Rab35 regulates skeletogenesis and gastrulation by facilitating actin remodeling and vesicular trafficking

Remsburg, Carolyn; Testa, Michael; Song, Jia L.

doi:10.1016/j.cdev.2021.203660

Cited by 14 publications

(23 citation statements)

References 66 publications

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“…One recent study suggested an outer intestinal embryo is formed by Rab35 knockdown that might disturb the whole embryonic intracellular F-actin polarity (Remsburg et al, 2021). The results of the present study support this suggestion, and further indicate that the intracellular F-actin polarity on the vegetal pole side of the embryo is particularly important for accurate gastrulation and the intracellular pH controlled by H + /K + ion pump is involved in this process.…”

Section: Discussionmentioning

confidence: 99%

Partial exogastrulation due to apical-basal polarity of F-actin distribution disruption in sea urchin embryo by omeprazole

Watanabe

Yasui

Kurose

et al. 2021

Preprint

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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.

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Section: Discussionmentioning

confidence: 99%

Partial exogastrulation due to apical-basal polarity of F-actin distribution disruption in sea urchin embryo by omeprazole

Watanabe

Yasui

Kurose

et al. 2021

Preprint

View full text Add to dashboard Cite

show abstract

“…One recent study suggested that an outer intestinal embryo is formed upon Rab35 knockdown that may disturb the whole embryonic intracellular F-actin polarity [20].…”

Section: Discussionmentioning

confidence: 99%

“…Exogastrulation was also observed via Rab35 knockdown, which was also suggested to disturb whole embryonic cytoskeleton distribution [20].…”

Section: Introductionmentioning

confidence: 97%

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

Watanabe

Yasui

Kurose

et al. 2021

Preprint

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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.

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“…To measure the average intensity levels of arbitrary fluorescent units (intensity) in larvae immunolabeled with serotonin and SynB, maximum intensity projection images were analyzed with ImageJ (Schneider, 2012;Remsburg et al, 2021). Serotonin and SynB expression within the ciliary band was measured and the background was subtracted.…”

Section: Imaging and Phenotypingmentioning

confidence: 99%

microRNA-1 represses signaling pathway components to impact embryonic structures derived from all three germ layers

Sampilo

Song

2022

Preprint

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microRNAs are evolutionarily conserved non-coding RNAs that direct post-transcriptional regulation of target transcripts. We use the sea urchin embryo to achieve a comprehensive understanding the function of miR-1 in a developing embryo. Results indicate that miR-1 regulates gut contractions, specification, and positioning of serotonergic neurons, as well as mesodermally-derived muscles, pigment cells, and skeletogenic cells. Gain-of-function of miR-1 generally leads to more severe developmental defects than its loss-of-function. We identified that miR-1 directly suppresses Ets1/2, Tbr, and VegfR7 of the skeletogenic gene regulatory network, and Notch, Nodal, and Wnt1 signaling components. We found that miR-1-mediated direct suppression of Nodal may indirectly regulate FoxQ2 to impact serotonergic neurons. Excess miR-1 may lead to decreased Nodal and Notch that result in decreased circumpharnygeal muscle fibers and the number of pigment cells. The striking ectopic skeletal branching induced by miR-1 mimic injections may be explained by miR-1-mediated direct suppression of Nodal that leads to expression changes of Vegf3, and Fgfa that mediate skeletogenesis. This work demonstrates that miR-1 plays a diverse regulatory role that impacts tissues derived from all germ layers.

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Rab35 regulates skeletogenesis and gastrulation by facilitating actin remodeling and vesicular trafficking

Cited by 14 publications

References 66 publications

Partial exogastrulation due to apical-basal polarity of F-actin distribution disruption in sea urchin embryo by omeprazole

Partial exogastrulation due to apical-basal polarity of F-actin distribution disruption in sea urchin embryo by omeprazole

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

microRNA-1 represses signaling pathway components to impact embryonic structures derived from all three germ layers

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