XB-ART-55114
BMC Biol
January 1, 2018;
16
(1):
79.
A gene regulatory network underlying the formation of pre-placodal ectoderm in Xenopus laevis.
Abstract
BACKGROUND: The neural plate border ectoderm gives rise to key developmental structures during embryogenesis, including the neural crest and the preplacodal ectoderm. Many sensory organs and ganglia of vertebrates develop from cranial placodes, which themselves arise from preplacodal ectoderm, defined by expression of transcription factor Six1 and its coactivator Eya1. Here we elucidate the gene regulatory network underlying the specification of the preplacodal ectoderm in Xenopus, and the functional interactions among transcription factors that give rise to this structure. RESULTS: To elucidate the gene regulatory network upstream of preplacodal ectoderm formation, we use gain- and loss-of-function studies to explore the role of early ectodermal transcription factors for establishing the preplacodal ectoderm and adjacent ectodermal territories, and the role of Six1 and Eya1 in feedback regulation of these transcription factors. Our findings suggest that transcription factors with expression restricted to ventral (non-neural) ectoderm (AP2, Msx1, FoxI1, Vent2, Dlx3, GATA2) and those restricted to dorsal (neural) ectoderm (Pax3, Hairy2b, Zic1) are required for specification of both preplacodal ectoderm and neural crest in a context-dependent fashion and are cross-regulated by Eya1 and Six1. CONCLUSION: These findings allow us to elucidate a detailed gene regulatory network at the neural plate border upstream of preplacodal ectoderm formation based on functional interactions between ectodermal transcription factors. We propose a new model to explain the formation of immediately juxtaposed preplacodal ectoderm and neural crest territories at the neural plate border, uniting previous models.
PubMed ID: 30012125
PMC ID: PMC6048776
Article link: BMC Biol
Grant support: [+]
GOIPG/2013/472 Irish Research Council, n/a National University of Ireland, Galway
Species referenced: Xenopus laevis
Genes referenced: dlx3 eya1 foxd3 foxi1 foxi4.2 gata2 hes4 msx1 myc npb pax3 pdf six1 sox3 tfap2a ventx2.1 ventx2.2 zic1
GO keywords: neural crest formation [+]
Morpholinos: dlx3 MO1 eya1 MO1 eya1 MO2 foxi4.2 MO1 hes4 MO1 hes4 MO2 msx1 MO1 pax3 MO1 six1 MO1 six1 MO2 tfap2a MO1 ventx2.1 MO2 zic1 MO1
Article Images: [+] show captions
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Brzezinski, Photoreceptor cell fate specification in vertebrates. 2016, Pubmed
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Luo, Induction of neural crest in Xenopus by transcription factor AP2alpha. 2003, Pubmed , Xenbase
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Mizuseki, Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. 1998, Pubmed , Xenbase
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Nichane, Hairy2-Id3 interactions play an essential role in Xenopus neural crest progenitor specification. 2009, Pubmed , Xenbase
Nichane, Hairy2 functions through both DNA-binding and non DNA-binding mechanisms at the neural plate border in Xenopus. 2009, Pubmed , Xenbase
Nimmo, Primed and ready: understanding lineage commitment through single cell analysis. 2016, Pubmed
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Onichtchouk, The Xvent-2 homeobox gene is part of the BMP-4 signalling pathway controlling [correction of controling] dorsoventral patterning of Xenopus mesoderm. 1996, Pubmed , Xenbase
Pandur, Xenopus Six1 gene is expressed in neurogenic cranial placodes and maintained in the differentiating lateral lines. 2000, Pubmed , Xenbase
Penzel, Characterization and early embryonic expression of a neural specific transcription factor xSOX3 in Xenopus laevis. 1998, Pubmed , Xenbase
Pieper, Differential distribution of competence for panplacodal and neural crest induction to non-neural and neural ectoderm. 2012, Pubmed , Xenbase
Plouhinec, A molecular atlas of the developing ectoderm defines neural, neural crest, placode, and nonneural progenitor identity in vertebrates. 2017, Pubmed , Xenbase
Pohl, Temporal and spatial expression patterns of FoxD2 during the early development of Xenopus laevis. 2002, Pubmed , Xenbase
Riddiford, Dissecting the pre-placodal transcriptome to reveal presumptive direct targets of Six1 and Eya1 in cranial placodes. 2017, Pubmed , Xenbase
Roellig, Dynamic transcriptional signature and cell fate analysis reveals plasticity of individual neural plate border cells. 2017, Pubmed
Rogers, Xenopus Sox3 activates sox2 and geminin and indirectly represses Xvent2 expression to induce neural progenitor formation at the expense of non-neural ectodermal derivatives. 2009, Pubmed , Xenbase
Rogers, Sox3 expression is maintained by FGF signaling and restricted to the neural plate by Vent proteins in the Xenopus embryo. 2008, Pubmed , Xenbase
Rogers, The response of early neural genes to FGF signaling or inhibition of BMP indicate the absence of a conserved neural induction module. 2012, Pubmed , Xenbase
Saint-Jeannet, Establishing the pre-placodal region and breaking it into placodes with distinct identities. 2014, Pubmed , Xenbase
Sasai, Requirement of FoxD3-class signaling for neural crest determination in Xenopus. 2001, Pubmed , Xenbase
Sato, Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. 2005, Pubmed , Xenbase
Sauka-Spengler, Evolution of the neural crest viewed from a gene regulatory perspective. 2009, Pubmed
Schlosser, Making senses development of vertebrate cranial placodes. 2011, Pubmed , Xenbase
Schlosser, Induction and specification of cranial placodes. 2006, Pubmed , Xenbase
Schlosser, Early embryonic specification of vertebrate cranial placodes. 2015, Pubmed , Xenbase
Schlosser, Molecular anatomy of placode development in Xenopus laevis. 2004, Pubmed , Xenbase
Schlosser, Eya1 and Six1 promote neurogenesis in the cranial placodes in a SoxB1-dependent fashion. 2008, Pubmed , Xenbase
Simões-Costa, Establishing neural crest identity: a gene regulatory recipe. 2015, Pubmed
Steventon, Differential requirements of BMP and Wnt signalling during gastrulation and neurulation define two steps in neural crest induction. 2009, Pubmed , Xenbase
Su, Progressively restricted expression of a new homeobox-containing gene during Xenopus laevis embryogenesis. 1991, Pubmed , Xenbase
Suzuki, Xenopus msx1 mediates epidermal induction and neural inhibition by BMP4. 1997, Pubmed , Xenbase
Trevers, Neural induction by the node and placode induction by head mesoderm share an initial state resembling neural plate border and ES cells. 2018, Pubmed
Tribulo, Regulation of Msx genes by a Bmp gradient is essential for neural crest specification. 2004, Pubmed , Xenbase
Walmsley, Negative control of Xenopus GATA-2 by activin and noggin with eventual expression in precursors of the ventral blood islands. 1994, Pubmed , Xenbase
Woda, Dlx proteins position the neural plate border and determine adjacent cell fates. 2003, Pubmed , Xenbase
Zhang, Repression of nodal expression by maternal B1-type SOXs regulates germ layer formation in Xenopus and zebrafish. 2004, Pubmed , Xenbase
de Crozé, Reiterative AP2a activity controls sequential steps in the neural crest gene regulatory network. 2011, Pubmed , Xenbase
Bang, Expression of Pax-3 is initiated in the early neural plate by posteriorizing signals produced by the organizer and by posterior non-axial mesoderm. 1997, Pubmed , Xenbase
Bhat, A gene network that coordinates preplacodal competence and neural crest specification in zebrafish. 2013, Pubmed
Brugmann, Six1 promotes a placodal fate within the lateral neurogenic ectoderm by functioning as both a transcriptional activator and repressor. 2005, Pubmed , Xenbase
Brzezinski, Photoreceptor cell fate specification in vertebrates. 2016, Pubmed
Buitrago-Delgado, NEURODEVELOPMENT. Shared regulatory programs suggest retention of blastula-stage potential in neural crest cells. 2015, Pubmed , Xenbase
Christophorou, Activation of Six1 target genes is required for sensory placode formation. 2009, Pubmed
David, Xenopus Eya1 demarcates all neurogenic placodes as well as migrating hypaxial muscle precursors. 2001, Pubmed , Xenbase
Feledy, Inhibitory patterning of the anterior neural plate in Xenopus by homeodomain factors Dlx3 and Msx1. 1999, Pubmed , Xenbase
Friedle, Cooperative interaction of Xvent-2 and GATA-2 in the activation of the ventral homeobox gene Xvent-1B. 2002, Pubmed , Xenbase
Grocott, The peripheral sensory nervous system in the vertebrate head: a gene regulatory perspective. 2012, Pubmed
Hintze, Cell interactions, signals and transcriptional hierarchy governing placode progenitor induction. 2017, Pubmed
Hong, The activity of Pax3 and Zic1 regulates three distinct cell fates at the neural plate border. 2007, Pubmed , Xenbase
Hu, Multilineage gene expression precedes commitment in the hemopoietic system. 1997, Pubmed
Jaurena, Zic1 controls placode progenitor formation non-cell autonomously by regulating retinoic acid production and transport. 2016, Pubmed , Xenbase
Kuo, Opl: a zinc finger protein that regulates neural determination and patterning in Xenopus. 1998, Pubmed , Xenbase
Kwon, Identification of early requirements for preplacodal ectoderm and sensory organ development. 2011, Pubmed
Ladher, Xom: a Xenopus homeobox gene that mediates the early effects of BMP-4. 1996, Pubmed , Xenbase
Li, Eya protein phosphatase activity regulates Six1-Dach-Eya transcriptional effects in mammalian organogenesis. 2003, Pubmed
Litsiou, A balance of FGF, BMP and WNT signalling positions the future placode territory in the head. 2006, Pubmed
Longabaugh, Visualization, documentation, analysis, and communication of large-scale gene regulatory networks. 2009, Pubmed
Longabaugh, Computational representation of developmental genetic regulatory networks. 2005, Pubmed
Luo, Distinct roles for Distal-less genes Dlx3 and Dlx5 in regulating ectodermal development in Xenopus. 2002, Pubmed , Xenbase
Luo, Induction of neural crest in Xenopus by transcription factor AP2alpha. 2003, Pubmed , Xenbase
Luo, Transcription factor AP-2 is an essential and direct regulator of epidermal development in Xenopus. 2002, Pubmed , Xenbase
Marchal, BMP inhibition initiates neural induction via FGF signaling and Zic genes. 2009, Pubmed , Xenbase
Matsuo-Takasaki, An essential role of Xenopus Foxi1a for ventral specification of the cephalic ectoderm during gastrulation. 2005, Pubmed , Xenbase
McLarren, DLX5 positions the neural crest and preplacode region at the border of the neural plate. 2003, Pubmed
Meulemans, Gene-regulatory interactions in neural crest evolution and development. 2004, Pubmed
Milet, Neural crest induction at the neural plate border in vertebrates. 2012, Pubmed , Xenbase
Milet, Pax3 and Zic1 drive induction and differentiation of multipotent, migratory, and functional neural crest in Xenopus embryos. 2013, Pubmed , Xenbase
Mizuseki, Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. 1998, Pubmed , Xenbase
Monsoro-Burq, Msx1 and Pax3 cooperate to mediate FGF8 and WNT signals during Xenopus neural crest induction. 2005, Pubmed , Xenbase
Monsoro-Burq, Neural crest induction by paraxial mesoderm in Xenopus embryos requires FGF signals. 2003, Pubmed , Xenbase
Nichane, Hairy2-Id3 interactions play an essential role in Xenopus neural crest progenitor specification. 2009, Pubmed , Xenbase
Nichane, Hairy2 functions through both DNA-binding and non DNA-binding mechanisms at the neural plate border in Xenopus. 2009, Pubmed , Xenbase
Nimmo, Primed and ready: understanding lineage commitment through single cell analysis. 2016, Pubmed
Northcutt, The genesis of neural crest and epidermal placodes: a reinterpretation of vertebrate origins. 1983, Pubmed
Onichtchouk, The Xvent-2 homeobox gene is part of the BMP-4 signalling pathway controlling [correction of controling] dorsoventral patterning of Xenopus mesoderm. 1996, Pubmed , Xenbase
Pandur, Xenopus Six1 gene is expressed in neurogenic cranial placodes and maintained in the differentiating lateral lines. 2000, Pubmed , Xenbase
Penzel, Characterization and early embryonic expression of a neural specific transcription factor xSOX3 in Xenopus laevis. 1998, Pubmed , Xenbase
Pieper, Differential distribution of competence for panplacodal and neural crest induction to non-neural and neural ectoderm. 2012, Pubmed , Xenbase
Plouhinec, A molecular atlas of the developing ectoderm defines neural, neural crest, placode, and nonneural progenitor identity in vertebrates. 2017, Pubmed , Xenbase
Pohl, Temporal and spatial expression patterns of FoxD2 during the early development of Xenopus laevis. 2002, Pubmed , Xenbase
Riddiford, Dissecting the pre-placodal transcriptome to reveal presumptive direct targets of Six1 and Eya1 in cranial placodes. 2017, Pubmed , Xenbase
Roellig, Dynamic transcriptional signature and cell fate analysis reveals plasticity of individual neural plate border cells. 2017, Pubmed
Rogers, Xenopus Sox3 activates sox2 and geminin and indirectly represses Xvent2 expression to induce neural progenitor formation at the expense of non-neural ectodermal derivatives. 2009, Pubmed , Xenbase
Rogers, Sox3 expression is maintained by FGF signaling and restricted to the neural plate by Vent proteins in the Xenopus embryo. 2008, Pubmed , Xenbase
Rogers, The response of early neural genes to FGF signaling or inhibition of BMP indicate the absence of a conserved neural induction module. 2012, Pubmed , Xenbase
Saint-Jeannet, Establishing the pre-placodal region and breaking it into placodes with distinct identities. 2014, Pubmed , Xenbase
Sasai, Requirement of FoxD3-class signaling for neural crest determination in Xenopus. 2001, Pubmed , Xenbase
Sato, Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. 2005, Pubmed , Xenbase
Sauka-Spengler, Evolution of the neural crest viewed from a gene regulatory perspective. 2009, Pubmed
Schlosser, Making senses development of vertebrate cranial placodes. 2011, Pubmed , Xenbase
Schlosser, Induction and specification of cranial placodes. 2006, Pubmed , Xenbase
Schlosser, Early embryonic specification of vertebrate cranial placodes. 2015, Pubmed , Xenbase
Schlosser, Molecular anatomy of placode development in Xenopus laevis. 2004, Pubmed , Xenbase
Schlosser, Eya1 and Six1 promote neurogenesis in the cranial placodes in a SoxB1-dependent fashion. 2008, Pubmed , Xenbase
Simões-Costa, Establishing neural crest identity: a gene regulatory recipe. 2015, Pubmed
Steventon, Differential requirements of BMP and Wnt signalling during gastrulation and neurulation define two steps in neural crest induction. 2009, Pubmed , Xenbase
Su, Progressively restricted expression of a new homeobox-containing gene during Xenopus laevis embryogenesis. 1991, Pubmed , Xenbase
Suzuki, Xenopus msx1 mediates epidermal induction and neural inhibition by BMP4. 1997, Pubmed , Xenbase
Trevers, Neural induction by the node and placode induction by head mesoderm share an initial state resembling neural plate border and ES cells. 2018, Pubmed
Tribulo, Regulation of Msx genes by a Bmp gradient is essential for neural crest specification. 2004, Pubmed , Xenbase
Walmsley, Negative control of Xenopus GATA-2 by activin and noggin with eventual expression in precursors of the ventral blood islands. 1994, Pubmed , Xenbase
Woda, Dlx proteins position the neural plate border and determine adjacent cell fates. 2003, Pubmed , Xenbase
Zhang, Repression of nodal expression by maternal B1-type SOXs regulates germ layer formation in Xenopus and zebrafish. 2004, Pubmed , Xenbase
de Crozé, Reiterative AP2a activity controls sequential steps in the neural crest gene regulatory network. 2011, Pubmed , Xenbase