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Cell migration in the Xenopus gastrula

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Xenopus gastrulation movements are in large part based on the rearrangement of cells by differential cell‐on‐cell migration within multilayered tissues. Different patterns of migration‐based cell intercalation drive endoderm and mesoderm internalization and their positioning along their prospective body axes. C‐cadherin, fibronectin, integrins, and focal contact components are expressed in all gastrula cells and play putative roles in cell‐on‐cell migration, but their actual functions in this respect are not yet understood. The gastrula can be subdivided into two motility domains, and in the vegetal, migratory domain, two modes of cell migration are discerned. Vegetal endoderm cells show ingression‐type migration, a variant of amoeboid migration characterized by the lack of locomotory protrusions and by macropinocytosis as a mechanism of trailing edge resorption. Mesendoderm and prechordal mesoderm cells use lamellipodia in a mesenchymal mode of migration. Gastrula cell motility can be dissected into traits, such as cell polarity, adhesion, mobility, or protrusive activity, which are controlled separately yet in complex, combinatorial ways. Cells can instantaneously switch between different combinations of traits, showing plasticity as they respond to substratum properties. This article is categorized under: Early Embryonic Development > Gastrulation and Neurulation
Tissue separation and guidance of migration at Brachet's cleft. Left panel shows a gradient of sf‐PDGF‐A in the mesoderm. Pink, mesoderm; light blue, ectoderm. An enlargement of the boxed area (Brachet's cleft) is shown in the middle panel. Close cell–cell contacts compatible with cadherin adhesion and ephrin‐Eph interaction are schematically depicted in (a). Intermediate adhesive cell contacts compatible with fibronectin (FN)‐integrin interaction and the recognition of FN‐bound lf‐PDGF‐A by the PDGFR‐α receptor are shown in (b)
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Cell morphology and substratum of migration in different regions of the gastrula. (a) Leading edge mesendoderm (LEM) cells (pink) appear as a mixture of vegetal‐like and prechordal mesoderm (PCM)‐like types. Cells facing the blastocoel roof (BCR) (light blue) are oriented toward the animal pole in a shingled arrangement. Deep in the LEM, both cells devoid of protrusions and those that extend protrusions at the leading edge can be found. (b) PCM cells (dark pink) are unipolar and spindle‐shaped. They extend lamelliform protrusions in the direction of their migration toward the BCR. (c) Vegetal endoderm cells (beige) show blunt fronts and flattened trailing ends that undergo macropinocytosis during tail retraction. Large gaps are present between the cells. C‐cadherin, fibronectin (FN), and integrin α5β1 are found on all gastrula cell membranes except on the apical side of the epithelial layer that surrounds the embryo. Dark blue, CM; light blue, ectoderm; white, epithelium
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Cell rearrangement is driven by differential migration in multiple tissues. (a–e) Left panels show the direction of cell migration and the change in tissue shape. Longer arrows in darker shades of gray represent faster movements. Right panels show local cell rearrangement patterns. Dashed blue arrows indicate tissue constriction and elongation; solid blue arrows indicate tissue shear movements
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Cells use various combinations of motility processes to generate different modes of migration. Motility‐related processes at the front (top right), middle (top middle), and rear end of cells (top left) are depicted. From different combinations of these processes, different modes of cell migration are derived (bottom). For symbols, see box (top right)
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Gastrula tissue rearrangement in the Xenopus embryo. Schematic drawings of Xenopus embryos at the onset of gastrulation (Stage 10), at early (Stage 10.5), and middle gastrulation (Stage 11). Black arrows, active cell movement; white arrows, passive cell movements; yellow, bottle cells. BCR (ectoderm), blastocoel roof; CM, chordamesoderm; LEM, leading edge mesendoderm; PCM, prechordal mesoderm
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Cell motility domains in the Xenopus gastrula. Top panel, left: Graded nodal/activin signaling activity. Middle: Motility domains. Vegetal and animal domains are outlined by red and blue lines, respectively, and subdivided according to marker gene expression patterns. Right: Expression of ligands and receptors of major cell guidance systems. Bottom: Cells from animal and vegetal motility domains behave differently in vitro. They adhere to fibronectin (FN) and weakly to FN‐coated gelatin, but not to bovine serum albumin, and those from the animal motility domain require higher FN density for attachment. Question marks indicate that the in vitro behavior of these cells is not known. Blue arrows, direction of cell migration
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