Cited by 263Wnt/β-catenin signaling in development and cancerDevelopmental Biology and Gene RegulationPlanarian Biology and Electrostimulation

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Frizzled-7 signalling controls tissue separation during Xenopus gastrulation

Winklbauer, Rudolf, Medina, Araceli, Swain, Rajeeb K., Steinbeisser, Herbert·2001·Nature

DOI 10.1038/35101621

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Abstract

Cell signalling through Frizzled receptors has evolved to considerable complexity within the metazoans. The Frizzled-dependent signalling cascade comprises several branches, whose differential activation depends on specific Wnt ligands, Frizzled receptor isoforms and the cellular context. In Xenopus laevis embryos, the canonical beta-catenin pathway contributes to the establishment of the dorsal-ventral axis. A different branch, referred to as the planar cell polarity pathway, is essential for cell polarization during elongation of the axial mesoderm by convergent extension. Here we demonstrate that a third branch of the cascade is independent of Dishevelled function and involves signalling through trimeric G proteins and protein kinase C (PKC). During gastrulation, Frizzled-7 (Fz7)-dependent PKC signalling controls cell-sorting behaviour in the mesoderm. Loss of zygotic Fz7 function results in the inability of involuted anterior mesoderm to separate from the ectoderm, which leads to severe gastrulation defects. This result provides a developmentally relevant in vivo function for the Fz/PKC pathway in vertebrates.

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Wnt11 controls cell contact persistence by local accumulation of Frizzled 7 at the plasma membrane
Witzel, S., Zimyanin, V. L., Carreira-Barbosa, F., Tada, M., & Heisenberg, C. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200606017 · Cited by 130
“Additionally, “knocking down” the presumed Wnt11 receptor Frizzled 7 (Fz7) in X. laevis embryos causes defects in germ layer separation at the onset of gastrulation (Winklbauer et al., 2001).”
BackgroundInfluential
Wnt signaling during development of the gastrointestinal tract
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“Wnt11, Wnt5b, and Fz7 have all been shown to signal through the planar polarity pathway (Djiane et al., 2000; Heisenberg et al., 2000; Pandur et al., 2002; Tada and Smith, 2000; Winklbauer et al., 2001).”
The Atypical Cadherin Flamingo Links Frizzled and Notch Signaling in Planar Polarity Establishment in the Drosophila Eye
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Daple is a novel non-receptor GEF required for trimeric G protein activation in Wnt signaling
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“Other Wnts, for example, Wnt5a deviate from this canonical paradigm, and trigger so-called non-canonical pathways (Kühl et al., 2000; Niehrs, 2001; Winklbauer et al., 2001).”
Background
Xenopus paraxial protocadherin has signaling functions and is involved in tissue separation
Medina, A., Swain, R. K., Kuerner, K., & Steinbeißer, H. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600329 · Cited by 122
“Injection of Xfz7 alone induced separation behavior in only 30% of the explants (Winklbauer et al, 2001).”
MethodInfluentialSelf-citation
Guidance of mesoderm cell migration in theXenopusgastrula requires PDGF signaling
Nagel, M., Tahinci, E., Symes, K., & Winklbauer, R. (2004) · Development · doi:10.1242/dev.01141 · Cited by 115
“Moreover, similar phenotypes are obtained when migration is blocked by FN antibodies (Ramos and DeSimone, 1996), or when the shear between BCR and mesoderm is mechanically alleviated by the fusion of the two layers (Winklbauer et al., 2001).”
BackgroundSelf-citation
Frodo interacts with Dishevelled to transduce Wnt signals
Gloy, J., Hikasa, H., & Sokol, S. Y. (2002) · Nature Cell Biology · doi:10.1038/ncb784 · Cited by 114
“As a Dsh-interacting protein, Frodo may also be involved in Wnt/Dsh signalling to other targets, including the control of morphogenetic movements or cell adhesion in Xenopus embryo”
Zebrafish Gastrulation: Cell Movements, Signals, and Mechanisms
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Non-canonical Wnt signaling in Xenopus: regulation of axis formation and gastrulation
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Association of Dishevelled with Eph tyrosine kinase receptor and ephrin mediates cell repulsion
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Essential roles of Gα12/13 signaling in distinct cell behaviors driving zebrafish convergence and extension gastrulation movements
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BackgroundInfluential
PCP effector gene Inturned is an important regulator of cilia formation and embryonic development in mammals
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A Novel Set of Wnt-Frizzled Fusion Proteins Identifies Receptor Components That Activate β-Catenin-dependent Signaling
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“1 with RNA encoding Xfz7 ΔC , a mutant non-canonical Wnt receptor lacking the cytoplasmic tail that includes the Xdsh binding sit”
Method
Profilin is an effector for Daam1 in non-canonical Wnt signaling and is required for vertebrate gastrulation
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“Profilin is an evolutionarily conserved actin binding protein that is involved in actin polymerization (Watanabe and Higashida, 2004; Witke, 2004).”
BackgroundResultInfluential
RACK1 is a novel interaction partner of PTK7 that is required for neural tube closure
Wehner, P., Shnitsar, I., Urlaub, H., & Borchers, A. (2011) · Development · doi:10.1242/dev.056291 · Cited by 100
“, 1996), DSH-myc (Sokol, 1996), FZ7-myc (Winklbauer et al., 2001), PKC1-GFP (Sivak et al.”
Method
Gene expression analysis in human osteoblasts exposed to dexamethasone identifies altered developmental pathways as putative drivers of osteoporosis
Hurson, C. J., Butler, J. S., Keating, D., Murray, D. W., Sadlier, D. M., O’Byrne, J., & Doran, P. (2007) · BMC Musculoskeletal Disorders · doi:10.1186/1471-2474-8-12 · Cited by 100
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“(Wacker et al., 2000; Winklbauer et al., 2001).”
Background
Waif1/5T4 Inhibits Wnt/β-Catenin Signaling and Activates Noncanonical Wnt Pathways by Modifying LRP6 Subcellular Localization
Kagermeier-Schenk, B., Wehner, D., Özhan, G., Yamamoto, H., Li, J., Kirchner, K., Hoffmann, C., Stern, P. L., Kikuchi, A., Schambony, A., et al. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.10.015 · Cited by 99
Noncanonical Wnt Signaling Orchestrates Early Developmental Events toward Hematopoietic Cell Fate from Human Embryonic Stem Cells
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“This was consistent with observations in the developing mouse embryo, in which unique changes in the Fzd7 expression were induced upon Wnt11 exposure and were reflective of morphogenesis (Djiane et al., 2000; Winklbauer et al., 2001).”
BackgroundResult
Cell Sorting in Development
Krens, G., & Heisenberg, C. (2011) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-385065-2.00006-2 · Cited by 91
chongmaguereveals an essential role for laminin-mediated boundary formation in chordate convergence and extension movements
Veeman, M. T., Nakatani, Y., Hendrickson, C., Ericson, V. R., Lin, C., & Smith, W. C. (2007) · Development · doi:10.1242/dev.010892 · Cited by 91
“Tissue separation defects have also been described in Xenopus and zebrafish embryos with perturbed non-canonical Wnt/PCP signaling (Ulrich et al., 2003; Winklbauer et al., 2001).”
Background
Nuclear signaling from cadherin adhesion complexes
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Frizzled7: A Promising Achilles’ Heel for Targeting the Wnt Receptor Complex to Treat Cancer
Phesse, T. J., Flanagan, D. J., & Vincan, E. (2016) · Cancers · doi:10.3390/cancers8050050 · Cited by 93
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BackgroundInfluential
Mechanisms of boundary formation by Eph receptor and ephrin signaling
Cayuso, J., Xu, Q., & Wilkinson, D. G. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.11.013 · Cited by 87
“During this translocation, mesoderm cells come into direct contact with ectoderm cells but mixing is prevented by a mechanism involving non-canonical Wnt signaling and activation of RhoA and Rho kinase (Chung et al., 2007; Winklbauer et al., 2001).”
Background
Back and forth between cell fate specification and movement during vertebrate gastrulation
Heisenberg, C., & Solnica‐Krezel, L. (2008) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2008.07.011 · Cited by 86
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“This phenotype is indistinguishable from that seen in the tadpoles in which gastrulation movements are specifically impaired (Sokol, 1996; Deardorff et al, 1998; Djiane et al, 2000; Tada and Smith, 2000; Winklbauer et al, 2001).”
Flamingo regulates epiboly and convergence/extension movements through cell cohesive and signalling functions during zebrafish gastrulation
Carreira-Barbosa, F., Kajita, M., Morel, V., Wada, H., Okamoto, H., Arias, A. M., Fujita, Y., Wilson, S. W., & Tada, M. (2008) · Development · doi:10.1242/dev.026542 · Cited by 89
“Early stages of zebrafish eye formation require the coordinated activity of Wnt11, Fz5, and the Wnt/betacatenin pathway.”
Influential
Activation of Gβγ signaling downstream of Wnt-11/Xfz7 regulates Cdc42 activity during Xenopus gastrulation
Penzo‐Méndez, A., Umbhauer, M., Djiane, A., Boucaut, J., & Riou, J. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00067-8 · Cited by 89
“Depletion of Xfz7 encoded by one of the two Xfz7 pseudoalleles is sufficient to cause isolated mesendodermal tissue to mix with blastocoel roof, instead of remaining separated (Winklbauer et al., 2001).”
BackgroundInfluential
MicroRNAs Are Involved in the Regulation of Ovary Development in the Pathogenic Blood Fluke Schistosoma japonicum
Zhu, L., Zhao, J., Wang, J., Hu, C., Peng, J., Luo, R., Zhou, C., Liu, J., Lin, J., Jin, Y., et al. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005423 · Cited by 83
Endothelial Cells Stimulate T Cell NFAT Nuclear Translocation in the Presence of Cyclosporin A: Involvement of the wnt/Glycogen Synthase Kinase-3β Pathway
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Background
Frizzled7 mediates canonical Wnt signaling in neural crest induction
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BackgroundMethodInfluential
Organising cells into tissues: new roles for cell adhesion molecules in planar cell polarity
Saburi, S., & McNeill, H. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2005.08.011 · Cited by 76
Ca2+ signaling and early embryonic patterning during the Blastula and Gastrula Periods of Zebrafish and Xenopus development
Webb, S., & Miller, A. L. (2006) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2006.08.004 · Cited by 74
“[77] demonstrated that when the function of the zygotic Frizzled-7 was inhibited, the normal separation that occurs between the involuted anterior mesoderm and the ectoderm was blocked, but convergent extension was not affected.”
Background
Comparative transcriptional profiling of two human embryonic stem cell lines
Rao, R. R., Calhoun, J. D., Qin, X., Rekaya, R., Clark, J. K., & Stice, S. L. (2004) · Biotechnology and Bioengineering · doi:10.1002/bit.20245 · Cited by 72
“For example, Fzd7 has been shown to be involved in tissue separation during gastrulation (Winklbauer et al., 2001 ).”
Background

Authors: Winklbauer, R., Medina, A., Swain, R. K., & Steinbeisser, H.
Affiliations: Max Planck Institute for Developmental Biology (DE)
ORCID: Winklbauer, Rudolf
Swain, Rajeeb K.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2001-10
Volume: 413
Issue: 6858
Pages: 856-860
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/35101621
OpenAlex: W1664587663
Cited by: 263
References: 21
Citations by year: 2026: 3 · 2025: 1 · 2023: 2 · 2022: 5 · 2021: 3 · 2020: 3 · 2019: 4 · 2018: 5 · 2017: 7 · 2016: 9 · 2015: 8 · 2014: 8 · 2013: 5 · 2012: 11
FWCI: 8.96
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Planarian Biology and Electrostimulation
Keywords: Frizzled-7, Wnt signaling, gastrulation, Xenopus laevis, protein kinase C, trimeric G proteins, cell sorting, mesoderm, ectoderm, planar cell polarity, convergent extension, dorsal-ventral axis, β-catenin signaling
MeSH terms: Animals, Cytoskeletal Proteins, Embryo, Nonmammalian, Fibroblast Growth Factors, Gastrula, Mesoderm, Morphogenesis, Protein Kinase C, Receptors, Cell Surface, Xenopus laevis, Signal Transduction, Trans-Activators, Gene Expression, Oligonucleotides, Antisense, Cell Polarity, GTP-Binding Proteins, Xenopus Proteins, Receptors, G-Protein-Coupled, beta Catenin

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Frizzled-7 signalling controls tissue separation during Xenopus gastrulation

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