Transgenic analysis of a SoxB gene reveals neural progenitor cells in the cnidarian Nematostella vectensis
Abstract
Bilaterian neurogenesis is characterized by the generation of diverse neural cell types from dedicated neural stem/progenitor cells (NPCs). However, the evolutionary origin of NPCs is unclear, as neurogenesis in representatives of the bilaterian sister group, the Cnidaria, occurs via interstitial stem cells that also possess broader, non-neural, developmental potential. We address this question by analysing neurogenesis in an anthozoan cnidarian, Nematostella vectensis. Using a transgenic reporter line, we show that NvSoxB(2) – an orthologue of bilaterian SoxB genes that have conserved roles in neurogenesis – is expressed in a cell population that gives rise to sensory neurons, ganglion neurons and nematocytes: the three primary neural cell types of cnidarians. EdU labelling together with in situ hybridization, and within the NvSoxB(2)::mOrange transgenic line, demonstrates that cells express NvSoxB(2) before mitosis and identifies asymmetric behaviours of sibling cells within NvSoxB(2)+ lineages. Morpholino-mediated gene knockdown of NvSoxB(2) blocks the formation of all three neural cell types, thereby identifying NvSoxB(2) as an essential positive regulator of nervous system development. Our results demonstrate that diverse neural cell types derive from an NvSoxB(2)-expressing population of mitotic cells in Nematostella and that SoxB genes are ancient components of a neurogenic program. To our knowledge this is the first description of a lineage-restricted, multipotent cell population outside the Bilateria and we propose that neurogenesis via dedicated, SoxB-expressing NPCs predates the split between cnidarians and bilaterians.
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In Nematostella, Elav1 marks a large neuronal subpopulation but is not a pan-neuronal marker, because it is part of a larger population marked by SoxB(2).
“In Nematostella, it indeed marks a large neuronal subpopulation [26,27], but is not a pan-neuronal marker (figure 2a,e), as it is part of a larger population marked by SoxB(2) [29]”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [29]
Analysis of the SoxB(2)::mOrange transgenic line showed that neurites can extend in any direction from the onset of differentiation.
“Analysis of the SoxB(2)::mOrange transgenic line, which broadly labels neural progenitors and their progeny, showed that neurites can extend in any direction from the onset of differentiation [29].”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [29]
The most aboral region, the apical organ, remains free of Elav1 and SoxB(2) neural cell bodies.
“Notably, the most aboral region, the ‘apical organ’, often referred to as a sensory centre, remains free of Elav1 and SoxB(2) neural cell bodies [27,29].”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [29]
SoxB(2) marks a population of cells that gives rise to ganglion and sensory neurons and cnidocytes, representing a general neural progenitor population.
“Using a SoxB(2) transgenic reporter line, Richards and Rentzsch showed that SoxB(2) marks a population of cells that gives rise to ganglion and sensory neurons and cnidocytes, thus representing a general neural progenitor population [29].”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [29]
The BMP signalling gradient in Nematostella has been detected only considerably later (at gastrula stage) than the occurrence of the first neural progenitor cells (at mid-blastula stage), and early neural differentiation is not biased along the directive axis.
“However, this BMP signalling gradient has been detected only considerably later (at gastrula stage, [39,40]) than the occurrence of the first neural progenitor cells (NPCs; at mid-blastula stage [29]) and early neural differentiation is not biased along the directive axis [26,27,29,41].”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [29]
Members of the Sox family of genes are involved in the patterning of the neural field and the production of the components of the neural lineage.
“It has been shown that members of the Sox family of genes are involved in the patterning of the neural field and the production of the components of the neural lineage [28,29].”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [29]
Daughter cells of one neural progenitor in Nematostella can have different cell cycle characteristics.
“The tracing of EdU-labelled dividing SoxB(2)-positive cells suggested that daughter cells of one neural progenitor in Nematostella can have different cell cycle characteristics [29]”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [29]
Knockdown of SoxB(2) strongly reduces the production of neurons and cnidocytes.
“The knockdown of SoxB(2) strongly reduces the production of neurons and cnidocytes.”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [29]
The molecular control of neurogenesis in cnidarians is remarkably similar to that in vertebrates: Notch signaling controls the number of neural progenitor cells, soxB and bHLH transcription factor genes regulate their development, and Wnt signaling gradients pattern the nervous system.
“The molecular control of neurogenesis is remarkably similar to that in vertebrates: Notch signalling controls the number of neural progenitor cells, soxB and bHLH transcription factor encoding genes regulate their further development and Wnt signaling gradients are involved in the patterning of the nervous system [99–101].”
From Back to the Basics: Cnidarians Start to Fire (2017) · cites this paper as [100]
The use of cell type-specific promoters for reporter genes has improved the visualization of neuronal morphology and the tracking of the developmental origin of nerve cells.
“The use of cell type-specific promoters for reporter genes has also improved the visualization of neuronal morphology and tracking of the developmental origin of nerve cells [98,100].”
From Back to the Basics: Cnidarians Start to Fire (2017) · cites this paper as [100]
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- Authors
- Richards, G. S., & Rentzsch, F.
- Affiliations
- University of Bergen (NO)
- ORCID
- Rentzsch, Fabian
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2014-12-15
- Volume
- 141
- Issue
- 24
- Pages
- 4681-4689
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2027035529
- Semantic Scholar
- 8fac58c117ed05e6e6f67b362e89c865e91665f6
- Cited by
- 110
- References
- 49
- Citations by year
- 2026: 7 · 2025: 12 · 2024: 11 · 2023: 8 · 2022: 10 · 2021: 3 · 2020: 12 · 2019: 9 · 2018: 9 · 2017: 11 · 2016: 9 · 2015: 9
- FWCI
- 7.04
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Development (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- Nematostella vectensis, neural progenitor cells, interstitial stem cells, brain development, sensory neurons, ganglionic neurons, nematocytes, asymmetric cell division, morpholino knockdown
- MeSH terms
- Animals, Biological Evolution, Ganglia, Immunohistochemistry, Sensory Receptor Cells, Sea Anemones, In Situ Hybridization, In Situ Hybridization, Fluorescence, Gene Transfer Techniques, Cell Lineage, Reverse Transcriptase Polymerase Chain Reaction, Multipotent Stem Cells, Neurogenesis, SOXB2 Transcription Factors, Gene Knockdown Techniques, Nematocyst, Neural Stem Cells, Morpholinos
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