Oriented cell divisions asymmetrically segregate aPKC and generate cell fate diversity in the earlyXenopusembryo

Abstract

A key feature of early vertebrate development is the formation of superficial, epithelial cells that overlie nonepithelial deep cells. In Xenopus, deep and superficial cells show a range of differences, including a different competence for primary neurogenesis. We show that the two cell populations are generated during the blastula stages by perpendicularly oriented divisions. These take place during several cell divisions, in a variable pattern, but at a percentage that varies little between embryos and from one division to the next. The orientation of division correlates with cell shape suggesting that simple geometric rules may control the orientation of division in this system. We show that dividing cells are molecularly polarised such that aPKC is localised to the external, apical, membrane. Membrane localised aPKC can be seen as early as the one-cell stage and during the blastula divisions, it is preferentially inherited by superficial cells. Finally, we show that when 64-cell stage isolated blastomeres divide perpendicularly and the daughters are cultured separately, only the progeny of the cells that inherit the apical membrane turn on the bHLH gene, ESR6e. We conclude that oriented cell divisions generate the superficial and deep cells and establish cell fate diversity between them.Movie available online

Contribution of JAM-1 to epithelial differentiation and tight-junction biogenesis in the mouse preimplantation embryo

“…In these models, cell fate diversification can occur by atypical PKC phosphorylation of cytoskeletal components, resulting in different inheritance of determinant proteins (Betschinger et al, 2003). Similar to the current study, atypical PKC is localized to the apical membrane of blastomeres during cleavage of Xenopus embryos, in which a role in asymmetric cell division has been proposed (Chalmers et al, 2003). These data on the Par gene complex indicate that apical membrane PKCζ at compaction might contribute similarly to the process of early lineage diversification in the mouse embryo through cytoskeletal reorganization and cell polarity.…”

Large-scale mechanical properties of Xenopus embryonic epithelium

“…1 E-G and Fig. S1 E, G, and H), as indicated by the apical marker aPKC (21) and basolateral markers C-cadherin (19,20) and integrinβ1 (22). Asymmetrical divisions may be induced by radial cell elongation in spherules (see below); such divisions also occur at earlier stages in the embryo when cells are likewise more columnar (18).…”

Membrane dynamics of cleavage furrow closure in Xenopus laevis

“…The two membrane domains quickly specialize during early cleavage, reflecting the kinds of functional polarization seen in other epithelia. For example, aPKC, originally covering the entire egg surface before cleavage, is selectively retained on apical surfaces and excluded from basolateral surfaces (Chalmers et al, 2003), whereas various components of cadherin-mediated cell-cell adhesion, absent from the original egg surface, become associated exclusively with the new membrane (Angres et al, 1991;Ginsberg et al, 1991;Gawantka et al, 1992;Schneider et al, 1993;Fagotto and Gumbiner, 1994;Chalmers et al, 2005). Expansion of the basolateral domain is accomplished during cleavage furrow advance by insertion of large amounts of new membrane along the cleavage plane by means of localized exocytosis from a maternally synthesized pool of vesicles (Roberts et al, 1992).…”