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Establishment of the Dorsal–Ventral Axis inXenopus Embryos Coincides with the Dorsal Enrichment of Dishevelled That Is Dependent on Cortical Rotation

Journal Article · · Journal of Cell Biology
 [1];  [2];  [3];  [4];  [4];  [4]
  1. Univ. of Washington, Seattle, WA (United States). Howard Hughes Medical Inst. Center for Developmental Biology. Dept. of Pharmacology; DOE/OSTI
  2. Univ. of Washington, Seattle, WA (United States). Howard Hughes Medical Inst. Center for Developmental Biology. Dept. of Pharmacology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Univ. of Washington, Seattle, WA (United States). Howard Hughes Medical Inst. Center for Developmental Biology. Dept. of Pharmacology
Examination of the subcellular localization of Dishevelled (Dsh) in fertilized Xenopus eggs revealed that Dsh is associated with vesicle-like organelles that are enriched on the prospective dorsal side of the embryo after cortical rotation. Dorsal enrichment of Dsh is blocked by UV irradiation of the vegetal pole, a treatment that inhibits development of dorsal cell fates, linking accumulation of Dsh and specification of dorsal cell fates. Investigation of the dynamics of Dsh localization using Dsh tagged with green fluorescent protein (Dsh-GFP) demonstrated that Dsh-GFP associates with small vesicle-like organelles that are directionally transported along the parallel array of microtubules towards the prospective dorsal side of the embryo during cortical rotation. Perturbing the assembly of the microtubule array with D2O, a treatment that promotes the random assembly of the array and the dorsalization of embryos, randomizes translocation of Dsh-GFP. Conversely, UV irradiation of the vegetal pole abolishes movement of Dsh-GFP. Finally, we demonstrate that overexpression of Dsh can stabilize β-catenin in Xenopus. These data suggest that the directional translocation of Dsh along microtubules during cortical rotation and its subsequent enrichment on the prospective dorsal side of the embryo play a role in locally activating a maternal Wnt pathway responsible for establishing dorsal cell fates in Xenopus.
Research Organization:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
Sponsoring Organization:
National Institutes of Health (NIH); USDOD; USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1625112
Journal Information:
Journal of Cell Biology, Journal Name: Journal of Cell Biology Journal Issue: 2 Vol. 146; ISSN 0021-9525
Publisher:
Rockefeller University PressCopyright Statement
Country of Publication:
United States
Language:
English

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Subcellular localization and signaling properties of dishevelled in developing vertebrate embryos journal July 2006
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Zebrafish Naked1 and Naked2 antagonize both canonical and non-canonical Wnt signaling journal September 2007
Asymmetric developmental potential along the animal–vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled journal October 2007
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Single blastomere expression profiling of Xenopus laevis embryos of 8 to 32-cells reveals developmental asymmetry journal July 2013
Interaction among Gsk-3, Gbp, Axin, and APC in Xenopus Axis Specification journal February 2000
Colocalization and Redistribution of Dishevelled and Actin during WNT-Induced Mesenchymal Morphogenesis journal June 2000
Asymmetric p38 Activation in Zebrafish journal September 2000
Apical Membrane Localization of the Adenomatous Polyposis Coli Tumor Suppressor Protein and Subcellular Distribution of the β-Catenin Destruction Complex in Polarized Epithelial Cells journal January 2001
PI4K2β constrains non-canonical Wnt-PCP signalling and is localised by PAR-1 (MARK2/3) phosphorylation preprint June 2019
PR72, a novel regulator of Wnt signaling required for Naked cuticle function journal January 2005
Cancer as an Embryological Phenomenon and Its Developmental Pathways: A Hypothesis regarding the Contribution of the Noncanonical Wnt Pathway journal March 2019
Shroom3 functions downstream of planar cell polarity to regulate myosin II distribution and cellular organization during neural tube closure journal January 2015
β-Catenin/Tcf-regulated transcription prior to the midblastula transition journal December 2002
Two Oppositely Localised Frizzled RNAs as Axis Determinants in a Cnidarian Embryo journal March 2007
Hecate/Grip2a Acts to Reorganize the Cytoskeleton in the Symmetry-Breaking Event of Embryonic Axis Induction journal June 2014
Modulation of the β-Catenin Signaling Pathway by the Dishevelled-Associated Protein Hipk1 journal February 2009
Intracellular Spatial Localization Regulated by the Microtubule Network journal April 2012
The role of the histone variant H2A.Z in early Xenopus laevis development other January 2007
SEC14 and Spectrin Domains 1 (Sestd1), Dishevelled 2 (Dvl2) and Dapper Antagonist of Catenin-1 (Dact1) co-regulate the Wnt/Planar Cell Polarity (PCP) pathway during mammalian development journal November 2013
Asymmetric Localization of Ck2α During Xenopus Oogenesis journal January 2013
Identifizierung spezifischer Eigenschaften individueller LEF/TCF-Transkriptionsfaktoren in der Neuralentwicklung von Xenopus laevis text January 2008
Reorganization of Vegetal Cortex Microtubules and Its Role in Axis Induction in the Early Vertebrate Embryo book May 2017
Promoter methylation of the secreted frizzled-related protein 1 geneSFRP1 is frequent in hepatocellular carcinoma journal January 2006
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XIdax, an inhibitor of the canonical Wnt pathway, is required for anterior neural structure formation inXenopus journal January 2004
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