Dynamic shape changes of ECM-producing cells drive morphogenesis of ball-and-socket joints in the fly leg

Abstract

SUMMARYAnimal body shape is framed by the skeleton, which is composed of extracellular matrix (ECM). Although how the body plan manifests in skeletal morphology has been studied intensively, cellular mechanisms that directly control skeletal ECM morphology remain elusive. In particular, how dynamic behaviors of ECM-secreting cells, such as shape changes and movements, contribute to ECM morphogenesis is unclear. Strict control of ECM morphology is crucial in the joints, where opposing sides of the skeleton must have precisely reciprocal shapes to fit each other. Here we found that, in the development of ball-and-socket joints in the Drosophila leg, the two sides of ECM form sequentially. We show that distinct cell populations produce the 'ball' and the 'socket', and that these cells undergo extensive shape changes while depositing ECM. We propose that shape changes of ECM-producing cells enable the sequential ECM formation to allow the morphological coupling of adjacent components. Our results highlight the importance of dynamic cell behaviors in precise shaping of skeletal ECM architecture.

Joint morphology in the insect leg: evolutionary history inferred from Notch loss-of-function phenotypes in Drosophila

“…Immunohistochemistry and confocal and electron microscopy were carried out as described (Tajiri et al, 2010). For electron microscopy of the mayfly tarsal joints, for which only samples stored in 70% ethanol were available, the initial fixation was modified as follows: samples were directly fixed in 2.5% glutaraldehyde, 2% formaldehyde, 70% ethanol for 2 hours at room temperature, then in 2.5% glutaraldehyde, 2% formaldehyde, 0.1 M cacodylate buffer for 1 hour at room temperature, and then stored in the solution at 4°C.…”

“…We previously proposed a two-process model, in which the conjunction of cell differentiation and cell movement during development sculpts the joint morphology of the adult Drosophila tarsus (distal leg) (Tajiri et al, 2010) (Fig. 1A).…”

Ancestral reconstruction of tick lineages

“…Development of ball and socket joints in the Neoptera has been linked to Notch signalling and consequent cell differentiation and movement (Tajiri et al 2011(Tajiri et al , 2010.…”

Mechanical Control of Whole Body Shape by a Single Cuticular Protein Obstructor-E in Drosophila melanogaster

“…The fixed samples were embedded in 1% agarose in PBS and processed as described in [42], with small modifications. The embedded samples were postfixed with 1% OsO4 in 0.05M cacodylate buffer for 3 hours at room temperature, and then were dehydrated with a series of ethanol and propylene oxide.…”