Blastocoel-spanning filopodia in cleavage-stage Xenopus laevis: Potential roles in morphogen distribution and detection

In the frog Xenopus laevis, dorsal–ventral axis specification involves cytoskeleton-dependent transport of localized transcripts and proteins during the first cell cycle, and activation of the canonical Wnt pathway to locally stabilize translated beta-catenin which, by as early as the 32-cell stage, commits nuclei in prospective dorsal lineages to the subsequent expression of dorsal target genes. Maternal ligands important for activating this dorsal-specific signaling pathway are thought to interact with secreted glypicans and coreceptors in the blastocoel. While diffusion between cells is generally thought of as sufficient to accomplish the distribution of secreted maternal ligands to their appropriate targets, signaling may also involve other potential mechanisms, including direct transfer of morphogens via membrane-bounded entities, such as argosomes, exosomes, or even filopodia. In Xenopus, the blastocoel-facing, basolateral surfaces where signaling interactions ostensibly take place have not been previously examined in detail. Here, we report that the cleavage-stage blastocoel is traversed by hundreds of extremely long cellular protrusions that maintain long-term contacts between nonadjacent blastomeres during expansion of the interstitial space in early embryogenesis. The involvement of these protrusions in early embryonic patterning is suggested by the discoveries that (a) they fragment into microvesicles, whose resorption facilitates considerable exchange of cytoplasm and membrane between blastomeres; and (b) they are active in caveolar endocytosis, a prerequisite for ligand-receptor signaling.