Neural stem cell pools in the vertebrate adult brain: Homeostasis from cell‐autonomous decisions or community rules?

Dray, Nicolas; Than‐Trong, Emmanuel; Bally‐Cuif, Laure

doi:10.1002/bies.202000228

Cited by 20 publications

(20 citation statements)

References 103 publications

(119 reference statements)

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“…Specifically, in the zebrafish telencephalon, Notch3 is expressed in RGCs and promotes quiescence of NSCs [27]. This signaling originates, at least in part, from the progenitor population itself [28,29]. Notch signaling appears to serve as an intrinsic signaling cue for the regulation of quiescence and the maintenance of the stem cell population in mammals and fish [1,9].…”

Section: Introductionmentioning

confidence: 99%

Neuron-Radial Glial Cell Communication via BMP/Id1 Signaling Is Key to Long-Term Maintenance of the Regenerative Capacity of the Adult Zebrafish Telencephalon

Zhang

Lübke

Chen

et al. 2021

Cells

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The central nervous system of adult zebrafish displays an extraordinary neurogenic and regenerative capacity. In the zebrafish adult brain, this regenerative capacity relies on neural stem cells (NSCs) and the careful management of the NSC pool. However, the mechanisms controlling NSC pool maintenance are not yet fully understood. Recently, Bone Morphogenetic Proteins (BMPs) and their downstream effector Id1 (Inhibitor of differentiation 1) were suggested to act as key players in NSC maintenance under constitutive and regenerative conditions. Here, we further investigated the role of BMP/Id1 signaling in these processes, using different genetic and pharmacological approaches. Our data show that BMPs are mainly expressed by neurons in the adult telencephalon, while id1 is expressed in NSCs, suggesting a neuron-NSC communication via the BMP/Id1 signaling axis. Furthermore, manipulation of BMP signaling by conditionally inducing or repressing BMP signaling via heat-shock, lead to an increase or a decrease of id1 expression in the NSCs, respectively. Induction of id1 was followed by an increase in the number of quiescent NSCs, while knocking down id1 expression caused an increase in NSC proliferation. In agreement, genetic ablation of id1 function lead to increased proliferation of NSCs, followed by depletion of the stem cell pool with concomitant failure to heal injuries in repeatedly injured mutant telencephala. Moreover, pharmacological inhibition of BMP and Notch signaling suggests that the two signaling systems cooperate and converge onto the transcriptional regulator her4.1. Interestingly, brain injury lead to a depletion of NSCs in animals lacking BMP/Id1 signaling despite an intact Notch pathway. Taken together, our data demonstrate how neurons feedback on NSC proliferation and that BMP1/Id1 signaling acts as a safeguard of the NSC pool under regenerative conditions.

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Section: Introductionmentioning

confidence: 99%

Neuron-Radial Glial Cell Communication via BMP/Id1 Signaling Is Key to Long-Term Maintenance of the Regenerative Capacity of the Adult Zebrafish Telencephalon

Zhang

Lübke

Chen

et al. 2021

Cells

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“…NSCs are organized as an epitheliallike structure lining ventricles that has to be maintained functional for very long periods of time (often over years). To understand NSC population homeostasis, it is essential to integrate large-scale and long-term imaging of the NSC pool and the zebrafish telencephalon has recently emerged as a unique model for these studies (34,35). To study cellular and mechanical functions of NSCs over the entire dorsal telencephalon (pallium) we can image whole-mount immunostainings against ZO1 (a component of tight junctions (5)), highlighting apical domains of the NSCs.…”

Section: Accurate Measurements Of Cell Morphology: Deprojmentioning

confidence: 99%

“…In vertebrate adult brains, neural stem cells (NSCs) are organized in a pool forming an epithelium. The coordination of their behavior, such as division or differentiation, are in part regulated via local cell-cell interactions (4) but is also regulated via large-scale coordination (5). Thus, the elucidation of biological questions related to processes involving complex epithelia now require the imaging of large tissues, while reaching single cell resolution and single cell shape quantitation.…”

Section: Introductionmentioning

confidence: 99%

LocalZProjectorandDeProj: A toolbox for local 2D projection and accurate morphometrics of large 3D microscopy images

Herbert

Valon

Mancini

et al. 2021

Preprint

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BackgroundQuantitative imaging of epithelial tissues prompts for bioimage analysis tools that are widely applicable and accurate. In the case of imaging 3D tissues, a common post-processing step consists in projecting the acquired 3D volume on a 2D plane mapping the tissue surface. Indeed, while segmenting the tissue cells is amenable on 2D projections, it is still very difficult and cumbersome in 3D. However, for many specimen and models used in Developmental and Cell Biology, the complex content of the image volume surrounding the epithelium in a tissue often reduces the visibility of the biological object in the projection, compromising its subsequent analysis. In addition, the projection will distort the geometry of the tissue and can lead to strong artifacts in the morphology measurement.ResultsHere we introduce DProj a user-friendly tool-box built to robustly project epithelia on their 2D surface from 3D volumes, and to produce accurate morphology measurement corrected for the projection distortion, even for very curved tissues. DProj is built upon two components. LocalZProjector is a user-friendly and configurable Fiji plugin that generates 2D projections and height-maps from potentially large 3D stacks (larger than 40 GB per time-point) by only incorporating the signal of interest, despite a possibly complex image content. DeProj is a MATLAB tool that generates correct morphology measurements by combining the height-map output (such as the one offered by LocalZProjector) and the results of the cell segmentation on the 2D projection. In this paper we demonstrate DProj effectiveness over a wide range of different biological samples. We then compare its performance and accuracy against similar existing tools.ConclusionsWe find that LocalZProjector performs well even in situations where the volume to project contains spurious structures. We show that it can process large images without a pre-processing step. We study the impact of geometrical distortions on morphological measurements induced by the projection. We measured very large distortions which are then corrected by DeProj, providing accurate outputs.

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“…Generally, the process of neural regeneration is based on a complex network of transcription factors and regulators, signaling pathways, as well as non-coding areas of the genome, giving rise to non-coding RNA molecules [ 20 , 21 , 22 ]. It is pivotal that there is tight spatial and temporal control of this network to maintain the balance between homeostasis and regeneration [ 23 , 24 ]. One chance to battle neurodegenerative diseases is to identify key players of this complex network and reactivate neurogenesis from NSCs in the adult mammalian brain.…”

Section: Introductionmentioning

confidence: 99%

mdka Expression Is Associated with Quiescent Neural Stem Cells during Constitutive and Reactive Neurogenesis in the Adult Zebrafish Telencephalon

et al. 2022

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In contrast to mammals, adult zebrafish display an extraordinary capacity to heal injuries and repair damage in the central nervous system. Pivotal for the regenerative capacity of the zebrafish brain at adult stages is the precise control of neural stem cell (NSC) behavior and the maintenance of the stem cell pool. The gene mdka, a member of a small family of heparin binding growth factors, was previously shown to be involved in regeneration in the zebrafish retina, heart, and fin. Here, we investigated the expression pattern of the gene mdka and its paralogue mdkb in the zebrafish adult telencephalon under constitutive and regenerative conditions. Our findings show that only mdka expression is specifically restricted to the telencephalic ventricle, a stem cell niche of the zebrafish telencephalon. In this brain region, mdka is particularly expressed in the quiescent stem cells. Interestingly, after brain injury, mdka expression remains restricted to the resting stem cell, which might suggest a role of mdka in regulating stem cell quiescence.

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Neural stem cell pools in the vertebrate adult brain: Homeostasis from cell‐autonomous decisions or community rules?

Cited by 20 publications

References 103 publications

Neuron-Radial Glial Cell Communication via BMP/Id1 Signaling Is Key to Long-Term Maintenance of the Regenerative Capacity of the Adult Zebrafish Telencephalon

Neuron-Radial Glial Cell Communication via BMP/Id1 Signaling Is Key to Long-Term Maintenance of the Regenerative Capacity of the Adult Zebrafish Telencephalon

LocalZProjectorandDeProj: A toolbox for local 2D projection and accurate morphometrics of large 3D microscopy images

mdka Expression Is Associated with Quiescent Neural Stem Cells during Constitutive and Reactive Neurogenesis in the Adult Zebrafish Telencephalon

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