panakova, D., Sprong, H., Marois, E., Thiele, C. & Eaton, S. Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 435, 58–65 (2005)

    ADS  CAS  Article  Google Scholar 

  10. Ramirez-Weber, F. A. & Kornberg, T. B. Cytonemes: cellular processes that project to the principal signalling center in Drosophila imaginal discs. Cell 97, 599–607 (1999)

    CAS  Article  Google Scholar 

  11. Sato, M. & Saigo, K. Involvement of pannier and u-shaped in regulation of decapentaplegic-dependent wingless expression in developing Drosophila notum. Mech. Dev. 93, 127–138 (2000)

    CAS  Article  Google Scholar 

  12. Moreno, E., Basler, K. & Morata, G. Cells compete for Decapentaplegic survival factor to prevent apoptosis in Drosophila wing development. Nature 416, 755–759 (2002)

    ADS  CAS  Article  Google Scholar 

  13. Nellen, D., Burke, R., Struhl, G. & Basler, K. Direct and long-range action of a DPP morphogen gradient. Cell 85, 357–368 (1996)

    CAS  Article  Google Scholar 

  14. Zigmond, S. H. Recent quantitative studies of actin filament turnover during cell locomotion. Cell Motil. Cytoskeleton 25, 309–316 (1993)

    CAS  Article  Google Scholar 

  15. Kranewitter, W. J., Danninger, C. & Gimona, M. GEF at work: Vav in protruding filopodia. Cell Motil. Cytoskeleton 49, 154–160 (2001)

    CAS  Article  Google Scholar 

  16. Teleman, A. A. & Cohen, S. M. Dpp gradient formation in the Drosophila wing imaginal disc. Cell 103, 971–980 (2000)

    CAS  Article  Google Scholar 

  17. Ribeiro, C., Ebner, A. & Affolter, M. In vivo imaging reveals different cellular functions for FGF and Dpp signalling in tracheal branching morphogenesis. Dev. Cell 2, 677–683 (2002)

    CAS  Article  Google Scholar 

  18. Wolf, C., Gerlach, N. & Schuh, R. Drosophila tracheal system formation involves FGF-dependent cell extensions contacting bridge cells. EMBO Rep. 3, 563–568 (2002)

    CAS  Article  Google Scholar 

  19. Sato, M. & Kornberg, T. B. FGF is an essential mitogen and chemoattractant for the air sacs of the Drosophila tracheal system. Dev. Cell 3, 195–207 (2002)

    CAS  Article  Google Scholar 

  20. De Joussineau, C. et al. Delta-promoted filopodia mediate long-range lateral inhibition in Drosophila. Nature 426, 555–559 (2003)

    ADS  CAS  Article  Google Scholar 

  21. Chou, Y. H. & Chien, C. T. Scabrous controls ommatidial rotation in the Drosophila compound eye. Dev. Cell 3, 839–850 (2002)

    CAS  Article  Google Scholar 

  22. Akiyama-Oda, Y. & Oda, H. Early patterning of the spider embryo: a cluster of mesenchymal cells at the cumulus produces Dpp signals received by germ disc epithelial cells. Development 130, 1735–1747 (2003)

    CAS  Article  Google Scholar 

  23. Lidke, D. S. et al. Quantum dot ligands provide new insights into erbB/HER receptor-mediated signal transduction. Nature Biotechnol. 22, 198–203 (2004)

    CAS  Article  Google Scholar 

  24. Brand, A. H. & Perrimon, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415 (1993)

    CAS  Google Scholar 

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We gratefully acknowledge many helpful discussions with G. Ehrenkaufer, and thank K. Moses, E. Bier, L. Luo, and F. Chanut for fly stocks. This work was supported by a grant from the NIH to T.B.K.

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Correspondence to Thomas B. Kornberg.

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Reprints and permissions information is available at The authors declare no competing financial interests.

Supplementary information

Supplementary Tables S1 and S2

Supplementary Table S1: regional differences of cytoneme length in the wing disc. Supplementary Table S2: distribution of Tkv:GFP punctae in flattened and unflattened wing discs. (DOC 31 kb)

Supplementary Figure S1

Profiles of uncompressed and compressed wing discs. (PDF 961 kb)

Supplementary Figure Legend

Full text description of the above Supplementary Figure. (DOC 19 kb)

Supplementary Video S1

Punctae are motile, moving in both anterograde and retrograde directions and associate with cytonemes. (MOV 3527 kb)

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Hsiung, F., Ramirez-Weber, FA., David Iwaki, D. et al. Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic. Nature 437, 560–563 (2005).

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