Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation

Gong, Yandong; Mo, Chunhui; Fraser, Scott E.

doi:10.1038/nature02796

Cited by 385 publications

(319 citation statements)

References 31 publications

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“…The observation that noncanonical Wnt signaling is dispensable during early and midgastrulation is consistent with the previous observation that slow dorsal migration of lateral mesoderm is normal in tri mutants and in tri mutants injected with MO against the tri gene (Jessen et al, 2002). At the same stage, axial mesoderm requires Wnt11 function for normal extension and dorsal regions use noncanonical Wnt signaling to organize planes of cell division (Gong et al, 2004).…”

Section: Many Cell Behaviors Contribute To Convergence and Extension supporting

confidence: 91%

“…Embryonic morphology has been the primary assay, although study of the cellular bases of these defects have been initiated. For example, Wnt signaling controls cell elongation and orientation (Topczewski et al, 2001;Jessen et al, 2002;Kilian et al, 2003), orientation of cell division planes, (Gong et al, 2004), formation of and stability of cellular protrusions (Wallingford et al, 2000;Ulrich et al, 2003), and speed of cell movement (Topczewski et al, 2001;Jessen et al, 2002;Marlow et al, 2002). Additional pathways that influence C&E movements have been identified.…”

Section: Introductionmentioning

confidence: 99%

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Initiation of convergence and extension movements of lateral mesoderm during zebrafish gastrulation

Sepich

Calmelet

Kiskowski

et al. 2005

Developmental Dynamics

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Embryonic morphogenesis is accomplished by cellular movements, rearrangements, and cell fate inductions. Vertebrate gastrulation entails morphogenetic processes that generate three germ layers, endoderm, mesoderm, and ectoderm, shaped into head, trunk, and tail. To understand how cell migration mechanistically contributes to tissue shaping during gastrulation, we examined migration of lateral mesoderm in the zebrafish. Our results illustrate that cell behaviors, different from mediolaterally oriented cell intercalation, also promote convergence and extension (C&E). During early gastrulation, upon internalization, individually migrating mesendodermal cells contribute to the elongation of the mesoderm by moving animally, without dorsal movement. Convergence toward dorsal starts later, by 70% epiboly (7.7 hpf). Depending on location along the Animal-Vegetal axis, an animal or vegetal bias is added to the dorsalward movement, so that paths fan out and the lateral mesoderm both converges and extends. Onset of convergence is independent of noncanonical Wnt signaling but is delayed when Stat3 signaling is compromised. To understand which aspects of motility are controlled by guidance cues, we measured turning behavior of lateral mesodermal cells. We show that cells exhibit directional preference, directionally-regulated speed, and turn toward dorsal when off-course. We estimate that ectoderm could supply from a fraction to all the dorsalward displacement seen in mesoderm cells. Using mathematical modeling, we demonstrate that directional preference is sufficient to account for mesoderm convergence and extension, and that, at minimum, two sources of guidance cues could orient cell paths realistically if located in the dorsal midline. Developmental Dynamics 234:279 -292, 2005.

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Section: Many Cell Behaviors Contribute To Convergence and Extension supporting

confidence: 91%

Section: Introductionmentioning

confidence: 99%

Initiation of convergence and extension movements of lateral mesoderm during zebrafish gastrulation

Sepich

Calmelet

Kiskowski

et al. 2005

Developmental Dynamics

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“…A number of biological studies have suggested that the long axes of cells (Jacobson and Gordon 1976) are key determinants of mitosis orientation (O'Connell and Wang 2000). Other relevant factors may include cell signalling, biochemical factors, mechanical stresses and tissue deformation (Brodland and Veldhuis 2002;Gong et al 2004;Nelson et al 2005). In turn, regularly oriented mitosis, regardless of its origin, has been implicated as a significant driver of tissue motions (Philip et al 1992;Brodland and Veldhuis 2002;Gong et al 2004).…”

Section: Results and Conclusionmentioning

confidence: 99%

Detection of mitoses in embryonic epithelia using motion field analysis

Siva¹,

Brodland²,

Clausi³

2009

Computer Methods in Biomechanics and Biomedical Engineering

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Although computer simulations indicate that mitosis may be important to the mechanics of morphogenetic movements, algorithms to identify mitoses in bright field images of embryonic epithelia have not previously been available. Here, the authors present an algorithm that identifies mitoses and their orientations based on the motion field between successive images. Within this motion field, the algorithm seeks 'mitosis motion field prototypes' characterised by convergent motion in one direction and divergent motion in the orthogonal direction, the local motions produced by the division process. The algorithm uses image processing, vector field analyses and pattern recognition to identify occurrences of this prototype and to determine its orientation. When applied to time-lapse images of gastrulation and neurulation-stage amphibian (Ambystoma mexicanum) embryos, the algorithm achieves identification accuracies of 68 and 67%, respectively and angular accuracies of the order of 308, values sufficient to assess the role of mitosis in these developmental processes.

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“…In contrast, nls-tagged markers (both GFP-and lacZ-based) and native fluorescent proteins become dispersed throughout the cell during mitosis, so that tracking of that cell becomes much more difficult (discussed in more detail by Hadjantonakis and Papaioannou, 2004). GFP fusions to histones have been used to label nuclei in live transgenic or retrovirally transduced zebrafish, flies, and quail (Das et al, 2003;Gong et al, 2004;Koster and Fraser, 2001;LaRue et al, 2003;Savoian and Rieder, 2002). Recently, we described a constitutively expressed fusion cDNA encoding a human histone H2B tagged with a C-terminal GFP that permits imaging and cell tracking at nuclear resolution in vivo in mouse embryos (Hadjantonakis and Papaioannou, 2004).…”

Section: Introductionmentioning

confidence: 99%

Using a histone yellow fluorescent protein fusion for tagging and tracking endothelial cells in ES cells and mice

Fraser

Hadjantonakis

Sahr

et al. 2005

genesis

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SummaryWe report the first endothelial lineage-specific transgenic mouse allowing live imaging at subcellular resolution. We generated an H2B-EYFP fusion protein which can be used for fluorescent labeling of nucleosomes and used it to specifically label endothelial cells in mice and in differentiating embryonic stem (ES) cells. A fusion cDNA encoding a human histone H2B tagged at its C-terminus with enhanced yellow fluorescent protein (EYFP) was expressed under the control of an Flk1 promoter and intronic enhancer. The Flk1::H2B-EYFP transgenic mice are viable and high levels of chromatin-localized reporter expression are maintained in endothelial cells of developing embryos and in adult animals upon breeding. The onset of fluorescence in differentiating ES cells and in embryos corresponds with the beginning of endothelial cell specification. These transgenic lines permit real-time imaging in normal and pathological vasculogenesis and angiogenesis to track individual cells and mitotic events at a level of detail that is unprecedented in the mouse.

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Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation

Cited by 385 publications

References 31 publications

Initiation of convergence and extension movements of lateral mesoderm during zebrafish gastrulation

Initiation of convergence and extension movements of lateral mesoderm during zebrafish gastrulation

Detection of mitoses in embryonic epithelia using motion field analysis

Using a histone yellow fluorescent protein fusion for tagging and tracking endothelial cells in ES cells and mice

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