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CRISPR/Cas9-engineered Gad1 elimination in rats leads to complex behavioral changes: implications for schizophrenia

GABAergic dysfunctions have been implicated in the pathogenesis of schizophrenia, especially the associated cognitive impairments. The GABA synthetic enzyme glutamate decarboxylase 67-kDa isoform (GAD67) encoded by the GAD1 gene is downregulated in the brains of patients with schizophrenia. Furtherm...

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Autores principales: Fujihara, Kazuyuki, Yamada, Kazuo, Ichitani, Yukio, Kakizaki, Toshikazu, Jiang, Weiru, Miyata, Shigeo, Suto, Takashi, Kato, Daiki, Saito, Shigeru, Watanabe, Masahiko, Kajita, Yuki, Ohshiro, Tomokazu, Mushiake, Hajime, Miyasaka, Yoshiki, Mashimo, Tomoji, Yasuda, Hiroki, Yanagawa, Yuchio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7723991/
https://www.ncbi.nlm.nih.gov/pubmed/33293518
http://dx.doi.org/10.1038/s41398-020-01108-6
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author Fujihara, Kazuyuki
Yamada, Kazuo
Ichitani, Yukio
Kakizaki, Toshikazu
Jiang, Weiru
Miyata, Shigeo
Suto, Takashi
Kato, Daiki
Saito, Shigeru
Watanabe, Masahiko
Kajita, Yuki
Ohshiro, Tomokazu
Mushiake, Hajime
Miyasaka, Yoshiki
Mashimo, Tomoji
Yasuda, Hiroki
Yanagawa, Yuchio
author_facet Fujihara, Kazuyuki
Yamada, Kazuo
Ichitani, Yukio
Kakizaki, Toshikazu
Jiang, Weiru
Miyata, Shigeo
Suto, Takashi
Kato, Daiki
Saito, Shigeru
Watanabe, Masahiko
Kajita, Yuki
Ohshiro, Tomokazu
Mushiake, Hajime
Miyasaka, Yoshiki
Mashimo, Tomoji
Yasuda, Hiroki
Yanagawa, Yuchio
author_sort Fujihara, Kazuyuki
collection PubMed
description GABAergic dysfunctions have been implicated in the pathogenesis of schizophrenia, especially the associated cognitive impairments. The GABA synthetic enzyme glutamate decarboxylase 67-kDa isoform (GAD67) encoded by the GAD1 gene is downregulated in the brains of patients with schizophrenia. Furthermore, a patient with schizophrenia harboring a homozygous mutation of GAD1 has recently been discovered. However, it remains unclear whether loss of function of GAD1 leads to the symptoms observed in schizophrenia, including cognitive impairment. One of the obstacles faced in experimental studies to address this issue is the perinatal lethality of Gad1 knockout (KO) mice, which precluded characterization at the adult stage. In the present study, we successfully generated Gad1 KO rats using CRISPR/Cas9 genome editing technology. Surprisingly, 33% of Gad1 KO rats survived to adulthood and could be subjected to further characterization. The GABA concentration in the Gad1 KO cerebrum was reduced to ~52% of the level in wild-type rats. Gad1 KO rats exhibited impairments in both spatial reference and working memory without affecting adult neurogenesis in the hippocampus. In addition, Gad1 KO rats showed a wide range of behavioral alterations, such as enhanced sensitivity to an NMDA receptor antagonist, hypoactivity in a novel environment, and decreased preference for social novelty. Taken together, the results suggest that Gad1 KO rats could provide a novel model covering not only cognitive deficits but also other aspects of the disorder. Furthermore, the present study teaches an important lesson: differences between species should be considered when developing animal models of human diseases.
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spelling pubmed-77239912020-12-17 CRISPR/Cas9-engineered Gad1 elimination in rats leads to complex behavioral changes: implications for schizophrenia Fujihara, Kazuyuki Yamada, Kazuo Ichitani, Yukio Kakizaki, Toshikazu Jiang, Weiru Miyata, Shigeo Suto, Takashi Kato, Daiki Saito, Shigeru Watanabe, Masahiko Kajita, Yuki Ohshiro, Tomokazu Mushiake, Hajime Miyasaka, Yoshiki Mashimo, Tomoji Yasuda, Hiroki Yanagawa, Yuchio Transl Psychiatry Article GABAergic dysfunctions have been implicated in the pathogenesis of schizophrenia, especially the associated cognitive impairments. The GABA synthetic enzyme glutamate decarboxylase 67-kDa isoform (GAD67) encoded by the GAD1 gene is downregulated in the brains of patients with schizophrenia. Furthermore, a patient with schizophrenia harboring a homozygous mutation of GAD1 has recently been discovered. However, it remains unclear whether loss of function of GAD1 leads to the symptoms observed in schizophrenia, including cognitive impairment. One of the obstacles faced in experimental studies to address this issue is the perinatal lethality of Gad1 knockout (KO) mice, which precluded characterization at the adult stage. In the present study, we successfully generated Gad1 KO rats using CRISPR/Cas9 genome editing technology. Surprisingly, 33% of Gad1 KO rats survived to adulthood and could be subjected to further characterization. The GABA concentration in the Gad1 KO cerebrum was reduced to ~52% of the level in wild-type rats. Gad1 KO rats exhibited impairments in both spatial reference and working memory without affecting adult neurogenesis in the hippocampus. In addition, Gad1 KO rats showed a wide range of behavioral alterations, such as enhanced sensitivity to an NMDA receptor antagonist, hypoactivity in a novel environment, and decreased preference for social novelty. Taken together, the results suggest that Gad1 KO rats could provide a novel model covering not only cognitive deficits but also other aspects of the disorder. Furthermore, the present study teaches an important lesson: differences between species should be considered when developing animal models of human diseases. Nature Publishing Group UK 2020-12-08 /pmc/articles/PMC7723991/ /pubmed/33293518 http://dx.doi.org/10.1038/s41398-020-01108-6 Text en © The Author(s) 2020 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/.
spellingShingle Article
Fujihara, Kazuyuki
Yamada, Kazuo
Ichitani, Yukio
Kakizaki, Toshikazu
Jiang, Weiru
Miyata, Shigeo
Suto, Takashi
Kato, Daiki
Saito, Shigeru
Watanabe, Masahiko
Kajita, Yuki
Ohshiro, Tomokazu
Mushiake, Hajime
Miyasaka, Yoshiki
Mashimo, Tomoji
Yasuda, Hiroki
Yanagawa, Yuchio
CRISPR/Cas9-engineered Gad1 elimination in rats leads to complex behavioral changes: implications for schizophrenia
title CRISPR/Cas9-engineered Gad1 elimination in rats leads to complex behavioral changes: implications for schizophrenia
title_full CRISPR/Cas9-engineered Gad1 elimination in rats leads to complex behavioral changes: implications for schizophrenia
title_fullStr CRISPR/Cas9-engineered Gad1 elimination in rats leads to complex behavioral changes: implications for schizophrenia
title_full_unstemmed CRISPR/Cas9-engineered Gad1 elimination in rats leads to complex behavioral changes: implications for schizophrenia
title_short CRISPR/Cas9-engineered Gad1 elimination in rats leads to complex behavioral changes: implications for schizophrenia
title_sort crispr/cas9-engineered gad1 elimination in rats leads to complex behavioral changes: implications for schizophrenia
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7723991/
https://www.ncbi.nlm.nih.gov/pubmed/33293518
http://dx.doi.org/10.1038/s41398-020-01108-6
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