Regulated delivery controls Drosophila Hedgehog, Wingless and Decapentaplegic signaling

Morphogen signaling proteins disperse across tissues to activate signal transduction in target cells. We investigated dispersion of Hedgehog (Hh), Wnt homolog Wingless (Wg), and Bone morphogenic protein homolog Decapentaplegic (Dpp) in the Drosophila wing imaginal disc. We discovered that delivery of Hh, Wg, and Dpp to their respective targets is regulated. We found that <5% of Hh and <25% of Wg are taken up by disc cells and activate signaling. The amount of morphogen that is taken up and initiates signaling did not change when the level of morphogen expression was varied between 50-200% (Hh) or 50-350% (Wg). Similar properties were observed for Dpp. We analyzed an area of 150 mm x 150 mm that includes Hh-responding cells of the disc as well as overlying tracheal cells and myoblasts that are also activated by disc-produced Hh. We found that the extent of signaling in the disc was unaffected by the presence or absence of the tracheal and myoblast cells, suggesting that the mechanism that disperses Hh specifies its destinations to particular cells, and that target cells do not take up Hh from a common pool.

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Regulated delivery controls Drosophila Hedgehog, Wingless and Decapentaplegic signaling

10.1101/2020.08.12.247759 ◽

2020 ◽

Author(s):

Ryo Hatori ◽

Thomas B. Kornberg

Keyword(s):

Signal Transduction ◽

Imaginal Disc ◽

Wing Disc ◽

Bone Morphogenic Protein ◽

Wing Imaginal Disc ◽

Target Cells ◽

Signaling Proteins ◽

Common Pool ◽

Drosophila Wing ◽

Disc Cells

AbstractMorphogen signaling proteins disperse across tissues to activate signal transduction in target cells. We investigated dispersion of Hedgehog (Hh), Wingless (Wg), and Bone morphogenic protein homolog Decapentaplegic (Dpp) in the Drosophila wing imaginal disc, and found that delivery to targets is regulated. Cells take up <5% Hh produced, and neither amounts taken up nor extent of signaling changes under conditions of Hh production from 50-200% normal amounts. Similarly, cells take up <25% Wg produced, and variation in Wg production from 50-700% normal has no effect on amounts taken up or signaling. Similar properties were observed for Dpp. Wing disc-produced Hh signals to disc-associated tracheal and myoblast as well as an approximately equal number of disc cells, but the extent of signaling in the disc is unaffected by the presence or absence of the tracheal cells and myoblasts. These findings show that target cells do not take up signaling proteins from a common pool and that both the amount and destination of delivered morphogens are regulated..SummaryThe extent of Hh, Wg, and Dpp signaling is independent of the amount of signal produced or the number of recipient cells.

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Hedgehog Signal Transduction in the Posterior Compartment of the Drosophila Wing Imaginal Disc

Molecular Cell ◽

10.1016/s1097-2765(00)00046-0 ◽

2000 ◽

Vol 6 (2) ◽

pp. 479-485 ◽

Cited By ~ 21

Author(s):

F.-A. Ramírez-Weber ◽

D.J. Casso ◽

P. Aza-Blanc ◽

T. Tabata ◽

T.B. Kornberg

Keyword(s):

Signal Transduction ◽

Imaginal Disc ◽

Wing Imaginal Disc ◽

Posterior Compartment ◽

Drosophila Wing ◽

Hedgehog Signal Transduction ◽

Hedgehog Signal

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Microarray Comparison of Anterior and Posterior Drosophila Wing Imaginal Disc Cells Identifies Novel Wing Genes

G3 Genes|Genome|Genetics ◽

10.1534/g3.113.006569 ◽

2013 ◽

Vol 3 (8) ◽

pp. 1353-1362 ◽

Cited By ~ 11

Author(s):

Daniel M. Ibrahim ◽

Brian Biehs ◽

Thomas B. Kornberg ◽

Ansgar Klebes

Keyword(s):

Imaginal Disc ◽

Wing Imaginal Disc ◽

Drosophila Wing ◽

Disc Cells

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Compartments and the control of growth in the Drosophila wing imaginal disc

Development ◽

10.1242/dev.02618 ◽

2006 ◽

Vol 133 (22) ◽

pp. 4421-4426 ◽

Cited By ~ 40

Author(s):

F. A. Martin ◽

G. Morata

Keyword(s):

Imaginal Disc ◽

Wing Imaginal Disc ◽

Drosophila Wing

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Control of growth and patterning of the Drosophila wing imaginal disc by EGFR-mediated signaling

Development ◽

10.1242/dev.129.6.1369 ◽

2002 ◽

Vol 129 (6) ◽

pp. 1369-1376 ◽

Cited By ~ 2

Author(s):

Myriam Zecca ◽

Gary Struhl

Keyword(s):

Gene Expression ◽

Imaginal Disc ◽

Ectopic Expression ◽

Growth Factor Receptor ◽

Wing Disc ◽

Wing Imaginal Disc ◽

Egfr Signaling ◽

Drosophila Wing ◽

Compartment Boundary ◽

Egfr Ligand

The subdivision of the Drosophila wing imaginal disc into dorsoventral (DV) compartments and limb-body wall (wing-notum) primordia depends on Epidermal Growth Factor Receptor (EGFR) signaling, which heritably activates apterous (ap) in D compartment cells and maintains Iroquois Complex (Iro-C) gene expression in prospective notum cells. We examine the source, identity and mode of action of the EGFR ligand(s) that specify these subdivisions. Of the three known ligands for the Drosophila EGFR, only Vein (Vn), but not Spitz or Gurken, is required for wing disc development. We show that Vn activity is required specifically in the dorsoproximal region of the wing disc for ap and Iro-C gene expression. However, ectopic expression of Vn in other locations does not reorganize ap or Iro-C gene expression. Hence, Vn appears to play a permissive rather than an instructive role in organizing the DV and wing-notum segregations, implying the existance of other localized factors that control where Vn-EGFR signaling is effective. After ap is heritably activated, the level of EGFR activity declines in D compartment cells as they proliferate and move ventrally, away from the source of the instructive ligand. We present evidence that this reduction is necessary for D and V compartment cells to interact along the compartment boundary to induce signals, like Wingless (Wg), which organize the subsequent growth and differentiation of the wing primordium.

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