A Cdc42-mediated supracellular network drives polarized forces and Drosophila egg chamber extension

Abstract

Actomyosin supracellular networks emerge during development and tissue repair. These cytoskeletal structures are able to generate large scale forces that can extensively remodel epithelia driving tissue buckling, closure and extension. How supracellular networks emerge, are controlled and mechanically work still remain elusive. During Drosophila oogenesis, the egg chamber elongates along the anterior-posterior axis. Here we show that a dorsal-ventral polarized supracellular F-actin network, running around the egg chamber on the basal side of follicle cells, emerges from polarized intercellular filopodia that radiate from basal stress fibers and extend penetrating neighboring cell cortexes. Filopodia can be mechanosensitive and function as cell-cell anchoring sites. The small GTPase Cdc42 governs the formation and distribution of intercellular filopodia and stress fibers in follicle cells. Finally, our study shows that a Cdc42-dependent supracellular cytoskeletal network provides a scaffold integrating local oscillatory actomyosin contractions at the tissue scale to drive global polarized forces and tissue elongation.

Cellular and Supracellular Planar Polarity: A Multiscale Cue to Elongate the Drosophila Egg Chamber

“…In addition, actomyosin dissection along a line parallel to the DV axis results in much slower recoil compared to a linear dissection along the orthogonal direction (i.e., the AP axis). This shows that the egg chamber during S9-S10 is under anisotropic tension with higher tension along the DV axis ( Popkova et al, 2020 ). Both intercellular filopodia and stress-fibers are under the control of the activity of the small GTPase Cdc42.…”

“…During S9 and S10, the actin bundles contract under the action of the myosin (MyoII) motor protein to form an active contracting scaffold that directs egg extension ( Popkova et al, 2020 ). How are polarized scaffolds formed?…”

“…Basal actomyosin periodic contractions reduce the follicle cell basal area along the dorsal-ventral (DV) direction ( He et al, 2010 ), supporting the hypothesis that basal actomyosin networks drive DV polarized tension, remodeling basal surface area. In a recent study, stress-fiber tension anisotropy, at the basal side of follicle cells, was directly probed and measured by implementing infrared (IR) femtosecond (fs) laser ablation to dissect the actomyosin cytoskeleton with subcellular precision ( Popkova et al, 2020 ). During S9, tension in the medial-basal network of follicle cells is an order of magnitude higher along the DV axis compared to the AP axis.…”

“…How are forces transmitted between follicle cells to establish tissue scale contractile tension? Supracellular F-actin bundles form across cells mediated by bi-directionally polarized filopodia ( Popkova et al, 2020 ; Figure 2C ). These long cell extensions, eventually culminating with E-cadherin based junctions, reciprocally interdigitate penetrating the actomyosin cortices of opposing cells.…”

“…Follicle cell filopodia are tension sensitive: IR fs dissection of stress-fibers juxtaposed to filopodia induce tension release and filopodia retraction. In addition, filopodia can mediate cell-cell coupling eventually functioning as mechanical anchors bridging cell cortexes ( Popkova et al, 2020 ). Santa-Cruz Mateos et al (2020) report that F-actin protrusions increase in follicle cells neighboring integrin-mutant cells.…”