scholarly journals H+/K+ Ion Pump Enhances Cytoskeletal Polarity to Drive Gastrulation in Sea Urchin Embryo

Author(s):  
Kaichi Watanabe ◽  
Yuhei Yasui ◽  
Yuta Kurose ◽  
Masashi Fujii ◽  
Takashi Yamamoto ◽  
...  

Abstract Gastrulation is a universal process in the morphogenesis of many animal embryos. In sea urchin embryos, it involves the invagination of a single-layered vegetal plate into the blastocoel. Although morphological and molecular events in gastrulation have been well studied, the mechanical driving forces and the regulatory mechanism underlying gastrulation is not fully understood. In this study, structural features and cytoskeletal distributions were studied in sea urchin embryos using an “exogastrulation” model induced by inhibiting the H+/K+ ion pump with omeprazole. The vegetal poles of the exogastrulating embryos showed reduced roundness indices, intracellular pH polarization, and intracellular F-actin polarization at the pre-early gastrulation stage compared with normal embryos. Gastrulation stopped when F-actin polymerization or degradation was inhibited via 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.

2021 ◽  
Author(s):  
Kaichi Watanabe ◽  
Yuhei Yasui ◽  
Yuta Kurose ◽  
Masashi Fujii ◽  
Takashi Yamamoto ◽  
...  

Gastrulation 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.


1998 ◽  
Vol 95 (16) ◽  
pp. 9343-9348 ◽  
Author(s):  
Athula H. Wikramanayake ◽  
Ling Huang ◽  
William H. Klein

In sea urchin embryos, the animal-vegetal axis is specified during oogenesis. After fertilization, this axis is patterned to produce five distinct territories by the 60-cell stage. Territorial specification is thought to occur by a signal transduction cascade that is initiated by the large micromeres located at the vegetal pole. The molecular mechanisms that mediate the specification events along the animal–vegetal axis in sea urchin embryos are largely unknown. Nuclear β-catenin is seen in vegetal cells of the early embryo, suggesting that this protein plays a role in specifying vegetal cell fates. Here, we test this hypothesis and show that β-catenin is necessary for vegetal plate specification and is also sufficient for endoderm formation. In addition, we show that β-catenin has pronounced effects on animal blastomeres and is critical for specification of aboral ectoderm and for ectoderm patterning, presumably via a noncell-autonomous mechanism. These results support a model in which a Wnt-like signal released by vegetal cells patterns the early embryo along the animal–vegetal axis. Our results also reveal similarities between the sea urchin animal–vegetal axis and the vertebrate dorsal–ventral axis, suggesting that these axes share a common evolutionary origin.


Zygote ◽  
1997 ◽  
Vol 5 (2) ◽  
pp. 127-138 ◽  
Author(s):  
Rajnikant Patel ◽  
Elizabeth M. Wright ◽  
Michael Whitaker

SummaryDuring the early mitotic cell cycles of the sea urchin embryo, the cell oscillates between S-phase and M-phase. In the presence of aphidicolin, a DNA synthesis inhibitor, a checkpoint control blocks the activation of the p34cdc2 protein kinase, by keeping it in the inactive, tyrosine phosphorylated form, and the embryos do not enter mitosis. Caffeine has been shown to bypass the G2/M-phase checkpoint in mammalian cells and in cycling Xenopus extracts and to induce mitosis despite the presence of damaged or unreplicated DNA. In this study we show that caffeine also induces mitosis and cell division in sea urchin embryos, in the presence of unreplicated DNA, by stimulating the tyrosine dephosphorylation of p34cdc2 and switching on its protein kinase activity. We also show that the caffeine-induced activation of the p34cdc2 protein kinase is not mediated by either of the two second messengers, calcium and cAMP, or by inhibition of the p34cdc2 tyrosine kinase. Thus, none of the mechanisms proposed for caffeine's action can explain how it overrides the S-phase checkpoint in the early cell cycles of the sea urchin embryo.


1980 ◽  
Vol 87 (1) ◽  
pp. 309-313 ◽  
Author(s):  
E Spiegel ◽  
M Burger ◽  
M Spiegel

The presence of fibronectin in developing sea urchin embryos was studied uing immunofluorescence staining. The fluorescence pattern indicates that fibronectin is found on the cell surfaces and between cells in the blastula and gastrula stages, indicating that it plays a role in cell adhesion. Its presence on invaginating cells also suggests its involvement in morphogenesis during early development.


Sign in / Sign up

Export Citation Format

Share Document