<i>Drosophila</i> adult muscle precursors form a network of interconnected cells and are specified by the <i>rhomboid</i>-triggered EGF pathway

Figeac, Nicolas; Jagla, Teresa; Aradhya, Rajaguru; Ponte, Jean Philippe Da; Jagla, Krzysztof

doi:10.1242/dev.049080

Cited by 43 publications

(56 citation statements)

References 35 publications

(40 reference statements)

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“…4C-C″). Double staining for IsletH-GFP and Zfh1, a general AMP marker (Sellin et al, 2009;Figeac et al, 2010), previously established that the DA2 PC gives rise to a mixed DA2/AMP lineage (Boukhatmi et al, 2012). Similarly, one AM PC daughter cell is Zfh1 positive (Fig.…”

Section: Am and Tarm Lineage Analysesmentioning

confidence: 70%

An Org-1–Tup transcriptional cascade reveals different types of alary muscles connecting internal organs in Drosophila

et al. 2014

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The T-box transcription factor Tbx1 and the LIM-homeodomain transcription factor Islet1 are key components in regulatory circuits that generate myogenic and cardiogenic lineage diversity in chordates. We show here that Org-1 and Tup, the Drosophila orthologs of Tbx1 and Islet1, are co-expressed and required for formation of the heart-associated alary muscles (AMs) in the abdomen. The same holds true for lineage-related muscles in the thorax that have not been described previously, which we name thoracic alary-related muscles (TARMs). Lineage analyses identified the progenitor cell for each AM and TARM. Three-dimensional highresolution analyses indicate that AMs and TARMs connect the exoskeleton to the aorta/heart and to different regions of the midgut, respectively, and surround-specific tracheal branches, pointing to an architectural role in the internal anatomy of the larva. Org-1 controls tup expression in the AM/TARM lineage by direct binding to two regulatory sites within an AM/TARM-specific cis-regulatory module, tupAME. The contributions of Org-1 and Tup to the specification of Drosophila AMs and TARMs provide new insights into the transcriptional control of Drosophila larval muscle diversification and highlight new parallels with gene regulatory networks involved in the specification of cardiopharyngeal mesodermal derivatives in chordates.

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Section: Am and Tarm Lineage Analysesmentioning

confidence: 70%

An Org-1–Tup transcriptional cascade reveals different types of alary muscles connecting internal organs in Drosophila

et al. 2014

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“…3C,CЈ,F,FЈ), although one of these rapidly became undetectable. The observation of about one extra Lb + cell in this area upon blocking cell death (Figeac et al, 2010) suggests to us that this fourth cell normally undergoes apoptosis. Consistent with previous findings with Lb as a marker, one of the three Org-1 + and Lb + cells was seen to form M8, whereas the other two formed the two lAMPs (Fig.…”

Section: Org-1 Is Expressed In Two Characterized Somatic Muscle Lineamentioning

confidence: 83%

“…This maintenance might be regulated by inputs shared with two separate later-acting enhancer elements upstream of lbe (termed LAMPE) and lbl (termed LME). Both of these elements include homeodomain binding motifs that probably mediate autoregulation by Lb, in addition to ETS domain and Mef2-binding motifs, respectively, that also contribute to full activity in M8 (Figeac et al, 2010). In org-1 mutants, the lbl-SBM enhancer is inactive not only early but also late, possibly because Lb protein is not available for autoregulation.…”

Section: Research Articlementioning

confidence: 99%

“…Lbe is expressed directly adjacent to Slou in a promuscular cluster and then two muscle progenitors. One of these progenitors forms muscle 8 (SBM) and a lateral adult muscle precursor (lAMP), which continue to express Lb, whereas the other forms a second Lb + lAMP and a sibling that probably undergoes apoptosis (Jagla et al, 1998;Knirr et al, 1999;Figeac et al, 2010). Genetic and genomic analyses indicate that Lb has important functions in the specification and/or differentiation of muscle 8 (Junion et al, 2007;Bataille et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Org-1, the Drosophila ortholog of Tbx1, is a direct activator of known identity genes during muscle specification

et al. 2012

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SUMMARYMembers of the T-Box gene family of transcription factors are important players in regulatory circuits that generate myogenic and cardiogenic lineage diversities in vertebrates. We show that during somatic myogenesis in Drosophila, the single ortholog of vertebrate Tbx1, optomotor-blind-related-gene-1 (org-1), is expressed in a small subset of muscle progenitors, founder cells and adult muscle precursors, where it overlaps with the products of the muscle identity genes ladybird (lb) and slouch (slou). In addition, org-1 is expressed in the lineage of the heart-associated alary muscles. org-1 null mutant embryos lack Lb and Slou expression within the muscle lineages that normally co-express org-1. As a consequence, the respective muscle fibers and adult muscle precursors are either severely malformed or missing, as are the alary muscles. To address the mechanisms that mediate these regulatory interactions between Org-1, Lb and Slou, we characterized distinct enhancers associated with somatic muscle expression of lb and slou. We demonstrate that these lineage-and stage-specific cis-regulatory modules (CRMs) bind Org-1 in vivo, respond to org-1 genetically and require T-box domain binding sites for their activation. In summary, we propose that org-1 is a common and direct upstream regulator of slou and lb in the developmental pathway of these two neighboring muscle lineages. Cross-repression between slou and lb and combinatorial activation of lineage-specific targets by Org-1-Slou and Org-1-Lb, respectively, then leads to the distinction between the two lineages. These findings provide new insights into the regulatory circuits that control the proper pattering of the larval somatic musculature in Drosophila.

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“…Since WHPs give rise to adult tissues, we suggest that both connections serve to keep the WHPs together and in close proximity to their future target site. Similarly, adult muscle precursors (AMPs) are interconnected by cellular extensions (Figeac et al, 2010) and are either associated as adepithelial cells with the imaginal discs or with peripheral nerves (Bate et al, 1991). We further suggest that WHPs are immobile during their connection with the trachea.…”

Section: The Role Of Instructive Signals From Surrounding Tissues In mentioning

confidence: 99%

In vivo imaging of Drosophila wing heart development during pupal stages

Tögel

Pass²,

Paululat³

2013

Int. J. Dev. Biol.

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Wing hearts are small pumping organs that maintain the flow of hemolymph through the wing veins of insects. In Drosophila, these organs consist of parallel oriented muscle cells and a simple epithelium of connective tissue. Both tissues originate from eight embryonic wing heart progenitors (WHPs), which remain dormant until late larval stages. Most of the differentiation and maturation takes place during the pupal stage following head eversion. In this study, we have used the tissue specific expression of Gal4 enhancer lines, in combination with the live cell markers GFP and DsRed to investigate pupal wing heart development in conjunction with the surrounding tissues. We found that WHPs interact with the tracheal system and specific expression domains of the adult epidermis. Additionally, wing heart development occurs simultaneously with the remodeling of the dorso-lateral epidermis into the scutellum and the scutellar arms. Myogenesis in wing hearts comprises known processes such as founder cell specification, but also new features like removal of growing myotubes, and nuclei movement. Wing heart epithelium development is accomplished by the mesenchymal-epithelial transition of WHPs and occurs slightly delayed to muscle development. The epithelium represents a novel mesodermally derived secondary epithelium. Moreover, we have identified a nerve that runs along the epithelium and innervates the wing heart muscle cells.

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Drosophila adult muscle precursors form a network of interconnected cells and are specified by the rhomboid-triggered EGF pathway

Cited by 43 publications

References 35 publications

An Org-1–Tup transcriptional cascade reveals different types of alary muscles connecting internal organs in Drosophila

An Org-1–Tup transcriptional cascade reveals different types of alary muscles connecting internal organs in Drosophila

Org-1, the Drosophila ortholog of Tbx1, is a direct activator of known identity genes during muscle specification

In vivo imaging of Drosophila wing heart development during pupal stages

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