XB-ART-55820
EMBO Rep
2019 Jun 01;206:. doi: 10.15252/embr.201845842.
Show Gene links
Show Anatomy links
New roles for Wnt and BMP signaling in neural anteroposterior patterning.
Polevoy H
,
Gutkovich YE
,
Michaelov A
,
Volovik Y
,
Elkouby YM
,
Frank D
.
???displayArticle.abstract???
During amphibian development, neural patterning occurs via a two-step process. Spemann's organizer secretes BMP antagonists that induce anterior neural tissue. A subsequent caudalizing step re-specifies anterior fated cells to posterior fates such as hindbrain and spinal cord. The neural patterning paradigm suggests that a canonical Wnt-signaling gradient acts along the anteroposterior axis to pattern the nervous system. Wnt activity is highest in the posterior, inducing spinal cord, at intermediate levels in the trunk, inducing hindbrain, and is lowest in anterior fated forebrain, while BMP-antagonist levels are constant along the axis. Our results in Xenopus laevis challenge this paradigm. We find that inhibition of canonical Wnt signaling or its downstream transcription factors eliminates hindbrain, but not spinal cord fates, an observation not compatible with a simple high-to-low Wnt gradient specifying all fates along the neural anteroposterior axis. Additionally, we find that BMP activity promotes posterior spinal cord cell fate formation in an FGF-dependent manner, while inhibiting hindbrain fates. These results suggest a need to re-evaluate the paradigms of neural anteroposterior pattern formation during vertebrate development.
???displayArticle.pubmedLink??? 30936121
???displayArticle.pmcLink??? PMC6549026
???displayArticle.link??? EMBO Rep
References [+] :
Aamar,
Xenopus Meis3 protein forms a hindbrain-inducing center by activating FGF/MAP kinase and PCP pathways.
2004, Pubmed,
Xenbase
Aamar, Xenopus Meis3 protein forms a hindbrain-inducing center by activating FGF/MAP kinase and PCP pathways. 2004, Pubmed , Xenbase
Anderson, An FGF3-BMP Signaling Axis Regulates Caudal Neural Tube Closure, Neural Crest Specification and Anterior-Posterior Axis Extension. 2016, Pubmed
Bae, Identification of Pax3 and Zic1 targets in the developing neural crest. 2014, Pubmed , Xenbase
Beck, Molecular pathways needed for regeneration of spinal cord and muscle in a vertebrate. 2003, Pubmed , Xenbase
Beck, The role of BMP signaling in outgrowth and patterning of the Xenopus tail bud. 2001, Pubmed , Xenbase
Bel-Vialar, Initiating Hox gene expression: in the early chick neural tube differential sensitivity to FGF and RA signaling subdivides the HoxB genes in two distinct groups. 2002, Pubmed , Xenbase
Bin-Nun, PTK7 modulates Wnt signaling activity via LRP6. 2014, Pubmed , Xenbase
Bonstein, Paraxial-fated mesoderm is required for neural crest induction in Xenopus embryos. 1998, Pubmed , Xenbase
Borday, An atlas of Wnt activity during embryogenesis in Xenopus tropicalis. 2018, Pubmed , Xenbase
Carron, Specification of anteroposterior axis by combinatorial signaling during Xenopus development. 2016, Pubmed , Xenbase
Darras, Anteroposterior axis patterning by early canonical Wnt signaling during hemichordate development. 2018, Pubmed
Davis, The fate of cells in the tailbud of Xenopus laevis. 2000, Pubmed , Xenbase
Deardorff, Frizzled-8 is expressed in the Spemann organizer and plays a role in early morphogenesis. 1998, Pubmed , Xenbase
De Robertis, Dorsal-ventral patterning and neural induction in Xenopus embryos. 2004, Pubmed , Xenbase
Dibner, The Meis3 protein and retinoid signaling interact to pattern the Xenopus hindbrain. 2004, Pubmed , Xenbase
Dibner, XMeis3 protein activity is required for proper hindbrain patterning in Xenopus laevis embryos. 2001, Pubmed , Xenbase
Domingos, The Wnt/beta-catenin pathway posteriorizes neural tissue in Xenopus by an indirect mechanism requiring FGF signalling. 2001, Pubmed , Xenbase
Dorey, FGF signalling: diverse roles during early vertebrate embryogenesis. 2010, Pubmed , Xenbase
Elkouby, NULL 2010, Pubmed
Elkouby, A hindbrain-repressive Wnt3a/Meis3/Tsh1 circuit promotes neuronal differentiation and coordinates tissue maturation. 2012, Pubmed , Xenbase
Elkouby, Mesodermal Wnt signaling organizes the neural plate via Meis3. 2010, Pubmed , Xenbase
EYAL-GILADI, Dynamic aspects of neural induction in amphibia. 1954, Pubmed
Faas, Overlapping functions of Cdx1, Cdx2, and Cdx4 in the development of the amphibian Xenopus tropicalis. 2009, Pubmed , Xenbase
Fainsod, On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo. 1994, Pubmed , Xenbase
Fletcher, FGF8 spliceforms mediate early mesoderm and posterior neural tissue formation in Xenopus. 2006, Pubmed , Xenbase
Fonar, Focal adhesion kinase protein regulates Wnt3a gene expression to control cell fate specification in the developing neural plate. 2011, Pubmed , Xenbase
Frank, Hindbrain induction and patterning during early vertebrate development. 2019, Pubmed
Gamse, Vertebrate anteroposterior patterning: the Xenopus neurectoderm as a paradigm. 2000, Pubmed , Xenbase
Gentsch, In vivo T-box transcription factor profiling reveals joint regulation of embryonic neuromesodermal bipotency. 2013, Pubmed , Xenbase
Goto, FGF and canonical Wnt signaling cooperate to induce paraxial mesoderm from tailbud neuromesodermal progenitors through regulation of a two-step epithelial to mesenchymal transition. 2017, Pubmed , Xenbase
Gutkovich, Xenopus Meis3 protein lies at a nexus downstream to Zic1 and Pax3 proteins, regulating multiple cell-fates during early nervous system development. 2010, Pubmed , Xenbase
Harland, Neural induction. 2000, Pubmed , Xenbase
Harland, In situ hybridization: an improved whole-mount method for Xenopus embryos. 1991, Pubmed , Xenbase
Hashiguchi, Anteroposterior and dorsoventral patterning are coordinated by an identical patterning clock. 2013, Pubmed , Xenbase
Henig, A POU protein regulates mesodermal competence to FGF in Xenopus. 1998, Pubmed , Xenbase
Hudry, Molecular insights into the origin of the Hox-TALE patterning system. 2014, Pubmed , Xenbase
In der Rieden, Xwnt8 directly initiates expression of labial Hox genes. 2010, Pubmed , Xenbase
Isaacs, Regulation of Hox gene expression and posterior development by the Xenopus caudal homologue Xcad3. 1998, Pubmed , Xenbase
James, Bmp signaling promotes intermediate mesoderm gene expression in a dose-dependent, cell-autonomous and translation-dependent manner. 2005, Pubmed
Janssens, Direct control of Hoxd1 and Irx3 expression by Wnt/beta-catenin signaling during anteroposterior patterning of the neural axis in Xenopus. 2010, Pubmed , Xenbase
Jones, Bone morphogenetic protein-4 (BMP-4) acts during gastrula stages to cause ventralization of Xenopus embryos. 1996, Pubmed , Xenbase
Keenan, FGF signal transduction and the regulation of Cdx gene expression. 2006, Pubmed , Xenbase
Keren, p38 MAP kinase regulates the expression of XMyf5 and affects distinct myogenic programs during Xenopus development. 2005, Pubmed , Xenbase
Kiecker, A morphogen gradient of Wnt/beta-catenin signalling regulates anteroposterior neural patterning in Xenopus. 2001, Pubmed , Xenbase
Knöchel, Structure and expression of Xenopus tropicalis BMP-2 and BMP-4 genes. 2001, Pubmed , Xenbase
Kolm, Xenopus hindbrain patterning requires retinoid signaling. 1997, Pubmed , Xenbase
Kudoh, Distinct roles for Fgf, Wnt and retinoic acid in posteriorizing the neural ectoderm. 2002, Pubmed
Li, The posteriorizing gene Gbx2 is a direct target of Wnt signalling and the earliest factor in neural crest induction. 2009, Pubmed , Xenbase
Lombardo, Expression and functions of FGF-3 in Xenopus development. 1998, Pubmed , Xenbase
Lupo, Multiple roles of Activin/Nodal, bone morphogenetic protein, fibroblast growth factor and Wnt/β-catenin signalling in the anterior neural patterning of adherent human embryonic stem cell cultures. 2013, Pubmed
Martin, Canonical Wnt signaling dynamically controls multiple stem cell fate decisions during vertebrate body formation. 2012, Pubmed , Xenbase
Martin, Factors that coordinate mesoderm specification from neuromesodermal progenitors with segmentation during vertebrate axial extension. 2016, Pubmed
Maves, FGF3 and FGF8 mediate a rhombomere 4 signaling activity in the zebrafish hindbrain. 2002, Pubmed
McGrew, Wnt and FGF pathways cooperatively pattern anteroposterior neural ectoderm in Xenopus. 1997, Pubmed , Xenbase
McNulty, Knockdown of the complete Hox paralogous group 1 leads to dramatic hindbrain and neural crest defects. 2005, Pubmed , Xenbase
Merzdorf, The zic1 gene is an activator of Wnt signaling. 2006, Pubmed , Xenbase
Metzis, Nervous System Regionalization Entails Axial Allocation before Neural Differentiation. 2018, Pubmed
Monsoro-Burq, Neural crest induction by paraxial mesoderm in Xenopus embryos requires FGF signals. 2003, Pubmed , Xenbase
Monsoro-Burq, Msx1 and Pax3 cooperate to mediate FGF8 and WNT signals during Xenopus neural crest induction. 2005, Pubmed , Xenbase
Nagai, The expression of the mouse Zic1, Zic2, and Zic3 gene suggests an essential role for Zic genes in body pattern formation. 1997, Pubmed
Nordström, Progressive induction of caudal neural character by graded Wnt signaling. 2002, Pubmed
Pera, Active signals, gradient formation and regional specificity in neural induction. 2014, Pubmed , Xenbase
Plouhinec, Pax3 and Zic1 trigger the early neural crest gene regulatory network by the direct activation of multiple key neural crest specifiers. 2014, Pubmed , Xenbase
Polevoy, FoxD1 protein interacts with Wnt and BMP signaling to differentially pattern mesoderm and neural tissue. 2017, Pubmed , Xenbase
Pownall, Two phases of Hox gene regulation during early Xenopus development. 1998, Pubmed , Xenbase
Re'em-Kalma, Competition between noggin and bone morphogenetic protein 4 activities may regulate dorsalization during Xenopus development. 1995, Pubmed , Xenbase
Ribisi, Ras-mediated FGF signaling is required for the formation of posterior but not anterior neural tissue in Xenopus laevis. 2000, Pubmed , Xenbase
Salzberg, A Meis family protein caudalizes neural cell fates in Xenopus. 1999, Pubmed , Xenbase
Sato, Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. 2005, Pubmed , Xenbase
Schohl, Beta-catenin, MAPK and Smad signaling during early Xenopus development. 2002, Pubmed , Xenbase
Shimizu, Cdx-Hox code controls competence for responding to Fgfs and retinoic acid in zebrafish neural tissue. 2006, Pubmed
Skromne, Repression of the hindbrain developmental program by Cdx factors is required for the specification of the vertebrate spinal cord. 2007, Pubmed
Snir, Xenopus laevis POU91 protein, an Oct3/4 homologue, regulates competence transitions from mesoderm to neural cell fates. 2006, Pubmed , Xenbase
Stern, Neural induction: old problem, new findings, yet more questions. 2005, Pubmed , Xenbase
Taniguchi, The posterior neural plate in axolotl gives rise to neural tube or turns anteriorly to form somites of the tail and posterior trunk. 2017, Pubmed
Toivonen, Morphogenetic interaction of presumptive neural and mesodermal cells mixed in different ratios. 1968, Pubmed
Tuazon, Temporally coordinated signals progressively pattern the anteroposterior and dorsoventral body axes. 2015, Pubmed , Xenbase
Tzouanacou, Redefining the progression of lineage segregations during mammalian embryogenesis by clonal analysis. 2009, Pubmed
Walshe, Establishment of hindbrain segmental identity requires signaling by FGF3 and FGF8. 2002, Pubmed
Weisinger, Inhibition of BMPs by follistatin is required for FGF3 expression and segmental patterning of the hindbrain. 2008, Pubmed
White, How degrading: Cyp26s in hindbrain development. 2008, Pubmed
Young, Spalt-like 4 promotes posterior neural fates via repression of pou5f3 family members in Xenopus. 2014, Pubmed , Xenbase
Zetser, MAP kinase converts MyoD into an instructive muscle differentiation factor in Xenopus. 2001, Pubmed , Xenbase