Abstract
Contractile tension is critical for musculoskeletal system development and maintenance. In insects, the muscular force is transmitted to the exoskeleton through the tendon cells and tendon apical extracellular matrix (ECM). In Drosophila, we found tendon cells secrete Dumpy (Dpy), a zona pellucida domain (ZPD) protein, to form the force-resistant filaments in the exuvial space, anchoring the tendon cells to the pupal cuticle. We showed that Dpy undergoes filamentous conversion in response to the tension increment during indirect flight muscle development. We also found another ZPD protein Quasimodo (Qsm) protects the notum epidermis from collapsing under the muscle tension by enhancing the tensile strength of Dpy filaments. Qsm is co-transported with Dpy in the intracellular vesicles and diffuses into the exuvial space after secretion. Tissue-specific qsm expression rescued the qsm mutant phenotypes in distant tissues, suggesting Qsm can function in a long-range, non-cell-autonomous manner. In the cell culture assay, Qsm interacts with Dpy-ZPD and promotes secretion and polymerization of Dpy-ZPD. The roles of Qsm underlies the positive feedback mechanism of force-dependent organization of Dpy filaments, providing new insights into apical ECM remodeling through the unconventional interaction of ZPD proteins.
Highlights
Mechanical force of muscles is transmitted to the skeleton through tendons
Force-dependent formation of Dpy filaments To study the localization of Dpy in the notum muscle insertion sites, pupae of the Dpy-YFP knockin strain[26,27] were imaged live at the anterior notum margin where dorsal-longitudinal muscles (DLM) form tendon structures (Figure 1A–E)
Tendon cells labeled with stripe enhancer are specialized parts of the body wall epidermis that simultaneously connect with developing muscles through basolateral elongations in the body cavity and with the pupal cuticle in the apical surface (Figures 1A and 1B; 17.5 h APF)
Summary
Mechanical force of muscles is transmitted to the skeleton through tendons. Loss of applied force results in developmental atrophy of tendon tissues and severe motor disorder.[1,2] The mechanical tension is critical to myotendinous system development and maintenance, in part via regulating the secretion and organization of the collagen extracellular matrix (ECM) of the vertebrate tendon.[3,4] During muscle development, tendon cells and ECM develop resistance to increasing contractility in the developing muscles to keep the musculoskeletal system from collapsing. The process by which mechanical force regulates the dynamic organization of tendon ECM in vertebrates is unclear. We used Drosophila indirect flight muscles (IFM) and the associated tendon cells as a model to identify key molecular components of tendon ECM maturation
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