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Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic

Nature volume 437, pages 560–563 (2005)Cite this article

Abstract

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.

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Acknowledgements

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.

Author information

Author notes

  1. Felipe-Andrès Ramirez-Weber

    Present address: Department of Biology, Cell and Molecular Biology Group, San Francisco State University, San Francisco, California, 94132, USA

Authors and Affiliations

  1. Department of Biochemistry and Biophysics, University of California, California, 94143, San Francisco, USA

    Frank Hsiung, Felipe-Andrès Ramirez-Weber, D. David Iwaki & Thomas B. Kornberg

Authors
  1. Frank Hsiung
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  2. Felipe-Andrès Ramirez-Weber
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  3. D. David Iwaki
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Corresponding author

Correspondence to Thomas B. Kornberg.

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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). https://doi.org/10.1038/nature03951

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