Programming of neural progenitors of the adult subependymal zone towards a glutamatergic neuron lineage by neurogenin 2

Although adult subependymal zone (SEZ) neural stem cells mostly generate GABAergic interneurons, a small progenitor population expresses the proneural gene Neurog2 and produces glutamatergic neurons. Here, we determined whether Neurog2 could respecify SEZ neural stem cells and their progeny toward a...

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Autores: Peron, Sophie, Miyakoshi, L.M., Brill, M.S., Manzano-Franco, D., Serrano-López, J., Fan, W., Marichal, Nicolás, Ghanem, Alexander, Conzelmann, Karl-Klaus, Karow, Marisa, Ortega, F., Gascón, Sergio, Berninger, Benedikt
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/347226
Acesso em linha:http://hdl.handle.net/10261/347226
Access Level:acceso abierto
Palavra-chave:adult neurogenesis
adult subventricular zone
fate reprogramming
neural specification
neural stem cell
neurogenin 2
olfactory bulb
proneural gene
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oai_identifier_str oai:digital.csic.es:10261/347226
network_acronym_str ES
network_name_str España
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dc.title.none.fl_str_mv Programming of neural progenitors of the adult subependymal zone towards a glutamatergic neuron lineage by neurogenin 2
title Programming of neural progenitors of the adult subependymal zone towards a glutamatergic neuron lineage by neurogenin 2
spellingShingle Programming of neural progenitors of the adult subependymal zone towards a glutamatergic neuron lineage by neurogenin 2
Peron, Sophie
adult neurogenesis
adult subventricular zone
fate reprogramming
neural specification
neural stem cell
neurogenin 2
olfactory bulb
proneural gene
title_short Programming of neural progenitors of the adult subependymal zone towards a glutamatergic neuron lineage by neurogenin 2
title_full Programming of neural progenitors of the adult subependymal zone towards a glutamatergic neuron lineage by neurogenin 2
title_fullStr Programming of neural progenitors of the adult subependymal zone towards a glutamatergic neuron lineage by neurogenin 2
title_full_unstemmed Programming of neural progenitors of the adult subependymal zone towards a glutamatergic neuron lineage by neurogenin 2
title_sort Programming of neural progenitors of the adult subependymal zone towards a glutamatergic neuron lineage by neurogenin 2
dc.creator.none.fl_str_mv Peron, Sophie
Peron, Sophie
Miyakoshi, L.M.
Miyakoshi, L.M.
Brill, M.S.
Brill, M.S.
Manzano-Franco, D.
Manzano-Franco, D.
Serrano-López, J.
Serrano-López, J.
Fan, W.
Fan, W.
Marichal, Nicolás
Marichal, Nicolás
Ghanem, Alexander
Ghanem, Alexander
Conzelmann, Karl-Klaus
Conzelmann, Karl-Klaus
Karow, Marisa
Karow, Marisa
Ortega, F.
Ortega, F.
Gascón, Sergio
Berninger, Benedikt
author Peron, Sophie
author_facet Peron, Sophie
Miyakoshi, L.M.
Brill, M.S.
Manzano-Franco, D.
Serrano-López, J.
Fan, W.
Marichal, Nicolás
Ghanem, Alexander
Conzelmann, Karl-Klaus
Karow, Marisa
Ortega, F.
Gascón, Sergio
Berninger, Benedikt
author_role author
author2 Miyakoshi, L.M.
Brill, M.S.
Manzano-Franco, D.
Serrano-López, J.
Fan, W.
Marichal, Nicolás
Ghanem, Alexander
Conzelmann, Karl-Klaus
Karow, Marisa
Ortega, F.
Gascón, Sergio
Berninger, Benedikt
author2_role author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Institute of Molecular Biology (Germany)
Johannes Gutenberg University Mainz
Ministerio de Ciencia e Innovación (España)
Universidad Complutense de Madrid
Banco Santander
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv adult neurogenesis
adult subventricular zone
fate reprogramming
neural specification
neural stem cell
neurogenin 2
olfactory bulb
proneural gene
topic adult neurogenesis
adult subventricular zone
fate reprogramming
neural specification
neural stem cell
neurogenin 2
olfactory bulb
proneural gene
description Although adult subependymal zone (SEZ) neural stem cells mostly generate GABAergic interneurons, a small progenitor population expresses the proneural gene Neurog2 and produces glutamatergic neurons. Here, we determined whether Neurog2 could respecify SEZ neural stem cells and their progeny toward a glutamatergic fate. Retrovirus-mediated expression of Neurog2 induced the glutamatergic lineage markers TBR2 and TBR1 in cultured SEZ progenitors, which differentiated into functional glutamatergic neurons. Likewise, Neurog2-transduced SEZ progenitors acquired glutamatergic neuron hallmarks in vivo. Intriguingly, they failed to migrate toward the olfactory bulb and instead differentiated within the SEZ or the adjacent striatum, where they received connections from local neurons, as indicated by rabies virus-mediated monosynaptic tracing. In contrast, lentivirus-mediated expression of Neurog2 failed to reprogram early SEZ neurons, which maintained GABAergic identity and migrated to the olfactory bulb. Our data show that NEUROG2 can program SEZ progenitors toward a glutamatergic identity but fails to reprogram their neuronal progeny.
publishDate 2023
dc.date.none.fl_str_mv 2023
2024
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/347226
url http://hdl.handle.net/10261/347226
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
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info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-099345-B-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-128796OB-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-109155RB-I00
info:eu-repo/grantAgreement/MINECO//RYC-2015-19185
http://dx.doi.org/10.1016/j.stemcr.2023.10.019
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Cell Press
publisher.none.fl_str_mv Cell Press
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
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spelling Programming of neural progenitors of the adult subependymal zone towards a glutamatergic neuron lineage by neurogenin 2Peron, SophiePeron, SophieMiyakoshi, L.M.Miyakoshi, L.M.Brill, M.S.Brill, M.S.Manzano-Franco, D.Manzano-Franco, D.Serrano-López, J.Serrano-López, J.Fan, W.Fan, W.Marichal, NicolásMarichal, NicolásGhanem, AlexanderGhanem, AlexanderConzelmann, Karl-KlausConzelmann, Karl-KlausKarow, MarisaKarow, MarisaOrtega, F.Ortega, F.Gascón, SergioBerninger, Benediktadult neurogenesisadult subventricular zonefate reprogrammingneural specificationneural stem cellneurogenin 2olfactory bulbproneural geneAlthough adult subependymal zone (SEZ) neural stem cells mostly generate GABAergic interneurons, a small progenitor population expresses the proneural gene Neurog2 and produces glutamatergic neurons. Here, we determined whether Neurog2 could respecify SEZ neural stem cells and their progeny toward a glutamatergic fate. Retrovirus-mediated expression of Neurog2 induced the glutamatergic lineage markers TBR2 and TBR1 in cultured SEZ progenitors, which differentiated into functional glutamatergic neurons. Likewise, Neurog2-transduced SEZ progenitors acquired glutamatergic neuron hallmarks in vivo. Intriguingly, they failed to migrate toward the olfactory bulb and instead differentiated within the SEZ or the adjacent striatum, where they received connections from local neurons, as indicated by rabies virus-mediated monosynaptic tracing. In contrast, lentivirus-mediated expression of Neurog2 failed to reprogram early SEZ neurons, which maintained GABAergic identity and migrated to the olfactory bulb. Our data show that NEUROG2 can program SEZ progenitors toward a glutamatergic identity but fails to reprogram their neuronal progeny.We are grateful to Ana Beltrán-Arranz and Laia Torres-Masjoan for help with monosynaptic tracing experiments. We are grateful to Dr. Magdalena Götz for support throughout the project. We acknowledge the Microscopy Core Facility of the Institute of Molecular Biology (IMB) in Mainz. This work was supported by a grant from the Wellcome Trust (206410/Z/17/Z). For the purpose of open access, the authors have applied a CC BY public copyright license to any author-accepted manuscript version arising from this submission. Furthermore, this work was supported by grants from the Deutsche Forschungsgemeinschaft to B.B. (CRC1080, project number 221828878; BE 4182 11-1, project number 357058359) and to M.S.B. (LE 4610 1, project number 450131873); the Research Initiative of the State of Rhineland-Palatinate at the Johannes Gutenberg University Mainz (ReALity) to B.B.; the Spanish Ministry of Science and Innovation (MICINN) to S.G. (grants RTI2018-099345-B-I00 and PID2021-128796OB-I00) and F.O. (PID2019-109155RB-I00 and BFU2015- 70067REDC); and the Inneruniversitäre Forschungsförderung Stufe 1 of the Universitätsmedizin Mainz to S.P. N.M. was supported by a fellowship from the Human Frontiers Science Program (LT000646/2015), W.F. by a fellowship from the China Scholarship Council, J.S.-L. by a fellowship from the UCM-Santander (CT82/20-CT83/20), and S.G. by the Ramón y Cajal Programme (RYC-2015-19185).Cell PressInstitute of Molecular Biology (Germany)Johannes Gutenberg University MainzMinisterio de Ciencia e Innovación (España)Universidad Complutense de MadridBanco SantanderConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2024202420232024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/347226reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-099345-B-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-128796OB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-109155RB-I00info:eu-repo/grantAgreement/MINECO//RYC-2015-19185http://dx.doi.org/10.1016/j.stemcr.2023.10.019Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3472262026-05-22T06:33:51Z
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