groucho and hedgehog regulate engrailed expression in the anterior compartment of the Drosophila wing

Development ◽  
1995 ◽  
Vol 121 (10) ◽  
pp. 3467-3476 ◽  
Author(s):  
J.F. de Celis ◽  
M. Ruiz-Gomez
Keyword(s):  
Cell Growth ◽  
Normal Growth ◽  
Wing Disc ◽  
Anterior Compartment ◽  
Drosophila Wing ◽  
Compartment Boundary ◽  
Ectopic Activation ◽  
Selector Genes ◽  
Dorsoventral Boundary ◽  
Anterior Posterior

Drosophila imaginal discs are divided into units called compartments. Cells belonging to the same compartment are related by lineage and express a characteristic set of ‘selector genes’. The borders between compartments act as organizing centres that influence cell growth within compartments. Thus, in the cells immediately anterior to the anterior-posterior compartment boundary the presence of the hedgehog product causes expression of decapentaplegic, which, in turn, influences the growth and patterning of the wing disc. The normal growth of the disc requires that posterior-specific genes, such as hedgehog and engrailed are not expressed in cells of the anterior compartment. Here we show that hedgehog can activate engrailed in the anterior compartment and that both hedgehog and engrailed are specifically repressed in anterior cells by the activity of the neurogenic gene groucho. In groucho mutant discs, hedgehog and engrailed are expressed at the dorsoventral boundary of the anterior compartment, leading to the ectopic activation of decapentaplegic and patched and to a localised increase in cell growth associated with pattern duplications. The presence of engrailed in the anterior compartment causes the transformation of anterior into posterior structures.

Nubbin encodes a POU-domain protein required for proximal-distal patterning in the Drosophila wing

Development ◽  
1995 ◽  
Vol 121 (2) ◽  
pp. 589-599 ◽  
Author(s):  
M. Ng ◽  
F.J. Diaz-Benjumea ◽  
S.M. Cohen
Keyword(s):  
Growth Control ◽  
Normal Growth ◽  
Control Center ◽  
Genetic Mosaics ◽  
Drosophila Wing ◽  
Pou Domain ◽  
Compartment Boundary ◽  
Wing Structures ◽  
Wing Imaginal Discs ◽  
Anterior Posterior

The nubbin gene is required for normal growth and patterning of the wing in Drosophila. We report here that nubbin encodes a member of the POU family of transcription factors. Regulatory mutants which selectively remove nubbin expression from wing imaginal discs lead to loss of wing structures. Although nubbin is expressed throughout the wing primordium, analysis of genetic mosaics suggests a localized requirement for nubbin activity in the wing hinge. These observations suggest the existence of a novel proximal-distal growth control center in the wing hinge, which is required in addition to the well characterized anterior-posterior and dorsal-ventral compartment boundary organizing centers.

scholarly journals Membrane potential regulates Hedgehog signaling and compartment boundary maintenance in the Drosophila wing disc

2020 ◽  
Author(s):  
Maya Emmons-Bell ◽  
Riku Yasutomi ◽  
Iswar K. Hariharan
Keyword(s):  
Membrane Potential ◽  
Hedgehog Signaling ◽  
Membrane Depolarization ◽  
Wing Disc ◽  
Anterior Compartment ◽  
Drosophila Wing ◽  
Compartment Boundary ◽  
Boundary Maintenance ◽  
Elevated Expression ◽  
Hh Signaling

AbstractThe Drosophila wing imaginal disc is composed of two lineage-restricted populations of cells separated by a smooth boundary. Hedgehog (Hh) from posterior cells activates a signaling pathway in anterior cells near the boundary which is necessary for boundary maintenance. Here, we show that membrane potential is patterned in the wing disc. Anterior cells near the boundary, where Hh signaling is most active, are more depolarized than posterior cells across the boundary. Elevated expression of the ENaC channel Ripped Pocket (Rpk), observed in these anterior cells, requires Hh. Antagonizing Rpk reduces depolarization and disrupts the compartment boundary. Using genetic and optogenetic manipulations, we show that membrane depolarization promotes membrane localization of Smoothened and augments Hh signaling. Thus, membrane depolarization and Hh-dependent signaling mutually reinforce each other in this region. Finally, clones of depolarized cells survive preferentially in the anterior compartment and clones of hyperpolarized cells survive preferentially in the posterior compartment.

patched overexpression alters wing disc size and pattern: transcriptional and post-transcriptional effects on hedgehog targets

Development ◽  
1995 ◽  
Vol 121 (12) ◽  
pp. 4161-4170 ◽  
Author(s):  
R.L. Johnson ◽  
J.K. Grenier ◽  
M.P. Scott
Keyword(s):  
Protein Kinase ◽  
Protein Kinase A ◽  
Target Genes ◽  
Critical Role ◽  
Wing Disc ◽  
Wing Vein ◽  
Anterior Compartment ◽  
Protein Levels ◽  
Anterior Posterior ◽  
Kinase A

The membrane protein, Patched, plays a critical role in patterning embryonic and imaginal tissues in Drosophila. patched constitutively inactivates the transcription of target genes such as wingless, decapentaplegic, and patched itself. The secreted protein, Hedgehog, induces transcription of target genes by opposing the Patched signaling pathway. Using the Gal4 UAS system we have overexpressed patched in wing imaginal discs and found that high Patched levels, expressed in either normal or ectopic patterns, result in loss of wing vein patterning in both compartments centering at the anterior/posterior border. In addition, patched inhibits the formation of the mechanosensory neurons, the campaniform sensilla, in the wing blade. The patched wing vein phenotype is modulated by mutations in hedgehog and cubitus interruptus (ci). Patched overexpression inhibits transcription of patched and decapentaplegic and post-transcriptionally decreases the amount of Ci protein at the anterior/posterior boundary. In hedgehogMrt wing discs, which express ectopic hedgehog, Ci levels are correspondingly elevated, suggesting that hedgehog relieves patched repression of Ci accumulation. Protein kinase A also regulates Ci; protein kinase A mutant clones in the anterior compartment have increased levels of Ci protein. Thus patched influences wing disc patterning by decreasing Ci protein levels and inactivating hedgehog target genes in the anterior compartment.

Smoothened-mediated Hedgehog signalling is required for the maintenance of the anterior-posterior lineage restriction in the developing wing of Drosophila

Development ◽  
1997 ◽  
Vol 124 (20) ◽  
pp. 4053-4063 ◽  
Author(s):  
S.S. Blair ◽  
A. Ralston
Keyword(s):  
Gene Expression ◽  
Cellular Mechanisms ◽  
Hedgehog Signalling ◽  
Compartment Boundary ◽  
Complex Process ◽  
Normal Site ◽  
Selector Genes ◽  
Signalling Models ◽  
To Receive ◽  
Anterior Posterior

It is thought that the posterior expression of the ‘selector’ genes engrailed and invected control the subdivision of the growing wing imaginal disc of Drosophila into anterior and posterior lineage compartments. At present, the cellular mechanisms by which separate lineage compartments are maintained are not known. Most models have assumed that the presence or absence of selector gene expression autonomously drives the expression of compartment-specific adhesion or recognition molecules that inhibit intermixing between compartments. However, our present understanding of Hedgehog signalling from posterior to anterior cells raises some interesting alternative models based on a cell's response to signalling. We show here that anterior cells that lack smoothened, and thus the ability to receive the Hedgehog signal, no longer obey a lineage restriction in the normal position of the anterior-posterior boundary. Rather these clones extend into anatomically posterior territory, without any changes in engrailed/invected gene expression. We have also examined clones lacking both en and inv; these too show complex behaviors near the normal site of the compartment boundary, and do not always cross entirely into anatomically anterior territory. Our results suggest that compartmentalization is a complex process involving intercompartmental signalling; models based on changes in affinity or growth will be discussed.

Role of knot (kn) in Wing Patterning in Drosophila

Genetics ◽  
1997 ◽  
Vol 147 (3) ◽  
pp. 1203-1212 ◽  
Author(s):  
Katerina Nestoras ◽  
Helena Lee ◽  
Jym Mohler
Keyword(s):  
Hedgehog Signaling ◽  
Imaginal Disc ◽  
Hedgehog Signaling Pathway ◽  
Posterior Compartment ◽  
Drosophila Wing ◽  
Compartment Boundary ◽  
Hh Signaling ◽  
Embryonic Segmentation ◽  
Anterior Posterior

We have undertaken a genetic analysis of new strong alleles of knot (kn). The original kn1 mutation causes an alteration of wing patterning similar to that associated with mutations of fused (fu), an apparent fusion of veins 3 and 4 in the wing. However, unlike fu, strong kn mutations do not affect embryonic segmentation and indicate that kn is not a component of a general Hh (Hedgehog)-signaling pathway. Instead we find that kn has a specific role in those cells of the wing imaginal disc that are subject to ptc-mediated Hh-signaling. Our results suggest a model for patterning the medial portion of the Drosophila wing, whereby the separation of veins 3 and 4 is maintained by kn activation in the intervening region in response to Hh-signaling across the adjacent anterior-posterior compartment boundary.

Hedgehog is required for activation of engrailed during regeneration of fragmented Drosophila imaginal discs

Development ◽  
1999 ◽  
Vol 126 (8) ◽  
pp. 1591-1599 ◽  
Author(s):  
M.C. Gibson ◽  
G. Schubiger
Keyword(s):  
Normal Growth ◽  
Imaginal Discs ◽  
Ideal Model ◽  
Posterior Compartment ◽  
Anterior Compartment ◽  
In Vivo Culture ◽  
Pattern Regulation ◽  
Regulative Capacity ◽  
Anterior Posterior

Surgically fragmented Drosophila appendage primordia (imaginal discs) engage in wound healing and pattern regulation during short periods of in vivo culture. Prothoracic leg disc fragments possess exceptional regulative capacity, highlighted by the ability of anterior cells to convert to posterior identity and establish a novel posterior compartment. This anterior/posterior conversion violates developmental lineage restrictions essential for normal growth and patterning of the disc, and thus provides an ideal model for understanding how cells change fate during epimorphic pattern regulation. Here we present evidence that the secreted signal encoded by hedgehog directs anterior/posterior conversion by activating the posterior-specific transcription factor engrailed in regulating anterior cells. In the absence of hedgehog activity, prothoracic leg disc fragments fail to undergo anterior/posterior conversion, but can still regenerate missing anterior pattern elements. We suggest that hedgehog-independent regeneration within the anterior compartment (termed integration) is mediated by the positional cues encoded by wingless and decapentaplegic. Taken together, our results provide a novel mechanistic interpretation of imaginal disc pattern regulation and permit speculation that similar mechanisms could govern appendage regeneration in other organisms.

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.

scholarly journals The function of engrailed and the specification of Drosophila wing pattern

Development ◽  
1995 ◽  
Vol 121 (10) ◽  
pp. 3447-3456 ◽  
Author(s):  
I. Guillen ◽  
J.L. Mullor ◽  
J. Capdevila ◽  
E. Sanchez-Herrero ◽  
G. Morata ◽  
...  
Keyword(s):  
Wing Disc ◽  
Gene Products ◽  
Wing Pattern ◽  
Related Gene ◽  
Posterior Compartment ◽  
Anterior Compartment ◽  
Drosophila Wing ◽  
Partial Inactivation ◽  
Autoregulatory Mechanism ◽  
Adult Drosophila

The adult Drosophila wing (as the other appendages) is subdivided into anterior and posterior compartments that exhibit characteristic patterns. The engrailed (en) gene has been proposed to be paramount in the specification of the posterior compartment identity. Here, we explore the adult en function by targeting its expression in different regions of the wing disc. In the anterior compartment, ectopic en expression gives rise to the substitution of anterior structures by posterior ones, thus demonstrating its role in specification of posterior patterns. The en-expressing cells in the anterior compartment also induce high levels of the hedgehog (hh) and decapentaplegic (dpp) gene products, which results in local duplications of anterior patterns. Besides, hh is able to activate en and the engrailed-related gene invected (inv) in this compartment. In the posterior compartment we find that elevated levels of en product result in partial inactivation of the endogenous en and inv genes, indicating the existence of a negative autoregulatory mechanism. We propose that en has a dual role: a general one for patterning of the appendage, achieved through the activation of secreted proteins like hh and dpp, and a more specific one, determining posterior identity, in which the inv gene may be implicated.

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.

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