An actomyosin-based barrier inhibits cell mixing at compartmental boundaries in Drosophila embryos
ABSTRACT 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.
- SourceAvailable from: Kenzo Ivanovitch
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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. "
ABSTRACT: During forebrain morphogenesis, there is extensive reorganisation of the cells destined to form the eyes, telencephalon and diencephalon. Little is known about the molecular mechanisms that regulate region-specific behaviours and that maintain the coherence of cell populations undergoing specific morphogenetic processes. In this study, we show that the activity of the Eph/Ephrin signalling pathway maintains segregation between the prospective eyes and adjacent regions of the anterior neural plate during the early stages of forebrain morphogenesis in zebrafish. Several Ephrins and Ephs are expressed in complementary domains in the prospective forebrain and combinatorial abrogation of their activity results in incomplete segregation of the eyes and telencephalon and in defective evagination of the optic vesicles. Conversely, expression of exogenous Ephs or Ephrins in regions of the prospective forebrain where they are not usually expressed changes the adhesion properties of the cells, resulting in segregation to the wrong domain without changing their regional fate. The failure of eye morphogenesis in rx3 mutants is accompanied by a loss of complementary expression of Ephs and Ephrins, suggesting that this pathway is activated downstream of the regional fate specification machinery to establish boundaries between domains undergoing different programmes of morphogenesis.Development 09/2013; 140(20). DOI:10.1242/dev.097048 · 6.27 Impact Factor
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- "Severing of a tip results in the immediate closure of the stolonal lumen and its disuse until the tip is fully reconstituted and active (unpublished observations). If adherens junctional ring contractions do drive tip pulsations, the nerves are not likely involved in these tip movements, since contraction of adherens junctional rings is driven by Ca2+–calmodulin dependent myosin light chain kinase phosphorylation of myosin II –. Rather, we suggest that the nerves found at stolon tips trigger the stolon axial muscle fiber contraction, initiating return flow to polyps. "
ABSTRACT: The muscular anatomy of the athecate hydroid Podocoryna carnea hydrorhiza is elucidated. The polyp-stolon junction is characterized by an opening, here called the chloe, in the otherwise continuous hydrorhizal perisarc. The chloe is elliptical when the polyp first arises, but takes on a more complex outline as multiple stolons anastomose to communicate with that polyp. Surrounding the polyp base are spots, here called anchors, which autofluoresce at the same wavelengths as perisarc and which, like perisarc, contain chitin as assessed by Calcofluor White, Congo Red and wheat germ agglutinin staining. Anchors remain after living tissues are digested using KOH. Collagen IV staining indicates that the mesoglea is pegged to the anchors and rhodamine phallodin staining detects cytoskeletal F-actin fibers of the basal epidermis surrounding the anchors. Longitudinal muscle fibers of the polyp broaden at the polyp base and are inserted into the mesoglea of the underlying stolon, but were neither observed to extend along the stolonal axis nor to attach to the anchors. Circular muscular fibers of the polyp extend into stolons as a dense collection of strands running along the proximal-distal axis of the stolon. These gastrodermal axial muscular fibers extend to the stolon tip. Epidermal cells at the stolon tip and the polyp bud display a regular apical latticework of F-actin staining. A similar meshwork of F-actin staining was found in the extreme basal epidermis of all stolons. Immunohistochemical staining for tubulin revealed nerves at stolon tips, but at no other hydrorhizal locations. These studies bear on the mechanisms by which the stolon tip and polyp bud pulsate, the manner in which the stolon lumen closes, and on the developmental origin of the basal epidermis of the hydrorhiza.PLoS ONE 08/2013; 8(8):e72221. DOI:10.1371/journal.pone.0072221 · 3.23 Impact Factor
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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. "
ABSTRACT: During development, mechanical forces cause changes in size, shape, number, position, and gene expression of cells. They are therefore integral to any morphogenetic processes. Force generation by actin-myosin networks and force transmission through adhesive complexes are two self-organizing phenomena driving tissue morphogenesis. Coordination and integration of forces by long-range force transmission and mechanosensing of cells within tissues produce large-scale tissue shape changes. Extrinsic mechanical forces also control tissue patterning by modulating cell fate specification and differentiation. Thus, the interplay between tissue mechanics and biochemical signaling orchestrates tissue morphogenesis and patterning in development.Cell 05/2013; 153(5):948-962. DOI:10.1016/j.cell.2013.05.008 · 33.12 Impact Factor