Analysis of forkhead and snail expression reveals epithelial–mesenchymal transitions during embryonic and larval development of Nematostella vectensis
Open accessAbstract
The winged helix transcription factor Forkhead and the zinc finger transcription factor Snail are crucially involved in germ layer formation in Bilateria. Here, we isolated and characterized a homolog of forkhead/HNF3 (FoxA/group 1) and of snail from a diploblast, the sea anemone Nematostella vectensis. We show that Nematostella forkhead expression starts during late Blastula stage in a ring of cells that demarcate the blastopore margin during early gastrulation, thereby marking the boundary between ectodermal and endodermal tissue. snail, by contrast, is expressed in a complementary pattern in the center of forkhead-expressing cells marking the presumptive endodermal cells fated to ingress during gastrulation. In a significant portion of early gastrulating embryos, forkhead is expressed asymmetrically around the blastopore. While snail-expressing cells form the endodermal cell mass, forkhead marks the pharynx anlage throughout embryonic and larval development. In the primary polyp, forkhead remains expressed in the pharynx. The detailed analysis of forkhead and snail expression during Nematostella embryonic and larval development further suggests that endoderm formation results from epithelial invagination, mesenchymal immigration, and reorganization of the endodermal epithelial layer, that is, by epithelial-mesenchymal transitions (EMT) in combination with extensive morphogenetic movements. snail also governs EMT at different processes during embryonic development in Bilateria. Our data indicate that the function of snail in Diploblasts is to regulate motility and cell adhesion, supporting that the triggering of changes in cell behavior is the ancestral role of snail in Metazoa.
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Fox gene expression in Nematostella and Hydra suggests that the mucociliary epithelium around the gastric opening represents the ancient site of activity of the foxA, B, C, D, E superfamily.
“in Nematostella, foxB [122] and foxA [123] are expressed in the ectodermal ciliated pharynx and foxC [122] in pharyngeal endoderm; in Hydra, foxA/budhead [124] is likewise expressed in the endoderm around the oral opening, suggesting that the mucociliary epithelium around the gastric opening represents the ancient site of activity of the foxA, B, C, D, E superfamily.”
From Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution (2015) · cites this paper as [123]
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- Authors
- Fritzenwanker, J. H., Saina, M., & Technau, U.
- Affiliations
- Technische Universität Darmstadt (DE)
- Corresponding author
- Technau, Ulrich
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2004-11
- Volume
- 275
- Issue
- 2
- Pages
- 389-402
- ISSN
- 0012-1606 (ISSN-L)
- OpenAlex
- W2084448229
- Cited by
- 165
- References
- 79
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 5 · 2023: 5 · 2022: 8 · 2021: 2 · 2020: 5 · 2019: 10 · 2018: 6 · 2017: 10 · 2016: 11 · 2015: 7 · 2014: 10 · 2013: 6 · 2012: 2
- FWCI
- 5.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 3216 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Planarian Biology and Electrostimulation
- Keywords
- forkhead transcription factor, Snail transcription factor, epithelial-mesenchymal transition, Nematostella vectensis, sea anemone, gastrulation, endoderm formation, blastopore, larval development, cell motility, cell adhesion, germ layer formation, morphogenetic movements
- MeSH terms
- Snail Family Transcription Factors, Amino Acid Sequence, Animals, Cell Differentiation, DNA-Binding Proteins, Epithelial Cells, Mesoderm, Models, Genetic, Molecular Sequence Data, Nuclear Proteins, Phylogeny, Sea Anemones, Transcription Factors, Likelihood Functions, Sequence Alignment, In Situ Hybridization, Sequence Analysis, DNA, DNA Primers, DNA, Complementary, Gene Expression Regulation, Developmental, Reverse Transcriptase Polymerase Chain Reaction, Forkhead Transcription Factors
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