Feedback regulation of<i>Drosophila</i>BMP signaling by the novel extracellular protein Larval Translucida

Szuperák, Milán; Salah, Samia; Meyer, Emily J.; Nagarajan, Usha; Ikmi, Aissam; Gibson, Matthew C.

doi:10.1242/dev.059477

Cited by 42 publications

(50 citation statements)

References 70 publications

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“…As in the embryo (Reim et al, 2003;Hamaguchi et al, 2004;Hatton-Ellis et al, 2007), Doc in the peripheral wing pouch is activated by Dpp (Szuperák et al, 2011). The formation of the double-crescent pattern requires, in addition, Doc repression.…”

Section: The Dynamic Doc Expression Pattern Is Regulated By Mutual Anmentioning

confidence: 99%

The Dorsocross T-box transcription factors promote tissue morphogenesis in the Drosophila wing imaginal disc

2012

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The Drosophila wing imaginal disc is subdivided into notum, hinge and blade territories during the third larval instar by formation of several deep apical folds. The molecular mechanisms of these subdivisions and the subsequent initiation of morphogenic processes during metamorphosis are poorly understood. Here, we demonstrate that the Dorsocross (Doc) T-box genes promote the progression of epithelial folds that not only separate the hinge and blade regions of the wing disc but also contribute to metamorphic development by changing cell shapes and bending the wing disc. We found that Doc expression was restricted by two inhibitors, Vestigial and Homothorax, leading to two narrow Doc stripes where the folds separating hinge and blade are forming. Doc mutant clones prevented the lateral extension and deepening of these folds at the larval stage and delayed wing disc bending in the early pupal stage. Ectopic Doc expression was sufficient to generate deep apical folds by causing a basolateral redistribution of the apical microtubule web and a shortening of cells. Cells of both the endogenous blade/hinge folds and of folds elicited by ectopic Doc expression expressed Matrix metalloproteinase 2 (Mmp2). In these folds, integrins and extracellular matrix proteins were depleted. Overexpression of Doc along the blade/hinge folds caused precocious wing disc bending, which could be suppressed by co-expressing MMP2RNAi.

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Section: The Dynamic Doc Expression Pattern Is Regulated By Mutual Anmentioning

confidence: 99%

The Dorsocross T-box transcription factors promote tissue morphogenesis in the Drosophila wing imaginal disc

2012

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“…Mad and Medea without Schnurri bind to AEs to regulate a different set of target genes, notably dad [101]. Other targets of BMP signaling include sal , omb , vg and ltl [102–105]. Another set of targets have distinct D/V patterns in the early embryo, including zen , race , and ush [91,106], and induction of labial expression by Dpp is required for gut development [107].…”

Section: Smad Proteinsmentioning

confidence: 99%

Strategies for exploring TGF-β signaling in Drosophila

Peterson

O’Connor

2014

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The TGF-beta pathway is an evolutionarily conserved signal transduction module that mediates diverse biological processes in animals. In Drosophila, both the BMP and Activin branches are required for viability. Studies rooted in classical and molecular genetic approaches continue to uncover new developmental roles for TGF-beta signaling. We present an overview of the secreted ligands, transmembrane receptors and cellular Smad transducer proteins that comprise the core pathway in Drosophila. An assortment of tools have been developed to conduct tissue-specific loss and gain-of-function experiments for these pathway components. We discuss the deployment of these reagents, with an emphasis on appropriate usage and limitations of the available tools. Throughout, we note reagents that are in need of further improvement of development, and signaling features requiring further study. A general theme is that comparison of phenotypes for ligands, receptors, and Smads can be used to map tissue interactions, and to separate canonical and non-canonical signaling activities. Core TGF-beta signaling components are subject to multiple layers of regulation, and are coupled to context-specific inputs and outputs. In addition to fleshing out how TGF-beta signaling serves the fruit fly, we anticipate that future studies will uncover new regulatory nodes and modes and will continue to advance paradigms for how TGF-beta signaling regulates general developmental processes.

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“…While we were not able to identify an orthologue of tok, the presence of a distinct tld orthologue in E. balteatus suggests that the dipteran gene duplication giving rise to tld and tok occurred before the origin of the amnioserosa (Figure 3D). BMP ligand activity in D. melanogaster is additionally modulated by Twisted gastrulation (Tsg) [51,52], Crossveinless (Cv) [53,54], Shrew (Srw) [26,55], as well as the membrane associated factors Crossveinless-2 (Cv-2) [56,57], Kekkon 5 (Kek5) [58], Pentagone (Pent) [59] and Larval Translucida (Ltl) [60]. We identified E. balteatus homologues of cv-2, kek5 (Figure 3E) as well as tsg, cv and an additional cv paralogue, Eba-cv-like (Figure 3F).…”

Section: Resultsmentioning

confidence: 99%

BMP signaling components in embryonic transcriptomes of the hover fly Episyrphus balteatus (Syrphidae)

et al. 2011

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BackgroundIn animals, signaling of Bone Morphogenetic Proteins (BMPs) is essential for dorsoventral (DV) patterning of the embryo, but how BMP signaling evolved with changes in embryonic DV differentiation is largely unclear. Based on the extensive knowledge of BMP signaling in Drosophila melanogaster, the morphological diversity of extraembryonic tissues in different fly species provides a comparative system to address this question. The closest relatives of D. melanogaster with clearly distinct DV differentiation are hover flies (Diptera: Syrphidae). The syrphid Episyrphus balteatus is a commercial bio-agent against aphids and has been established as a model organism for developmental studies and chemical ecology. The dorsal blastoderm of E. balteatus gives rise to two extraembryonic tissues (serosa and amnion), whereas in D. melanogaster, the dorsal blastoderm differentiates into a single extraembryonic epithelium (amnioserosa). Recent studies indicate that several BMP signaling components of D. melanogaster, including the BMP ligand Screw (Scw) and other extracellular regulators, evolved in the dipteran lineage through gene duplication and functional divergence. These findings raise the question of whether the complement of BMP signaling components changed with the origin of the amnioserosa.ResultsTo search for BMP signaling components in E. balteatus, we generated and analyzed transcriptomes of freshly laid eggs (0-30 minutes) and late blastoderm to early germband extension stages (3-6 hours) using Roche/454 sequencing. We identified putative E. balteatus orthologues of 43% of all annotated D. melanogaster genes, including the genes of all BMP ligands and other BMP signaling components.ConclusionThe diversification of several BMP signaling components in the dipteran linage of D. melanogaster preceded the origin of the amnioserosa.[Transcriptome sequence data from this study have been deposited at the NCBI Sequence Read Archive (SRP005289); individually assembled sequences have been deposited at GenBank (JN006969-JN006986).]

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Feedback regulation ofDrosophilaBMP signaling by the novel extracellular protein Larval Translucida

Cited by 42 publications

References 70 publications

The Dorsocross T-box transcription factors promote tissue morphogenesis in the Drosophila wing imaginal disc

The Dorsocross T-box transcription factors promote tissue morphogenesis in the Drosophila wing imaginal disc

Strategies for exploring TGF-β signaling in Drosophila

BMP signaling components in embryonic transcriptomes of the hover fly Episyrphus balteatus (Syrphidae)

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