XB-ART-52066
Genesis
January 1, 2016;
54
(6):
334-49.
Neural transcription factors bias cleavage stage blastomeres to give rise to neural ectoderm.
Gaur S
,
Mandelbaum M
,
Herold M
,
Majumdar HD
,
Neilson KM
,
Maynard TM
,
Mood K
,
Daar IO
,
Moody SA
.
Abstract
The decision by embryonic ectoderm to give rise to epidermal versus neural derivatives is the result of signaling events during blastula and gastrula stages. However, there also is evidence in Xenopus that cleavage stage blastomeres contain maternally derived molecules that bias them toward a neural fate. We used a blastomere explant culture assay to test whether maternally deposited transcription factors bias 16-cell blastomere precursors of epidermal or neural ectoderm to express early zygotic neural genes in the absence of gastrulation interactions or exogenously supplied signaling factors. We found that Foxd4l1, Zic2, Gmnn, and Sox11 each induced explants made from ventral, epidermis-producing blastomeres to express early neural genes, and that at least some of the Foxd4l1 and Zic2 activities are required at cleavage stages. Similarly, providing extra Foxd4l1 or Zic2 to explants made from dorsal, neural plate-producing blastomeres significantly increased the expression of early neural genes, whereas knocking down either significantly reduced them. These results show that maternally delivered transcription factors bias cleavage stage blastomeres to a neural fate. We demonstrate that mouse and human homologs of Foxd4l1 have similar functional domains compared to the frog protein, as well as conserved transcriptional activities when expressed in Xenopus embryos and blastomere explants. genesis 54:334-349, 2016. © 2016 Wiley Periodicals, Inc.
PubMed ID: 27092474
PMC ID: PMC4912902
Article link: Genesis
Grant support: [+]
R01 DE022065 NIDCR NIH HHS, Z01 BC010006-13 Intramural NIH HHS, ZIA BC010006 NCI NIH HHS , ZIA BC010006 Intramural NIH HHS, U54 HD090257 NICHD NIH HHS
Species referenced: Xenopus laevis
Genes referenced: chrd.1 ctnnb1 foxd4l1.1 foxd4l1.2 gmnn irx1 krt12.4 neurog2 sia1 sox11 sox2 tbxt tle4 zic1 zic2
Morpholinos: foxd4l1.1 MO1 foxd4l1.2 MO1 zic2 MO1 zic2 MO2 zic2 MO3 zic2 MO4
Phenotypes: Xla Wt + Hsa.foxd4 (fig.6.a) [+]
Xla Wt + Hsa.foxd4
(fig.6.b)
Xla Wt + Hsa.foxd4 (fig.6.c)
Xla Wt + Hsa.foxd4l1.1 (fig.6.a)
Xla Wt + Hsa.foxd4l1.1 (fig.6.b)
Xla Wt + Hsa.foxd4l1.1 (fig.6.c)
Xla Wt + foxd4l1.1 (fig.6.a)
Xla Wt + foxd4l1.1 (fig.6.b)
Xla Wt + foxd4l1.1 (fig.6.c)
Xla Wt + Hsa.foxd4 (fig.6.c)
Xla Wt + Hsa.foxd4l1.1 (fig.6.a)
Xla Wt + Hsa.foxd4l1.1 (fig.6.b)
Xla Wt + Hsa.foxd4l1.1 (fig.6.c)
Xla Wt + foxd4l1.1 (fig.6.a)
Xla Wt + foxd4l1.1 (fig.6.b)
Xla Wt + foxd4l1.1 (fig.6.c)
Article Images: [+] show captions
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Kodjabachian, Siamois functions in the early blastula to induce Spemann's organiser. 2001, Pubmed , Xenbase
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Koyano, The Xenopus Sox3 gene expressed in oocytes of early stages. 1997, Pubmed , Xenbase
Kroll, Geminin, a neuralizing molecule that demarcates the future neural plate at the onset of gastrulation. 1998, Pubmed , Xenbase
Kuo, Opl: a zinc finger protein that regulates neural determination and patterning in Xenopus. 1998, Pubmed , Xenbase
Kuroda, Neural induction in Xenopus: requirement for ectodermal and endomesodermal signals via Chordin, Noggin, beta-Catenin, and Cerberus. 2004, Pubmed , Xenbase
Laurent, The Xenopus homeobox gene twin mediates Wnt induction of goosecoid in establishment of Spemann's organizer. 1998, Pubmed , Xenbase
Lee, Neural transcription factors: from embryos to neural stem cells. 2014, Pubmed , Xenbase
Levine, Proposal of a model of mammalian neural induction. 2007, Pubmed
Li, Location of transient ectodermal progenitor potential in mouse development. 2013, Pubmed
Lombard-Banek, Single-Cell Mass Spectrometry for Discovery Proteomics: Quantifying Translational Cell Heterogeneity in the 16-Cell Frog (Xenopus) Embryo. 2016, Pubmed , Xenbase
Matsuda, A New Nomenclature of Xenopus laevis Chromosomes Based on the Phylogenetic Relationship to Silurana/Xenopus tropicalis. 2015, Pubmed , Xenbase
Mattioni, Regulation of protein activities by fusion to steroid binding domains. 1995, Pubmed
Medina, Cortical rotation is required for the correct spatial expression of nr3, sia and gsc in Xenopus embryos. 1998, Pubmed , Xenbase
Miyata, Regional differences of proteins in isolated cells of early embryos of Xenopus laevis. 1987, 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
Moody, Segregation of fate during cleavage of frog (Xenopus laevis) blastomeres. 1991, Pubmed , Xenbase
Moody, Fates of the blastomeres of the 16-cell stage Xenopus embryo. 1987, Pubmed , Xenbase
Moody, On becoming neural: what the embryo can tell us about differentiating neural stem cells. 2013, Pubmed , Xenbase
Nakata, Xenopus Zic family and its role in neural and neural crest development. 1999, Pubmed , Xenbase
Neilson, Specific domains of FoxD4/5 activate and repress neural transcription factor genes to control the progression of immature neural ectoderm to differentiating neural plate. 2012, Pubmed , Xenbase
Onjiko, Single-cell mass spectrometry reveals small molecules that affect cell fates in the 16-cell embryo. 2015, Pubmed , Xenbase
Pandur, Multiple maternal influences on dorsal-ventral fate of Xenopus animal blastomeres. 2002, Pubmed , Xenbase
Pera, Active signals, gradient formation and regional specificity in neural induction. 2014, Pubmed , Xenbase
Peshkin, On the Relationship of Protein and mRNA Dynamics in Vertebrate Embryonic Development. 2015, Pubmed , Xenbase
Pinho, Distinct steps of neural induction revealed by Asterix, Obelix and TrkC, genes induced by different signals from the organizer. 2011, Pubmed
Pourebrahim, Transcription factor Zic2 inhibits Wnt/β-catenin protein signaling. 2011, Pubmed , Xenbase
Reid, Transcriptional integration of Wnt and Nodal pathways in establishment of the Spemann organizer. 2012, Pubmed , Xenbase
Reversade, Regulation of ADMP and BMP2/4/7 at opposite embryonic poles generates a self-regulating morphogenetic field. 2005, Pubmed , Xenbase
Robert, Deciphering key features in protein structures with the new ENDscript server. 2014, Pubmed
Rogers, Neural induction and factors that stabilize a neural fate. 2009, Pubmed , Xenbase
Sasai, Identifying the missing links: genes that connect neural induction and primary neurogenesis in vertebrate embryos. 1998, Pubmed
Schneider, Beta-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. 1997, Pubmed , Xenbase
Sherman, Foxd4 is essential for establishing neural cell fate and for neuronal differentiation. 2017, Pubmed , Xenbase
Sievers, Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. 2011, Pubmed
Sokol, Pre-existent pattern in Xenopus animal pole cells revealed by induction with activin. 1991, Pubmed , Xenbase
Spemann, Induction of embryonic primordia by implantation of organizers from a different species. 1923. 2001, Pubmed
Sudou, Dynamic in vivo binding of transcription factors to cis-regulatory modules of cer and gsc in the stepwise formation of the Spemann-Mangold organizer. 2012, Pubmed , Xenbase
Sullivan, foxD5a, a Xenopus winged helix gene, maintains an immature neural ectoderm via transcriptional repression that is dependent on the C-terminal domain. 2001, Pubmed , Xenbase
White, Maternal control of pattern formation in Xenopus laevis. 2007, Pubmed , Xenbase
Wills, BMP antagonists and FGF signaling contribute to different domains of the neural plate in Xenopus. 2010, Pubmed , Xenbase
Xu, Maternal xNorrin, a canonical Wnt signaling agonist and TGF-β antagonist, controls early neuroectoderm specification in Xenopus. 2012, Pubmed , Xenbase
Yaklichkin, FoxD3 and Grg4 physically interact to repress transcription and induce mesoderm in Xenopus. 2007, Pubmed , Xenbase
Yan, Microarray identification of novel downstream targets of FoxD4L1/D5, a critical component of the neural ectodermal transcriptional network. 2010, Pubmed , Xenbase
Yan, foxD5 plays a critical upstream role in regulating neural ectodermal fate and the onset of neural differentiation. 2009, Pubmed , Xenbase
Yanai, Mapping gene expression in two Xenopus species: evolutionary constraints and developmental flexibility. 2011, Pubmed , Xenbase
Yang, Beta-catenin/Tcf-regulated transcription prior to the midblastula transition. 2002, Pubmed , Xenbase
Zernicka-Goetz, The first cell-fate decisions in the mouse embryo: destiny is a matter of both chance and choice. 2006, Pubmed
Zernicka-Goetz, Cleavage pattern and emerging asymmetry of the mouse embryo. 2005, Pubmed
Zhang, The Sox axis, Nodal signaling, and germ layer specification. 2007, Pubmed , Xenbase
Zhang, The beta-catenin/VegT-regulated early zygotic gene Xnr5 is a direct target of SOX3 regulation. 2003, Pubmed , Xenbase
Zhang, Repression of nodal expression by maternal B1-type SOXs regulates germ layer formation in Xenopus and zebrafish. 2004, Pubmed , Xenbase
Bae, Siamois and Twin are redundant and essential in formation of the Spemann organizer. 2011, Pubmed , Xenbase
Bates, Coco regulates dorsoventral specification of germ layers via inhibition of TGFβ signalling. 2013, Pubmed , Xenbase
Bauer, The cleavage stage origin of Spemann's Organizer: analysis of the movements of blastomere clones before and during gastrulation in Xenopus. 1994, Pubmed , Xenbase
Bowes, Xenbase: gene expression and improved integration. 2009, Pubmed , Xenbase
Brewster, Gli/Zic factors pattern the neural plate by defining domains of cell differentiation. 1998, Pubmed , Xenbase
Carnac, The homeobox gene Siamois is a target of the Wnt dorsalisation pathway and triggers organiser activity in the absence of mesoderm. 1996, Pubmed , Xenbase
Cha, Foxi2 is an animally localized maternal mRNA in Xenopus, and an activator of the zygotic ectoderm activator Foxi1e. 2012, Pubmed , Xenbase
Cuykendall, Identification of germ plasm-associated transcripts by microarray analysis of Xenopus vegetal cortex RNA. 2010, Pubmed , Xenbase
Darras, Animal and vegetal pole cells of early Xenopus embryos respond differently to maternal dorsal determinants: implications for the patterning of the organiser. 1997, Pubmed , Xenbase
Davidson, How embryos work: a comparative view of diverse modes of cell fate specification. 1990, Pubmed , Xenbase
De Domenico, Molecular asymmetry in the 8-cell stage Xenopus tropicalis embryo described by single blastomere transcript sequencing. 2015, Pubmed , Xenbase
De Robertis, Spemann's organizer and self-regulation in amphibian embryos. 2006, Pubmed
Ding, Pre-MBT patterning of early gene regulation in Xenopus: the role of the cortical rotation and mesoderm induction. 1998, Pubmed , Xenbase
Dupont, Germ-layer specification and control of cell growth by Ectodermin, a Smad4 ubiquitin ligase. 2005, Pubmed , Xenbase
Fujimi, Xenopus Zic3 controls notochord and organizer development through suppression of the Wnt/β-catenin signaling pathway. 2011, Pubmed , Xenbase
Gallagher, Autonomous differentiation of dorsal axial structures from an animal cap cleavage stage blastomere in Xenopus. 1991, Pubmed , Xenbase
Grant, Blastomere explants to test for cell fate commitment during embryonic development. 2013, Pubmed , Xenbase
Grant, Novel animal pole-enriched maternal mRNAs are preferentially expressed in neural ectoderm. 2014, Pubmed , Xenbase
Hainski, Xenopus maternal RNAs from a dorsal animal blastomere induce a secondary axis in host embryos. 1993, Pubmed , Xenbase
Heasman, Patterning the early Xenopus embryo. 2006, Pubmed , Xenbase
Hiraoka, XLS13A and XLS13B: SRY-related genes of Xenopus laevis. 1997, Pubmed , Xenbase
Houston, Maternal Xenopus Zic2 negatively regulates Nodal-related gene expression during anteroposterior patterning. 2005, Pubmed , Xenbase
Hyodo-Miura, Involvement of NLK and Sox11 in neural induction in Xenopus development. 2002, Pubmed , Xenbase
Ishibashi, Expression of Siamois and Twin in the blastula Chordin/Noggin signaling center is required for brain formation in Xenopus laevis embryos. 2007, Pubmed , Xenbase
Jackson, Update of human and mouse forkhead box (FOX) gene families. 2010, Pubmed
Jonas, Epidermal keratin gene expressed in embryos of Xenopus laevis. 1985, Pubmed , Xenbase
Kageura, Pattern formation in 8-cell composite embryos of Xenopus laevis. 1986, Pubmed , Xenbase
Kageura, Three regions of the 32-cell embryo of Xenopus laevis essential for formation of a complete tadpole. 1995, Pubmed , Xenbase
Kageura, Spatial distribution of the capacity to initiate a secondary embryo in the 32-cell embryo of Xenopus laevis. 1991, Pubmed , Xenbase
Kageura, Pattern regulation in defect embryos of Xenopus laevis. 1984, Pubmed , Xenbase
Kessler, Siamois is required for formation of Spemann's organizer. 1998, Pubmed , Xenbase
Khokha, Depletion of three BMP antagonists from Spemann's organizer leads to a catastrophic loss of dorsal structures. 2005, Pubmed , Xenbase
King, Putting RNAs in the right place at the right time: RNA localization in the frog oocyte. 2004, Pubmed , Xenbase
Kinoshita, Competence prepattern in the animal hemisphere of the 8-cell-stage Xenopus embryo. 1993, Pubmed , Xenbase
Klein, Conserved structural domains in FoxD4L1, a neural forkhead box transcription factor, are required to repress or activate target genes. 2013, Pubmed , Xenbase
Klein, The first cleavage furrow demarcates the dorsal-ventral axis in Xenopus embryos. 1987, Pubmed , Xenbase
Klein, Early neural ectodermal genes are activated by Siamois and Twin during blastula stages. 2015, Pubmed , Xenbase
Klein, Correlations between cell fate and the distribution of proteins that are synthesized before the midblastula transition in Xenopus. 2019, Pubmed , Xenbase
Kodjabachian, Siamois functions in the early blastula to induce Spemann's organiser. 2001, Pubmed , Xenbase
Kolm, Efficient hormone-inducible protein function in Xenopus laevis. 1995, Pubmed , Xenbase
Koyano, The Xenopus Sox3 gene expressed in oocytes of early stages. 1997, Pubmed , Xenbase
Kroll, Geminin, a neuralizing molecule that demarcates the future neural plate at the onset of gastrulation. 1998, Pubmed , Xenbase
Kuo, Opl: a zinc finger protein that regulates neural determination and patterning in Xenopus. 1998, Pubmed , Xenbase
Kuroda, Neural induction in Xenopus: requirement for ectodermal and endomesodermal signals via Chordin, Noggin, beta-Catenin, and Cerberus. 2004, Pubmed , Xenbase
Laurent, The Xenopus homeobox gene twin mediates Wnt induction of goosecoid in establishment of Spemann's organizer. 1998, Pubmed , Xenbase
Lee, Neural transcription factors: from embryos to neural stem cells. 2014, Pubmed , Xenbase
Levine, Proposal of a model of mammalian neural induction. 2007, Pubmed
Li, Location of transient ectodermal progenitor potential in mouse development. 2013, Pubmed
Lombard-Banek, Single-Cell Mass Spectrometry for Discovery Proteomics: Quantifying Translational Cell Heterogeneity in the 16-Cell Frog (Xenopus) Embryo. 2016, Pubmed , Xenbase
Matsuda, A New Nomenclature of Xenopus laevis Chromosomes Based on the Phylogenetic Relationship to Silurana/Xenopus tropicalis. 2015, Pubmed , Xenbase
Mattioni, Regulation of protein activities by fusion to steroid binding domains. 1995, Pubmed
Medina, Cortical rotation is required for the correct spatial expression of nr3, sia and gsc in Xenopus embryos. 1998, Pubmed , Xenbase
Miyata, Regional differences of proteins in isolated cells of early embryos of Xenopus laevis. 1987, 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
Moody, Segregation of fate during cleavage of frog (Xenopus laevis) blastomeres. 1991, Pubmed , Xenbase
Moody, Fates of the blastomeres of the 16-cell stage Xenopus embryo. 1987, Pubmed , Xenbase
Moody, On becoming neural: what the embryo can tell us about differentiating neural stem cells. 2013, Pubmed , Xenbase
Nakata, Xenopus Zic family and its role in neural and neural crest development. 1999, Pubmed , Xenbase
Neilson, Specific domains of FoxD4/5 activate and repress neural transcription factor genes to control the progression of immature neural ectoderm to differentiating neural plate. 2012, Pubmed , Xenbase
Onjiko, Single-cell mass spectrometry reveals small molecules that affect cell fates in the 16-cell embryo. 2015, Pubmed , Xenbase
Pandur, Multiple maternal influences on dorsal-ventral fate of Xenopus animal blastomeres. 2002, Pubmed , Xenbase
Pera, Active signals, gradient formation and regional specificity in neural induction. 2014, Pubmed , Xenbase
Peshkin, On the Relationship of Protein and mRNA Dynamics in Vertebrate Embryonic Development. 2015, Pubmed , Xenbase
Pinho, Distinct steps of neural induction revealed by Asterix, Obelix and TrkC, genes induced by different signals from the organizer. 2011, Pubmed
Pourebrahim, Transcription factor Zic2 inhibits Wnt/β-catenin protein signaling. 2011, Pubmed , Xenbase
Reid, Transcriptional integration of Wnt and Nodal pathways in establishment of the Spemann organizer. 2012, Pubmed , Xenbase
Reversade, Regulation of ADMP and BMP2/4/7 at opposite embryonic poles generates a self-regulating morphogenetic field. 2005, Pubmed , Xenbase
Robert, Deciphering key features in protein structures with the new ENDscript server. 2014, Pubmed
Rogers, Neural induction and factors that stabilize a neural fate. 2009, Pubmed , Xenbase
Sasai, Identifying the missing links: genes that connect neural induction and primary neurogenesis in vertebrate embryos. 1998, Pubmed
Schneider, Beta-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. 1997, Pubmed , Xenbase
Sherman, Foxd4 is essential for establishing neural cell fate and for neuronal differentiation. 2017, Pubmed , Xenbase
Sievers, Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. 2011, Pubmed
Sokol, Pre-existent pattern in Xenopus animal pole cells revealed by induction with activin. 1991, Pubmed , Xenbase
Spemann, Induction of embryonic primordia by implantation of organizers from a different species. 1923. 2001, Pubmed
Sudou, Dynamic in vivo binding of transcription factors to cis-regulatory modules of cer and gsc in the stepwise formation of the Spemann-Mangold organizer. 2012, Pubmed , Xenbase
Sullivan, foxD5a, a Xenopus winged helix gene, maintains an immature neural ectoderm via transcriptional repression that is dependent on the C-terminal domain. 2001, Pubmed , Xenbase
White, Maternal control of pattern formation in Xenopus laevis. 2007, Pubmed , Xenbase
Wills, BMP antagonists and FGF signaling contribute to different domains of the neural plate in Xenopus. 2010, Pubmed , Xenbase
Xu, Maternal xNorrin, a canonical Wnt signaling agonist and TGF-β antagonist, controls early neuroectoderm specification in Xenopus. 2012, Pubmed , Xenbase
Yaklichkin, FoxD3 and Grg4 physically interact to repress transcription and induce mesoderm in Xenopus. 2007, Pubmed , Xenbase
Yan, Microarray identification of novel downstream targets of FoxD4L1/D5, a critical component of the neural ectodermal transcriptional network. 2010, Pubmed , Xenbase
Yan, foxD5 plays a critical upstream role in regulating neural ectodermal fate and the onset of neural differentiation. 2009, Pubmed , Xenbase
Yanai, Mapping gene expression in two Xenopus species: evolutionary constraints and developmental flexibility. 2011, Pubmed , Xenbase
Yang, Beta-catenin/Tcf-regulated transcription prior to the midblastula transition. 2002, Pubmed , Xenbase
Zernicka-Goetz, The first cell-fate decisions in the mouse embryo: destiny is a matter of both chance and choice. 2006, Pubmed
Zernicka-Goetz, Cleavage pattern and emerging asymmetry of the mouse embryo. 2005, Pubmed
Zhang, The Sox axis, Nodal signaling, and germ layer specification. 2007, Pubmed , Xenbase
Zhang, The beta-catenin/VegT-regulated early zygotic gene Xnr5 is a direct target of SOX3 regulation. 2003, Pubmed , Xenbase
Zhang, Repression of nodal expression by maternal B1-type SOXs regulates germ layer formation in Xenopus and zebrafish. 2004, Pubmed , Xenbase