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

Animals Brain Cell Proliferation Feedback Neural Stem Cells Neurogenesis Zebrafish
Notch signaling adult neural stem cell analytical modeling intrinsic niche pallium population behavior quiescence spatial statistics spatiotemporal homeostasis zebrafish

Journal

Cell stem cell
ISSN: 1875-9777
Titre abrégé: Cell Stem Cell
Pays: United States
ID NLM: 101311472

Informations de publication

Date de publication:
05 08 2021
Historique:
received: 23 07 2020
revised: 21 12 2020
accepted: 16 03 2021
pubmed: 7 4 2021
medline: 24 9 2021
entrez: 6 4 2021
Statut: ppublish

Résumé

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.

Identifiants

DOI: 10.1016/j.stem.2021.03.014 PMID: 33823144 PMC: PMC8363814
pubmed: 33823144
pii: S1934-5909(21)00120-X
doi: 10.1016/j.stem.2021.03.014
pmc: PMC8363814
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1457-1472.e12

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

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Auteurs

Nicolas Dray (N)

Zebrafish Neurogenetics Unit, Institut Pasteur, UMR3738, CNRS, team supported by La Ligue Nationale Contre le Cancer, 75015 Paris, France. Electronic address: nicolas.dray@pasteur.fr.

Laure Mancini (L)

Zebrafish Neurogenetics Unit, Institut Pasteur, UMR3738, CNRS, team supported by La Ligue Nationale Contre le Cancer, 75015 Paris, France; Sorbonne Université, Collège doctoral, 75005 Paris, France.

Udi Binshtok (U)

School of Neurobiology, Biochemistry, and Biophysics, The George S. Wise Faculty of Life Sciences, Tel Aviv University, 69978 Tel Aviv, Israel.

Felix Cheysson (F)

Université Paris-Saclay, AgroParisTech, INRAE, UMR MIA-Paris, 75005 Paris, France; Epidemiology and Modeling of Bacterial Evasion to Antibacterials Unit (EMEA), Institut Pasteur, 75015 Paris, France; Anti-infective Evasion and Pharmacoepidemiology Team, Centre for Epidemiology and Public Health (CESP), INSERM/UVSQ, Villejuif Cedex, France.

Willy Supatto (W)

Laboratory for Optics and Biosciences, Ecole Polytechnique, CNRS, INSERM, IP Paris, 91128 Palaiseau, France.

Pierre Mahou (P)

Laboratory for Optics and Biosciences, Ecole Polytechnique, CNRS, INSERM, IP Paris, 91128 Palaiseau, France.

Sébastien Bedu (S)

Zebrafish Neurogenetics Unit, Institut Pasteur, UMR3738, CNRS, team supported by La Ligue Nationale Contre le Cancer, 75015 Paris, France.

Sara Ortica (S)

Zebrafish Neurogenetics Unit, Institut Pasteur, UMR3738, CNRS, team supported by La Ligue Nationale Contre le Cancer, 75015 Paris, France.

Emmanuel Than-Trong (E)

Zebrafish Neurogenetics Unit, Institut Pasteur, UMR3738, CNRS, team supported by La Ligue Nationale Contre le Cancer, 75015 Paris, France.

Monika Krecsmarik (M)

Zebrafish Neurogenetics Unit, Institut Pasteur, UMR3738, CNRS, team supported by La Ligue Nationale Contre le Cancer, 75015 Paris, France.

Sébastien Herbert (S)

Department of Developmental and Stem Cell Biology, Institut Pasteur, 75015 Paris, France; Image Analysis Hub, Institut Pasteur, 75015 Paris, France.

Jean-Baptiste Masson (JB)

Department of Neuroscience and Department of Computational Biology, Institut Pasteur, 75015 Paris, France.

Jean-Yves Tinevez (JY)

Image Analysis Hub, Institut Pasteur, 75015 Paris, France.

Gabriel Lang (G)

Université Paris-Saclay, AgroParisTech, INRAE, UMR MIA-Paris, 75005 Paris, France.

Emmanuel Beaurepaire (E)

Laboratory for Optics and Biosciences, Ecole Polytechnique, CNRS, INSERM, IP Paris, 91128 Palaiseau, France.

David Sprinzak (D)

School of Neurobiology, Biochemistry, and Biophysics, The George S. Wise Faculty of Life Sciences, Tel Aviv University, 69978 Tel Aviv, Israel. Electronic address: davidsp@tauex.tau.ac.il.

Laure Bally-Cuif (L)

Zebrafish Neurogenetics Unit, Institut Pasteur, UMR3738, CNRS, team supported by La Ligue Nationale Contre le Cancer, 75015 Paris, France. Electronic address: laure.bally-cuif@pasteur.fr.

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Classifications MeSH

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