Dataset Information

Actomyosin contractility and Discs large contribute to junctional conversion in guiding cell alignment within the Drosophila embryonic epithelium.

ABSTRACT: Proper control of epithelial morphogenesis is vital to development and is often disrupted in disease. After germ band extension, the cells of the Drosophila ventral embryonic epidermis are packed in a two-dimensional polygonal array. Although epithelial cell rearrangements are being studied productively in several tissues, the ventral epidermis is of particular interest as the final cell arrangement is, uniquely, far from equilibrium. We show that over the course of several hours, a subset of cells within each parasegment adopts a rectilinear configuration and aligns into parallel columns. Live imaging shows that this is accomplished by the shrinkage of select cell interfaces, as three-cell junctions are converted to four-cell junctions. Additionally, we show that non-muscle Myosin II and the polarity proteins Discs large (Dlg) and Bazooka are enriched along cell interfaces in a complex but reproducible pattern that suggests their involvement in junctional conversion and cell alignment. Indeed, depletion of Myosin II or dlg disrupts these processes. These results show that tight spatial regulation of actomyosin contractility is required to produce this high-energy arrangement of cells.

SUBMITTER: Simone RP

PROVIDER: S-EPMC2847470 | biostudies-literature | 2010 Apr

REPOSITORIES: biostudies-literature

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Actomyosin contractility and Discs large contribute to junctional conversion in guiding cell alignment within the Drosophila embryonic epithelium.

Simone Robert P RP DiNardo Stephen S

Development (Cambridge, England) 20100401 8

Proper control of epithelial morphogenesis is vital to development and is often disrupted in disease. After germ band extension, the cells of the Drosophila ventral embryonic epidermis are packed in a two-dimensional polygonal array. Although epithelial cell rearrangements are being studied productively in several tissues, the ventral epidermis is of particular interest as the final cell arrangement is, uniquely, far from equilibrium. We show that over the course of several hours, a subset of ce ...[more]

PMID: 20332153

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Project description:BackgroundNotch-Delta signaling functions across a wide array of animal systems to break symmetry in a sheet of undifferentiated cells and generate cells with different fates, a process known as lateral inhibition. Unlike many other signaling systems, however, since both the ligand and receptor are transmembrane proteins, the activation of Notch by Delta depends strictly on cell-cell contact. Furthermore, the binding of the ligand to the receptor may not be sufficient to induce signaling, since recent work in cell culture suggests that ligand-induced Notch signaling also requires a mechanical pulling force. This tension exposes a cleavage site in Notch that, when cut, activates signaling. Although it is not known if mechanical tension contributes to signaling in vivo, others have suggested that this is how endocytosis of the receptor-ligand complex contributes to the cleavage and activation of Notch. In a similar way, since Notch-mediated lateral inhibition at a distance in the dorsal thorax of the pupal fly is mediated via actin-rich protrusions, it is possible that cytoskeletal forces generated by networks of filamentous actin and non-muscle myosin during cycles of protrusion extension and retraction also contribute to Notch signaling.ResultsTo test this hypothesis, we carried out a detailed analysis of the role of myosin II-dependent tension in Notch signaling in the developing fly and in cell culture. Using dynamic fluorescence-based reporters of Notch, we found that myosin II is important for signaling in signal sending and receiving cells in both systems-as expected if myosin II-dependent tension across the Notch-Delta complex contributes to Notch activation. While myosin II was found to contribute most to signaling at a distance, it was also required for maximal signaling between adjacent cells that share lateral contacts and for signaling between cells in culture.ConclusionsTogether these results reveal a previously unappreciated role for non-muscle myosin II contractility in Notch signaling, providing further support for the idea that force contributes to the cleavage and activation of Notch in the context of ligand-dependent signaling, and a new paradigm for actomyosin-based mechanosensation.

Dataset Information

Actomyosin contractility and Discs large contribute to junctional conversion in guiding cell alignment within the Drosophila embryonic epithelium.

Publications

Actomyosin contractility and Discs large contribute to junctional conversion in guiding cell alignment within the Drosophila embryonic epithelium.

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