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.

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    • "In Drosophila, apically positioned contractile networks of actomyosin generate forces that are critical for germ band extension, ventral and dorsal closure, and various invaginations (Costa et al., 1994; Winter et al., 2001; Bertet et al., 2004; Nikolaidou and Barrett, 2004; Zallen and Wieschaus, 2004; Dawes-Hoang et al., 2005; Franke et al., 2005; Blankenship et al., 2006; Simões et al., 2006; Corrigall et al., 2007; Kolesnikov and Beckendorf, 2007; Mulinari et al., 2008; Xu et al., 2008). Our lab has shown that Drosophila Shroom, like Shroom3, binds to Rock and F-actin and induces robust apical constriction (Bolinger et al., 2010). "
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    ABSTRACT: Shroom3 is an actin-associated regulator of cell morphology that is required for neural tube closure, formation of the lens placode, and gut morphogenesis in mice and has been linked to chronic kidney disease and directional heart looping in humans. Numerous studies have shown that Shroom3 likely regulates these developmental processes by directly binding to Rho-kinase and facilitating the assembly of apically positioned contractile actomyosin networks. We have characterized the molecular basis for the neural tube defects caused by an ENU-induced mutation that results in an arginine-to-cysteine amino acid substitution at position 1838 of mouse Shroom3. We show that this substitution has no effect on Shroom3 expression or localization but ablates Rock binding and renders Shroom3 non-functional for the ability to regulate cell morphology. Our results indicate that Rock is the major downstream effector of Shroom3 in the process of neural tube morphogenesis. Based on sequence conservation and biochemical analysis, we predict that the Shroom-Rock interaction is highly conserved across animal evolution and represents a signaling module that is utilized in a variety of biological processes.
    Biology Open 08/2014; 3(9). DOI:10.1242/bio.20147450 · 2.42 Impact Factor
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    • "During Drosophila embryogenesis, a series of cellular rearrangements promote the doubling of body length and the formation of an elongated body axis (Bertet et al., 2004; Blankenship et al., 2006; Irvine and Wieschaus, 1994), and live-imaging studies have shown that these rearrangements include the formation and resolution of rosettes (Blankenship et al., 2006). Similar to rosette formation during zebrafish NM development, this process is myosin-II dependent. "
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    ABSTRACT: Multicellular rosettes have recently been appreciated as important cellular intermediates that are observed during the formation of diverse organ systems. These rosettes are polarized, transient epithelial structures that sometimes recapitulate the form of the adult organ. Rosette formation has been studied in various developmental contexts, such as in the zebrafish lateral line primordium, the vertebrate pancreas, the Drosophila epithelium and retina, as well as in the adult neural stem cell niche. These studies have revealed that the cytoskeletal rearrangements responsible for rosette formation appear to be conserved. By contrast, the extracellular cues that trigger these rearrangements in vivo are less well understood and are more diverse. Here, we review recent studies of the genetic regulation and cellular transitions involved in rosette formation. We discuss and compare specific models for rosette formation and highlight outstanding questions in the field.
    Development 07/2014; 141(13):2549-2558. DOI:10.1242/dev.101444 · 6.46 Impact Factor
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    • "The xit genomic transgene was inserted into the 86Fb region (ZH102D) by phiC31 mediated transgenesis (Bishof 2007). The following mutations and transgenes were used wol[2], gny[f04215] (Haecker et al., 2008, Shaik et al., 2011), ubiquitin-E-CadherinGFP (Oda and Tsukita, 2001), 117GFP (resille, GFP exon trap in CG8668) (Blankenship et al., 2006) and Reticulon-GFP (Retl1-GFP, Morin et al., 2001). Stocks were obtained from the Bloomington stock center, if not otherwise noted. "
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    ABSTRACT: The majority of membrane and secreted proteins, including many developmentally important signalling proteins, receptors and adhesion molecules, are cotranslationally N-glycosylated in the endoplasmic reticulum. The structure of the N-glycan is invariant for all substrates and conserved in eukaryotes. Correspondingly, the enzymes are conserved, which successively assemble the glycan precursor from activated monosaccharides prior to transfer to nascent proteins. Despite the well-defined biochemistry, the physiological and developmental role of N-glycosylation and of the responsible enzymes has not been much investigated in metazoa. We identified a mutation in the Drosophila gene, xiantuan (xit, CG4542), which encodes one of the conserved enzymes involved in addition of the terminal glucose residues to the glycan precursor. xit is required for timely apical constriction of mesoderm precursor cells and ventral furrow formation in early embryogenesis. Furthermore, cell intercalation in the lateral epidermis during germband extension is impaired in xit mutants. xit affects glycosylation and intracellular distribution of E-Cadherin, albeit not the total amount of E-Cadherin protein. As depletion of E-Cadherin by RNAi induces a similar cell intercalation defect, E-Cadherin may be the major xit target that is functionally relevant for germband extension.
    Developmental Biology 06/2014; 390(2). DOI:10.1016/j.ydbio.2014.03.007 · 3.55 Impact Factor
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