Noncanonical Wnt signaling regulates midline convergence of organ primordia during zebrafish development

Abstract

Several components of noncanonical Wnt signaling pathways are involved in the control of convergence and extension (CE) movements during zebrafish and Xenopus gastrulation. However, the complexity of these pathways and the wide patterns of expression and activity displayed by some of their components immediately suggest additional morphogenetic roles beyond the control of CE. Here we show that the key modular intracellular mediator Dishevelled, through a specific activation of RhoA GTPase, controls the process of convergence of endoderm and organ precursors toward the embryonic midline in the zebrafish embryo. We also show that three Wnt noncanonical ligands wnt4a, silberblick/wnt11, and wnt11-related regulate this process by acting in a largely redundant way. The same ligands are also required, nonredundantly, to control specific aspects of CE that involve interaction of Dishevelled with mediators different from that of RhoA GTPase. Overall, our results uncover a late, previously unexpected role of noncanonical Wnt signaling in the control of midline assembly of organ precursors during vertebrate embryo development.[Keywords: Heart; endoderm; noncanonical Wnt signaling; Dishevelled; RhoA] Supplemental material is available at http://genesdev.org.

Sfrp5 coordinates foregut specification and morphogenesis by antagonizing both canonical and noncanonical Wnt11 signaling

“…Our results indicate that this is mediated by Wnt/PCP signaling, consistent with reports that redundant Wnt11, Wnt11-R, and Wnt4a ligands promote midline CE of endodermal progenitors in zebrafish (Matsui et al 2005). While future studies will be needed to precisely describe the cell behaviors mediating CE of the Xenopus gut and to determine how these are regulated by the PCP pathway, our inhibitor studies shed some light on this.…”

Early temporal‐specific responses and differential sensitivity to lithium and Wnt‐3A exposure during heart development

“…The canonical Wnt-mediated processes we observed potentiated by lithium exposure in chick embryos take place much earlier in the heart fields than what had been analyzed for the noncanonical Wnt11-mediated events that were reported being necessary for cardiac cell differentiation in avian and Xenopus embryos (Eisenberg et al, 1997;Eisenberg and Eisenberg, 1999;Pandur et al, 2002). In addition, Wnt11 in zebrafish also seems to control the later process of midline movements of heart primordia by Dishevelled-mediated activation of RhoA GTPase (Matsui et al, 2005). We propose that the early canonical Wnt signaling wave within the heart fields first is involved coordinately with BMP signaling to define the cardiac domain and sets up the dorsal boundary of the cardiac compartment as detected by increased ␤-catenin localization at the boundary (Linask, 1992a,b;Linask et al, 1997).…”

Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii

“…The floor plate corresponds to the vertebrate CNS dorsal midline and is thought to be homologous to the Platynereis ventral midline 13,14 , therefore pointing out a deep evolutionary conservation of the expression of wnt4 genes in bilaterians. However, floor plate-secreted Wnt4 proteins are not involved in the control of cell proliferation and differentiation in the vertebrate neural tube and instead have been shown to control the antero-posterior guidance of commissural axons 50 , as well as some other unrelated processes such as segmental patterning 51 and midline convergence of organ primordia 52 . By controlling neural cell differentiation and proliferation, ventral midlinesecreted Pdu-Wnt4 would therefore have a strikingly different function than its vertebrate homologue, and would be functionally comparable to the vertebrate Wnt1 and Wnt3a produced by the roof plate of the neural tube 4 .…”