Multicellular Rosette Formation Links Planar Cell Polarity to Tissue Morphogenesis

Developmental Biology Program, Sloan-Kettering Institute, New York, New York 10021, USA.
Developmental Cell (Impact Factor: 9.71). 11/2006; 11(4):459-70. DOI: 10.1016/j.devcel.2006.09.007
Source: PubMed


Elongation of the body axis is accompanied by the assembly of a polarized cytoarchitecture that provides the basis for directional cell behavior. We find that planar polarity in the Drosophila embryo is established through a sequential enrichment of actin-myosin cables and adherens junction proteins in complementary surface domains. F-actin accumulation at AP interfaces represents the first break in planar symmetry and occurs independently of proper junctional protein distribution at DV interfaces. Polarized cells engage in a novel program of locally coordinated behavior to generate multicellular rosette structures that form and resolve in a directional fashion. Actin-myosin structures align across multiple cells during rosette formation, and adherens junction proteins assemble in a stepwise fashion during rosette resolution. Patterning genes essential for axis elongation selectively affect the frequency and directionality of rosette formation. We propose that the generation of higher-order rosette structures links local cell interactions to global tissue reorganization during morphogenesis.

Full-text preview

Available from:
    • "The germband will also cover the ventral surface once the presumptive mesoderm invaginates during gastrulation (Rusch and Levine, 1996). Once gastrulation begins, germband cells start intercalating between one another in a convergent extension process that lengthens the germband in the anterior–posterior direction (Irvine and Wieschaus, 1994; Blankenship et al., 2006; Lecuit and Lenne, 2007). Because the cells are confined within a semirigid vitelline membrane, this extension causes the germband to curl around the posterior end of the embryo and onto the dorsal surface, making a U-shaped tissue when viewed laterally. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Background: Heat shocks applied at the onset of gastrulation in early Drosophila embryos frequently lead to phenocopies of U-shaped mutants - having characteristic failures in the late morphogenetic processes of germband retraction and dorsal closure. The pathway from non-specific heat stress to phenocopied abnormalities is unknown. Results: Drosophila embryos subjected to 30-min, 38-°C heat shocks at gastrulation appear to recover and restart morphogenesis. Post-heat-shock development appears normal, albeit slower, until a large fraction of embryos develop amnioserosa holes (diameters > 100 µm). These holes are positively correlated with terminal U-shaped phenocopies. They initiate between amnioserosa cells and open over tens of minutes by evading normal wound healing responses. They are not caused by tissue-wide increases in mechanical stress or decreases in cell-cell adhesion, but instead appear to initiate from isolated apoptosis of amnioserosa cells. Conclusions: The pathway from heat shock to U-shaped phenocopies involves the opening of one or more large holes in the amnioserosa that compromise its structural integrity and lead to failures in morphogenetic processes that rely on amnioserosa-generated tensile forces. The proposed mechanism by which heat shock leads to hole initiation and expansion is heterochonicity - i.e., disruption of morphogenetic coordination between embryonic and extra-embryonic cell types. This article is protected by copyright. All rights reserved.
    No preview · Article · Oct 2015 · Developmental Dynamics
  • Source
    • "First, GBE does not show spatial periodicity but a great deal of spatial heterogeneity and temporal stochasticity [6] [7]. Second, a high percentage of the cells form rosettes during GBE [6], which are not considered in the current model. Finally, imposing 2D periodicity in the model would preclude tissue-scale convergentextension , as global cell movement and tissue contraction would violate the periodicity. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Germband extension during Drosophila development features the merging of cells along the dorsal-ventral (DV) axis and their separation along the anterior-posterior (AP) axis. This intercalation process involves planar cell polarity, anisotropic contractile forces along cell edges, and concerted cell deformation and movement. Although prior experiments have probed each of these factors separately, the connection among them remains unclear. This paper presents a chemo-mechanical model that integrates the three factors into a coherent framework. The model predicts the polarization of Rho-kinase, myosin and Bazooka downstream of an anisotropic Shroom distribution. In particular, myosin accumulates on cell edges along the DV axis, causing them to contract into a vertex. Subsequently, medial myosin in the cells anterior and posterior to the vertex helps to elongate it into a new edge parallel to the body axis. Thus, the tissue extends along the AP axis and narrows in the transverse direction through neighbor exchange. Model predictions of the polarity of the proteins and cell and tissue deformation are in good agreement with experimental observations.
    Full-text · Article · Sep 2015 · Physical Biology
  • Source
    • "The best-studied example of this is during Drosophila germ-band extension. Here, actomyosin contractility is polarised to the anterior– posterior (AP) cell interfaces, Fig. 3B (Bertet et al., 2004; Blankenship et al., 2006; Kasza et al., 2014; Simões et al., 2014; Zallen and apical lateral basal A B contractile forces adhesion forces Fig. 3. Apical, lateral and basal forces regulate cell shape in an epithelium. (A) The cell shape of an epithelial cell is regulated by the relative sizes of their apical, lateral and basal surfaces. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The shape of a single animal cell is determined both by its internal cytoskeleton and through physical interactions with its environment. In a tissue context, this extracellular environment is made up largely of other cells and the extracellular matrix. As a result, the shape of cells residing within an epithelium will be determined both by forces actively generated within the cells themselves and by their deformation in response to forces generated elsewhere in the tissue as they propagate through cell-cell junctions. Together these complex patterns of forces combine to drive epithelial tissue morphogenesis during both development and homeostasis. Here we review the role of both active and passive cell shape changes and mechanical feedback control in tissue morphogenesis in different systems.
    Full-text · Article · Jan 2015 · Developmental Biology
Show more