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Review
. 2009 Oct;20(8):986-97.
doi: 10.1016/j.semcdb.2009.09.004. Epub 2009 Sep 15.

Regulation of convergence and extension movements during vertebrate gastrulation by the Wnt/PCP pathway

Isabelle Roszko  1 , Atsushi Sawada, Lilianna Solnica-Krezel
Affiliations
Review

Regulation of convergence and extension movements during vertebrate gastrulation by the Wnt/PCP pathway

Isabelle Roszko et al. Semin Cell Dev Biol. 2009 Oct.

Abstract

Vertebrate gastrulation entails massive cell movements that establish and shape the germ layers. During gastrulation, the individual cell behaviors are strictly coordinated in time and space by various signaling pathways. These pathways instruct the cells about proliferation, shape, fate and migration into proper location. Convergence and extension (C&E) movements during vertebrate gastrulation play a major role in the shaping of the embryonic body. In vertebrates, the Wnt/Planar Cell Polarity (Wnt/PCP) pathway is a key regulator of C&E movements, essential for several polarized cell behaviors, including directed cell migration, and mediolateral and radial cell intercalation. However, the molecular mechanisms underlying the acquisition of Planar Cell Polarity by highly dynamic mesenchymal cells engaged in C&E are still not well understood. Here we review new evidence implicating the Wnt/PCP pathway in specific cell behaviors required for C&E during zebrafish gastrulation, in comparison to other vertebrates. We also discuss findings on the molecular regulation and the interaction of the Wnt/PCP pathway with other signaling pathways during gastrulation movements.

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Figures

Fig. 1
Fig. 1. Morphogenetic movements involved in zebrafish gastrulation
(A), at the beginning of gastrulation (shield stage), the blastoderm envelops half of the syncytial yolk cell. The dorsal side is noticeable at this stage by a thickening of the blastoderm, called the embryonic shield. At the blastoderm margin, the prospective mesendodermal cells undergo internalization. Internalization occurs by involution of cell sheaths in the ventral and lateral domains and by ingression of individual cells in the dorsal domain. The internalized cells migrate towards the animal pole/anterior (green arrow), while the epiboly movement (purple arrow) towards the vegetal pole continues. In the dorsal shield region, some convergence movements are observed (blue arrow). (B), at midgastrulation (75% epiboly), the major changes in mesendodermal cell movements include the termination of the internalization and the shift from the animal pole/anterior migration to convergence towards dorsal (blue arrow). However, the animal pole/anterior migration continues in the dorsal region (green arrow). These movements contribute a major part to extension of the anterior-posterior axis (orange arrow). In the ventral domain, the cells do not undergo convergence towards dorsal, but migrate towards the vegetal pole (yellow arrow). Epiboly continues at this stage until the blastoderm encloses the entire yolk cell at 9.5 hpf (purple arrows). (C), at tail bud stage, the entire yolk cell is covered by the blastoderm and epiboly is completed. Convergence of the lateral and dorsal cell populations towards the dorsal midline and their simultaneous extension along the anterior-posterior axis is the major cell movement (blue arrows). Dorsal cell populations undergo fast extension (orange arrow) and modest convergence. A hypothetical gradient of a chemoattractant emanating from the dorsal midline (green) and a ventral to dorsal BMP gradient (dark blue) present in the gastrula tissues and proposed to influence gastrulation cell movements are shown in the background.
Fig 2
Fig 2. Different cell behaviors along the dorso-ventral axis of the zebrafish gastrula
During zebrafish gastrulation the cell movements change over time, depending on the gastrulation stage, but also in space, depending on the localization of the cells in particular domains. The midgastrula stage is represented. Several domains can be distinguished along the dorso-ventral gastrula axis according to the type of mesodermal cell movements (showed by magnified I, II, III, IV, V regions). In the most ventral domain (I) the cells undergo migration towards the vegetal pole. In the ventro-lateral domain (II) the cells undergo slow convergence movements along irregular migration paths, as cells located closer to the animal pole bias their trajectories animally and those closer to the vegetal pole bias their trajectories vegetally, the entire population converges and also extends along the anterior-posterior axis. In the lateral domain (III) the cells undergo fast convergence movements along straight migration paths; the cell packing is increased. In the latero-dorsal domain (IV), migration and the cell packing are increased and the cells undergo polarized radial and medio-lateral intercalation movements that drive modest convergence and extension. In the dorsal domain, the most anterior cells undergo anterior directed migration, while more posterior cells undergo massive cell intercalation movements contributing to fast extension and modest convergence.
Fig 3
Fig 3. Schematic illustration of the canonical Wnt (Wnt/β-catenin) and the non-canonical Wnt/Planar Cell Polarity (Wnt/PCP) signaling pathways in vertebrates
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