<i>Insm1</i>
            -expressing neurons and secretory cells develop from a common pool of progenitors in the sea anemone
            <i>Nematostella vectensis</i>

Tournière, Océane; Gahan, James M; Busengdal, Henriette; Bartsch, Natascha; Rentzsch, Fabian

doi:10.1126/sciadv.abi7109

Cited by 21 publications

(13 citation statements)

References 85 publications

(149 reference statements)

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“…While cnidocytes and neurons have commonly been regarded as sister cell types (Richards & Rentzsch, 2014), our data suggest that neurons and gland cells are actually more closely related and have a common progenitor cell, characterized by Insm1 expression, which supports recent evidence of this relationship (Tournière et al, 2021). This also reveals similarities to the relationships within the interstitial cell lineage in Hydra , where neurons and gland cells have a common progenitor state, while nematogenesis is distinct (Siebert et al, 2019).…”

Section: Discussionsupporting

confidence: 83%

Single cell transcriptomics identifies conserved regulators of neurosecretory lineages

Steger

Cole

Denner

et al. 2022

Preprint

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SUMMARYCommunication in bilaterian nervous systems is mediated by electrical and secreted signals, however, the evolutionary origin and relation of neurons to other secretory cell types has not been elucidated. Here we use developmental single cell RNA-sequencing in the cnidarian Nematostella vectensis, representing an early evolutionary lineage with a simple nervous system. Validated by transgenics, we demonstrate that neurons, stinging cells, and gland cells arise from a common multipotent progenitor population. We identify the conserved transcription factor gene SoxC as a key upstream regulator of all neurosecretory lineages and demonstrate that SoxC knockdown eliminates both neuronal and secretory cell types. While in vertebrates and many other bilaterians neurogenesis is largely restricted to early developmental stages, we show that in the sea anemone differentiation of neurosecretory cells is maintained throughout all life stages, and follows the same molecular trajectories from embryo to adulthood, ensuring lifelong homeostasis of neurosecretory cell lineages.

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Section: Discussionsupporting

confidence: 83%

Single cell transcriptomics identifies conserved regulators of neurosecretory lineages

Steger

Cole

Denner

et al. 2022

Preprint

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“…We confirmed this assumption by showing that a subset of progeny cells from Vasa2+/Piwi1+ cells consists of soxB(2) -expressing neural progenitor cells. Previous studies using transgenic reporter lines and single cell RNA-seq analysis have shown that multipotent soxB(2) + neural progenitor cells generate gland cells, neurons and cnidocytes during larval and potentially post-larval development (Richards and Rentzsch, 2014; Steger et al, 2022; Tournière et al, 2022). However, the stem cell populations upstream of such progenitors remain so far unidentified.…”

Section: Discussionmentioning

confidence: 99%

An adult stem-like cell population generates germline and neurons in the sea anemoneNematostella vectensis

Miramón-Puértolas

Steinmetz

2023

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Most genetic research animals (e.g., vertebrates, insects, nematodes) segregate germline and soma during early embryogenesis. In contrast, some highly regenerative bilaterian (e.g., planarians) and non-bilaterian animals (e.g., hydrozoan cnidarians) retain adult stem cells with both germinal and somatic potentials. As these cells have been studied in only few phyla, their biology and evolution remain mostly enigmatic. Here, we aimed to identify and characterize adult stem cells and their cell lineages in the sea anemoneNematostella vectensisby combining gene expression analysis, immunostainings, and meganuclease-mediated and CRISPR/Cas9-mediated knock-in reporter lines of conserved germline and multipotency genes (e.g.,vasa2, piwi1). We found a small population ofvasa2+/piwi1+cells in the gastrodermal folds of juvenile and adult sea anemones that generates germline and a diversity of somatic, mostly proliferative cells. Using a combination ofsoxB(2)+neural progenitor and piwi1 reporter lines, we found that the somatic progeny fromvasa2+/piwi1+cells includessoxB(2)+neural progenitors. Our results strongly support the existence of an adult Vasa2+/Piwi1+ multipotent stem-like cell population that derives both germline and somatic lineages inNematostella. The similarities of lineages and gene expression profiles betweenNematostellaVasa2+/Piwi1+ stem-like cells and hydrozoan interstitial stem cells support their evolutionary conservation among cnidarians.

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“…Alternatively, it could be evidence of a common evolutionary origin for endoderm and neural cells. This would be supported by recent work suggesting that parts of the digestive system in the cnidaria Nematostella are of ectodermal origin (Steinmetz et al, 2017), and that a common progenitor generates neurons and secretory cells in this species (Tournière et al, 2022) (Steger et al, 2022). A deeper understanding of the GRNs in neural tissue and endoderm will be needed to explore this possibility.…”

Section: Discussionmentioning

confidence: 76%

Developmental cell fate choice employs two distinct cis regulatory strategies

Delás

Kalaitzis

Fawzi

et al. 2022

Preprint

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In many developing tissues the patterns of gene expression that assign cell fate are organised by secreted signals functioning in a graded manner over multiple cell diameters. Cis Regulatory Elements (CREs) interpret these graded inputs to control gene expression. How this is accomplished remains poorly understood. In the neural tube, a gradient of the morphogen Sonic hedgehog allocates neural progenitor identity. Here, we uncover two distinct ways in which CREs translate graded Shh signaling into differential gene expression. In the majority of ventral neural progenitors a common set of CREs are used to control gene activity. These CREs integrate cell type specific inputs to control gene expression. By contrast, the most ventral progenitors use a unique set of CREs. These are established by the pioneer factor FOXA2, paralleling the role of FOXA2 in endoderm. Moreover, FOXA2 binds a subset of the same sites in neural and endoderm cells. Together the data identify distinct cis regulatory strategies for the interpretation of morphogen signaling and raise the possibility of an evolutionarily conserved role for FOXA2-mediated regulatory strategy across tissues.

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Insm1 -expressing neurons and secretory cells develop from a common pool of progenitors in the sea anemone Nematostella vectensis

Cited by 21 publications

References 85 publications

Single cell transcriptomics identifies conserved regulators of neurosecretory lineages

Single cell transcriptomics identifies conserved regulators of neurosecretory lineages

An adult stem-like cell population generates germline and neurons in the sea anemoneNematostella vectensis

Developmental cell fate choice employs two distinct cis regulatory strategies

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