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.

14 Reads
  • Source
    • "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. "
    [Show abstract] [Hide abstract]
    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
  • Source
    • "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]. "
    [Show abstract] [Hide abstract]
    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
  • Source
    • "Hence, it is likely that Rho-dependent actomyosin contraction plays distinct roles regulating (1) concerted apical constriction and (2) subsequent resolution of the 'rosette-like' structures into elongating tubules. The formation of multicellular rosettes provides an efficient mechanism for rearrangement of cells into a single epithelial layer (Zallen and Blankenship, 2008). Similarly to other elongating epithelia, we have found multicellular 'rosette-like' structures in the pancreatic epithelium at the time at which epithelial remodelling starts, suggesting that rosette arrangements might contribute to the transition from stratified to monolayered epithelium in the pancreas too. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The development of functional organ architecture relies on coordinated morphogenesis and growth. In the developing pancreas, the branching epithelium is organised in discrete domains, delineating one specific domain of progenitor cells at the tip of the branches. The molecular mechanisms underlying the coordinated action of branching and proliferation in organ formation are largely unknown. Here, we identify the RhoGAP protein Stard13 as an essential regulator of pancreas tissue architecture in the mammalian embryo. Conditional ablation of Stard13 expression in the pancreas disrupts epithelial morphogenesis and tip-domain organisation, resulting in hampered proliferation of tip progenitors and subsequent organ hypoplasia. Stard13 acts by regulating Rho signalling spatially and temporally during pancreas development. Our findings provide new insights into the mechanisms that shape pancreatic epithelium to create a mature organ and establish a functional link between Rho-mediated control of epithelial remodelling and organ size determination, involving reciprocal interaction of actin-MAL/SRF and MAPK signalling pathways.
    Development 11/2012; 140(1). DOI:10.1242/dev.082701 · 6.46 Impact Factor
Show more


14 Reads
Available from