XB-ART-56750
Dev Biol
January 1, 2020;
462
(1):
20-35.
Chromatin accessibility and histone acetylation in the regulation of competence in early development.
Abstract
As development proceeds, inductive cues are interpreted by competent tissues in a spatially and temporally restricted manner. While key inductive signaling pathways within competent cells are well-described at a molecular level, the mechanisms by which tissues lose responsiveness to inductive signals are not well understood. Localized activation of Wnt signaling before zygotic gene activation in Xenopus laevis leads to dorsal development, but competence to induce dorsal genes in response to Wnts is lost by the late blastula stage. We hypothesize that loss of competence is mediated by changes in histone modifications leading to a loss of chromatin accessibility at the promoters of Wnt target genes. We use ATAC-seq to evaluate genome-wide changes in chromatin accessibility across several developmental stages. Based on overlap with p300 binding, we identify thousands of putative cis-regulatory elements at the gastrula stage, including sites that lose accessibility by the end of gastrulation and are enriched for pluripotency factor binding motifs. Dorsal Wnt target gene promoters are not accessible after the loss of competence in the early gastrula while genes involved in mesoderm and neural crest development maintain accessibility at their promoters. Inhibition of histone deacetylases increases acetylation at the promoters of dorsal Wnt target genes and extends competence for dorsal gene induction by Wnt signaling. Histone deacetylase inhibition, however, is not sufficient to extend competence for mesoderm or neural crest induction. These data suggest that chromatin state regulates the loss of competence to inductive signals in a context-dependent manner.
PubMed ID: 32119833
PMC ID: PMC7225061
Article link: Dev Biol
Grant support: [+]
R01 GM111816 NIGMS NIH HHS , R35 GM131810 NIGMS NIH HHS , R01 GM115517 NIGMS NIH HHS , R01 HL141759 NHLBI NIH HHS , R01 GM132438 NIGMS NIH HHS , T32 HL007439 NHLBI NIH HHS , T32 GM007170 NIGMS NIH HHS , F31 GM116588 NIGMS NIH HHS
Species referenced: Xenopus laevis
Genes referenced: 1a11 axin2 barhl2 cdx2 chrd.1 crebbp gsc hoxa1 hoxd1 jarid2 lefty myod1 nodal3.1 pax3 pou3f2 pou5f3.1 pou5f3.2 pou5f3.3 sia1 sia2 snai1 snai2 tbxt tcf3 twist1 vegt wnt5b wnt8a
Antibodies: H3f3a Ab24 H3f3a Ab26 H3f3a Ab39 IgG Ab1
GEO Series: GSE138905: Xenbase, NCBI
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Bae, Siamois and Twin are redundant and essential in formation of the Spemann organizer. 2011, Pubmed , Xenbase
Beisel, Silencing chromatin: comparing modes and mechanisms. 2011, Pubmed
Blythe, Chromatin immunoprecipitation in early Xenopus laevis embryos. 2009, Pubmed , Xenbase
Blythe, beta-Catenin primes organizer gene expression by recruiting a histone H3 arginine 8 methyltransferase, Prmt2. 2010, Pubmed , Xenbase
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Bright, Assay for Transposase-Accessible Chromatin-Sequencing Using Xenopus Embryos. 2020, Pubmed , Xenbase
Buenrostro, Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. 2014, Pubmed
Cadigan, TCFs and Wnt/β-catenin signaling: more than one way to throw the switch. 2012, Pubmed
Cao, High-resolution mapping of h1 linker histone variants in embryonic stem cells. 2013, Pubmed
Cao, Xenopus POU factors of subclass V inhibit activin/nodal signaling during gastrulation. 2007, 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, Wnt5a and Wnt11 interact in a maternal Dkk1-regulated fashion to activate both canonical and non-canonical signaling in Xenopus axis formation. 2009, Pubmed , Xenbase
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Darken, Axis induction by wnt signaling: Target promoter responsiveness regulates competence. 2001, Pubmed , Xenbase
De Robertis, The establishment of Spemann's organizer and patterning of the vertebrate embryo. 2001, Pubmed , Xenbase
Ding, Spemann organizer transcriptome induction by early beta-catenin, Wnt, Nodal, and Siamois signals in Xenopus laevis. 2018, Pubmed , Xenbase
Elurbe, Regulatory remodeling in the allo-tetraploid frog Xenopus laevis. 2018, Pubmed , Xenbase
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Gao, A novel role for Ascl1 in the regulation of mesendoderm formation via HDAC-dependent antagonism of VegT. 2016, Pubmed , Xenbase
Gentsch, Maternal pluripotency factors initiate extensive chromatin remodelling to predefine first response to inductive signals. 2020, Pubmed , Xenbase
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Gupta, Developmental enhancers are marked independently of zygotic Nodal signals in Xenopus. 2014, Pubmed , Xenbase
Gurdon, Activation of muscle-specific actin genes in Xenopus development by an induction between animal and vegetal cells of a blastula. 1985, Pubmed , Xenbase
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Happel, Histone H1 and its isoforms: contribution to chromatin structure and function. 2009, Pubmed
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Hecht, The p300/CBP acetyltransferases function as transcriptional coactivators of beta-catenin in vertebrates. 2000, Pubmed , Xenbase
Heinz, Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. 2010, Pubmed
Henig, A POU protein regulates mesodermal competence to FGF in Xenopus. 1998, Pubmed , Xenbase
Herberg, Histone H3 lysine 9 trimethylation is required for suppressing the expression of an embryonically activated retrotransposon in Xenopus laevis. 2016, Pubmed , Xenbase
Hontelez, Embryonic transcription is controlled by maternally defined chromatin state. 2016, Pubmed , Xenbase
Hoppler, Expression of a dominant-negative Wnt blocks induction of MyoD in Xenopus embryos. 1997, Pubmed , Xenbase
Houston, Repression of organizer genes in dorsal and ventral Xenopus cells mediated by maternal XTcf3. 2002, Pubmed , Xenbase
Huang, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. 2009, Pubmed
Ishibashi, Expression of Siamois and Twin in the blastula Chordin/Noggin signaling center is required for brain formation in Xenopus laevis embryos. 2008, Pubmed , Xenbase
Jacobs, The transcription factor Grainy head primes epithelial enhancers for spatiotemporal activation by displacing nucleosomes. 2019, Pubmed
Kao, Lithium-induced respecification of pattern in Xenopus laevis embryos. 2009, Pubmed , Xenbase
Kao, The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. 1988, Pubmed , Xenbase
Karimi, Xenbase: a genomic, epigenomic and transcriptomic model organism database. 2019, Pubmed , Xenbase
Kengaku, Basic fibroblast growth factor induces differentiation of neural tube and neural crest lineages of cultured ectoderm cells from Xenopus gastrula. 1994, Pubmed , Xenbase
Kessler, Siamois is required for formation of Spemann's organizer. 1998, Pubmed , Xenbase
Kim, Two-Element Transcriptional Regulation in the Canonical Wnt Pathway. 2018, Pubmed , Xenbase
Kjolby, Genome-wide identification of Wnt/β-catenin transcriptional targets during Xenopus gastrulation. 2017, Pubmed , Xenbase
Kodjabachian, Siamois functions in the early blastula to induce Spemann's organiser. 2002, Pubmed , Xenbase
Lamb, Neural induction by the secreted polypeptide noggin. 1993, Pubmed , Xenbase
Laurent, The Xenopus homeobox gene twin mediates Wnt induction of goosecoid in establishment of Spemann's organizer. 1998, Pubmed , Xenbase
Lee, Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition. 2014, Pubmed
Leichsenring, Pou5f1 transcription factor controls zygotic gene activation in vertebrates. 2013, Pubmed , Xenbase
Lemaire, Expression cloning of Siamois, a Xenopus homeobox gene expressed in dorsal-vegetal cells of blastulae and able to induce a complete secondary axis. 1995, Pubmed , Xenbase
Levy, The competence of marginal zone cells to become Spemann's organizer is controlled by Xcad2. 2002, Pubmed , Xenbase
Liao, featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. 2014, Pubmed
Livigni, A conserved Oct4/POUV-dependent network links adhesion and migration to progenitor maintenance. 2014, Pubmed , Xenbase
Love, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. 2015, Pubmed
Lu, Identification and mechanism of regulation of the zebrafish dorsal determinant. 2011, Pubmed
Mancilla, Neural crest formation in Xenopus laevis: mechanisms of Xslug induction. 1996, Pubmed , Xenbase
Matsukawa, The requirement of histone modification by PRDM12 and Kdm4a for the development of pre-placodal ectoderm and neural crest in Xenopus. 2015, Pubmed , Xenbase
McDaniel, Continued Activity of the Pioneer Factor Zelda Is Required to Drive Zygotic Genome Activation. 2019, Pubmed
Moon, From cortical rotation to organizer gene expression: toward a molecular explanation of axis specification in Xenopus. 1998, Pubmed , Xenbase
Nakamura, Tissue- and stage-specific Wnt target gene expression is controlled subsequent to β-catenin recruitment to cis-regulatory modules. 2017, Pubmed , Xenbase
Paraiso, Endodermal Maternal Transcription Factors Establish Super-Enhancers during Zygotic Genome Activation. 2020, Pubmed , Xenbase
Park, Kaiso/p120-catenin and TCF/beta-catenin complexes coordinately regulate canonical Wnt gene targets. 2005, Pubmed , Xenbase
Peng, Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. 2010, Pubmed , Xenbase
Perino, Chromatin Control of Developmental Dynamics and Plasticity. 2017, Pubmed
Piccolo, Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. 1996, Pubmed , Xenbase
Ramakrishnan, The Wnt Transcriptional Switch: TLE Removal or Inactivation? 2019, Pubmed
Rao, Histone deacetylase activity has an essential role in establishing and maintaining the vertebrate neural crest. 2018, Pubmed , Xenbase
Robinson, Integrative genomics viewer. 2011, Pubmed
Rosa, Mesoderm induction in amphibians: the role of TGF-beta 2-like factors. 1988, Pubmed , Xenbase
Ruzov, The interaction of xKaiso with xTcf3: a revised model for integration of epigenetic and Wnt signalling pathways. 2009, Pubmed , Xenbase
Saint-Jeannet, Regulation of dorsal fate in the neuraxis by Wnt-1 and Wnt-3a. 1998, Pubmed , Xenbase
Schneider, Stage-specific histone modification profiles reveal global transitions in the Xenopus embryonic epigenome. 2011, Pubmed , Xenbase
Schneider, Beta-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. 1997, Pubmed , Xenbase
Schohl, Beta-catenin, MAPK and Smad signaling during early Xenopus development. 2002, Pubmed , Xenbase
Sena, Barhl2 maintains T cell factors as repressors and thereby switches off the Wnt/β-Catenin response driving Spemann organizer formation. 2020, Pubmed , Xenbase
Session, Genome evolution in the allotetraploid frog Xenopus laevis. 2016, Pubmed , Xenbase
Shahbazian, Functions of site-specific histone acetylation and deacetylation. 2007, Pubmed
Shiomi, Histone H3 Lysine 27 Trimethylation Leads to Loss of Mesendodermal Competence During Gastrulation in Zebrafish Ectodermal Cells. 2017, Pubmed , Xenbase
Skirkanich, An essential role for transcription before the MBT in Xenopus laevis. 2011, Pubmed , Xenbase
Slack, Mesoderm induction in early Xenopus embryos by heparin-binding growth factors. 1987, Pubmed , Xenbase
Smith, A nodal-related gene defines a physical and functional domain within the Spemann organizer. 1995, Pubmed , Xenbase
Sokol, Wnt signaling and dorso-ventral axis specification in vertebrates. 1999, Pubmed
Sokol, A mouse macrophage factor induces head structures and organizes a body axis in Xenopus. 1990, Pubmed , Xenbase
Starks, Combined analysis of dissimilar promoter accessibility and gene expression profiles identifies tissue-specific genes and actively repressed networks. 2019, Pubmed
Steinbach, Temporal restriction of MyoD induction and autocatalysis during Xenopus mesoderm formation. 1998, Pubmed , Xenbase
Sudarwati, Mesoderm formation in the anuranXenopus laevis (Daudin). 2019, Pubmed
Tao, Maternal wnt11 activates the canonical wnt signaling pathway required for axis formation in Xenopus embryos. 2005, Pubmed , Xenbase
Tien, Snail2/Slug cooperates with Polycomb repressive complex 2 (PRC2) to regulate neural crest development. 2015, Pubmed , Xenbase
Wu, Neural crest induction by the canonical Wnt pathway can be dissociated from anterior-posterior neural patterning in Xenopus. 2005, Pubmed , Xenbase
Wu, Wnt-frizzled signaling in neural crest formation. 2003, Pubmed
Yan, Maternal Huluwa dictates the embryonic body axis through β-catenin in vertebrates. 2019, Pubmed , Xenbase
Yang, Beta-catenin/Tcf-regulated transcription prior to the midblastula transition. 2003, Pubmed , Xenbase
Yang-Snyder, A frizzled homolog functions in a vertebrate Wnt signaling pathway. 1997, Pubmed , Xenbase
Zaret, Developmental competence of the gut endoderm: genetic potentiation by GATA and HNF3/fork head proteins. 1999, Pubmed
Asashima, Mesodermal induction in early amphibian embryos by activin A (erythroid differentiation factor). 2020, Pubmed , Xenbase
Aybar, Early induction of neural crest cells: lessons learned from frog, fish and chick. 2003, Pubmed , Xenbase
Bae, Siamois and Twin are redundant and essential in formation of the Spemann organizer. 2011, Pubmed , Xenbase
Beisel, Silencing chromatin: comparing modes and mechanisms. 2011, Pubmed
Blythe, Chromatin immunoprecipitation in early Xenopus laevis embryos. 2009, Pubmed , Xenbase
Blythe, beta-Catenin primes organizer gene expression by recruiting a histone H3 arginine 8 methyltransferase, Prmt2. 2010, Pubmed , Xenbase
Brannon, A beta-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus. 1997, Pubmed , Xenbase
Bright, Assay for Transposase-Accessible Chromatin-Sequencing Using Xenopus Embryos. 2020, Pubmed , Xenbase
Buenrostro, Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. 2014, Pubmed
Cadigan, TCFs and Wnt/β-catenin signaling: more than one way to throw the switch. 2012, Pubmed
Cao, High-resolution mapping of h1 linker histone variants in embryonic stem cells. 2013, Pubmed
Cao, Xenopus POU factors of subclass V inhibit activin/nodal signaling during gastrulation. 2007, 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, Wnt5a and Wnt11 interact in a maternal Dkk1-regulated fashion to activate both canonical and non-canonical signaling in Xenopus axis formation. 2009, Pubmed , Xenbase
Charney, Foxh1 Occupies cis-Regulatory Modules Prior to Dynamic Transcription Factor Interactions Controlling the Mesendoderm Gene Program. 2017, Pubmed , Xenbase
Christian, Interactions between Xwnt-8 and Spemann organizer signaling pathways generate dorsoventral pattern in the embryonic mesoderm of Xenopus. 1993, Pubmed , Xenbase
Dale, Mesoderm induction in Xenopus laevis: a quantitative study using a cell lineage label and tissue-specific antibodies. 1986, Pubmed , Xenbase
Darken, Axis induction by wnt signaling: Target promoter responsiveness regulates competence. 2001, Pubmed , Xenbase
De Robertis, The establishment of Spemann's organizer and patterning of the vertebrate embryo. 2001, Pubmed , Xenbase
Ding, Spemann organizer transcriptome induction by early beta-catenin, Wnt, Nodal, and Siamois signals in Xenopus laevis. 2018, Pubmed , Xenbase
Elurbe, Regulatory remodeling in the allo-tetraploid frog Xenopus laevis. 2018, Pubmed , Xenbase
Fagotto, Induction of the primary dorsalizing center in Xenopus by the Wnt/GSK/beta-catenin signaling pathway, but not by Vg1, Activin or Noggin. 1997, Pubmed , Xenbase
Fredieu, Xwnt-8 and lithium can act upon either dorsal mesodermal or neurectodermal cells to cause a loss of forebrain in Xenopus embryos. 1997, Pubmed , Xenbase
Gao, A novel role for Ascl1 in the regulation of mesendoderm formation via HDAC-dependent antagonism of VegT. 2016, Pubmed , Xenbase
Gentsch, Maternal pluripotency factors initiate extensive chromatin remodelling to predefine first response to inductive signals. 2020, Pubmed , Xenbase
Green, The biological effects of XTC-MIF: quantitative comparison with Xenopus bFGF. 1990, Pubmed , Xenbase
Gupta, Developmental enhancers are marked independently of zygotic Nodal signals in Xenopus. 2014, Pubmed , Xenbase
Gurdon, Activation of muscle-specific actin genes in Xenopus development by an induction between animal and vegetal cells of a blastula. 1985, Pubmed , Xenbase
Hamilton, Difference in XTcf-3 dependency accounts for change in response to beta-catenin-mediated Wnt signalling in Xenopus blastula. 2001, Pubmed , Xenbase
Happel, Histone H1 and its isoforms: contribution to chromatin structure and function. 2009, Pubmed
Heasman, Beta-catenin signaling activity dissected in the early Xenopus embryo: a novel antisense approach. 2000, Pubmed , Xenbase
Hecht, The p300/CBP acetyltransferases function as transcriptional coactivators of beta-catenin in vertebrates. 2000, Pubmed , Xenbase
Heinz, Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. 2010, Pubmed
Henig, A POU protein regulates mesodermal competence to FGF in Xenopus. 1998, Pubmed , Xenbase
Herberg, Histone H3 lysine 9 trimethylation is required for suppressing the expression of an embryonically activated retrotransposon in Xenopus laevis. 2016, Pubmed , Xenbase
Hontelez, Embryonic transcription is controlled by maternally defined chromatin state. 2016, Pubmed , Xenbase
Hoppler, Expression of a dominant-negative Wnt blocks induction of MyoD in Xenopus embryos. 1997, Pubmed , Xenbase
Houston, Repression of organizer genes in dorsal and ventral Xenopus cells mediated by maternal XTcf3. 2002, Pubmed , Xenbase
Huang, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. 2009, Pubmed
Ishibashi, Expression of Siamois and Twin in the blastula Chordin/Noggin signaling center is required for brain formation in Xenopus laevis embryos. 2008, Pubmed , Xenbase
Jacobs, The transcription factor Grainy head primes epithelial enhancers for spatiotemporal activation by displacing nucleosomes. 2019, Pubmed
Kao, Lithium-induced respecification of pattern in Xenopus laevis embryos. 2009, Pubmed , Xenbase
Kao, The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. 1988, Pubmed , Xenbase
Karimi, Xenbase: a genomic, epigenomic and transcriptomic model organism database. 2019, Pubmed , Xenbase
Kengaku, Basic fibroblast growth factor induces differentiation of neural tube and neural crest lineages of cultured ectoderm cells from Xenopus gastrula. 1994, Pubmed , Xenbase
Kessler, Siamois is required for formation of Spemann's organizer. 1998, Pubmed , Xenbase
Kim, Two-Element Transcriptional Regulation in the Canonical Wnt Pathway. 2018, Pubmed , Xenbase
Kjolby, Genome-wide identification of Wnt/β-catenin transcriptional targets during Xenopus gastrulation. 2017, Pubmed , Xenbase
Kodjabachian, Siamois functions in the early blastula to induce Spemann's organiser. 2002, Pubmed , Xenbase
Lamb, Neural induction by the secreted polypeptide noggin. 1993, Pubmed , Xenbase
Laurent, The Xenopus homeobox gene twin mediates Wnt induction of goosecoid in establishment of Spemann's organizer. 1998, Pubmed , Xenbase
Lee, Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition. 2014, Pubmed
Leichsenring, Pou5f1 transcription factor controls zygotic gene activation in vertebrates. 2013, Pubmed , Xenbase
Lemaire, Expression cloning of Siamois, a Xenopus homeobox gene expressed in dorsal-vegetal cells of blastulae and able to induce a complete secondary axis. 1995, Pubmed , Xenbase
Levy, The competence of marginal zone cells to become Spemann's organizer is controlled by Xcad2. 2002, Pubmed , Xenbase
Liao, featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. 2014, Pubmed
Livigni, A conserved Oct4/POUV-dependent network links adhesion and migration to progenitor maintenance. 2014, Pubmed , Xenbase
Love, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. 2015, Pubmed
Lu, Identification and mechanism of regulation of the zebrafish dorsal determinant. 2011, Pubmed
Mancilla, Neural crest formation in Xenopus laevis: mechanisms of Xslug induction. 1996, Pubmed , Xenbase
Matsukawa, The requirement of histone modification by PRDM12 and Kdm4a for the development of pre-placodal ectoderm and neural crest in Xenopus. 2015, Pubmed , Xenbase
McDaniel, Continued Activity of the Pioneer Factor Zelda Is Required to Drive Zygotic Genome Activation. 2019, Pubmed
Moon, From cortical rotation to organizer gene expression: toward a molecular explanation of axis specification in Xenopus. 1998, Pubmed , Xenbase
Nakamura, Tissue- and stage-specific Wnt target gene expression is controlled subsequent to β-catenin recruitment to cis-regulatory modules. 2017, Pubmed , Xenbase
Paraiso, Endodermal Maternal Transcription Factors Establish Super-Enhancers during Zygotic Genome Activation. 2020, Pubmed , Xenbase
Park, Kaiso/p120-catenin and TCF/beta-catenin complexes coordinately regulate canonical Wnt gene targets. 2005, Pubmed , Xenbase
Peng, Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. 2010, Pubmed , Xenbase
Perino, Chromatin Control of Developmental Dynamics and Plasticity. 2017, Pubmed
Piccolo, Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. 1996, Pubmed , Xenbase
Ramakrishnan, The Wnt Transcriptional Switch: TLE Removal or Inactivation? 2019, Pubmed
Rao, Histone deacetylase activity has an essential role in establishing and maintaining the vertebrate neural crest. 2018, Pubmed , Xenbase
Robinson, Integrative genomics viewer. 2011, Pubmed
Rosa, Mesoderm induction in amphibians: the role of TGF-beta 2-like factors. 1988, Pubmed , Xenbase
Ruzov, The interaction of xKaiso with xTcf3: a revised model for integration of epigenetic and Wnt signalling pathways. 2009, Pubmed , Xenbase
Saint-Jeannet, Regulation of dorsal fate in the neuraxis by Wnt-1 and Wnt-3a. 1998, Pubmed , Xenbase
Schneider, Stage-specific histone modification profiles reveal global transitions in the Xenopus embryonic epigenome. 2011, Pubmed , Xenbase
Schneider, Beta-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. 1997, Pubmed , Xenbase
Schohl, Beta-catenin, MAPK and Smad signaling during early Xenopus development. 2002, Pubmed , Xenbase
Sena, Barhl2 maintains T cell factors as repressors and thereby switches off the Wnt/β-Catenin response driving Spemann organizer formation. 2020, Pubmed , Xenbase
Session, Genome evolution in the allotetraploid frog Xenopus laevis. 2016, Pubmed , Xenbase
Shahbazian, Functions of site-specific histone acetylation and deacetylation. 2007, Pubmed
Shiomi, Histone H3 Lysine 27 Trimethylation Leads to Loss of Mesendodermal Competence During Gastrulation in Zebrafish Ectodermal Cells. 2017, Pubmed , Xenbase
Skirkanich, An essential role for transcription before the MBT in Xenopus laevis. 2011, Pubmed , Xenbase
Slack, Mesoderm induction in early Xenopus embryos by heparin-binding growth factors. 1987, Pubmed , Xenbase
Smith, A nodal-related gene defines a physical and functional domain within the Spemann organizer. 1995, Pubmed , Xenbase
Sokol, Wnt signaling and dorso-ventral axis specification in vertebrates. 1999, Pubmed
Sokol, A mouse macrophage factor induces head structures and organizes a body axis in Xenopus. 1990, Pubmed , Xenbase
Starks, Combined analysis of dissimilar promoter accessibility and gene expression profiles identifies tissue-specific genes and actively repressed networks. 2019, Pubmed
Steinbach, Temporal restriction of MyoD induction and autocatalysis during Xenopus mesoderm formation. 1998, Pubmed , Xenbase
Sudarwati, Mesoderm formation in the anuranXenopus laevis (Daudin). 2019, Pubmed
Tao, Maternal wnt11 activates the canonical wnt signaling pathway required for axis formation in Xenopus embryos. 2005, Pubmed , Xenbase
Tien, Snail2/Slug cooperates with Polycomb repressive complex 2 (PRC2) to regulate neural crest development. 2015, Pubmed , Xenbase
Wu, Neural crest induction by the canonical Wnt pathway can be dissociated from anterior-posterior neural patterning in Xenopus. 2005, Pubmed , Xenbase
Wu, Wnt-frizzled signaling in neural crest formation. 2003, Pubmed
Yan, Maternal Huluwa dictates the embryonic body axis through β-catenin in vertebrates. 2019, Pubmed , Xenbase
Yang, Beta-catenin/Tcf-regulated transcription prior to the midblastula transition. 2003, Pubmed , Xenbase
Yang-Snyder, A frizzled homolog functions in a vertebrate Wnt signaling pathway. 1997, Pubmed , Xenbase
Zaret, Developmental competence of the gut endoderm: genetic potentiation by GATA and HNF3/fork head proteins. 1999, Pubmed