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WIREs Dev Biol
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Specification of anteroposterior axis by combinatorial signaling during Xenopus development

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The specification of anteroposterior (AP) axis is a fundamental and complex patterning process that sets up the embryonic polarity and shapes a multicellular organism. This process involves the integration of distinct signaling pathways to coordinate temporal–spatial gene expression and morphogenetic movements. In the frog Xenopus, extensive embryological and molecular studies have provided major advance in understanding the mechanism implicated in AP patterning. Following fertilization, cortical rotation leads to the transport of maternal determinants to the dorsal region and creates the primary dorsoventral (DV) asymmetry. The activation of maternal Wnt/ß‐catenin signaling and a high Nodal signal induces the formation of the Nieuwkoop center in the dorsal‐vegetal cells, which then triggers the formation of the Spemann organizer in the overlying dorsal marginal zone. It is now well established that the Spemann organizer plays a central role in building the vertebrate body axes because it provides patterning information for both DV and AP polarities. The antagonistic interactions between signals secreted in the Spemann organizer and the opposite ventral region pattern the mesoderm along the DV axis, and this DV information is translated into AP positional values during gastrulation. The formation of anterior neural tissue requires simultaneous inhibition of zygotic Wnt and bone morphogenetic protein (BMP) signals, while an endogenous gradient of Wnt, fibroblast growth factors (FGFs), retinoic acid (RA) signaling, and collinearly expressed Hox genes patterns the trunk and posterior regions. Collectively, DV asymmetry is mostly coupled to AP polarity, and cell–cell interactions mediated essentially by the same regulatory networks operate in DV and AP patterning. WIREs Dev Biol 2016, 5:150–168. doi: 10.1002/wdev.217 This article is categorized under: Early Embryonic Development > Development to the Basic Body Plan
Specification of the dorsoventral (DV) axis and formation of the Spemann organizer. (a) Cortical rotation following fertilization leads to the accumulation of ß‐catenin on the dorsal side, with maternal VegT localized to the vegetal hemisphere during cleavage stages. (b) The expression of Xnr genes is induced by VegT at mid‐blastula transition. ß‐catenin also contributes to the induction of the higher levels of Xnr gene expression in the dorsal‐vegetal cells. The Nieuwkoop center (NC) results in a combined activity of Nodal and Wnt/ß‐catenin signaling. The Blastula Chordin‐ and Noggin‐Expressing (BCNE) center expresses maternal Wnt/ß‐catenin target genes along with Chordin and Noggin, and is required for brain formation. (C) The Spemann organizer is formed above the dorsal lip of blastopore at the early gastrula stage and comprises distinct cell populations including anterior endoderm (camel), prechordal mesoderm (turquoise), and chordamesoderm (dark green). These cells involute during gastrulation to underline the noninvoluting neuroectoderm (light green). An active ventral gastrula center (red) is formed on the opposite side of the Spemann organizer, which can be also represented by the entire nonorganizer mesoderm. Molecular interaction between the Spemann organizer and the ventral gastrula center patterns the mesoderm along the DV axis.
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Transcriptional derepression and embryonic axis formation. (a) A normal larval stage Xenopus embryo. (b) Formation of a secondary axis without anterior structures following DSCR6 overexpression in the ventral region (I and II refer to the primary and the induced axis, respectively). (c) Proposed model of DSCR6 function in transcriptional derepression. DSCR6 interacts directly with components within the polycomb repressive complex (PRC) 1 and 2. In the absence of DSCR6, the complexes bind chromatin and repress the transcription of mesoderm genes. The interaction between DSCR6 and BMI1 and EZH2 removes PRC1 and PRC2 from chromatin and contributes to transcriptional derepression.
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Regulatory networks involving Wnt, fibroblast growth factor (FGF), and retinoic acid (RA) in anteroposterior (AP) patterning. Xcad3 represents one of the transcriptional targets of later Wnt/ß‐catenin signaling. It also forms a regulatory loop with FGF and participates in AP patterning of the trunk and tail regions through activation of Hoxa7 and Hoxb9 expression. In hindbrain patterning, there exits a feed‐forward regulatory mechanism between Hox genes and RA synthesis. Hoxd1 is required for hindbrain patterning and may be a direct target of RA signaling, while Hoxa1 directly regulates the expression of Raldh2, which functions to increase RA concentration in the hindbrain region.
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Endogenous morphogens gradients pattern the anteroposterior (AP) axis. In the anterior region, Wnt, fibroblast growth factor (FGF), bone morphogenetic protein (BMP), and retinoic acid (RA) signaling activity is kept low due to presence of negative regulators. An appropriate RA concentration is required for hindbrain patterning, and a high concentration of Wnt, FGF, and BMP specifies the posterior region (see text for detail).
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Specification of the anteroposterior (AP) axis and neural induction by vertical and planar signals. The axial mesendoderm possesses an AP polarity characterized by the presence of anterior endoderm, prechordal mesoderm, and chordamesoderm. Wnt and bone morphogenetic protein antagonists are secreted by the anterior endoderm and prechordal mesoderm to promote brain formation. The neuroectoderm can be patterned along the AP axis through vertical induction by region‐specific signals transmitted from the axial mesendoderm (small arrows). Planar induction (thick red arrow) acting in the plane of the neuroectoderm mostly patterns the posterior region.
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Dorsoventral (DV) and anteroposterior (AP) patterning by inductive and antagonistic signals emanated by the Spemann organizer and the ventral gastrula center (red). At the early to middle gastrula stage, both the Spemann organizer and the ventral gastrula center express a panel of extracellular proteins and transcription factors. They functionally interact and form a complex regulatory network to pattern the embryonic axes. The list of genes shown here is certainly not complete. The Spemann organizer is shown by different colors to represent its heterogeneity.
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