Cadherin switch marks germ layer formation in the diploblastic sea anemone <i>Nematostella vectensis</i>

Pukhlyakova, Ekaterina; Kirillova, Anastasia; Kraus, Yulia; Zimmermann, Bob; Technau, Ulrich

doi:10.1242/dev.174623

Cited by 18 publications

(22 citation statements)

References 86 publications

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“…This is similar to that observed in the pEN cell aggregates in separate cultures (Figure 6f, f′, n, n′) (Table 1). Other types of cadherins might contribute to the sorting of pEN cells from pEC cells, as recently reported in the lower invertebrate sea anemone Nematostella vectensis (Pukhlyakova et al., 2019).…”

Section: Discussionsupporting

confidence: 52%

“…The cellular basis of germ layer formation differs among animal species. Embryonic cells exhibit various morphogenetic behaviors and characteristics in their epithelia, including internalization, epiboly, convergence, and extension, which are evident in stratified and monolayer epithelial forms (Giger & David, 2017; Pukhlyakova et al., 2019; Solnica‐Krezel, 2005; Winklbauer & Müller, 2011), epithelial–mesenchymal transition, or reverse transition (Nowotschin et al., 2019). One essential commonality between cell behaviors is cell sorting, the ability of cells to recognize each other as the same or different.…”

Section: Introductionmentioning

confidence: 99%

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Cell sorting and germ layer formation in reconstructed starfish embryos

et al. 2021

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Germ layer formation is driven by embryonic cell sorting during the early developmental stages. Starfish (Patiria pectinifera) embryos have a connected endoderm and ectoderm, albeit with few contact surfaces between the epithelia. To better understand the association between cell sorting and germ layer formation, we reconstructed P. pectinifera embryos and examined their germ layer formation. Initial observations showed that the presumptive endodermal (pEN) and presumptive ectodermal (pEC) portions of the embryonic body at the late‐blastula stage were preserved throughout development. Based on this, cells that were dissociated from each dermal fragment were mixed in a reconstruction experiment. Our results showed that the pEN and pEC cells were located inside and outside the reaggregates, respectively, to form an embryonic body containing two epithelial layers, separated by a blastocoel. During this process, the pEN cells were motile and shifted from smaller clumps to form a large clump. In contrast, in reaggregates formed in separate cultures, the pEN cells showed strong adhesion abilities, whereas the pEC cells underwent epithelialization. Unlike that in pEN cells, the reaggregation of pEC cells preceded cadherin expression. Filamentous actin was similarly observed in both reaggregates. These results suggest that during the reconstruction of starfish embryos, germ layer formation occurs via the sorting of pEN and pEC cells, depending on their adhesiveness, motility, and epithelialization. In vivo, these properties might embody the physiological significance of cell adhesion in the germ layers constituting the epithelial monolayer.

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Section: Discussionsupporting

confidence: 52%

Section: Introductionmentioning

confidence: 99%

Cell sorting and germ layer formation in reconstructed starfish embryos

et al. 2021

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“…Animals were anesthetized in 7% MgCl2 prior to fixation. Fixation was performed for 1 hour at room temperature either with 4% paraformaldehyde (EMS, E15710) in PBS with 0.1% Tween (PTw 0.1%, Sigma, P1379) for phosphorylated histone 3 antibody staining (Chen et al, 2020) (pH3, Sigma # 05-806, 1:100), or with Lavdovsky's fixative (3.7% formaldehyde, 50% ethanol, 4% acetic acid) for Cadherin3 antibody detection (gift from Technau lab (Pukhlyakova et al, 2019), 1:500). Animals were permeabilized in 10% DMSO (Thermo Fisher,85190) in PBS for 20 minutes and washed with PBS with 0.2% Triton (Sigma, T8787) (PTx 0.2%), followed by 1hour incubation in blocking buffer containing PTx 0.1%, 0.1% DMSO, 1% BSA (Sigma, A2153), and 5% Goat serum (Sigma, G9023).…”

Section: Fixation and Immunostainingmentioning

confidence: 99%

Ethology of morphogenesis reveals the design principles of cnidarian size and shape development

Stokkermans

Chakrabarti

Moghe

et al. 2021

Preprint

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During development, organisms interact with their natural habits while undergoing morphological changes, yet it remains unclear whether the interplay between developing systems and their environments impacts animal morphogenesis. Here, we use the cnidarian Nematostella vectensis as a developmental model to uncover a mechanistic link between organism size, shape and behavior. Using quantitative live imaging, including extensive behavioral profiling, combined with molecular and biophysical experiments, we demonstrate that the muscular hydraulic machinery that controls body movement directly drives larva-polyp morphogenesis. Unexpectedly, size and shape development are differentially controlled by antagonistic muscles. A simple theoretical model shows how a combination of slow-priming and fast-pumping pressures generated by muscular hydraulics acts as a global mechanical regulator that coordinates tissue remodeling. Altogether, our findings illuminate how dynamic behavioral modes in the environment can be harnessed to drive morphogenetic trajectories, establishing ethology as a critical component of organismal morphogenesis, termed ethology of morphogenesis.

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“…A computational model for Nematostella gastrulation predicts that strain at the blastopore lip is promoted by reduction in cell adhesion in the adjacent domain of presumptive endoderm (Tamulonis et al, 2011), which is marked by Snail expression (Fritzenwanker et al, 2004;Hayward et al, 2015). Snail likely contributes to the observed "partial EMT" and progressive transformation of these oral-most cells into endoderm by repression of Par and cadherin gene expression (Fritzenwanker et al, 2004;Botman, et al, 2014;Salinas-Saavedra et al, 2018;Pukhlyakova et al, 2019). We can propose an equivalent mechanism in Clytia based on the predictions of a computational model in which a Nematostella-like gastrulation mode was converted into an ingression mode by increasing the extent of adhesion loss in the oral domain while maintaining apical cell constriction across all cells (van der Sande et al, 2020).…”

Section: Cell Ingressionmentioning

confidence: 99%

Cell shape changes during larval body plan development in Clytia hemisphaerica

Kraus

Houliston

2019

Preprint

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The cnidarian "planula" larva shows radial symmetry around a polarized, oral-aboral, body axis and comprises two epithelia cell layers, ectodermal and endodermal. This simple body plan is set up during gastrulation, a process which proceeds by a variety of modes amongst the diverse cnidarian species. In the hydrozoan laboratory model Clytia hemisphaerica, gastrulation involves a process termed unipolar cell ingression, in which the endoderm derives from mass epithelial-mesenchymal transition (EMT) at the future oral pole of a monoepithelial blastula. This contrasts markedly from the gastrulation mode in the anthozoan cnidarian Nematostella vectensis, in which endoderm formation primarily relies on cell sheet invagination. To understand the cellular basis of gastrulation in Clytia we have characterized in detail successive cell morphology changes during planula formation by Scanning and Transmission Electron Microscopy combined with confocal imaging. These changes accompany epithialization of the blastoderm, bottle cell formation followed by EMT in the oral domain, cohesive migration and intercalation of ingressed mesenchymal cells, and re-epithelialization of the endoderm. From our data we have reconstructed the cascade of morphogenetic events leading to the formation of planula larva. We also matched the domains of cell morphology changes to the expression of selected regulatory and marker genes expressed during gastrulation. We propose that cell ingression in Clytia not only provides the endoderm, but generates internal forces that shape the embryo in the course of gastrulation. These observations help build a more complete understanding of the cellular basis of morphogenesis and of the evolutionary plasticity of cnidarian gastrulation modes.

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Cadherin switch marks germ layer formation in the diploblastic sea anemone Nematostella vectensis

Cited by 18 publications

References 86 publications

Cell sorting and germ layer formation in reconstructed starfish embryos

Cell sorting and germ layer formation in reconstructed starfish embryos

Ethology of morphogenesis reveals the design principles of cnidarian size and shape development

Cell shape changes during larval body plan development in Clytia hemisphaerica

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