Coordinated Development of Muscles and Tendon-Like Structures: Early Interactions in the Drosophila Leg

Abstract

The formation of the musculoskeletal system is a remarkable example of tissue assembly. In both vertebrates and invertebrates, precise connectivity between muscles and skeleton (or exoskeleton) via tendons or equivalent structures is fundamental for movement and stability of the body. The molecular and cellular processes underpinning muscle formation are well-established and significant advances have been made in understanding tendon development. However, the mechanisms contributing to proper connection between these two tissues have received less attention. Observations of coordinated development of tendons and muscles suggest these tissues may interact during the different steps in their development. There is growing evidence that, depending on animal model and muscle type, these interactions can take place from progenitor induction to the final step of the formation of the musculoskeletal system. Here, we briefly review and compare the mechanisms behind muscle and tendon interaction throughout the development of vertebrates and Drosophila before going on to discuss our recent findings on the coordinated development of muscles and tendon-like structures in Drosophila leg. By altering apodeme formation (the functional Drosophila equivalent of tendons in vertebrates) during the early steps of leg development, we affect the spatial localization of subsequent myoblasts. These findings provide the first evidence of the developmental impact of early interactions between muscle and tendon-like precursors, and confirm the appendicular Drosophila muscle system as a valuable model for studying these processes.

Genetic Control of Muscle Diversification and Homeostasis: Insights from Drosophila

“…Unlike vertebrates, Drosophila does not have an internal skeleton and tendon cells help anchor the muscles firmly to the cuticular exoskeleton instead, which helps transmit the contractile forces to the body to generate motion. This makes them functionally similar to vertebrate tendons despite their distinct embryological origins, mesodermal for vertebrates and ectodermal for Drosophila [ 17 , 18 ]. The formation and maintenance of the MTJ is mediated through the ECM by specific integrin heterodimers on the muscle and tendon ends in Drosophila similar to vertebrates [ 19 , 20 , 21 , 22 ].…”

Amontillado is required forDrosophilaSlit processing and for tendon-mediated muscle patterning

“…In the Drosophila embryo each muscle is formed through fusion of a single founder cell with fusion-competent myoblasts, forming a syncytium that then elongates towards its attachment sites, the ectodermal tendon cells (Schejter and Baylies, 2010; Schnorrer and Dickson, 2004b; Soler et al, 2016). Once the elongating muscle comes in contact with its corresponding tendon, an integrin-mediated myotendinous junction (MTJ) is formed between both cell types (Bokel and Brown, 2002).…”

doublesexregulates sexually dimorphic beetle horn formation by integrating spatial and temporal developmental contexts in the Japanese rhinoceros beetleTrypoxylus dichotomus

“…In addition, we also found that apolysis occurring at 36 h APF can be another ununbiguous developmental marker. Larval mandibular tendons tightly connecting mandibular muscles and apodemes (Movie 1b) [35,36] were completely detached from apdemes at 36 h APF along with the apolysis occurring at every body part including the neighboring ocular region to know the timing of sexual dimorphism formation.…”

“…(b) The morphological character of the ocular and the mandibular apodeme at 24 h APF. Apolysis was incomplete in the ocular and the mandibular apodeme at 24 h APF [35,36]. After this stage, prepupal horn primordia can be readily dissected out due to apolysis at the ocular and the mandibular apodeme (Fig.…”