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Cortical overgrowth in a preclinical forebrain organoid model of CNTNAP2-associated autism spectrum disorder

We utilized forebrain organoids generated from induced pluripotent stem cells of patients with a syndromic form of Autism Spectrum Disorder (ASD) with a homozygous protein-truncating mutation in CNTNAP2, to study its effects on embryonic cortical development. Patients with this mutation present with...

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Autores principales: de Jong, Job O., Llapashtica, Ceyda, Genestine, Matthieu, Strauss, Kevin, Provenzano, Frank, Sun, Yan, Zhu, Huixiang, Cortese, Giuseppe P., Brundu, Francesco, Brigatti, Karlla W., Corneo, Barbara, Migliori, Bianca, Tomer, Raju, Kushner, Steven A., Kellendonk, Christoph, Javitch, Jonathan A., Xu, Bin, Markx, Sander
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8410758/
https://www.ncbi.nlm.nih.gov/pubmed/34471112
http://dx.doi.org/10.1038/s41467-021-24358-4
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author de Jong, Job O.
Llapashtica, Ceyda
Genestine, Matthieu
Strauss, Kevin
Provenzano, Frank
Sun, Yan
Zhu, Huixiang
Cortese, Giuseppe P.
Brundu, Francesco
Brigatti, Karlla W.
Corneo, Barbara
Migliori, Bianca
Tomer, Raju
Kushner, Steven A.
Kellendonk, Christoph
Javitch, Jonathan A.
Xu, Bin
Markx, Sander
author_facet de Jong, Job O.
Llapashtica, Ceyda
Genestine, Matthieu
Strauss, Kevin
Provenzano, Frank
Sun, Yan
Zhu, Huixiang
Cortese, Giuseppe P.
Brundu, Francesco
Brigatti, Karlla W.
Corneo, Barbara
Migliori, Bianca
Tomer, Raju
Kushner, Steven A.
Kellendonk, Christoph
Javitch, Jonathan A.
Xu, Bin
Markx, Sander
author_sort de Jong, Job O.
collection PubMed
description We utilized forebrain organoids generated from induced pluripotent stem cells of patients with a syndromic form of Autism Spectrum Disorder (ASD) with a homozygous protein-truncating mutation in CNTNAP2, to study its effects on embryonic cortical development. Patients with this mutation present with clinical characteristics of brain overgrowth. Patient-derived forebrain organoids displayed an increase in volume and total cell number that is driven by increased neural progenitor proliferation. Single-cell RNA sequencing revealed PFC-excitatory neurons to be the key cell types expressing CNTNAP2. Gene ontology analysis of differentially expressed genes (DEgenes) corroborates aberrant cellular proliferation. Moreover, the DEgenes are enriched for ASD-associated genes. The cell-type-specific signature genes of the CNTNAP2-expressing neurons are associated with clinical phenotypes previously described in patients. The organoid overgrowth phenotypes were largely rescued after correction of the mutation using CRISPR-Cas9. This CNTNAP2-organoid model provides opportunity for further mechanistic inquiry and development of new therapeutic strategies for ASD.
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spelling pubmed-84107582021-09-22 Cortical overgrowth in a preclinical forebrain organoid model of CNTNAP2-associated autism spectrum disorder de Jong, Job O. Llapashtica, Ceyda Genestine, Matthieu Strauss, Kevin Provenzano, Frank Sun, Yan Zhu, Huixiang Cortese, Giuseppe P. Brundu, Francesco Brigatti, Karlla W. Corneo, Barbara Migliori, Bianca Tomer, Raju Kushner, Steven A. Kellendonk, Christoph Javitch, Jonathan A. Xu, Bin Markx, Sander Nat Commun Article We utilized forebrain organoids generated from induced pluripotent stem cells of patients with a syndromic form of Autism Spectrum Disorder (ASD) with a homozygous protein-truncating mutation in CNTNAP2, to study its effects on embryonic cortical development. Patients with this mutation present with clinical characteristics of brain overgrowth. Patient-derived forebrain organoids displayed an increase in volume and total cell number that is driven by increased neural progenitor proliferation. Single-cell RNA sequencing revealed PFC-excitatory neurons to be the key cell types expressing CNTNAP2. Gene ontology analysis of differentially expressed genes (DEgenes) corroborates aberrant cellular proliferation. Moreover, the DEgenes are enriched for ASD-associated genes. The cell-type-specific signature genes of the CNTNAP2-expressing neurons are associated with clinical phenotypes previously described in patients. The organoid overgrowth phenotypes were largely rescued after correction of the mutation using CRISPR-Cas9. This CNTNAP2-organoid model provides opportunity for further mechanistic inquiry and development of new therapeutic strategies for ASD. Nature Publishing Group UK 2021-09-01 /pmc/articles/PMC8410758/ /pubmed/34471112 http://dx.doi.org/10.1038/s41467-021-24358-4 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
de Jong, Job O.
Llapashtica, Ceyda
Genestine, Matthieu
Strauss, Kevin
Provenzano, Frank
Sun, Yan
Zhu, Huixiang
Cortese, Giuseppe P.
Brundu, Francesco
Brigatti, Karlla W.
Corneo, Barbara
Migliori, Bianca
Tomer, Raju
Kushner, Steven A.
Kellendonk, Christoph
Javitch, Jonathan A.
Xu, Bin
Markx, Sander
Cortical overgrowth in a preclinical forebrain organoid model of CNTNAP2-associated autism spectrum disorder
title Cortical overgrowth in a preclinical forebrain organoid model of CNTNAP2-associated autism spectrum disorder
title_full Cortical overgrowth in a preclinical forebrain organoid model of CNTNAP2-associated autism spectrum disorder
title_fullStr Cortical overgrowth in a preclinical forebrain organoid model of CNTNAP2-associated autism spectrum disorder
title_full_unstemmed Cortical overgrowth in a preclinical forebrain organoid model of CNTNAP2-associated autism spectrum disorder
title_short Cortical overgrowth in a preclinical forebrain organoid model of CNTNAP2-associated autism spectrum disorder
title_sort cortical overgrowth in a preclinical forebrain organoid model of cntnap2-associated autism spectrum disorder
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8410758/
https://www.ncbi.nlm.nih.gov/pubmed/34471112
http://dx.doi.org/10.1038/s41467-021-24358-4
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