Wnt11b Is Involved in Cilia-Mediated Symmetry Breakage during Xenopus Left-Right Development

Walentek, Peter; Schneider, Isabelle; Schweickert, Axel; Blum, Martin

doi:10.1371/journal.pone.0073646

Cited by 36 publications

(50 citation statements)

References 80 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…3C), raising the question of whether laterality determination is affected by loss of Wnt5a and Wnt11. We have previously shown that PCP breaks bilateral symmetry by positioning cilia to the posterior side of the PNC cells (Nonaka et al, 2005;Song et al, 2010), and in Xenopus embryos knocking down Wnt11b results in left-right defects ( Walentek et al, 2013). In order to test whether Wnt5a and Wnt11 control PCP-regulated laterality determination, we examined asymmetric gene expression of Nodal and Pitx2 (Lowe et al, 1996;Logan et al, 1998).…”

Section: Wnt11mentioning

confidence: 99%

Wnt5aandWnt11regulate mammalian anterior-posterior axis elongation

et al. 2015

View full text Add to dashboard Cite

Mesoderm formation and subsequent anterior-posterior (A-P) axis elongation are fundamental aspects of gastrulation, which is initiated by formation of the primitive streak (PS). Convergent extension (CE) movements and epithelial-mesenchymal transition (EMT) are important for A-P axis elongation in vertebrate embryos. The evolutionarily conserved planar cell polarity (PCP) pathway regulates CE, and Wnts regulate many aspects of gastrulation including CE and EMT. However, the Wnt ligands that regulate A-P axis elongation in mammalian development remain unknown. Wnt11 and Wnt5a regulate axis elongation in lower vertebrates, but only Wnt5a, not Wnt11, regulates mammalian PCP signaling and A-P axis elongation in development. Here, by generating Wnt5a; Wnt11 compound mutants, we show that Wnt11 and Wnt5a play redundant roles during mouse A-P axis elongation. Both genes regulate trunk notochord extension through PCP-controlled CE of notochord cells, establishing a role for Wnt11 in mammalian PCP. We show that Wnt5a and Wnt11 are required for proper patterning of the neural tube and somites by regulating notochord formation, and provide evidence that both genes are required for the generation and migration of axial and paraxial mesodermal precursor cells by regulating EMT. Axial and paraxial mesodermal precursors ectopically accumulate in the PS at late gastrula stages in Wnt5a −/− ; Wnt11−/− embryos and these cells ectopically express epithelial cell adhesion molecules. Our data suggest that Wnt5a and Wnt11 regulate EMT by inducing p38 (Mapk14) phosphorylation. Our findings provide new insights into the role of Wnt5a and Wnt11 in mouse early development and also in cancer metastasis, during which EMT plays a crucial role.

show abstract

Section: Wnt11mentioning

confidence: 99%

Wnt5aandWnt11regulate mammalian anterior-posterior axis elongation

et al. 2015

View full text Add to dashboard Cite

show abstract

“…Obviously, consistent geometrical orientation as an expression of planar cell polarity must be achieved during both prenatal and postnatal ciliogenesis [Jones et al, 2007;Wallingford, 2010;Wallingford and Mitchell, 2011]. Using various model organisms such as Drosophila and Xenopus , a close connection between the planar cell polarity signaling pathway, cell division and migration, the cytoskeleton and the assembly of cilia has been demonstrated during embryogenesis [Hayes et al, 2007;Kim et al, 2010;Goodrich and Strutt, 2011;Kim et al, 2012;Walentek et al, 2013]. These interrelationships are of particular relevance with regard to breaking symmetry at the beginning of left-right patterning of the body plan.…”

Section: Introductionmentioning

confidence: 99%

Ciliary Beating Plane and Wave Propagation in the Bovine Oviduct

Schätz

Schneiter²,

Rička³

et al. 2013

Cells Tissues Organs

View full text Add to dashboard Cite

The uterine tube is an essential conduit for the gametes and zygote during reproduction. The necessary bidirectional conveyance occurs through peristalsis and ciliary activity, but unlike in respiratory tract, little is known about mucociliary transport in the uterine tube, and the direction of transport and the alignment of oviductal cilia have not been conclusively characterized. This study aimed to determine the uniformity in the axonemal orientation of motile cilia in the bovine uterine tube, to identify the direction of mucociliary transport and to relate the presumptive beating plane and the mucociliary transport direction to the long axis of the uterine tube. The angular spread of oviductal motile cilia was determined by electron microscopy, and by maintaining the accurate alignment of the samples throughout the processing steps, axonemal orientation was determined relative to the long axis of the oviduct. The direction of the effective mucociliary transport was determined by the analysis of video microscopic data recorded on explants. Vector-based analysis of electron micrographs yielded the mean angle of deviation between the ‘effective ciliary stroke', as derived from axonemal orientation, and the tubal longitudinal axis pointing towards the uterus to be 0.8°, with a standard deviation of 35.2°. The corresponding angular deviation of the short-wave propagation was -6.8° (SD 34.6°). These results show that oviductal motile cilia are rigorously aligned, that the beating plane of the cilia is parallel to the long axis of the uterine tube and that the ‘effective stroke' and mucociliary transport are directed towards the uterus.

show abstract

“…Activation of PCP-mediated morphogenetic processes requires non-canonical Wnts as ligands, and Wnt11 has been identified as one of the primary PCP ligands during zebrafish and Xenopus gastrulation (Heisenberg et al, 2000; Li et al, 2008; Schambony and Wedlich, 2007; Tada and Smith, 2000; Walentek et al, 2013). The potential role of Wnt11 as a PCP ligand in mammals, however, has remained less clear because Wnt11 mutant mice do not display some of the characteristic phenotypes observed consequent to mutation of core PCP genes Vangl2, Dvl and Celsr .…”

Section: Discussionmentioning

confidence: 99%

“…In Xenopus and zebrafish, Wnt5a and Wnt11 have been identified as two primary ligands capable of activating non-canonical Wnt/ PCP signaling to regulate tissue morphogenesis during gastrulation (Heisenberg et al, 2000; Kilian et al, 2003; Tada and Smith, 2000; Walentek et al, 2013; Wallingford et al, 2001), although in other context they can also activate canonical Wnt signaling (Cha et al, 2008; Cha et al, 2009; Tao et al, 2005). During gastrulation, Wnt11 acts in both cell-autonomous and cell-non-autonomous fashion to regulate polarized cell intercalation and directional migration of mesodermal and endodermal cells (Heisenberg et al, 2000; Ulrich et al, 2003; Witzel et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

“…During gastrulation, Wnt11 acts in both cell-autonomous and cell-non-autonomous fashion to regulate polarized cell intercalation and directional migration of mesodermal and endodermal cells (Heisenberg et al, 2000; Ulrich et al, 2003; Witzel et al, 2006). Consequently, perturbing Wnt11 expression results in failure of axial elongation and midline convergence of foregut endoderm in frog and zebrafish embryos (Heisenberg et al, 2000; Li et al, 2008; Matsui et al, 2005; Tada and Smith, 2000; Walentek et al, 2013). …”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Mapping the dynamic expression of Wnt11 and the lineage contribution of Wnt11-expressing cells during early mouse development

Sinha

Lin

Ding

et al. 2015

Developmental Biology

View full text Add to dashboard Cite

Planar cell polarity (PCP) signaling is an evolutionarily conserved mechanism that coordinates polarized cell behavior to regulate tissue morphogenesis during vertebrate gastrulation, neurulation and organogenesis. In Xenopus and zebrafish, PCP signaling is activated by non-canonical Wnts such as Wnt11, and detailed understanding of Wnt11 expression has provided important clues on when, where and how PCP may be activated to regulate tissue morphogenesis. To explore the role of Wnt11 in mammalian development, we established a Wnt11 expression and lineage map with high spatial and temporal resolution by creating and analyzing a tamoxifen-inducible Wnt11-CreER BAC (bacterial artificial chromosome) transgenic mouse line. Our short- and long-term lineage tracing experiments indicated that Wnt11-CreER could faithfully recapitulate endogenous Wnt11 expression, and revealed for the first time that cells transiently expressing Wnt11 at early gastrulation were fated to become specifically the progenitors of the entire endoderm. During mid-gastrulation, Wnt11-CreER expressing cells also contribute extensively to the endothelium in both embryonic and extraembryonic compartments, and the endocardium in all chambers of the developing heart. In contrast, Wnt11-CreER expression in the myocardium starts from late-gastrulation, and occurs in three transient, sequential waves: first in the precursors of the left ventricular (LV) myocardium from E7.0 to 8.0; subsequently in the right ventricular (RV) myocardium from E8.0 to 9.0; and finally in the superior wall of the outflow tract (OFT) myocardium from E8.5 to 10.5. These results provide formal genetic proof that the majority of the endocardium and myocardium diverge by mid-gastrulation in the mouse, and suggest a tight spatial and temporal control of Wnt11 expression in the myocardial lineage to coordinate with myocardial differentiation in the first and second heart field progenitors to form the LV, RV and OFT. The insights gained from this study will also guide future investigations to decipher the role of non-canonical Wnt/ PCP signaling in endoderm development, vasculogenesis and heart formation.

show abstract

Wnt11b Is Involved in Cilia-Mediated Symmetry Breakage during Xenopus Left-Right Development

Cited by 36 publications

References 80 publications

Wnt5aandWnt11regulate mammalian anterior-posterior axis elongation

Wnt5aandWnt11regulate mammalian anterior-posterior axis elongation

Ciliary Beating Plane and Wave Propagation in the Bovine Oviduct

Mapping the dynamic expression of Wnt11 and the lineage contribution of Wnt11-expressing cells during early mouse development

Contact Info

Product

Resources

About