Multicellular dynamics during epithelial elongation

Developmental Biology Program, Sloan-Kettering Institute, New York, NY 10065, USA.
Seminars in Cell and Developmental Biology (Impact Factor: 6.27). 07/2008; 19(3):263-70. DOI: 10.1016/j.semcdb.2008.01.005
Source: PubMed


The reorganization of multicellular populations to produce an elongated tissue structure is a conserved mechanism for shaping the body axis and several organ systems. In the Drosophila germband epithelium, this process is accompanied by the formation of a planar polarized network of junctional and cytoskeletal proteins in response to striped patterns of gene expression. Actomyosin cables and adherens junctions are dynamically remodeled during intercalation, providing the basis for polarized cell behavior. Quantitative analysis of cell behavior in living embryos reveals unexpected cell population dynamics that include the formation of multicellular rosette structures as well as local neighbor exchange.

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    • "One example is convergent extension (CE), which features the dynamic rearrangement of neighboring cells in a tissue (Fig. 3). Germ band elongation of the Drosophila along the AP axis of the embryo is an example of a CE mechanism where an epithelial tissue undergoes cell intercalation (Fig. 3A: [19]). Epithelial cells in this tissue dynamically rearrange their neighbors over time by junction remodeling and intercalate along the dorsal–ventral (DV) axis. "
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    ABSTRACT: Cell movement and local intercellular signaling are crucial components of morphogenesis during animal development. Intercellular signaling regulates the collective movement of a cell population via direct cell-cell contact. Cell movement, conversely, can influence local intercellular signaling by rearranging neighboring cells. Here, we first discuss theoretical models that address how intercellular signaling regulates collective cell movement during development. Examples include neural crest cell migration, convergent extension, and cell movement during vertebrate axis elongation. Second, we review theoretical studies on how cell movement may affect intercellular signaling, using the segmentation clock in zebrafish as an example. We propose that interplay between cell movement and intercellular signaling must be considered when studying morphogenesis in embryonic development.
    Seminars in Cell and Developmental Biology 05/2014; 35. DOI:10.1016/j.semcdb.2014.05.011 · 6.27 Impact Factor
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    • "However, unlike rosettes, tracheal pyramidal arrays include 'unequal' cells, namely tip and trailing cells; this is a crucial difference because tracheal cell rearrangement is precisely coupled to tip cell behaviour. In the Drosophila germ band, rosettes of similar cells act in rearranging cell clusters from being elongated along the embryonic dorsoventral axis to being elongated along the anteroposterior axis, without a significant difference in the type of cell cluster organisation (Zallen and Blankenship, 2008). Conversely, LTp/GB pyramids harbouring tip and trailing cells evolve into a new organisation of the cell cluster with increased anisotropy. "
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    ABSTRACT: The role of tip and rear cells in collective migration is still a matter of debate and their differences at the cytoskeletal level are poorly understood. Here, we analysed these issues in the Drosophila trachea, an organ that develops from the collective migration of clusters of cells that respond to Branchless (Bnl), a FGF homologue expressed in surrounding tissues. We track individual cells in the migratory cluster and characterize their features and unveil two prototypical types of cytoskeletal organization that account for tip and rear cells respectively. Indeed, once the former are specified, they remain as such throughout migration. Furthermore, we show that FGF signalling in a single tip cell can trigger the migration of the cells in the branch. Finally, we found specific Rac activation at the tip cells and analysed how FGF-independent cell features such as adhesion and motility act on coupling the behaviour of trailing and tip cells. Thus, the combined effect of FGF promoting leading cell behaviour and the modulation of cell properties in a cluster can account for the wide range of migratory events driven by FGF.
    Journal of Cell Science 11/2013; 127(2). DOI:10.1242/jcs.142737 · 5.43 Impact Factor
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    • "Rosette formation has been best described in the Drosophila embryo during axis elongation [52]. In this process, multicellular rosette structures are formed by intercalating populations, in which five or more cells meet at a single point [53]. "
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    ABSTRACT: Background Gastrulation is a key transition in embryogenesis; it requires self-organized cellular coordination, which has to be both robust to allow efficient development and plastic to provide adaptability. Despite the conservation of gastrulation as a key event in Metazoan embryogenesis, the morphogenetic mechanisms of self-organization (how global order or coordination can arise from local interactions) are poorly understood. Results We report a modular structure of cell internalization in Caenorhabditis elegans gastrulation that reveals mechanisms of self-organization. Cells that internalize during gastrulation show apical contractile flows, which are correlated with centripetal extensions from surrounding cells. These extensions converge to seal over the internalizing cells in the form of rosettes. This process represents a distinct mode of monolayer remodeling, with gradual extrusion of the internalizing cells and simultaneous tissue closure without an actin purse-string. We further report that this self-organizing module can adapt to severe topological alterations, providing evidence of scalability and plasticity of actomyosin-based patterning. Finally, we show that globally, the surface cell layer undergoes coplanar division to thin out and spread over the internalizing mass, which resembles epiboly. Conclusions The combination of coplanar division-based spreading and recurrent local modules for piecemeal internalization constitutes a system-level solution of gradual volume rearrangement under spatial constraint. Our results suggest that the mode of C. elegans gastrulation can be unified with the general notions of monolayer remodeling and with distinct cellular mechanisms of actomyosin-based morphogenesis.
    BMC Biology 11/2012; 10(1):94. DOI:10.1186/1741-7007-10-94 · 7.98 Impact Factor
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