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

Sophie Péron; Leo M Miyakoshi; Monika S Brill; Diana Manzano-Franco; Julia Serrano-López; Wenqiang Fan; Nicolas Marichal Negrin; Alexander Ghanem; Karl-Klaus Conzelmann; Marisa Karow; Felipe  Ortega; Sergio Gascón; Benedikt Berninger

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

Sophie Péron, Leo M Miyakoshi, Monika S Brill, Diana Manzano-Franco, Julia Serrano-López, Wenqiang Fan, Nicolas Marichal Negrin, Alexander Ghanem, Karl-Klaus Conzelmann, Marisa Karow, Felipe Ortega, Sergio Gascón, Benedikt Berninger

Developmental Neurobiology

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Abstract

While 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 towards 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 towards 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 towards a glutamatergic identity, but fails to reprogram their neuronal progeny.

Original language	English
Journal	Stem Cell Reports
Early online date	22 Nov 2023
Publication status	E-pub ahead of print - 22 Nov 2023

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Peron et al 2023_Stem Cell ReportsAccepted author manuscript, 9.16 MBLicence: CC BY

https://www.cell.com/stem-cell-reports/fulltext/S2213-6711(23)00421-6Licence: CC BY-NC-ND

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Péron, S., Miyakoshi, L. M., Brill, M. S., Manzano-Franco, D., Serrano-López, J., Fan, W., Marichal Negrin, N., Ghanem, A., Conzelmann, K.-K., Karow, M., Ortega, F., Gascón, S., & Berninger, B. (2023). Programming of neural progenitors of the adult subependymal zone towards a glutamatergic neuron lineage by neurogenin 2. Stem Cell Reports. Advance online publication. https://www.cell.com/stem-cell-reports/fulltext/S2213-6711(23)00421-6

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

abstract = "While 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 towards 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 towards 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 towards a glutamatergic identity, but fails to reprogram their neuronal progeny.",

author = "Sophie P{\'e}ron and Miyakoshi, {Leo M} and Brill, {Monika S} and Diana Manzano-Franco and Julia Serrano-L{\'o}pez and Wenqiang Fan and {Marichal Negrin}, Nicolas and Alexander Ghanem and Karl-Klaus Conzelmann and Marisa Karow and Felipe Ortega and Sergio Gasc{\'o}n and Benedikt Berninger",

year = "2023",

month = nov,

day = "22",

language = "English",

journal = "Stem Cell Reports",

issn = "2213-6711",

publisher = "CELL PRESS",

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Péron, S, Miyakoshi, LM, Brill, MS, Manzano-Franco, D, Serrano-López, J, Fan, W, Marichal Negrin, N, Ghanem, A, Conzelmann, K-K, Karow, M, Ortega, F, Gascón, S & Berninger, B 2023, 'Programming of neural progenitors of the adult subependymal zone towards a glutamatergic neuron lineage by neurogenin 2', Stem Cell Reports. <https://www.cell.com/stem-cell-reports/fulltext/S2213-6711(23)00421-6>

TY - JOUR

T1 - Programming of neural progenitors of the adult subependymal zone towards a glutamatergic neuron lineage by neurogenin 2

AU - Péron, Sophie

AU - Miyakoshi, Leo M

AU - Brill, Monika S

AU - Manzano-Franco, Diana

AU - Serrano-López, Julia

AU - Fan, Wenqiang

AU - Marichal Negrin, Nicolas

AU - Ghanem, Alexander

AU - Conzelmann, Karl-Klaus

AU - Karow, Marisa

AU - Ortega, Felipe

AU - Gascón, Sergio

AU - Berninger, Benedikt

PY - 2023/11/22

Y1 - 2023/11/22

N2 - While 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 towards 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 towards 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 towards a glutamatergic identity, but fails to reprogram their neuronal progeny.

AB - While 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 towards 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 towards 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 towards a glutamatergic identity, but fails to reprogram their neuronal progeny.

M3 - Article

SN - 2213-6711

JO - Stem Cell Reports

JF - Stem Cell Reports

ER -

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

Abstract

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