Abstract
ABSTRACTDuring Drosophila metamorphosis, nascent testis myotubes migrate from the prospective seminal vesicle of the genital disc onto pupal testes and then further to cover the testes with multinucleated smooth-like muscles. Here we show that DWnt2 is likely required for determination of testis-relevant myoblasts on the genital disc. Knock down of fibroblast growth factor receptor (FGFR) heartless by RNAi and a dominant-negative version revealed multiple functions of Heartless, namely regulation of the amount of myoblasts on the genital disc, connection of seminal vesicles and testes, and migration of muscles along the testes. Live imaging indicated that the downstream effector Stumps is required for migration of testis myotubes on the testis towards the apical tip. After myoblast fusion, myosin II is needed for migration of nascent testis myotubes, in which Thisbe-dependent fibroblast growth factor (FGF) signaling is activated. Cadherin-N is essential for connecting these single myofibers and for creating a firm testis muscle sheath that shapes and stabilizes the testis tubule. Based on these results, we propose a model for the migration of testis myotubes in which nascent testis myotubes migrate as a collective onto and along the testis, dependent on FGF-regulated expression of myosin II.
Highlights
Cell migration is essential for many developmental and physiological processes throughout the animal kingdom, and is implicated in diseases, e.g. cancer metastasis (Roca-Cusachs et al, 2013)
Based on our results, we propose a model in which testis myotube migration is divided into two Htl- and Cad-N-dependent phases. (i) After myoblast fusion, when Stumps and Cad-N are distributed along the plasma membrane of nascent testis myotubes that are in close contact to the adjacent epithelium of the prospective seminal vesicles, fibroblast growth factor (FGF) signaling initiates collective migration of nascent testis myotubes from the prospective seminal vesicle onto the testis (Fig. 8B). (ii) The coverage of the testes with muscles is achieved by collective cells migrating towards the testis tip, and this migration requires myosin II and the formation of a network of nascent myotubes with Cad-N-positive connections (Fig. 8C)
We propose that the ligand Ths and possibly Pyr binds Htl in nascent myotubes and thereby activates FGF signaling via Stumps during both phases of migration; the source of these ligands needs to be determined
Summary
Cell migration is essential for many developmental and physiological processes throughout the animal kingdom, and is implicated in diseases, e.g. cancer metastasis (Roca-Cusachs et al, 2013). We focus on the migration of muscle cells during the development of the male reproductive tract of Drosophila. Nascent myotubes migrate over the developing seminal vesicles onto the pupal testes and build the muscle sheath surrounding the adult testis (Kozopas et al, 1998; Kuckwa et al, 2016). This musculature is composed of multinucleated, smooth-like myofibers (Susic-Jung et al, 2012)
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