Genetic screen for regulators of <i>ind</i> expression identifies <i>shrew</i> as encoding a novel twisted gastrulation‐like protein involved in Dpp signaling

Bonds, Morgan; Sands, J. G.; Poulson, Will; Harvey, Canda; Ohlen, Tonia Von

doi:10.1002/dvdy.21360

Cited by 11 publications

(11 citation statements)

References 28 publications

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“…While a number of screens have already made use of the Df collection (Bonds et al 2007) or the transposon insertion collection (Kankel et al 2007;Chang et al 2008;Shalaby et al 2009) individually, the logistics of obtaining and screening all of the 16,000 lines is not feasible for many labs. Thus, we applied a hierarchical strategy for our screen ( Figure 1A) that would take advantage of both collections and also would assay LOF vs. neomorphic effects.…”

Section: Resultsmentioning

confidence: 99%

Parallel Genetic and Proteomic Screens Identify Msps as a CLASP–Abl Pathway Interactor in Drosophila

Lowery

Lee²,

Lu³

et al. 2010

Genetics

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Regulation of cytoskeletal structure and dynamics is essential for multiple aspects of cellular behavior, yet there is much to learn about the molecular machinery underlying the coordination between the cytoskeleton and its effector systems. One group of proteins that regulate microtubule behavior and its interaction with other cellular components, such as actin-regulatory proteins and transport machinery, is the plus-end tracking proteins (MT1TIPs). In particular, evidence suggests that the MT1TIP, CLASP, may play a pivotal role in the coordination of microtubules with other cellular structures in multiple contexts, although the molecular mechanism by which it functions is still largely unknown. To gain deeper insight into the functional partners of CLASP, we conducted parallel genetic and proteome-wide screens for CLASP interactors in Drosophila melanogaster. We identified 36 genetic modifiers and 179 candidate physical interactors, including 13 that were identified in both data sets. Grouping interactors according to functional classifications revealed several categories, including cytoskeletal components, signaling proteins, and translation/RNA regulators. We focused our initial investigation on the MT1TIP Minispindles (Msps), identified among the cytoskeletal effectors in both genetic and proteomic screens. Here, we report that Msps is a strong modifier of CLASP and Abl in the retina. Moreover, we show that Msps functions during axon guidance and antagonizes both CLASP and Abl activity. Our data suggest a model in which CLASP and Msps converge in an antagonistic balance in the Abl signaling pathway.

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Section: Resultsmentioning

confidence: 99%

Parallel Genetic and Proteomic Screens Identify Msps as a CLASP–Abl Pathway Interactor in Drosophila

Lowery

Lee²,

Lu³

et al. 2010

Genetics

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“…Indeed, genetic studies have revealed that Scw and Gbb interact with a distinct suite of extracellular modulators and have different affinities and preferences for the Type I receptors Tkv and Sax. In the early embryo, Scw signalling requires the Chordin orthologue Sog, the metalloprotease Tld, and the cysteinerich binding proteins Tsg and Srw, and is transduced by the Type I receptor Sax (Bonds et al 2007;Holley et al 1995;Neul and Ferguson 1998;Shimmi et al 2005a). In the pupal wing, Gbb signalling requires Sog, the metalloprotease Tok, and the cysteine-rich binding protein Cv, and is transduced primarily through the Type I receptor Tkv (Ray and Wharton 2001;Serpe et al 2005;Shimmi et al 2005a).…”

Section: A Unique Signalling Mode Has Evolved With Scwmentioning

confidence: 98%

“…Scw functions in the early embryo where it augments Dpp signalling along the dorsal-ventral axis to produce peak levels of BMP activity at the dorsal midline, thus, specifying cells that will become the extraembryonic amnioserosa (Arora et al 1994). Scw achieves this focusing of BMP activity by forming heterodimers with Dpp (Shimmi et al 2005b), interacting with a specific suite of extracellular modulators including the Chordin orthologue Short gastrulation (Sog), the metalloprotease Tolloid (Tld), and the cysteine-rich binding proteins Twisted gastrulation (Tsg) and Shrew (Srw) (Bonds et al 2007;Holley et al 1995;Neul and Ferguson 1998;O'Connor et al 2006;Shimmi and O'Connor 2003), and signalling through the Type I receptor Saxophone (Sax; Neul and Ferguson 1998;Nguyen et al 1998).…”

Section: Introductionmentioning

confidence: 99%

Rapid evolution of a novel signalling mechanism by concerted duplication and divergence of a BMP ligand and its extracellular modulators

2010

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Gene duplication and divergence is widely considered to be a fundamental mechanism for generating evolutionary novelties. The Bone Morphogenetic Proteins (BMPs) are a diverse family of signalling molecules found in all metazoan genomes that have evolved by duplication and divergence from a small number of ancestral types. In the fruit fly Drosophila, there are three BMPs: Decapentaplegic (Dpp) and Glass bottom boat (Gbb), which are the orthologues of vertebrate BMP2/4 and BMP5/6/7/8, respectively, and Screw (Scw), which, at the sequence level, is equally divergent from Dpp and Gbb. It has recently been shown that Scw has arisen from a duplication of Gbb in the lineage leading to higher Diptera. We show that since this duplication event, Gbb has maintained the ancestral BMP5/6/7/8 functionality while Scw has rapidly diverged. The evolution of Scw was accompanied by duplication and divergence of a suite of extracellular regulators that continue to diverge together in the higher Diptera. In addition, Scw has become restricted in its receptor specificity: Gbb proteins can signal through the Type I receptors Thick veins (Tkv) and Saxophone (Sax), while Scw signals through Sax. Thus, in a relatively short span of evolutionary time, the duplication event that gave rise to Scw produced not only a novel ligand but also a novel signalling mode that is functionally distinct from the ancestral Gbb mode. Our results demonstrate the plasticity of the BMP pathway not only in evolving new family members and new functions but also new signalling modes by redeploying key regulators in the pathway.

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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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Genetic screen for regulators of ind expression identifies shrew as encoding a novel twisted gastrulation‐like protein involved in Dpp signaling

Cited by 11 publications

References 28 publications

Parallel Genetic and Proteomic Screens Identify Msps as a CLASP–Abl Pathway Interactor in Drosophila

Parallel Genetic and Proteomic Screens Identify Msps as a CLASP–Abl Pathway Interactor in Drosophila

Rapid evolution of a novel signalling mechanism by concerted duplication and divergence of a BMP ligand and its extracellular modulators

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

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