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Regional requirements for Dishevelled signaling during Xenopus gastrulation: separable effects on blastopore closure, mesendoderm internalization and archenteron formation

Ewald, Andrew J. and Peyrot, Sara M. and Tyszka, J. Michael and Fraser, Scott E. and Wallingford, John B. (2004) Regional requirements for Dishevelled signaling during Xenopus gastrulation: separable effects on blastopore closure, mesendoderm internalization and archenteron formation. Development, 131 (24). pp. 6195-6209. ISSN 0950-1991. http://resolver.caltech.edu/CaltechAUTHORS:EWAdev04

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[img] Video (QuickTime) (Movie 1. A three-dimensional dataset of a late gastrula frog embryo, presented from several perspectives.) - Supplemental Material
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[img] Video (QuickTime) (Movie 2. A movie of normal frog gastrulation, viewed from the vegetal side. Note the coordinate inward movement of yolk plug and surface cells, with simultaneous blastopore closure.) - Supplemental Material
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[img] Video (QuickTime) (Movie 3. Gastrulation in an embryo circumferentially injected with Xdd1. Note the inward movement of yolk plug and surface cells without significant blastopore closure) - Supplemental Material
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[img] Video (QuickTime) (Movie 4. Normal blastopore closure in a control embryo) - Supplemental Material
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[img] Video (QuickTime) (Movie 5. Impaired blastopore closure in an embryo injected ventrally with Xdd1) - Supplemental Material
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[img] Video (QuickTime) (Movie 6. Severely impaired blastopore closure in an embryo dorsally injected with Xdd1) - Supplemental Material
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[img] Video (QuickTime) (Movie 7. Severely impaired blastopore closure in an embryo circumferentially injected with Xdd1) - Supplemental Material
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[img] Video (QuickTime) (Movie 8. A three dimensional dataset of a late gastrula frog embryo, depicting the surface of the embryo in yellow, and the internal cavities in pink) - Supplemental Material
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Abstract

During amphibian gastrulation, the embryo is transformed by the combined actions of several different tissues. Paradoxically, many of these morphogenetic processes can occur autonomously in tissue explants, yet the tissues in intact embryos must interact and be coordinated with one another in order to accomplish the major goals of gastrulation: closure of the blastopore to bring the endoderm and mesoderm fully inside the ectoderm, and generation of the archenteron. Here, we present high-resolution 3D digital datasets of frog gastrulae, and morphometrics that allow simultaneous assessment of the progress of convergent extension, blastopore closure and archenteron formation in a single embryo. To examine how the diverse morphogenetic engines work together to accomplish gastrulation, we combined these tools with time-lapse analysis of gastrulation, and examined both wild-type embryos and embryos in which gastrulation was disrupted by the manipulation of Dishevelled (Xdsh) signaling. Remarkably, although inhibition of Xdsh signaling disrupted both convergent extension and blastopore closure, mesendoderm internalization proceeded very effectively in these embryos. In addition, much of archenteron elongation was found to be independent of Xdsh signaling, especially during the second half of gastrulation. Finally, even in normal embryos, we found a surprising degree of dissociability between the various morphogenetic processes that occur during gastrulation. Together, these data highlight the central role of PCP signaling in governing distinct events of Xenopus gastrulation, and suggest that the loose relationship between morphogenetic processes may have facilitated the evolution of the wide variety of gastrulation mechanisms seen in different amphibian species.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1242/dev.01542DOIUNSPECIFIED
http://dev.biologists.org/cgi/content/abstract/131/24/6195PublisherUNSPECIFIED
Additional Information:Published by The Company of Biologists 2004. Accepted 21 October 2004. First published online 17 November 2004. We thank R. Harland, D. Parichy, D. Koos, C. Papan and S. Haigo for useful conversations and technical assistance. We thank Resolution Sciences Corporation (now Microscience Group) for instrument time; and R. Kerschmann, M. Reddington, L. Garrett, P. Guthrie, M. Bolles, M. Haugh and B. Herrera for technical assistance with SIM. A.J.E. thanks Z. Werb for space and support during the writing of this manuscript. This work was supported by funding from the Burroughs Wellcome Fund Interfaces Program via the Caltech Initiative in Computational Molecular Biology to A.J.E.; by an NIH R01 grant to Richard M. Harland; an NIH NICHD grant to S.E.F.; and by a Career Award in the Biomedical Sciences from the Burroughs Wellcome Fund to J.B.W. Supplementary material for this article is available at http://dev.biologists.org/cgi/content/full/131/24/6195/DC1.
Funders:
Funding AgencyGrant Number
Burroughs Wellcome FundUNSPECIFIED
Caltech Initiative in Computational Molecular BiologyUNSPECIFIED
National Institutes of HealthUNSPECIFIED
National Institute of Child Health and Human DevelopmentUNSPECIFIED
Subject Keywords:Gastrulation, Dishevelled, Morphogenesis, Xenopus
Record Number:CaltechAUTHORS:EWAdev04
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:EWAdev04
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:12090
Collection:CaltechAUTHORS
Deposited By: Archive Administrator
Deposited On:22 Oct 2008 21:41
Last Modified:26 Dec 2012 10:26

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