Odd-skipped and Stripe act downstream of Notch to promote the morphogenesis of long appendicular tendons inDrosophila

Abstract

Multiple tissue interactions take place during the development of the limb musculoskeletal system. While appendicular myogenesis has been extensively studied, development of connective tissue associated with muscles has received less attention. In the developing Drosophila leg, tendon-like connective tissue arises from clusters of epithelial cells that invaginate into the leg cavity and then elongate to form internal tube-shape structures along which muscle precursors are distributed. Here we show that stripe-positive appendicular precursors of tendon-like connective tissue are set up among intersegmental leg joint cells expressing odd-skipped genes, and that Notch signaling is necessary and locally sufficient to trigger stripe expression. This study also finds that odd-skipped genes and stripe are both required downstream of Notch to promote morphogenesis of tube-shaped internal tendons of the leg.

Genetic Control of Muscle Diversification and Homeostasis: Insights from Drosophila

“…The wing and leg imaginal discs generate Sr positive tendon-like precursor cell clusters starting from the third larval instar until the beginning of pupation. Sr expression is initiated by Notch signaling [ 227 , 228 ]. Leg muscles attach to the internal tendons on one end and the tendon cells in the exoskeleton on the other end.…”

Transcriptomic and genetic analyses identify the Krüppel-like factor dar1 as a master regulator of tube-shaped long tendon development

“…We had previously shown that precursors of the long tendons are clusters of epithelial cells selected among the cells of leg segmental joints. The Notch pathway initiates stripe expression, the key factor in tendon cell differentiation, in the leg tendon precursors (Laddada et al, 2019; Soler et al, 2004).…”

“…In all, nearly 65% (20/31, including stripe itself) of the candidate genes were positive for at least one readout and for eight of them this result was obtained with two different RNAi lines ( Table 1 ). Of these positive hits, we found odd and drm both members of the odd-skipped gene family that act downstream of the Notch pathway to promote leg tendon growth (Laddada et al, 2019). We also identified esg , which interferes with the Notch pathway during stem cell maintenance/differentiation (Korzelius et al, 2014), and which is required during tracheal morphogenesis (Miao and Hayashi, 2016).…”

“…Strikingly, the morphogenesis of the long tendons shares many similarities with the tubulogenesis that occurs during tracheal or salivary gland formation in Drosophila (Girdler and Röper, 2014; Hayashi and Kondo, 2018; Maruyama and Andrew, 2012). First, tendon cells undergo apical constriction followed by invagination without migration (Laddada et al, 2019). The cells then collectively migrate with extension of basal protrusions, leading to the elongation of a tube-shaped tendon ( Fig.…”

“…It has also been suggested that like for the developing salivary gland (Vining et al, 2005), elongating tendons could interact with surrounding tissues, especially with the myoblasts (Soler et al, 2016, 2004). We have already shown that long tendons originate from tendon precursors that are selected among the cells of leg segmental joints expressing odd-skipped (Laddada et al, 2019). While odd is sufficient to induce the primary invagination of the epithelial cells (Hao et al, 2003; Ibeas and Bray, 2003), stripe is required to make these cells competent to migrate and form a long tube-shaped tendon (Laddada et al, 2019).…”