Mechano-Chemical Enforcement of Tendon Apical ECM into Nano-Filaments During Drosophila Flight Muscle Development

Abstract

Contractile tension is critical for musculoskeletal system development and maintenance. In insects, the force transmission from the muscle to the exoskeleton depends on the tendon cells and tendon apical extracellular matrix (aECM). In Drosophila, 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. By live imaging, we showed that Dpy filaments undergo remodeling in response to the tension increase during indirect flight muscle development. Additionally, we found another ZPD protein, Quasimodo (Qsm), which plays a long-range, non-cell-autonomous role in Dpy filaments enforcement. Inside the cells, Qsm promotes secretion and polymerization of Dpy-ZPD. The dual role of Qsm underlies the positive feedback mechanism of force-dependent remodeling of Dpy filaments, providing new insights into aECM remodeling through the unconventional interaction of ZPD proteins.