The neurogenic fate of the hindbrain boundaries relies on Notch3-dependent asymmetric cell divisions

Hevia, Covadonga F.; Engel-Pizcueta, Carolyn; Udina, Frederic; Pujades, Cristina

doi:10.1016/j.celrep.2022.110915

Cited by 12 publications

(65 citation statements)

References 60 publications

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“…In agreement with our previous finding on chick HBs as reservoirs of NPSCs (Peretz et al, 2016), subsequent works confirmed that in zebrafish HBs similarly serve as pools of progenitors in an active proliferative state, regulated by Yap/Taz-TEAD activity (Voltes et al, 2019). Recent monitoring of the spatiotemporal dynamics of HB cells in zebrafish have revealed that they initiate as neuroepithelial-stem cells that divide symmetrically, while they later shift to become radial-glia progenitors undergoing asymmetrical division to contribute neurons to the hindbrain (Hevia et al, 2022). This transition was found to be triggered by Notch3 signaling.…”

Section: Hbs In Different Model Systemssupporting

confidence: 89%

“…Based on these results we have proposed that HBs of avians act as pools of Sox2 + NPSCs to provide proliferating progenitors to the intensely-differentiating Rhs. These findings were later reinforced in the zebrafish hindbrain, where HBs were suggested to act as regions of self-renewing progenitors that later on provide differentiating neurons to the hindbrain (Hevia et al, 2022;Voltes et al, 2019). However, as opposed to the chick embryo, Sox2 expression is not enriched in zebrafish HBs.…”

Section: Introductionmentioning

confidence: 98%

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Hindbrain boundaries as niches of neural progenitor/stem cells regulated by the extracellular matrix proteoglycan chondroitin sulphate

Hutchings

Nuriel

Lazar

et al. 2023

Preprint

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The interplay between neural progenitor/stem cells (NPSC) and their extracellular matrix (ECM), is a crucial regulatory mechanism that determines their behavior. Nonetheless, how the ECM dictates internal processes remains elusive. The hindbrain is valuable to examine this relationship, as cells in the hindbrain boundaries (HB), which arise between any two neighboring rhombomeres, express the NPSC-marker Sox2 while being surrounded with the ECM molecule chondroitin sulphate proteoglycan (CSPG), in chick and mouse embryos. CSPG expression was used to isolate HB/Sox2+ cells for RNA-sequencing, revealing their distinguished molecular properties as typical NPSCs, which express known and newly-identified genes relating to stem cells, cancer, matrisome and cell-cycle. In contrast, the CSPG-/non-HB cells, displayed clear neural-differentiation transcriptome. To address whether CSPG is significant for hindbrain development, its expression was manipulated in vivo and in vitro. CSPG-manipulations shifted the stem versus differentiation state of HB cells, evident by their behavior and altered gene expression. These results provide novel understanding on the uniqueness of hindbrain boundaries as repetitive pools of NPSCs in-between the rapidly-growing rhombomeres, which rely on their microenvironment to maintain undifferentiated during development.

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Section: Hbs In Different Model Systemssupporting

confidence: 89%

Section: Introductionmentioning

confidence: 98%

Hindbrain boundaries as niches of neural progenitor/stem cells regulated by the extracellular matrix proteoglycan chondroitin sulphate

Hutchings

Nuriel

Lazar

et al. 2023

Preprint

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“…The newborn neurons labelled by HuC/D expression are located in the hindbrain and the neuronal tube (Figure 2B’”). Several studies have reported that dividing cells in the retina and brain migrate apically towards the periphery of the tissue (Weber et al 2014; Hevia et al 2022). Correspondingly, the multimodal imaging shows the localisation of mitotic cells at the outer part of the retina and at the interfaces of the hindbrain and somites which are organ regions unconstrained by any surrounding tissue (Figure 2B, B’” and zoom in Supplementary figure 4).…”

Section: Resultsmentioning

confidence: 99%

Visualisation of gene expression within the context of tissues: an X-ray computed tomography-based multimodal approach

Kairišs,

Sokolova,

Zilova

et al. 2023

Preprint

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The development of an organism is orchestrated by the spatial and temporal expression of genes. Accurate visualisation of gene expression patterns in the context of the surrounding tissues offers a glimpse into the mechanisms that drive morphogenesis. We developed correlative light-sheet fluorescence microscopy and X-ray computed tomography approach to map gene expression patterns to the whole organism’s 3D anatomy at cellular resolution. We show that this multimodal approach is applicable to gene expression visualised by protein-specific antibodies and fluorescence RNAin situhybridisation, offering a detailed understanding of individual phenotypic variations in model organisms. Furthermore, the approach provides a unique possibility to identify tissues together with their 3D cellular and molecular composition in anatomically less-definedin vitromodels, such as organoids. We anticipate that the visual and quantitative insights into the 3D distribution of gene expression within tissue architecture, by the multimodal approach developed here, will be equally valuable for reference atlases of model organisms development, as well as for comprehensive screens and morphogenesis studies ofin vitromodels.

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“…The onset of neurogenesis and overall NPC division mode changes have been well described for areas of the zebrafish nervous system, such as the hindbrain, spinal cord, and retina (Boije et al., 2015; He et al., 2012; Hevia et al., 2021; Kimura et al., 2008; Nerli et al., 2022; Satou et al., 2012). In this experimental work, we extend the existing body of work with a quantitative characterization of the first wave of neurogenesis in the developing zebrafish telencephalon using machine‐learning‐based nuclear segmentation and clonal analysis methods (Figure 6E).…”

Section: Discussionmentioning

confidence: 96%

“…Despite the advances made in understanding how the production of neuronal diversity from embryonic NPCs is regulated (Ge et al., 2022; Lodato & Arlotta, 2015), our understanding of the molecular and cell biological mechanisms underlying individual NPC division mode and fate decisions is limited. For instance, studies using various NPC lineage‐tracing methods have demonstrated that there is remarkable heterogeneity in the division modes used by individual NPCs in the vertebrate nervous system (Dong et al., 2012; Gao et al., 2014; Gomes et al., 2011; He et al., 2012; Hevia et al., 2021; Llorca et al., 2019). Moreover, it is not clear whether the embryonic NPCs present at the onset of neurogenesis are equipotent in their ability to produce the different types of neurons (Ge et al., 2022; Zechner et al., 2020).…”

Section: Introductionmentioning

confidence: 99%

A quantitative characterization of early neuron generation in the developing zebrafish telencephalon

Casas Gimeno,

Dvorianinova,

Lembke

et al. 2023

Developmental Neurobiology

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The adult brain is made up of anatomically and functionally distinct regions with specific neuronal compositions. At the root of this neuronal diversity are neural stem and progenitor cells (NPCs) that produce many neurons throughout embryonic development. During development, NPCs switch from initial expanding divisions to neurogenic divisions, which marks the onset of neurogenesis. Here, we aimed to understand when NPCs switch division modes to generate the first neurons in the anterior‐most part of the zebrafish brain, the telencephalon. To this end, we used the deep learning‐based segmentation method Cellpose and clonal analysis of individual NPCs to assess the production of neurons by NPCs in the first 24 h of zebrafish telencephalon development. Our results provide a quantitative atlas detailing the production of telencephalic neurons and NPC division modes between 14 and 24 h postfertilization. We find that within this timeframe, the switch to neurogenesis is gradual, with considerable heterogeneity in individual NPC neurogenic potential and division rates. This quantitative characterization of initial neurogenesis in the zebrafish telencephalon establishes a basis for future studies aimed at illuminating the molecular mechanisms and regulators of early neurogenesis.

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The neurogenic fate of the hindbrain boundaries relies on Notch3-dependent asymmetric cell divisions

Cited by 12 publications

References 60 publications

Hindbrain boundaries as niches of neural progenitor/stem cells regulated by the extracellular matrix proteoglycan chondroitin sulphate

Hindbrain boundaries as niches of neural progenitor/stem cells regulated by the extracellular matrix proteoglycan chondroitin sulphate

Visualisation of gene expression within the context of tissues: an X-ray computed tomography-based multimodal approach

A quantitative characterization of early neuron generation in the developing zebrafish telencephalon

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