TY - JOUR
T1 - CRISPR/Cas9-engineered Gad1 elimination in rats leads to complex behavioral changes
T2 - implications for schizophrenia
AU - Fujihara, Kazuyuki
AU - Yamada, Kazuo
AU - Ichitani, Yukio
AU - Kakizaki, Toshikazu
AU - Jiang, Weiru
AU - Miyata, Shigeo
AU - Suto, Takashi
AU - Kato, Daiki
AU - Saito, Shigeru
AU - Watanabe, Masahiko
AU - Kajita, Yuki
AU - Ohshiro, Tomokazu
AU - Mushiake, Hajime
AU - Miyasaka, Yoshiki
AU - Mashimo, Tomoji
AU - Yasuda, Hiroki
AU - Yanagawa, Yuchio
N1 - Funding Information:
This work was supported by JSPS KAKENHI Grant Number JP26290002 (Y.Y.), JP15H05872 (Y.Y.), JP16H06276 [Platform of Advanced Animal Model Support, AdAMS] (Y.Y.), JP17H05550 (Y.Y.), JP17K17628 (K.F.), JP19K06881 (Y.Y.), JP15H05879 (H.M.), and AMED under Grant Number JP19dm0207001 (H.M.). This project was also partly supported by the Takeda Science Foundation (Y.Y.), the Life Science Foundation of Japan (K.F.), and the Collaborative Research Project of the Brain Research Institute, Niigata University (Y.Y.). We are grateful to Takumi Sato, Misuzu Umehara, Shunsuke Teshima, Kazuya Higeta, Yugo Nakajima, Sota Abe, and Yuki Fukuda for technical assistance. We thank Dr. Ryosuke Kaneko for his helpful comments on the analysis of data and the members of our laboratory for their support and encouragement. We also thank the staff at the Institute of Experimental Animal Research, Gunma University Graduate School of Medicine. Finally, we thank Dr. Takako Fujihara for her encouragement and critical comments as a clinical psychiatrist.
Publisher Copyright:
© 2020, The Author(s).
PY - 2020/12
Y1 - 2020/12
N2 - 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.
AB - 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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U2 - 10.1038/s41398-020-01108-6
DO - 10.1038/s41398-020-01108-6
M3 - Article
C2 - 33293518
AN - SCOPUS:85097309600
SN - 2158-3188
VL - 10
JO - Translational Psychiatry
JF - Translational Psychiatry
IS - 1
M1 - 426
ER -