scholarly journals Asymmetric requirement of Dpp/BMP morphogen dispersal in the Drosophila wing disc

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Shinya Matsuda ◽  
Jonas V. Schaefer ◽  
Yusuke Mii ◽  
Yutaro Hori ◽  
Dimitri Bieli ◽  
...  
Keyword(s):  
Wing Disc ◽  
Single Chain ◽  
Anterior Compartment ◽  
Morphogen Gradients ◽  
Lateral Wing ◽  
Protein Binders ◽  
Critical Requirement ◽  
Anterior Patterning ◽  
Wing Growth ◽  
Wing Pouch

AbstractHow morphogen gradients control patterning and growth in developing tissues remains largely unknown due to lack of tools manipulating morphogen gradients. Here, we generate two membrane-tethered protein binders that manipulate different aspects of Decapentaplegic (Dpp), a morphogen required for overall patterning and growth of the Drosophila wing. One is “HA trap” based on a single-chain variable fragment (scFv) against the HA tag that traps HA-Dpp to mainly block its dispersal, the other is “Dpp trap” based on a Designed Ankyrin Repeat Protein (DARPin) against Dpp that traps Dpp to block both its dispersal and signaling. Using these tools, we found that, while posterior patterning and growth require Dpp dispersal, anterior patterning and growth largely proceed without Dpp dispersal. We show that dpp transcriptional refinement from an initially uniform to a localized expression and persistent signaling in transient dpp source cells render the anterior compartment robust against the absence of Dpp dispersal. Furthermore, despite a critical requirement of dpp for the overall wing growth, neither Dpp dispersal nor direct signaling is critical for lateral wing growth after wing pouch specification. These results challenge the long-standing dogma that Dpp dispersal is strictly required to control and coordinate overall wing patterning and growth.

scholarly journals Asymmetric requirement of Dpp/BMP morphogen dispersal in the Drosophila wing disc

2020 ◽  
Author(s):  
Shinya Matsuda ◽  
Jonas V. Schaefer ◽  
Yusuke Mii ◽  
Yutaro Hori ◽  
Dimitri Bieli ◽  
...  
Keyword(s):  
Positional Information ◽  
Wing Disc ◽  
Morphogen Gradients ◽  
Drosophila Wing ◽  
Control Growth ◽  
Protein Functions ◽  
Underlying Mechanisms ◽  
Anterior Patterning ◽  
Wing Growth ◽  
And Control

SummaryMorphogen gradients provide positional information and control growth in developing tissues, but the underlying mechanisms remain largely unknown due to lack of tools manipulating morphogen gradients. Here, we generate two synthetic protein binder tools manipulating different parameters of Decapentaplegic (Dpp), a morphogen thought to control Drosophila wing disc patterning and growth by dispersal; while HA trap blocks Dpp dispersal, Dpp trap blocks Dpp dispersal and signaling in the source cells. Using these tools, we found that while posterior patterning and growth require Dpp dispersal, anterior patterning and growth largely proceed without Dpp dispersal. We show that dpp transcriptional refinement from an initially uniform to a localized expression and persistent signaling in transient dpp source cells render the anterior compartment robust to blocking Dpp dispersal. Furthermore, neither Dpp dispersal nor signaling is critical for lateral wing growth. These results challenge Dpp dispersal-centric mechanisms, and demonstrate the utility of customized protein binder tools to dissect protein functions.

Quantitative EM of gap junction distribution in mutant drosophila wing discs

1983 ◽  
Vol 41 ◽  
pp. 720-721
Author(s):  
J.S. Ryerse
Keyword(s):  
Gap Junctions ◽  
Growth Control ◽  
Intercellular Junctions ◽  
Wing Disc ◽  
En Bloc ◽  
Metabolic Cooperation ◽  
Drosophila Wing ◽  
Adult Wing ◽  
Wing Discs ◽  
Wing Pouch

Gap junctions are intercellular junctions found in both vertebrates and invertebrates through which ions and small molecules can pass. Their distribution in tissues could be of critical importance for ionic coupling or metabolic cooperation between cells or for regulating the intracellular movement of growth control and pattern formation factors. Studies of the distribution of gap junctions in mutants which develop abnormally may shed light upon their role in normal development. I report here the distribution of gap junctions in the wing pouch of 3 Drosophila wing disc mutants, vg (vestigial) a cell death mutant, 1(2)gd (lethal giant disc) a pattern abnormality mutant and 1(2)gl (lethal giant larva) a neoplastic mutant and compare these with wildtype wing discs.The wing pouch (the anlagen of the adult wing blade) of a wild-type wing disc is shown in Fig. 1 and consists of columnar cells (Fig. 5) joined by gap junctions (Fig. 6). 14000x EMs of conventionally processed, UA en bloc stained, longitudinally sectioned wing pouches were enlarged to 45000x with a projector and tracings were made on which the lateral plasma membrane (LPM) and gap junctions were marked.

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.

Role of the EGF receptor pathway in growth and patterning of the Drosophila wing through the regulation of vestigial

Development ◽  
1999 ◽  
Vol 126 (5) ◽  
pp. 975-985 ◽  
Author(s):  
R. Nagaraj ◽  
A.T. Pickup ◽  
R. Howes ◽  
K. Moses ◽  
M. Freeman ◽  
...  
Keyword(s):  
Egf Receptor ◽  
Regulatory Gene ◽  
Ectopic Expression ◽  
Wing Disc ◽  
Loss Of Function ◽  
Drosophila Wing ◽  
Expression Studies ◽  
Coordinated Expression ◽  
Wing Pouch

Growth and patterning of the Drosophila wing disc depends on the coordinated expression of the key regulatory gene vestigial both in the Dorsal-Ventral (D/V) boundary cells and in the wing pouch. We propose that a short-range signal originating from the core of the D/V boundary cells is responsible for activating EGFR in a zone of organizing cells on the edges of the D/V boundary. Using loss-of-function mutations and ectopic expression studies, we show that EGFR signaling is essential for vestigial transcription in these cells and for making them competent to undergo subsequent vestigial-mediated proliferation within the wing pouch.

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.

The roles of hedgehog and engrailed in patterning adult abdominal segments of Drosophila

Development ◽  
1997 ◽  
Vol 124 (19) ◽  
pp. 3703-3714 ◽  
Author(s):  
A. Kopp ◽  
M.A. Muskavitch ◽  
I. Duncan
Keyword(s):  
Ectopic Expression ◽  
Restrictive Temperature ◽  
Primary Role ◽  
Loss Of Function ◽  
Posterior Compartment ◽  
Anterior Portion ◽  
Posterior Portion ◽  
Anterior Compartment ◽  
Present Evidence ◽  
Anterior Patterning

We present evidence that hedgehog (hh) protein secreted by posterior compartment cells plays a key role in patterning the posterior portion of the anterior compartment in adult abdominal segments. Loss of function of hh in the hh(ts2) mutant causes the loss of posterior tergite characteristics in the anterior compartment, whereas ectopic expression driven by hs-hh or the gain-of-function allele hh(Mir) causes transformation of anterior structures toward the posterior. FLP-out hh-expressing clones in the anterior compartment induce surrounding wild-type cells to produce posterior tergite structures, establishing that hh functions nonautonomously. The effects of pulses of ectopic expression driven by hs-hh indicate that bristle type and pigmentation are patterned by hh at widely different times in pupal development. We also present evidence that the primary polarization of abdominal segments is symmetric. This symmetry is strikingly revealed by ectopic expression of engrailed (en). As expected, this transforms anterior compartment cells to posterior compartment identity. In addition, however, ectopic en expression causes an autonomous reversal of polarity in the anterior portion of the anterior compartment, but not the posterior portion. By determining the position of polarity reversal within en-expressing clones, we were able to define a cryptic line of symmetry that lies within the pigment band of the normal tergite. This line appears to be retained in hh(ts2) mutants raised at the restrictive temperature, suggesting it is not established by hh signaling. We argue that the primary role of hh in controlling polarity is to cause anterior compartment cells to reverse their interpretation of an underlying symmetric polarization. Consistent with this, we find that strong ectopic expression of hh causes mirror-symmetric double posterior patterning, whereas hh loss of function can cause mirror-symmetric double anterior patterning.

Repression of Teashirt marks the initiation of wing development

Development ◽  
2002 ◽  
Vol 129 (10) ◽  
pp. 2411-2418 ◽  
Author(s):  
Jun Wu ◽  
Stephen M. Cohen
Keyword(s):  
Body Wall ◽  
Larval Instar ◽  
Wing Disc ◽  
Wing Development ◽  
Homeodomain Protein ◽  
Zinc Finger Transcription Factor ◽  
Adult Wing ◽  
Combined Action ◽  
Wing Pouch ◽  
Early Activity

The wing imaginal disc comprises the primordia of the adult wing and the dorsal thoracic body wall. During second larval instar, the wing disc is subdivided into distinct domains that correspond to the presumptive wing and body wall. Early activity of the signaling protein Wingless has been implicated in the specification of the wing primordium. Wingless mutants can produce animals in which the wing is replaced by a duplication of thoracic structures. Specification of wing fate has been visualized by expression of the POU-homeodomain protein Nubbin in the presumptive wing territory and by repression of the homeodomain protein Homothorax. We report that repression of the zinc-finger transcription factor Teashirt (Tsh) is the earliest event in wing specification. Repression of Tsh by the combined action of Wingless and Decapentaplegic is required for wing pouch formation and for subsequent repression of Hth. Thus, repression of Tsh defines the presumptive wing earlier in development than repression of Hth, which must therefore be considered a secondary event.

Lineage-tracing cells born in different domains along the PD axis of the developing Drosophila leg

Development ◽  
1999 ◽  
Vol 126 (17) ◽  
pp. 3823-3830 ◽  
Author(s):  
K. Weigmann ◽  
S.M. Cohen
Keyword(s):  
Cell Fate ◽  
Imaginal Discs ◽  
Wing Disc ◽  
Lineage Tracing ◽  
Ligand Concentration ◽  
Signaling Proteins ◽  
Cell Fate Specification ◽  
Morphogen Gradients ◽  
Fate Specification ◽  
Lower Ligand

Patterning of the developing limbs by the secreted signaling proteins Wingless, Hedgehog and Dpp takes place while the imaginal discs are growing rapidly. Cells born in regions of high ligand concentration may be displaced through growth to regions of lower ligand concentration. We have used a novel lineage-tagging method to address the reversibility of cell fate specification by morphogen gradients. We find that responses to Hedgehog and Dpp in the wing disc are readily reversible. In the leg, we find that cells readily adopt more distal fates, but do not normally shift from distal to proximal fate. However, they can do so if given a growth advantage. These results indicate that cell fate specification by morphogen gradients remains largely reversible while the imaginal discs grow. In other systems, where growth and patterning are uncoupled, nonreversible specification events or ‘ratchet’ effects may be of functional significance.

scholarly journals Dpp spreading is required for medial but not for lateral wing disc growth

Nature ◽  
2015 ◽  
Vol 527 (7578) ◽  
pp. 317-322 ◽  
Author(s):  
Stefan Harmansa ◽  
Fisun Hamaratoglu ◽  
Markus Affolter ◽  
Emmanuel Caussinus
Keyword(s):  
Wing Disc ◽  
Lateral Wing

Drosophila Lyra Mutations Are Gain-of-Function Mutations of senseless

Genetics ◽  
2001 ◽  
Vol 157 (1) ◽  
pp. 307-315 ◽  
Author(s):  
Riitta Nolo ◽  
Lois A Abbott ◽  
Hugo J Bellen
Keyword(s):  
Apoptotic Cell ◽  
Ectopic Expression ◽  
Wing Disc ◽  
Brdu Incorporation ◽  
Wing Margin ◽  
Aberrant Expression ◽  
Severe Reduction ◽  
Wing Discs ◽  
Necessary And Sufficient ◽  
Wing Pouch

Abstract The Lyra mutation was first described by Jerry Coyne in 1935. Lyra causes recessive pupal lethality and adult heterozygous Lyra mutants exhibit a dominant loss of the anterior and posterior wing margins. Unlike many mutations that cause loss of wing tissue (e.g., scalloped, Beadex, cut, and apterous-Xasta), Lyra wing discs do not exhibit increased necrotic or apoptotic cell death, nor do they show altered BrdU incorporation. However, during wing disc eversion, loss of the anterior and posterior wing margins is apparent. We have previously shown that senseless, a gene that is necessary and sufficient for peripheral nervous system (PNS) development, is allelic to Lyra. Here we show by several genetic criteria that Lyra alleles are neomorphic alleles of senseless that cause ectopic expression of SENSELESS in the wing pouch. Similarly, overexpression of SENSELESS in the wing disc causes loss of wing margin tissue, thereby mimicking the Lyra phenotype. Lyra mutants display aberrant expression of DELTA, VESTIGIAL, WINGLESS, and CUT. As in Lyra mutants, overexpression of SENSELESS in some areas of the wing pouch also leads to loss of WINGLESS and CUT. In summary, our data indicate that overexpression of SENSELESS causes a severe reduction in NOTCH signaling that in turn may lead to decreased transcription of several key genes required for wing development, leading to a failure in cell proliferation and loss of wing margin tissue.

Sign in / Sign up

Export Citation Format

Share Document