Mesoderm Cell Migration in the Xenopus Gastrula

Abstract

We analyze the migration of the prospective head mesoderm (HM) across the blastocoel roof (BCR) during gastrulation of the Xenopus embryo. Cell spreading and the concomitant appearance of cytoplasmic lamellae depend on the interaction of HM cells with fibronectin (FN) fibrils, which cover the inner surface of the BCR. Isolated HM cells only extend short-lived filiform protrusions on non-adheasive substrates, but form lamelliform protrusions (usually two lamellae appear simultaneously at opposite ends of a cell) on a FN substrate. Isolated bipolar HM cells move in a step-wise mode of translocation, with in-built changes of the direction of migration. This ineffective mode of migration is altered when HM cells move as part of a larger aggregate, as occurs in the embryo, where the HM forms a coherent cell mass. A Ca⁺⁺-dependent cell-cell adhesion molecule, U-cadherin, mediates aggregate formation, which is one prerequisite for highly persistent migration. The second requirement is that the mesoderm aggregate moves on a proper substrate. The extracellular matrix of the inner BCR surface can be deposited on a plastic substrate. This conditioned substrate contains directional cues which guide the mesoderm to its target region. The migrating mesoderm becomes visibly polarized on conditioned substrate. Cells appear unipolar and extend protrusions in the direction of migration only, thus underlapping neighboring cells anteriorly. This shingle arrangement of HM cells is also observed in the embryo. We conclude that both cadherin-mediated cell-cell contact and aggregate formation, and a substrate containing guiding cues are required for the unipolar extension of locomotory protrusions, oriented underlapping of neighboring cells, and efficient, persistent, and directional migration of HM cells.