Abstract
BackgroundThe visceral musculature of Drosophila larvae comprises circular visceral muscles tightly interwoven with longitudinal visceral muscles. During myogenesis, the circular muscles arise by one-to-one fusion of a circular visceral founder cell (FC) with a visceral fusion-competent myoblast (FCM) from the trunk visceral mesoderm, and longitudinal muscles arise from FCs of the caudal visceral mesoderm. Longitudinal FCs migrate anteriorly under guidance of fibroblast growth factors during embryogenesis; it is proposed that they fuse with FCMs from the trunk visceral mesoderm to give rise to syncytia containing up to six nuclei.ResultsUsing fluorescence in situ hybridization and immunochemical analyses, we investigated whether these fusion events during migration use the same molecular repertoire and cellular components as fusion-restricted myogenic adhesive structure (FuRMAS), the adhesive signaling center that mediates myoblast fusion in the somatic mesoderm. Longitudinal muscles were formed by the fusion of one FC with Sns-positive FCMs, and defects in FCM specification led to defects in longitudinal muscle formation. At the fusion sites, Duf/Kirre and the adaptor protein Rols7 accumulated in longitudinal FCs, and Blow and F-actin accumulated in FCMs. The accumulation of these four proteins at the fusion sites argues for FuRMAS-like adhesion and signaling centers. Longitudinal fusion was disturbed in rols and blow single, and scar wip double mutants. Mutants of wasp or its interaction partner wip had no defects in longitudinal fusion.ConclusionsOur results indicated that all embryonic fusion events depend on the same cell-adhesion molecules, but that the need for Rols7 and regulators of F-actin distinctly differs. Rols7 was required for longitudinal visceral and somatic myoblast fusion but not for circular visceral fusion. Importantly, longitudinal fusion depended on Kette and SCAR/Wave but was independent of WASp-dependent Arp2/3 activation. Thus, the complexity of the players involved in muscle formation increases from binucleated circular muscles to longitudinal visceral muscles to somatic muscles.
Highlights
The visceral musculature of Drosophila larvae comprises circular visceral muscles tightly interwoven with longitudinal visceral muscles
At late stage 11, the trunk mesoderm contains on each side of the embryo a row of founder cell (FC) for the circular visceral muscles and two to three rows of fusion-competent myoblast (FCM), which have been proposed to be a common pool for circular visceral muscles and longitudinal visceral muscles
Longitudinal muscle development requires the F-actinregulating proteins Myoblast City, Blown fuse (Blow), and Kette Since we found fusion-restricted myogenic adhesive structure (FuRMAS)-like structures with actin foci during fusion of longitudinal FCs with FCMs (Figure 2E– H), we analyzed regulators of F-actin polymerization required for somatic myoblast fusion
Summary
The visceral musculature of Drosophila larvae comprises circular visceral muscles tightly interwoven with longitudinal visceral muscles. The body wall musculature of Drosophila melanogaster arises during embryogenesis and metamorphosis by fusion within the somatic mesoderm of two cell types: the founder cells (FCs) and the fusion-competent myoblasts (FCMs). This fusion generates syncytial myotubes that allow movement of larvae and adults (reviewed in [1,2]). The fate of circular FC is determined by both Delta/Notch signaling and Ras/MAPK signaling via the receptor tyrosine kinase ALK and its ligand Jelly Belly [15,16,17,18,19] These FCs fuse one-to-one with a visceral FCM. The binucleate cells stretch until they enclose the whole gut [8,10,11]
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