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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...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2021
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Materias: | |
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. |
format | Online Article Text |
id | pubmed-8011756 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
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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