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Single-cell analysis of the postnatal dorsal V-SVZ reveals a role for Bmpr1a signaling in silencing pallial germinal activity

The ventricular-subventricular zone (V-SVZ) is the largest neurogenic region of the postnatal forebrain, containing neural stem cells (NSCs) that emerge from both the embryonic pallium and subpallium. Despite of this dual origin, glutamatergic neurogenesis declines rapidly after birth, while GABAerg...

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Autores principales: Marcy, Guillaume, Foucault, Louis, Babina, Elodie, Capeliez, Timothy, Texeraud, Emeric, Zweifel, Stefan, Heinrich, Christophe, Hernandez-Vargas, Hector, Parras, Carlos, Jabaudon, Denis, Raineteau, Olivier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10162676/
https://www.ncbi.nlm.nih.gov/pubmed/37146152
http://dx.doi.org/10.1126/sciadv.abq7553
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author Marcy, Guillaume
Foucault, Louis
Babina, Elodie
Capeliez, Timothy
Texeraud, Emeric
Zweifel, Stefan
Heinrich, Christophe
Hernandez-Vargas, Hector
Parras, Carlos
Jabaudon, Denis
Raineteau, Olivier
author_facet Marcy, Guillaume
Foucault, Louis
Babina, Elodie
Capeliez, Timothy
Texeraud, Emeric
Zweifel, Stefan
Heinrich, Christophe
Hernandez-Vargas, Hector
Parras, Carlos
Jabaudon, Denis
Raineteau, Olivier
author_sort Marcy, Guillaume
collection PubMed
description The ventricular-subventricular zone (V-SVZ) is the largest neurogenic region of the postnatal forebrain, containing neural stem cells (NSCs) that emerge from both the embryonic pallium and subpallium. Despite of this dual origin, glutamatergic neurogenesis declines rapidly after birth, while GABAergic neurogenesis persists throughout life. We performed single-cell RNA sequencing of the postnatal dorsal V-SVZ for unraveling the mechanisms leading to pallial lineage germinal activity silencing. We show that pallial NSCs enter a state of deep quiescence, characterized by high bone morphogenetic protein (BMP) signaling, reduced transcriptional activity and Hopx expression, while in contrast, subpallial NSCs remain primed for activation. Induction of deep quiescence is paralleled by a rapid blockade of glutamatergic neuron production and differentiation. Last, manipulation of Bmpr1a demonstrates its key role in mediating these effects. Together, our results highlight a central role of BMP signaling in synchronizing quiescence induction and blockade of neuronal differentiation to rapidly silence pallial germinal activity after birth.
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spelling pubmed-101626762023-05-06 Single-cell analysis of the postnatal dorsal V-SVZ reveals a role for Bmpr1a signaling in silencing pallial germinal activity Marcy, Guillaume Foucault, Louis Babina, Elodie Capeliez, Timothy Texeraud, Emeric Zweifel, Stefan Heinrich, Christophe Hernandez-Vargas, Hector Parras, Carlos Jabaudon, Denis Raineteau, Olivier Sci Adv Biomedicine and Life Sciences The ventricular-subventricular zone (V-SVZ) is the largest neurogenic region of the postnatal forebrain, containing neural stem cells (NSCs) that emerge from both the embryonic pallium and subpallium. Despite of this dual origin, glutamatergic neurogenesis declines rapidly after birth, while GABAergic neurogenesis persists throughout life. We performed single-cell RNA sequencing of the postnatal dorsal V-SVZ for unraveling the mechanisms leading to pallial lineage germinal activity silencing. We show that pallial NSCs enter a state of deep quiescence, characterized by high bone morphogenetic protein (BMP) signaling, reduced transcriptional activity and Hopx expression, while in contrast, subpallial NSCs remain primed for activation. Induction of deep quiescence is paralleled by a rapid blockade of glutamatergic neuron production and differentiation. Last, manipulation of Bmpr1a demonstrates its key role in mediating these effects. Together, our results highlight a central role of BMP signaling in synchronizing quiescence induction and blockade of neuronal differentiation to rapidly silence pallial germinal activity after birth. American Association for the Advancement of Science 2023-05-05 /pmc/articles/PMC10162676/ /pubmed/37146152 http://dx.doi.org/10.1126/sciadv.abq7553 Text en Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY). https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Biomedicine and Life Sciences
Marcy, Guillaume
Foucault, Louis
Babina, Elodie
Capeliez, Timothy
Texeraud, Emeric
Zweifel, Stefan
Heinrich, Christophe
Hernandez-Vargas, Hector
Parras, Carlos
Jabaudon, Denis
Raineteau, Olivier
Single-cell analysis of the postnatal dorsal V-SVZ reveals a role for Bmpr1a signaling in silencing pallial germinal activity
title Single-cell analysis of the postnatal dorsal V-SVZ reveals a role for Bmpr1a signaling in silencing pallial germinal activity
title_full Single-cell analysis of the postnatal dorsal V-SVZ reveals a role for Bmpr1a signaling in silencing pallial germinal activity
title_fullStr Single-cell analysis of the postnatal dorsal V-SVZ reveals a role for Bmpr1a signaling in silencing pallial germinal activity
title_full_unstemmed Single-cell analysis of the postnatal dorsal V-SVZ reveals a role for Bmpr1a signaling in silencing pallial germinal activity
title_short Single-cell analysis of the postnatal dorsal V-SVZ reveals a role for Bmpr1a signaling in silencing pallial germinal activity
title_sort single-cell analysis of the postnatal dorsal v-svz reveals a role for bmpr1a signaling in silencing pallial germinal activity
topic Biomedicine and Life Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10162676/
https://www.ncbi.nlm.nih.gov/pubmed/37146152
http://dx.doi.org/10.1126/sciadv.abq7553
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