H+/K+ ion pump enhances cytoskeletal polarity to drive gastrulation in sea urchin embryo

Abstract

ABSTRACTGastrulation is a universal process in the morphogenesis of many animal embryos. In sea urchin embryos, it involves the invagination of single-layered vegetal plate into blastocoel. Although morphological and molecular events have been well studied for gastrulation, the mechanical driving forces and their regulatory mechanism underlying the gastrulation is not fully understood. In this study, structural features and cytoskeletal distributions were studied in sea urchin embryo using an “exogastrulation” model induced by inhibiting the H+/K+ ion pump with omeprazole. The vegetal pole sides of the exogastrulating embryos had reduced roundness indices, intracellular pH polarization, and intracellular F-actin polarization at the pre-early gastrulation compared with the normal embryo. Gastrulation stopped when F-actin polymerization or degradation was inhibited by RhoA or YAP1 knockout, although pH distributions were independent of such a knockout. A mathematical model of sea urchin embryos at the early gastrulation reproduced the shapes of both normal and exogastrulating embryos using cell-dependent cytoskeletal features based on F-actin and pH distributions. Thus, gastrulation required appropriate cell position-dependent intracellular F-actin distributions regulated by the H+/K+ ion pump through pH control.Summary statementThe H+/K+ ion pump is critical for normal gastrulation in sea urchin through pH regulation of cell-position dependent intracellular actin distributions.