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Dynamic spatiotemporal coordination of neural stem cell fate decisions occurs through local feedback in the adult vertebrate brain

Neural stem cell (NSC) populations persist in the adult vertebrate brain over a lifetime, and their homeostasis is controlled at the population level through unknown mechanisms. Here, we combine dynamic imaging of entire NSC populations in their in vivo niche over several weeks with pharmacological...

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Autores principales: Dray, Nicolas, Mancini, Laure, Binshtok, Udi, Cheysson, Felix, Supatto, Willy, Mahou, Pierre, Bedu, Sébastien, Ortica, Sara, Than-Trong, Emmanuel, Krecsmarik, Monika, Herbert, Sébastien, Masson, Jean-Baptiste, Tinevez, Jean-Yves, Lang, Gabriel, Beaurepaire, Emmanuel, Sprinzak, David, Bally-Cuif, Laure
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8363814/
https://www.ncbi.nlm.nih.gov/pubmed/33823144
http://dx.doi.org/10.1016/j.stem.2021.03.014
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author Dray, Nicolas
Mancini, Laure
Binshtok, Udi
Cheysson, Felix
Supatto, Willy
Mahou, Pierre
Bedu, Sébastien
Ortica, Sara
Than-Trong, Emmanuel
Krecsmarik, Monika
Herbert, Sébastien
Masson, Jean-Baptiste
Tinevez, Jean-Yves
Lang, Gabriel
Beaurepaire, Emmanuel
Sprinzak, David
Bally-Cuif, Laure
author_facet Dray, Nicolas
Mancini, Laure
Binshtok, Udi
Cheysson, Felix
Supatto, Willy
Mahou, Pierre
Bedu, Sébastien
Ortica, Sara
Than-Trong, Emmanuel
Krecsmarik, Monika
Herbert, Sébastien
Masson, Jean-Baptiste
Tinevez, Jean-Yves
Lang, Gabriel
Beaurepaire, Emmanuel
Sprinzak, David
Bally-Cuif, Laure
author_sort Dray, Nicolas
collection PubMed
description Neural stem cell (NSC) populations persist in the adult vertebrate brain over a lifetime, and their homeostasis is controlled at the population level through unknown mechanisms. Here, we combine dynamic imaging of entire NSC populations in their in vivo niche over several weeks with pharmacological manipulations, mathematical modeling, and spatial statistics and demonstrate that NSCs use spatiotemporally resolved local feedback signals to coordinate their decision to divide in adult zebrafish brains. These involve Notch-mediated short-range inhibition from transient neural progenitors and a dispersion effect from the dividing NSCs themselves exerted with a delay of 9–12 days. Simulations from a stochastic NSC lattice model capturing these interactions demonstrate that these signals are linked by lineage progression and control the spatiotemporal distribution of output neurons. These results highlight how local and temporally delayed interactions occurring between brain germinal cells generate self-propagating dynamics that maintain NSC population homeostasis and coordinate specific spatiotemporal correlations.
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spelling pubmed-83638142021-08-23 Dynamic spatiotemporal coordination of neural stem cell fate decisions occurs through local feedback in the adult vertebrate brain Dray, Nicolas Mancini, Laure Binshtok, Udi Cheysson, Felix Supatto, Willy Mahou, Pierre Bedu, Sébastien Ortica, Sara Than-Trong, Emmanuel Krecsmarik, Monika Herbert, Sébastien Masson, Jean-Baptiste Tinevez, Jean-Yves Lang, Gabriel Beaurepaire, Emmanuel Sprinzak, David Bally-Cuif, Laure Cell Stem Cell Article Neural stem cell (NSC) populations persist in the adult vertebrate brain over a lifetime, and their homeostasis is controlled at the population level through unknown mechanisms. Here, we combine dynamic imaging of entire NSC populations in their in vivo niche over several weeks with pharmacological manipulations, mathematical modeling, and spatial statistics and demonstrate that NSCs use spatiotemporally resolved local feedback signals to coordinate their decision to divide in adult zebrafish brains. These involve Notch-mediated short-range inhibition from transient neural progenitors and a dispersion effect from the dividing NSCs themselves exerted with a delay of 9–12 days. Simulations from a stochastic NSC lattice model capturing these interactions demonstrate that these signals are linked by lineage progression and control the spatiotemporal distribution of output neurons. These results highlight how local and temporally delayed interactions occurring between brain germinal cells generate self-propagating dynamics that maintain NSC population homeostasis and coordinate specific spatiotemporal correlations. Cell Press 2021-08-05 /pmc/articles/PMC8363814/ /pubmed/33823144 http://dx.doi.org/10.1016/j.stem.2021.03.014 Text en © 2021 The Author(s) https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Dray, Nicolas
Mancini, Laure
Binshtok, Udi
Cheysson, Felix
Supatto, Willy
Mahou, Pierre
Bedu, Sébastien
Ortica, Sara
Than-Trong, Emmanuel
Krecsmarik, Monika
Herbert, Sébastien
Masson, Jean-Baptiste
Tinevez, Jean-Yves
Lang, Gabriel
Beaurepaire, Emmanuel
Sprinzak, David
Bally-Cuif, Laure
Dynamic spatiotemporal coordination of neural stem cell fate decisions occurs through local feedback in the adult vertebrate brain
title Dynamic spatiotemporal coordination of neural stem cell fate decisions occurs through local feedback in the adult vertebrate brain
title_full Dynamic spatiotemporal coordination of neural stem cell fate decisions occurs through local feedback in the adult vertebrate brain
title_fullStr Dynamic spatiotemporal coordination of neural stem cell fate decisions occurs through local feedback in the adult vertebrate brain
title_full_unstemmed Dynamic spatiotemporal coordination of neural stem cell fate decisions occurs through local feedback in the adult vertebrate brain
title_short Dynamic spatiotemporal coordination of neural stem cell fate decisions occurs through local feedback in the adult vertebrate brain
title_sort dynamic spatiotemporal coordination of neural stem cell fate decisions occurs through local feedback in the adult vertebrate brain
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8363814/
https://www.ncbi.nlm.nih.gov/pubmed/33823144
http://dx.doi.org/10.1016/j.stem.2021.03.014
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