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      The Spemann organizer meets the anterior-most neuroectoderm at the equator of early gastrulae in amphibian species

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          Abstract

          The dorsal blastopore lip (known as the Spemann organizer) is important for making the body plan in amphibian gastrulation. The organizer is believed to involute inward and migrate animally to make physical contact with the prospective head neuroectoderm at the blastocoel roof of mid- to late-gastrula. However, we found that this physical contact was already established at the equatorial region of very early gastrula in a wide variety of amphibian species. Here we propose a unified model of amphibian gastrulation movement. In the model, the organizer is present at the blastocoel roof of blastulae, moves vegetally to locate at the region that lies from the blastocoel floor to the dorsal lip at the onset of gastrulation. The organizer located at the blastocoel floor contributes to the anterior axial mesoderm including the prechordal plate, and the organizer at the dorsal lip ends up as the posterior axial mesoderm. During the early step of gastrulation, the anterior organizer moves to establish the physical contact with the prospective neuroectoderm through the “subduction and zippering” movements. Subduction makes a trench between the anterior organizer and the prospective neuroectoderm, and the tissues face each other via the trench. Zippering movement, with forming Brachet's cleft, gradually closes the gap to establish the contact between them. The contact is completed at the equator of early gastrulae and it continues throughout the gastrulation. After the contact is established, the dorsal axis is formed posteriorly, but not anteriorly. The model also implies the possibility of constructing a common model of gastrulation among chordate species.

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          Most cited references37

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          Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos.

          We have cloned a cDNA encoding a novel polypeptide capable of inducing dorsal development in Xenopus embryos. RNA transcripts from this clone rescue normal development when injected into ventralized embryos and result in excessive head development at high doses. Therefore, we have named the cDNA noggin, noggin cDNA contains a single reading frame encoding a 26 kd protein with a hydrophobic amino-terminal sequence, suggesting that it is secreted. In Northern blot analysis this cDNA hybridizes to two mRNAs that are expressed both maternally and zygotically. Although noggin transcript is not localized in the oocyte and cleavage stage embryo, zygotic transcripts are initially restricted to the presumptive dorsal mesoderm and reach their highest levels at the gastrula stage in the dorsal lip of the blastopore (Spemann organizer). In the neurula, noggin is transcribed in the notochord and prechordal mesoderm. The activity of exogenous noggin RNA in embryonic axis induction and the localized expression of endogenous noggin transcripts suggest that noggin plays a role in normal dorsal development.
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            Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes.

            Y Sasai (1994)
            A Xenopus gene whose expression can be activated by the organizer-specific homeobox genes goosecoid and Xnot2 was isolated by differential screening. The chordin gene encodes a novel protein of 941 amino acids that has a signal sequence and four Cys-rich domains. The expression of chordin starts in Spemann's organizer subsequent to that of goosecoid, and its induction by activin requires de novo protein synthesis. Microinjection of chordin mRNA induces twinned axes and can completely rescue axial development in ventralized embryos. This molecule is a potent dorsalizing factor that is expressed at the right time and in the right place to regulate cell-cell interactions in the organizing centers of head, trunk, and tail development.
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              Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer.

              An abundant cDNA enriched in Spemann's organizer, cerberus, was isolated by differential screening. It encodes a secreted protein that is expressed in the anterior endomesoderm. Microinjection of cerberus mRNA into Xenopus embryos induces ectopic heads, and duplicated hearts and livers. The results suggest a role for a molecule expressed in the anterior endoderm in the induction of head structures in the vertebrate embryo.
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                Author and article information

                Journal
                Dev Growth Differ
                Dev. Growth Differ
                dgd
                Development, Growth & Differentiation
                BlackWell Publishing Ltd (Oxford, UK )
                0012-1592
                1440-169X
                April 2015
                10 March 2015
                : 57
                : 3
                : 218-231
                Affiliations
                [1 ]JT Biohistory Research Hall 1-1 Murasaki-cho, Takatsuki, Osaka, 569-1125, Japan
                [2 ]Department of Biological Sciences, Graduate School of Science, Osaka University Toyonaka, Osaka, 560-0043, Japan
                [3 ]Institute for Amphibian Biology, Hiroshima University Kagamiyama, Higashi-Hiroshima, Hiroshima, 739-8526, Japan
                Author notes
                * Author to whom all correspondence should be addressed. Email: hashimoto@ 123456brh.co.jp
                [†]

                These authors contributed equally to this work.

                Article
                10.1111/dgd.12200
                4402005
                25754292
                80c0be25-97f0-493a-a070-705a25baaa69
                © 2015 The Authors Development, Growth & Differentiation published by Wiley Publishing Asia Pty Ltd on behalf of Japanese Society of Developmental Biologists.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 20 November 2014
                : 08 January 2015
                : 20 January 2015
                Categories
                Original Articles

                Developmental biology
                amphibian,chordate,gastrulation,movement,spemann organizer
                Developmental biology
                amphibian, chordate, gastrulation, movement, spemann organizer

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