An actomyosin-based barrier inhibits cell mixing at compartmental boundaries in Drosophila embryos

Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3DY, UK.
Nature Cell Biology (Impact Factor: 19.68). 12/2009; 12(1):60-5; sup pp 1-9. DOI: 10.1038/ncb2005
Source: PubMed


Partitioning tissues into compartments that do not intermix is essential for the correct morphogenesis of animal embryos and organs. Several hypotheses have been proposed to explain compartmental cell sorting, mainly differential adhesion, but also regulation of the cytoskeleton or of cell proliferation. Nevertheless, the molecular and cellular mechanisms that keep cells apart at boundaries remain unclear. Here we demonstrate, in early Drosophila melanogaster embryos, that actomyosin-based barriers stop cells from invading neighbouring compartments. Our analysis shows that cells can transiently invade neighbouring compartments, especially when they divide, but are then pushed back into their compartment of origin. Actomyosin cytoskeletal components are enriched at compartmental boundaries, forming cable-like structures when the epidermis is mitotically active. When MyoII (non-muscle myosin II) function is inhibited, including locally at the cable by chromophore-assisted laser inactivation (CALI), in live embryos, dividing cells are no longer pushed back, leading to compartmental cell mixing. We propose that local regulation of actomyosin contractibility, rather than differential adhesion, is the primary mechanism sorting cells at compartmental boundaries.

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    • "The enrichment of actomyosin cables at boundaries between domains is a feature widely found during development in a variety of tissues. Not only is it present at the interface between rhombomeres and somites, but also at compartmental boundaries in Drosophila embryos and imaginal discs (Aliee et al., 2012; Dahmann et al., 2011; Landsberg et al., 2009; Monier et al., 2010). In all these tissues, the mechanical tension exerted by activated actomyosin maintains cell compartmentalisation. "
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    • "In turn, MyoIImediated cortical tension induces further MyoII recruitment on AP junctions of adjacent cells, leading to the formation of supracellular MyoII cables that trigger simultaneous intercalations of multiple cells contributing to germ-band elongation (Blankenship et al., 2006; Fernandez-Gonzalez et al., 2009). The formation of supracellular cables is also critical for compartment boundary formation preventing cell mixing due to cell divisions close to the boundary (Landsberg et al., 2009; Monier et al., 2010; Schilling et al., 2011; Aliee et al., 2012). Although Hedgehog and Wingless signaling have been implicated in supracellular cable formation at the boundary (Butler et al., 2009; Landsberg et al., 2009; Schilling et al., 2011), it is conceivable that a mechanical feedback, in which cable contraction promotes cable formation, might also be involved. "
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