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

Development ◽  
2002 ◽  
Vol 129 (6) ◽  
pp. 1369-1376 ◽  
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.

Subdivision of the Drosophila wing imaginal disc by EGFR-mediated signaling

Development ◽  
2002 ◽  
Vol 129 (6) ◽  
pp. 1357-1368 ◽  
Author(s):  
Myriam Zecca ◽  
Gary Struhl
Keyword(s):  
Imaginal Disc ◽  
Growth Factor Receptor ◽  
Subsequent Development ◽  
Wing Disc ◽  
Wing Imaginal Disc ◽  
Egfr Signaling ◽  
Drosophila Wing ◽  
Compartment Boundary ◽  
Epidermal Growth ◽  
Necessary And Sufficient

Growth and patterning of the Drosophila wing imaginal disc depends on its subdivision into dorsoventral (DV) compartments and limb (wing) and body wall (notum) primordia. We present evidence that both the DV and wing-notum subdivisions are specified by activation of the Drosophila Epidermal Growth Factor Receptor (EGFR). We show that EGFR signaling is necessary and sufficient to activate apterous (ap) expression, thereby segregating the wing disc into D (ap-ON) and V (ap-OFF) compartments. Similarly, we demonstrate that EGFR signaling directs the expression of Iroquois Complex (Iro-C) genes in prospective notum cells, rendering them distinct from, and immiscible with, neighboring wing cells. However, EGFR signaling acts only early in development to heritably activate ap, whereas it is required persistently during subsequent development to maintain Iro-C gene expression. Hence, as the disc grows, the DV compartment boundary can shift ventrally, beyond the range of the instructive EGFR signal(s), in contrast to the notum-wing boundary, which continues to be defined by EGFR input.

Boundaries in the Drosophila wing imaginal disc organize vein-specific genetic programs

Development ◽  
1998 ◽  
Vol 125 (21) ◽  
pp. 4245-4257 ◽  
Author(s):  
B. Biehs ◽  
M.A. Sturtevant ◽  
E. Bier
Keyword(s):  
Gene Expression ◽  
Cell Fate ◽  
Short Range ◽  
Imaginal Disc ◽  
Larval Instar ◽  
Wing Imaginal Disc ◽  
Control Of Gene Expression ◽  
Present Evidence ◽  
The Third ◽  
Drosophila Wing

Previous studies have suggested that vein primordia in Drosophila form at boundaries along the A/P axis between discrete sectors of the larval wing imaginal disc. Genes involved in initiating vein development during the third larval instar are expressed either in narrow stripes corresponding to vein primordia or in broader ‘provein’ domains consisting of cells competent to become veins. In addition, genes specifying the alternative intervein cell fate are expressed in complementary intervein regions. The regulatory relationships between genes expressed in narrow vein primordia, in broad provein stripes and in interveins remains unknown, however. In this manuscript, we provide additional evidence for veins forming in narrow stripes at borders of A/P sectors. These experiments further suggest that narrow vein primordia produce secondary short-range signal(s), which activate expression of provein genes in a broad pattern in neighboring cells. We also show that crossregulatory interactions among genes expressed in veins, proveins and interveins contribute to establishing the vein-versus-intervein pattern, and that control of gene expression in vein and intervein regions must be considered on a stripe-by-stripe basis. Finally, we present evidence for a second set of vein-inducing boundaries lying between veins, which we refer to as paravein boundaries. We propose that veins develop at both vein and paravein boundaries in more ‘primitive’ insects, which have up to twice the number of veins present in Drosophila. We present a model in which different A/P boundaries organize vein-specific genetic programs to govern the development of individual veins.

scholarly journals msh specifies dorsal cell fate in the Drosophila wing

Development ◽  
2001 ◽  
Vol 128 (17) ◽  
pp. 3263-3268 ◽  
Author(s):  
Marco Milán ◽  
Ulrich Weihe ◽  
Stanley Tiong ◽  
Welcome Bender ◽  
Stephen M. Cohen
Keyword(s):  
Cell Fate ◽  
Imaginal Disc ◽  
Homeobox Gene ◽  
Wing Imaginal Disc ◽  
Wing Development ◽  
Drosophila Wing ◽  
Compartment Boundary ◽  
Signaling Center ◽  
Dorsal Cells ◽  
Dorsal Cell Fate

Drosophila limbs develop from imaginal discs that are subdivided into compartments. Dorsal-ventral subdivision of the wing imaginal disc depends on apterous activity in dorsal cells. Apterous protein is expressed in dorsal cells and is responsible for (1) induction of a signaling center along the dorsal-ventral compartment boundary (2) establishment of a lineage restriction boundary between compartments and (3) specification of dorsal cell fate. Here, we report that the homeobox gene msh (muscle segment homeobox) acts downstream of apterous to confer dorsal identity in wing development.

scholarly journals Regulated delivery controls Drosophila Hedgehog, Wingless and Decapentaplegic signaling

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.

Serrate-mediated activation of Notch is specifically blocked by the product of the gene fringe in the dorsal compartment of the Drosophila wing imaginal disc

Development ◽  
1997 ◽  
Vol 124 (15) ◽  
pp. 2973-2981 ◽  
Author(s):  
R.J. Fleming ◽  
Y. Gu ◽  
N.A. Hukriede
Keyword(s):  
Imaginal Disc ◽  
Ectopic Expression ◽  
Wing Disc ◽  
Specific Response ◽  
Wing Margin ◽  
Drosophila Wing ◽  
Imaginal Wing Disc ◽  
Dorsoventral Boundary ◽  
Drosophila Cells ◽  
Notch Ligands

In the developing imaginal wing disc of Drosophila, cells at the dorsoventral boundary require localized Notch activity for specification of the wing margin. The Notch ligands Serrate and Delta are required on opposite sides of the presumptive wing margin and, even though activated forms of Notch generate responses on both sides of the dorsoventral boundary, each ligand generates a compartment-specific response. In this report we demonstrate that Serrate, which is expressed in the dorsal compartment, does not signal in the dorsal regions due to the action of the fringe gene product. Using ectopic expression, we show that regulation of Serrate by fringe occurs at the level of protein and not Serrate transcription. Furthermore, replacement of the N-terminal region of Serrate with the corresponding region of Delta abolishes the ability of fringe to regulate Serrate without altering Serrate-specific signaling.

A dual role for homothorax in inhibiting wing blade development and specifying proximal wing identities in Drosophila

Development ◽  
2000 ◽  
Vol 127 (7) ◽  
pp. 1499-1508 ◽  
Author(s):  
F. Casares ◽  
R.S. Mann
Keyword(s):  
Signal Transduction ◽  
Imaginal Disc ◽  
Target Genes ◽  
Notch Pathway ◽  
Wing Disc ◽  
Signal Transduction Pathways ◽  
Body Parts ◽  
Drosophila Wing ◽  
Compartment Boundary ◽  
Three Body

The Drosophila wing imaginal disc gives rise to three body parts along the proximo-distal (P-D) axis: the wing blade, the wing hinge and the mesonotum. Development of the wing blade initiates along part of the dorsal/ventral (D/V) compartment boundary and requires input from both the Notch and wingless (wg) signal transduction pathways. In the wing blade, wg activates the gene vestigial (vg), which is required for the wing blade to grow. wg is also required for hinge development, but wg does not activate vg in the hinge, raising the question of what target genes are activated by wg to generate hinge structures. Here we show that wg activates the gene homothorax (hth) in the hinge and that hth is necessary for hinge development. Further, we demonstrate that hth also limits where along the D/V compartment boundary wing blade development can initiate, thus helping to define the size and position of the wing blade within the disc epithelium. We also show that the gene teashirt (tsh), which is coexpressed with hth throughout most of wing disc development, collaborates with hth to repress vg and block wing blade development. Our results suggest that tsh and hth block wing blade development by repressing some of the activities of the Notch pathway at the D/V compartment boundary.

scholarly journals Feedback regulation of cytoneme-mediated transport shapes a tissue-specific FGF morphogen gradient

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Lijuan Du ◽  
Alex Sohr ◽  
Ge Yan ◽  
Sougata Roy
Keyword(s):  
Gene Expression ◽  
Transcription Factors ◽  
Imaginal Disc ◽  
Feedback Regulation ◽  
Wing Disc ◽  
Wing Imaginal Disc ◽  
Morphogen Gradient ◽  
Signaling Proteins ◽  
Tissue Specific ◽  
Gradient Formation

Gradients of signaling proteins are essential for inducing tissue morphogenesis. However, mechanisms of gradient formation remain controversial. Here we characterized the distribution of fluorescently-tagged signaling proteins, FGF and FGFR, expressed at physiological levels from the genomic knock-in alleles in Drosophila. FGF produced in the larval wing imaginal-disc moves to the air-sac-primordium (ASP) through FGFR-containing cytonemes that extend from the ASP to contact the wing-disc source. The number of FGF-receiving cytonemes extended by ASP cells decreases gradually with increasing distance from the source, generating a recipient-specific FGF gradient. Acting as a morphogen in the ASP, FGF activates concentration-dependent gene expression, inducing pointed-P1 at higher and cut at lower levels. The transcription-factors Pointed-P1 and Cut antagonize each other and differentially regulate formation of FGFR-containing cytonemes, creating regions with higher-to-lower numbers of FGF-receiving cytonemes. These results reveal a robust mechanism where morphogens self-generate precise tissue-specific gradient contours through feedback regulation of cytoneme-mediated dispersion.

Activation of knot (kn) specifies the 3–4 intervein region in the Drosophila wing

Development ◽  
2000 ◽  
Vol 127 (1) ◽  
pp. 55-63 ◽  
Author(s):  
J. Mohler ◽  
M. Seecoomar ◽  
S. Agarwal ◽  
E. Bier ◽  
J. Hsai
Keyword(s):  
Imaginal Disc ◽  
Target Gene ◽  
Egf Receptor ◽  
Ectopic Expression ◽  
Expression Domain ◽  
Gene Encoding ◽  
Direct Role ◽  
Free Zone ◽  
Drosophila Wing ◽  
Compartment Boundary

Hedgehog (Hh) plays an important role in Drosophila wing patterning by inducing expression of Dpp, which serves to organize the wing globally across the A-P axis. We show here how Hh signalling also plays a direct role in patterning the medial wing through the activation of the Hh-target gene, knot (kn). kn is expressed in Hh-responsive cells near the A-P compartment boundary, where its expression is dependent on fu, a component of Hh signalling. kn is required for the proper positioning of veins 3 and 4 and to prevent ectopic venation between them. Furthermore, the expansion anteriorly of the normal kn expression domain causes an associated anterior shift in the position of vein 3 in the resultant wing. Ectopic expression of kn elsewhere in the wing imaginal disc results in the failure to properly activate the vein initiation genes, rho and Dl. Expression of the gene encoding the EGF-receptor (EGFR), which is required for vein initiation and subsequent differentiation, is normally depressed in the 3–4 intervein region. This downregulation of EGFR in the medial portion of the imaginal disc is dependent on kn activity and ectopic expression of kn inactivates EGFR elsewhere in the wing primordium. We propose kn expression in Hh-responsive cells of the wing blade anlagen during the late third instar creates a zone of cells in the medial wing in which vein primordia cannot be induced. The primordia for veins 3 and 4 are laid down adjacent to the kn-imposed vein-free zone, presumably by a signalling factor (such as Vn) also synthesized in the medial region of the wing.

Regulation of Drosophila wing vein patterning: net encodes a bHLH protein repressing rhomboid and is repressed by rhomboid-dependent Egfr signalling

Development ◽  
2000 ◽  
Vol 127 (21) ◽  
pp. 4729-4741 ◽  
Author(s):  
D. Brentrup ◽  
H. Lerch ◽  
H. Jackle ◽  
M. Noll
Keyword(s):  
Imaginal Disc ◽  
Egf Receptor ◽  
Ectopic Expression ◽  
Wing Disc ◽  
Bhlh Protein ◽  
Wing Vein ◽  
Drosophila Wing ◽  
Vein Formation ◽  
Mutual Repression ◽  
Vein Patterning

The stereotyped pattern of veins in the Drosophila wing is generated in response to local EGF signalling. Mutations in the rhomboid (rho) gene, which encodes a sevenpass membrane protein required to enhance signalling transmitted by the EGF receptor (Egfr), inhibit vein development and disrupt the vein pattern. By contrast, net mutations produce ectopic veins in intervein regions. We have cloned the net gene and show that it encodes a basic HLH protein that probably acts as a transcriptional repressor. net and rho are expressed in mutually exclusive patterns during the development of the wing imaginal disc. Lack of net activity causes rho expression to expand, and vice versa. Furthermore, ectopic expression of net or rho results in their mutual repression and thus suppresses vein formation or generates tube-like wings composed of vein-like tissue. Egfr signalling and net exert mutually antagonising activities during the specification of vein versus intervein fate. While Egfr signalling represses net transcription, net exhibits a two-tiered control by repressing rho transcription and interfering with Egfr signalling downstream of Rho. Our results further suggest that net is required to maintain intervein development by restricting Egfr signalling, which promotes vein development, to the Net-free vein regions of the wing disc.

Hedgehog activity, independent of decapentaplegic, participates in wing disc patterning

Development ◽  
1997 ◽  
Vol 124 (6) ◽  
pp. 1227-1237 ◽  
Author(s):  
J.L. Mullor ◽  
M. Calleja ◽  
J. Capdevila ◽  
I. Guerrero
Keyword(s):  
Zinc Finger ◽  
Imaginal Disc ◽  
Zinc Finger Protein ◽  
Ectopic Expression ◽  
Wing Disc ◽  
Signal Molecule ◽  
Cubitus Interruptus ◽  
Drosophila Wing ◽  
Finger Protein

In the Drosophila wing imaginal disc, the Hedgehog (Hh) signal molecule induces the expression of decapentaplegic (dpp) in a band of cells abutting the anteroposterior (A/P) compartment border. It has been proposed that Dpp organizes the patterning of the entire wing disc. We have tested this proposal by studying the response to distinct levels of ectopic expression of Hh and Dpp, using the sensory organ precursors (SOPs) of the wing and notum and the presumptive wing veins as positional markers. Here, we show that Dpp specifies the position of most SOPs in the notum and of some of them in the wing. Close to the A/P compartment border, however, SOPs are specified by Hh rather than by Dpp alone. We also show that late signaling by Hh, after setting up dpp expression, is responsible for the formation of vein 3 and the scutellar region, and also for the determination of the distance between veins 3 and 4. One of the genes that mediates the Hh signal is the zinc-finger protein Cubitus interruptus (Ci). These results indicate that Hh has a Dpp-independent morphogenetic effect in the region of the wing disc near the A/P border.

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