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.

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.

STABILITY OF REGULATORY PROTEIN GRADIENTS INDUCED BY MORPHOGEN DPP IN DROSOPHILA WING DISC

2013 ◽  
Vol 23 (08) ◽  
pp. 1350138 ◽  
Author(s):  
HONGWEI YIN ◽  
XIAOYONG XIAO ◽  
XIAOQING WEN ◽  
TIANSHOU ZHOU
Keyword(s):  
Regulatory Network ◽  
Regulatory Protein ◽  
Reaction Rates ◽  
Wing Disc ◽  
Drosophila Wing ◽  
Major Reaction ◽  
Key Genes ◽  
Pattern Information ◽  
Protein Gradients ◽  
And Control

In the development of Drosophila wing disc, morphogen Dpp, which is a signaling molecule from a local region and disperses into anterior and posterior compartments, builds up a gradient with precise pattern information. Experiments have demonstrated that the key genes (brk, dad, omb and sal) and phosphorylated protein (pMad), which are activated by Dpp signaling molecules and form the gradients of the corresponding proteins of these genes, direct and control the spatial pattern of the wing disc. However, the regulatory network of these genes are in complex and nonlinear interaction with upstream regulators and downstream targets. In this paper, the mathematical model is built according to the regulatory relationships of these key genes. The stabilities of the gradients of these corresponding proteins are investigated. Furthermore, numerical simulations show that these gradients are robust with respect to some major reaction rates in this regulatory network.

scholarly journals Autonomous termination of proliferation in the Drosophila wing disc is TORC1 dependent

2020 ◽  
Author(s):  
Katrin Strassburger ◽  
Marilena Lutz ◽  
Sandra Müller ◽  
Aurelio A. Teleman
Keyword(s):  
Experimental Manipulation ◽  
Wing Disc ◽  
Wing Size ◽  
Final Size ◽  
Drosophila Wing ◽  
Adult Wing ◽  
Wing Discs ◽  
Underlying Mechanisms ◽  
Constant Growth ◽  
Wing Pouch

AbstractCells in a developing organ stop proliferating when the organ reaches a correct, final size. The underlying mechanisms are not understood. Although many signaling pathways and cell cycle components are required to sustain cell proliferation, which one of these turns off to terminate proliferation is not known. Here we study proliferation termination using Drosophila wing discs. We extend larval development to provide wing discs a constant growth-sustaining environment, allowing them to terminate proliferation autonomously. We find that the wing pouch, which forms the adult wing blade, terminates proliferation in the absence of brinker or warts, indicating that neither Dpp signaling nor Hippo/Yorkie signaling control final wing size. Instead, termination of proliferation coincides with reduced TORC1 activity and is bypassed by reactivating TORC1. Hence proliferation ceases due to reduced cell growth. Experimental manipulation of Dpp or Yki signaling can bypass proliferation termination in hinge and notum regions, suggesting that the mechanisms regulating proliferation termination may be distinct in different regions of the disc.One Sentence SummaryUsing Drosophila, Strassburger et al. investigate the termination of proliferation of an organ when it reaches its final size, and show this occurs due to a drop in TORC1 signaling.

scholarly journals Dpp controls growth and patterning in Drosophila wing precursors through distinct modes of action

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Pablo Sanchez Bosch ◽  
Ruta Ziukaite ◽  
Cyrille Alexandre ◽  
Konrad Basler ◽  
Jean-Paul Vincent
Keyword(s):  
Target Genes ◽  
Positional Information ◽  
Cell Fates ◽  
Drosophila Wing ◽  
The Subject ◽  
Spatio Temporal ◽  
Wing Growth ◽  
The Relationship ◽  
Anterior Posterior ◽  
Growth Threshold

Dpp, a member of the BMP family, is a morphogen that specifies positional information in Drosophila wing precursors. In this tissue, Dpp expressed along the anterior-posterior boundary forms a concentration gradient that controls the expression domains of target genes, which in turn specify the position of wing veins. Dpp also promotes growth in this tissue. The relationship between the spatio-temporal profile of Dpp signalling and growth has been the subject of debate, which has intensified recently with the suggestion that the stripe of Dpp is dispensable for growth. With two independent conditional alleles of dpp, we find that the stripe of Dpp is essential for wing growth. We then show that this requirement, but not patterning, can be fulfilled by uniform, low level, Dpp expression. Thus, the stripe of Dpp ensures that signalling remains above a pro-growth threshold, while at the same time generating a gradient that patterns cell fates.

scholarly journals Dpp from the anterior stripe of cells is crucial for the growth of the Drosophila wing disc

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Shinya Matsuda ◽  
Markus Affolter
Keyword(s):  
Null Allele ◽  
Growth Control ◽  
Wing Disc ◽  
The Other ◽  
Morphogen Gradient ◽  
Posterior Compartment ◽  
Time Points ◽  
Larval Stages ◽  
Drosophila Wing ◽  
Control Growth

The Dpp morphogen gradient derived from the anterior stripe of cells is thought to control growth and patterning of the Drosophila wing disc. However, the spatial-temporal requirement of dpp for growth and patterning remained largely unknown. Recently, two studies re-addressed this question. By generating a conditional null allele, one study proposed that the dpp stripe is critical for patterning but not for growth (Akiyama and Gibson, 2015). In contrast, using a membrane-anchored nanobody to trap Dpp, the other study proposed that Dpp dispersal from the stripe is required for patterning and also for medial wing disc growth, at least in the posterior compartment (Harmansa et al., 2015). Thus, growth control by the Dpp morphogen gradient remains under debate. Here, by removing dpp from the stripe at different time points, we show that the dpp stripe source is indeed required for wing disc growth, also during third instar larval stages.

scholarly journals A unified mechanism for the control of Drosophila wing growth by the morphogens Decapentaplegic and Wingless

PLoS Biology ◽  
2021 ◽  
Vol 19 (3) ◽  
pp. e3001111
Author(s):  
Myriam Zecca ◽  
Gary Struhl
Keyword(s):  
Temporal Change ◽  
Experimental Tests ◽  
Common Mechanism ◽  
Control Gene ◽  
Minimum Threshold ◽  
Cell Pattern ◽  
Drosophila Wing ◽  
Control Gene Expression ◽  
Control Growth ◽  
Wing Growth

Development of the Drosophila wing—a paradigm of organ development—is governed by 2 morphogens, Decapentaplegic (Dpp, a BMP) and Wingless (Wg, a Wnt). Both proteins are produced by defined subpopulations of cells and spread outwards, forming gradients that control gene expression and cell pattern as a function of concentration. They also control growth, but how is unknown. Most studies have focused on Dpp and yielded disparate models in which cells throughout the wing grow at similar rates in response to the grade or temporal change in Dpp concentration or to the different amounts of Dpp “equalized” by molecular or mechanical feedbacks. In contrast, a model for Wg posits that growth is governed by a progressive expansion in morphogen range, via a mechanism in which a minimum threshold of Wg sustains the growth of cells within the wing and recruits surrounding “pre-wing” cells to grow and enter the wing. This mechanism depends on the capacity of Wg to fuel the autoregulation of vestigial (vg)—the selector gene that specifies the wing state—both to sustain vg expression in wing cells and by a feed-forward (FF) circuit of Fat (Ft)/Dachsous (Ds) protocadherin signaling to induce vg expression in neighboring pre-wing cells. Here, we have subjected Dpp to the same experimental tests used to elucidate the Wg model and find that it behaves indistinguishably. Hence, we posit that both morphogens act together, via a common mechanism, to control wing growth as a function of morphogen range.

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.

Sign in / Sign up

Export Citation Format

Share Document