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The microcephaly gene Donson is essential for progenitors of cortical glutamatergic and GABAergic neurons

Biallelic mutations in DONSON, an essential gene encoding for a replication fork protection factor, were linked to skeletal abnormalities and microcephaly. To better understand DONSON function in corticogenesis, we characterized Donson expression and consequences of conditional Donson deletion in th...

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Autores principales: Venkataramanappa, Sathish, Schütz, Dagmar, Saaber, Friederike, Kumar, Praveen Ashok, Abe, Philipp, Schulz, Stefan, Stumm, Ralf
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8011756/
https://www.ncbi.nlm.nih.gov/pubmed/33739968
http://dx.doi.org/10.1371/journal.pgen.1009441
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author Venkataramanappa, Sathish
Schütz, Dagmar
Saaber, Friederike
Kumar, Praveen Ashok
Abe, Philipp
Schulz, Stefan
Stumm, Ralf
author_facet Venkataramanappa, Sathish
Schütz, Dagmar
Saaber, Friederike
Kumar, Praveen Ashok
Abe, Philipp
Schulz, Stefan
Stumm, Ralf
author_sort Venkataramanappa, Sathish
collection PubMed
description Biallelic mutations in DONSON, an essential gene encoding for a replication fork protection factor, were linked to skeletal abnormalities and microcephaly. To better understand DONSON function in corticogenesis, we characterized Donson expression and consequences of conditional Donson deletion in the mouse telencephalon. Donson was widely expressed in the proliferation and differentiation zones of the embryonic dorsal and ventral telencephalon, which was followed by a postnatal expression decrease. Emx1-Cre-mediated Donson deletion in progenitors of cortical glutamatergic neurons caused extensive apoptosis in the early dorsomedial neuroepithelium, thus preventing formation of the neocortex and hippocampus. At the place of the missing lateral neocortex, these mutants exhibited a dorsal extension of an early-generated paleocortex. Targeting cortical neurons at the intermediate progenitor stage using Tbr2-Cre evoked no apparent malformations, whereas Nkx2.1-Cre-mediated Donson deletion in subpallial progenitors ablated 75% of Nkx2.1-derived cortical GABAergic neurons. Thus, the early telencephalic neuroepithelium depends critically on Donson function. Our findings help explain why the neocortex is most severely affected in individuals with DONSON mutations and suggest that DONSON-dependent microcephaly might be associated with so far unrecognized defects in cortical GABAergic neurons. Targeting Donson using an appropriate recombinase is proposed as a feasible strategy to ablate proliferating and nascent cells in experimental research.
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spelling pubmed-80117562021-04-07 The microcephaly gene Donson is essential for progenitors of cortical glutamatergic and GABAergic neurons Venkataramanappa, Sathish Schütz, Dagmar Saaber, Friederike Kumar, Praveen Ashok Abe, Philipp Schulz, Stefan Stumm, Ralf PLoS Genet Research Article Biallelic mutations in DONSON, an essential gene encoding for a replication fork protection factor, were linked to skeletal abnormalities and microcephaly. To better understand DONSON function in corticogenesis, we characterized Donson expression and consequences of conditional Donson deletion in the mouse telencephalon. Donson was widely expressed in the proliferation and differentiation zones of the embryonic dorsal and ventral telencephalon, which was followed by a postnatal expression decrease. Emx1-Cre-mediated Donson deletion in progenitors of cortical glutamatergic neurons caused extensive apoptosis in the early dorsomedial neuroepithelium, thus preventing formation of the neocortex and hippocampus. At the place of the missing lateral neocortex, these mutants exhibited a dorsal extension of an early-generated paleocortex. Targeting cortical neurons at the intermediate progenitor stage using Tbr2-Cre evoked no apparent malformations, whereas Nkx2.1-Cre-mediated Donson deletion in subpallial progenitors ablated 75% of Nkx2.1-derived cortical GABAergic neurons. Thus, the early telencephalic neuroepithelium depends critically on Donson function. Our findings help explain why the neocortex is most severely affected in individuals with DONSON mutations and suggest that DONSON-dependent microcephaly might be associated with so far unrecognized defects in cortical GABAergic neurons. Targeting Donson using an appropriate recombinase is proposed as a feasible strategy to ablate proliferating and nascent cells in experimental research. Public Library of Science 2021-03-19 /pmc/articles/PMC8011756/ /pubmed/33739968 http://dx.doi.org/10.1371/journal.pgen.1009441 Text en © 2021 Venkataramanappa et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Venkataramanappa, Sathish
Schütz, Dagmar
Saaber, Friederike
Kumar, Praveen Ashok
Abe, Philipp
Schulz, Stefan
Stumm, Ralf
The microcephaly gene Donson is essential for progenitors of cortical glutamatergic and GABAergic neurons
title The microcephaly gene Donson is essential for progenitors of cortical glutamatergic and GABAergic neurons
title_full The microcephaly gene Donson is essential for progenitors of cortical glutamatergic and GABAergic neurons
title_fullStr The microcephaly gene Donson is essential for progenitors of cortical glutamatergic and GABAergic neurons
title_full_unstemmed The microcephaly gene Donson is essential for progenitors of cortical glutamatergic and GABAergic neurons
title_short The microcephaly gene Donson is essential for progenitors of cortical glutamatergic and GABAergic neurons
title_sort microcephaly gene donson is essential for progenitors of cortical glutamatergic and gabaergic neurons
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8011756/
https://www.ncbi.nlm.nih.gov/pubmed/33739968
http://dx.doi.org/10.1371/journal.pgen.1009441
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