Cell migration in the Xenopus gastrula

Abstract

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.

Ectoderm to mesoderm transition by down-regulation of actomyosin contractility

“…However, other systems rely instead on migration of cell masses. Gastrulation in Xenopus is a prototypical example of such type of morphogenesis [1]. Here, massive, coordinated cell migration results in the animally positioned ectoderm engulfing the vegetal endoderm, with the equatorial mesoderm positioned between the two germ layers.…”

“…Here, massive, coordinated cell migration results in the animally positioned ectoderm engulfing the vegetal endoderm, with the equatorial mesoderm positioned between the two germ layers. One of the main actors of early gastrulation is the prechordal mesoderm (PCM) which involutes and migrates collectively on the blastocoel roof (BCR) using the ectodermal cells and a thinly deposited fibronectin (FN) matrix as substrates [1,2]. As it does so, there is ongoing intercellular migration within the tissue that leads to extensive radial intercalations, resulting in progressive thinning of the tissue until eventually all cells contact the BCR.…”

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“…However, other systems rely instead on migration of cell masses. Gastrulation in Xenopus is a prototypical example of such type of morphogenesis [1]. Here, massive, coordinated cell migration results in the animally positioned ectoderm engulfing the vegetal endoderm, with the equatorial mesoderm positioned between the 2 germ layers.…”

“…Here, massive, coordinated cell migration results in the animally positioned ectoderm engulfing the vegetal endoderm, with the equatorial mesoderm positioned between the 2 germ layers. One of the main actors of early gastrulation is the prechordal mesoderm (PCM) which involutes and migrates collectively on the blastocoel roof (BCR) using the ectodermal cells and a thinly deposited fibronectin (FN) matrix as substrates [1,2]. As it does so, there is ongoing intercellular migration within the tissue that leads to extensive radial intercalations, resulting in progressive thinning of the tissue until eventually all cells contact the BCR.…”

“…The Xenopus embryo offers the unique possibility to easily dissect specific tissues, prepare explants and/or dissociate them into single cells, allowing the study of intrinsic cell and tissue properties in the absence of confounding influences of other surrounding embryonic structures. Importantly, the morphogenetic events occurring during Xenopus gastrulation are recapitulated in isolated explants, and furthermore, even individual dissociated cells have characteristics that clearly relate to the properties of the corresponding tissues: Ectoderm cells show higher cortical stiffness, higher cell-cell adhesion, and are largely immotile, while the softer mesoderm cells spread and migrate when laid on an FN substrate, similar to the mesoderm at the BCR [1,[3][4][5]. Note that there are 2 other mesodermal populations, the more anterior leading edge mesendoderm (LEM) and the posterior chordamesoderm (CM).…”