Wingless Enforces Strict Segregation

Science Signaling  12 Jan 2010:
Vol. 3, Issue 104, pp. ec17
DOI: 10.1126/scisignal.3104ec17

Differential signaling processes, like expression of the morphogen Wingless in anterior cells of the segmented Drosophila embryo and expression of the transcription factor Engrailed in the posterior cell, are important for proper cell compartmentalization during development, but precisely how such signals prevent cell mixing is not well understood. Monier et al. screened for genes whose products participate in this process by selecting mutants with altered pattern of expression of Engrailed. Along with genes encoding components of the Wnt signaling pathway, they identified genes encoding components of the actomyosin cytoskeleton. This led the authors to more closely explore the organization of myosin II (MyoII) and filamentous actin at the boundaries of segmental compartments. They found that MyoII actually formed a cable-like structure at the boundary. When Monier et al. watched movement of cells at the boundary, they observed that, when cells invaded the adjacent compartment (usually cells that had just divided), the MyoII cable stretched but then returned to its straightened resting form, apparently pushing the cell back where it belonged. The authors used chromophore-assisted laser inactivation to focus intense light from a laser on the MyoII cable in tissues from animals expressing nonmuscle MyoII regulatory light chain protein that was fused to green fluorescent protein (GFP). The intense stimulation of the chromatophore releases locally high concentrations of reactive oxygen species that inactivate target proteins within about 50 angstroms of the fusion protein. Such disruption of the MyoII cable allowed mixing of cells at the border, whereas similar targeting of a carboxy-terminal fragment of Moesin fused to GFP (which localizes to structures containing filamentous actin) did not. It remains to be determined how cells at the boundary are stimulated to form the barrier cable of MyoII, but the authors suggest that differential Wingless signaling may cause the cells to express distinct adhesion molecules, somehow leading to accumulation of actomyosin at the compartment boundary.

B. Monier, A. Pélissier-Monier, A. H. Brand, B. Sanson, An actomyosin-based barrier inhibits cell mixing at compartmental boundaries in Drosophila embryos. Nature Cell Biol. 12, 60–65 (2010). [PubMed]