XB-ART-36647
Dev Biol
2007 Dec 01;3121:90-102. doi: 10.1016/j.ydbio.2007.09.039.
Show Gene links
Show Anatomy links
The Xenopus Nieuwkoop center and Spemann-Mangold organizer share molecular components and a requirement for maternal Wnt activity.
???displayArticle.abstract???
In Xenopus embryos, the dorso-ventral and antero-posterior axes are established by the Spemann-Mangold organizer. According to the prevalent model of early development, the organizer is induced by the dorsalizing Nieuwkoop signal, which is secreted by the Nieuwkoop center. Formation of the center requires the maternal Wnt pathway, which is active on the dorsal side of embryos. Nevertheless, the molecular nature of the Nieuwkoop signal remains unclear. Since the Nieuwkoop center and the organizer both produce dorsalizing signals in vitro, we asked if they might share molecular components. We find that vegetal explants, the source of Nieuwkoop signal in recombination assays, express a number of organizer genes. The product of one of these genes, chordin, is required for signaling, suggesting that the organizer and the center share at least some molecular components. Furthermore, experiments with whole embryos show that maternal Wnt activity is required in the organizer just as it is needed in the Nieuwkoop center in vitro. We conclude that the maternal Wnt pathway generates the Nieuwkoop center in vitro and the organizer in vivo by activating a common set of genes, without the need of an intermediary signaling step.
???displayArticle.pubmedLink??? 17964564
???displayArticle.pmcLink??? PMC2170525
???displayArticle.link??? Dev Biol
???displayArticle.grants??? [+]
5R01 GM066977 NIGMS NIH HHS , HD40724 NICHD NIH HHS , P30-CA-08784 NCI NIH HHS , R37 GM037432-22 NIGMS NIH HHS , R37 GM374432 NIGMS NIH HHS , R37 GM037432 NIGMS NIH HHS , R01 GM066977 NIGMS NIH HHS , F32 HD040724 NICHD NIH HHS
Species referenced: Xenopus laevis
Genes referenced: cer1 chrd frzb gsc nog sia1 tbxt
???displayArticle.morpholinos??? chrd.1 MO1 chrd.1 MO2
???attribute.lit??? ???displayArticles.show???
|
|
|
|
|
|
|
Fig. 1. Organizer genes are expressed in vegetal pole explants. (A) Double in situ hybridization for chordin (BCIP, blue) and cerberus (BM Purple) in a sectioned stage 10 embryo. The two genes show overlap in endodermal-fated vegetal cells. (B–H) Stage 8.5 embryos were dissected and vegetal pole explants were cultured for 2 h before in situ hybridization for chordin (B, n = 12), cerberus (C, n = 9), gsc (D, n = 12), frzb (E, n = 15), noggin (F, n = 12), and Xbra (H, n = 14). All views are animal, dorsal side is to the right. (G1, 2) Vegetal explants were sectioned sagittally (n = 18), and each half was hybridized in situ for chordin (G1) or Xsox17β (G2). Internal views of the sections, dorsal side up, animal sides facing each other. (G1 + 2) The two halves juxtaposed and viewed from the animal side. (I–K) Timing and FGF-dependency of chordin expression in vegetal explants. (I) Stage 9 explant, immediately after dissection (n = 12). (J, K) Explants after 2 h incubation, in the absence (J, n = 15) or presence (K, n = 11) of the MEK inhibitor U0126, which blocks the FGF pathway. |
|
Fig. 5. Ectopic activation of the Wnt pathway in tier B and C cells induces expression of organizer genes only in injected cells. Double in situ hybridization of stage 9 embryos for the indicated organizer genes (purple) and coinjected LacZ (red). β-catenin (500 pg RNA) and LacZ (1 ng RNA) were injected at the 32 cell stage in the indicated tiers, on the ventral side of the embryo. Panels A, F, and K are dorsal views showing the wild-type expression pattern for Sia, gsc, and chordin, respectively. Activation of the genes in ventral cells is restricted to the injection site. chordin (21 embryos for tier B, 30 embryos for tier C) and Sia (24 embryos for tier B and 19 embryos for tier C) are activated in both tiers B and C (M, O, and C, E, respectively), but gsc (28 embryos for tier B and 22 for tier C) only in tier C (H, J). |
|
Supplementary Fig. S1. |
|
Supplementary Fig. S2. |
|
Supplementary Fig. S3. |
|
Supplementary Fig. S4. |
References [+] :
Agius, Endodermal Nodal-related signals and mesoderm induction in Xenopus. 2000, 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
Behrens, Functional interaction of beta-catenin with the transcription factor LEF-1. 1996, Pubmed , Xenbase
Birsoy, Vg 1 is an essential signaling molecule in Xenopus development. 2006, Pubmed , Xenbase
Blitz, Is chordin a long-range- or short-range-acting factor? Roles for BMP1-related metalloproteases in chordin and BMP4 autofeedback loop regulation. 2000, Pubmed , Xenbase
Boettger, The avian organizer. 2001, Pubmed , Xenbase
Bouwmeester, Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer. 1996, Pubmed , Xenbase
Brannon, Activation of Siamois by the Wnt pathway. 1996, Pubmed , Xenbase
Brannon, A beta-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus. 1997, 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
Cho, Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. 1991, Pubmed , Xenbase
Christian, Xwnt-8, a Xenopus Wnt-1/int-1-related gene responsive to mesoderm-inducing growth factors, may play a role in ventral mesodermal patterning during embryogenesis. 1991, Pubmed , Xenbase
Collart, The novel Smad-interacting protein Smicl regulates Chordin expression in the Xenopus embryo. 2005, Pubmed , Xenbase
Cui, Synergistic effects of Vg1 and Wnt signals in the specification of dorsal mesoderm and endoderm. 1996, Pubmed , Xenbase
Darken, Axis induction by wnt signaling: Target promoter responsiveness regulates competence. 2001, 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, Specification of cell fate in the sea urchin embryo: summary and some proposed mechanisms. 1998, Pubmed
Delaune, Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition. 2005, Pubmed , Xenbase
De Robertis, Dorsal-ventral patterning and neural induction in Xenopus embryos. 2004, Pubmed , Xenbase
De Robertis, The establishment of Spemann's organizer and patterning of the vertebrate embryo. 2000, Pubmed , Xenbase
Ding, Pre-MBT patterning of early gene regulation in Xenopus: the role of the cortical rotation and mesoderm induction. 1998, 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
Funayama, Embryonic axis induction by the armadillo repeat domain of beta-catenin: evidence for intracellular signaling. 1995, Pubmed , Xenbase
Gerhart, Evolution of the organizer and the chordate body plan. 2001, Pubmed
Gerhart, Pieter Nieuwkoop's contributions to the understanding of meso-endoderm induction and neural induction in chordate development. 1999, Pubmed , Xenbase
Gimlich, Cytoplasmic localization and chordamesoderm induction in the frog embryo. 1985, Pubmed , Xenbase
Gimlich, Acquisition of developmental autonomy in the equatorial region of the Xenopus embryo. 1986, Pubmed , Xenbase
Gimlich, Early cellular interactions promote embryonic axis formation in Xenopus laevis. 1984, Pubmed , Xenbase
Guger, beta-Catenin has Wnt-like activity and mimics the Nieuwkoop signaling center in Xenopus dorsal-ventral patterning. 1995, Pubmed , Xenbase
Harland, Formation and function of Spemann's organizer. 1997, Pubmed
He, Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos. 1995, Pubmed , Xenbase
Heasman, Overexpression of cadherins and underexpression of beta-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. 1994, Pubmed , Xenbase
Heasman, Patterning the early Xenopus embryo. 2006, Pubmed , Xenbase
Heasman, Patterning the Xenopus blastula. 1997, Pubmed , Xenbase
Henrique, Expression of a Delta homologue in prospective neurons in the chick. 1995, Pubmed , Xenbase
Houston, Repression of organizer genes in dorsal and ventral Xenopus cells mediated by maternal XTcf3. 2002, Pubmed , Xenbase
Jones, Nodal-related signals induce axial mesoderm and dorsalize mesoderm during gastrulation. 1995, Pubmed , Xenbase
Kageura, Three regions of the 32-cell embryo of Xenopus laevis essential for formation of a complete tadpole. 1995, Pubmed , Xenbase
Kessler, Siamois is required for formation of Spemann's organizer. 1997, Pubmed , Xenbase
Kimelman, Mesoderm induction: from caps to chips. 2006, Pubmed , Xenbase
Kodjabachian, Gastrulation in zebrafish: what mutants teach us. 1999, Pubmed
Kodjabachian, Embryonic induction: is the Nieuwkoop centre a useful concept? , Pubmed , Xenbase
Kofron, Wnt11/beta-catenin signaling in both oocytes and early embryos acts through LRP6-mediated regulation of axin. 2007, Pubmed , Xenbase
Ku, Xwnt-11: a maternally expressed Xenopus wnt gene. 1993, Pubmed , Xenbase
LaBonne, Localization of MAP kinase activity in early Xenopus embryos: implications for endogenous FGF signaling. 1997, Pubmed , Xenbase
Lane, Primitive and definitive blood share a common origin in Xenopus: a comparison of lineage techniques used to construct fate maps. 2002, Pubmed , Xenbase
Laurent, The Xenopus homeobox gene twin mediates Wnt induction of goosecoid in establishment of Spemann's organizer. 1997, 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
Leyns, Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. 1997, Pubmed , Xenbase
Mitchell, The FGFR pathway is required for the trunk-inducing functions of Spemann's organizer. 2001, Pubmed , Xenbase
Molenaar, XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. 1996, Pubmed , Xenbase
Moon, From cortical rotation to organizer gene expression: toward a molecular explanation of axis specification in Xenopus. 1998, Pubmed , Xenbase
Muñoz-Sanjuán, Gene profiling during neural induction in Xenopus laevis: regulation of BMP signaling by post-transcriptional mechanisms and TAB3, a novel TAK1-binding protein. 2002, Pubmed , Xenbase
Nagano, Dorsal induction from dorsal vegetal cells in Xenopus occurs after mid-blastula transition. 2000, Pubmed , Xenbase
Niehrs, Regionally specific induction by the Spemann-Mangold organizer. 2004, Pubmed
Oelgeschläger, Chordin is required for the Spemann organizer transplantation phenomenon in Xenopus embryos. 2003, Pubmed , Xenbase
Pierce, Regulation of Spemann organizer formation by the intracellular kinase Xgsk-3. 1995, Pubmed , Xenbase
Sasai, Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. 1994, Pubmed , Xenbase
Schier, Molecular genetics of axis formation in zebrafish. 2005, Pubmed
Schier, The zebrafish organizer. 1998, Pubmed
Schohl, Beta-catenin, MAPK and Smad signaling during early Xenopus development. 2002, Pubmed , Xenbase
Sive, Housing and Feeding of Xenopus laevis. 2007, Pubmed , Xenbase
Smith, Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. 1991, Pubmed , Xenbase
Smith, Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. 1992, Pubmed , Xenbase
Smith, Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. 1991, Pubmed , Xenbase
Smith, A nodal-related gene defines a physical and functional domain within the Spemann organizer. 1995, Pubmed , Xenbase
Standley, Maternal XTcf1 and XTcf4 have distinct roles in regulating Wnt target genes. 2006, Pubmed , Xenbase
Tao, Maternal wnt11 activates the canonical wnt signaling pathway required for axis formation in Xenopus embryos. 2005, Pubmed , Xenbase
Vodicka, Blastomere derivation and domains of gene expression in the Spemann Organizer of Xenopus laevis. 1995, Pubmed , Xenbase
Vonica, Zygotic Wnt activity is required for Brachyury expression in the early Xenopus laevis embryo. 2002, Pubmed , Xenbase
Vonica, TCF is the nuclear effector of the beta-catenin signal that patterns the sea urchin animal-vegetal axis. 2000, Pubmed , Xenbase
Wang, Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8. 1997, Pubmed , Xenbase
Weaver, Move it or lose it: axis specification in Xenopus. 2004, Pubmed , Xenbase
Wessely, Analysis of Spemann organizer formation in Xenopus embryos by cDNA macroarrays. 2004, Pubmed , Xenbase
Wessely, Neural induction in the absence of mesoderm: beta-catenin-dependent expression of secreted BMP antagonists at the blastula stage in Xenopus. 2001, Pubmed , Xenbase
Wylie, Maternal beta-catenin establishes a 'dorsal signal' in early Xenopus embryos. 1996, Pubmed , Xenbase
Xanthos, The roles of three signaling pathways in the formation and function of the Spemann Organizer. 2002, Pubmed , Xenbase
Yamanaka, A novel homeobox gene, dharma, can induce the organizer in a non-cell-autonomous manner. 1998, Pubmed , Xenbase
Yang, Beta-catenin/Tcf-regulated transcription prior to the midblastula transition. 2002, Pubmed , Xenbase
Yasuo, Role of Goosecoid, Xnot and Wnt antagonists in the maintenance of the notochord genetic programme in Xenopus gastrulae. 2001, Pubmed , Xenbase
Zeng, The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. 1997, Pubmed , Xenbase
Zon, Expression of GATA-binding proteins during embryonic development in Xenopus laevis. 1991, Pubmed , Xenbase
Zorn, Anterior endomesoderm specification in Xenopus by Wnt/beta-catenin and TGF-beta signalling pathways. 1999, Pubmed , Xenbase