Alpha-CaMKII deficiency causes immature dentate gyrus, a novel candidate endophenotype of psychiatric disorders

Elucidating the neural and genetic factors underlying psychiatric illness is hampered by current methods of clinical diagnosis. The identification and investigation of clinical endophenotypes may be one solution, but represents a considerable challenge in human subjects. Here we report that mice het...

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Published in	Molecular brain Vol. 1; no. 1; p. 6
Main Authors	Yamasaki, Nobuyuki, Maekawa, Motoko, Kobayashi, Katsunori, Kajii, Yasushi, Maeda, Jun, Soma, Miho, Takao, Keizo, Tanda, Koichi, Ohira, Koji, Toyama, Keiko, Kanzaki, Kouji, Fukunaga, Kohji, Sudo, Yusuke, Ichinose, Hiroshi, Ikeda, Masashi, Iwata, Nakao, Ozaki, Norio, Suzuki, Hidenori, Higuchi, Makoto, Suhara, Tetsuya, Yuasa, Shigeki, Miyakawa, Tsuyoshi
Format	Journal Article
Language	English
Published	London BioMed Central 10.09.2008 BioMed Central Ltd BMC
Subjects	Adult Animals Biomarkers - metabolism Biomedical and Life Sciences Biomedicine Calcium-Calmodulin-Dependent Protein Kinase Type 2 - deficiency Calcium-Calmodulin-Dependent Protein Kinase Type 2 - metabolism Cluster Analysis Dentate gyrus Dentate Gyrus - enzymology Dentate Gyrus - pathology Dentate Gyrus - physiopathology Dentate Gyrus - ultrastructure Endophenotypes Female Genetic aspects Humans Male Memory Disorders - complications Memory Disorders - physiopathology Mental Disorders - complications Mental Disorders - enzymology Mental Disorders - physiopathology Mental illness Mice Middle Aged Mossy Fibers, Hippocampal - physiopathology Mossy Fibers, Hippocampal - ultrastructure Neurology Neurosciences Physiological aspects Postmortem Changes Protein kinases Psychopharmacology Risk factors Synaptic Transmission - physiology Japan Schizophrenia Dentate Gyrus Mutant Mouse Startle Stimulus Granule Cell Layer
Online Access	Get full text
ISSN	1756-6606 1756-6606
DOI	10.1186/1756-6606-1-6

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Abstract	Elucidating the neural and genetic factors underlying psychiatric illness is hampered by current methods of clinical diagnosis. The identification and investigation of clinical endophenotypes may be one solution, but represents a considerable challenge in human subjects. Here we report that mice heterozygous for a null mutation of the alpha-isoform of calcium/calmodulin-dependent protein kinase II (alpha-CaMKII+/-) have profoundly dysregulated behaviours and impaired neuronal development in the dentate gyrus (DG). The behavioral abnormalities include a severe working memory deficit and an exaggerated infradian rhythm, which are similar to symptoms seen in schizophrenia, bipolar mood disorder and other psychiatric disorders. Transcriptome analysis of the hippocampus of these mutants revealed that the expression levels of more than 2000 genes were significantly changed. Strikingly, among the 20 most downregulated genes, 5 had highly selective expression in the DG. Whereas BrdU incorporated cells in the mutant mouse DG was increased by more than 50 percent, the number of mature neurons in the DG was dramatically decreased. Morphological and physiological features of the DG neurons in the mutants were strikingly similar to those of immature DG neurons in normal rodents. Moreover, c-Fos expression in the DG after electric footshock was almost completely and selectively abolished in the mutants. Statistical clustering of human post-mortem brains using 10 genes differentially-expressed in the mutant mice were used to classify individuals into two clusters, one of which contained 16 of 18 schizophrenic patients. Nearly half of the differentially-expressed probes in the schizophrenia-enriched cluster encoded genes that are involved in neurogenesis or in neuronal migration/maturation, including calbindin, a marker for mature DG neurons. Based on these results, we propose that an "immature DG" in adulthood might induce alterations in behavior and serve as a promising candidate endophenotype of schizophrenia and other human psychiatric disorders.
AbstractList	Elucidating the neural and genetic factors underlying psychiatric illness is hampered by current methods of clinical diagnosis. The identification and investigation of clinical endophenotypes may be one solution, but represents a considerable challenge in human subjects. Here we report that mice heterozygous for a null mutation of the alpha-isoform of calcium/calmodulin-dependent protein kinase II (alpha-CaMKII+/-) have profoundly dysregulated behaviours and impaired neuronal development in the dentate gyrus (DG). The behavioral abnormalities include a severe working memory deficit and an exaggerated infradian rhythm, which are similar to symptoms seen in schizophrenia, bipolar mood disorder and other psychiatric disorders. Transcriptome analysis of the hippocampus of these mutants revealed that the expression levels of more than 2000 genes were significantly changed. Strikingly, among the 20 most downregulated genes, 5 had highly selective expression in the DG. Whereas BrdU incorporated cells in the mutant mouse DG was increased by more than 50 percent, the number of mature neurons in the DG was dramatically decreased. Morphological and physiological features of the DG neurons in the mutants were strikingly similar to those of immature DG neurons in normal rodents. Moreover, c-Fos expression in the DG after electric footshock was almost completely and selectively abolished in the mutants. Statistical clustering of human post-mortem brains using 10 genes differentially-expressed in the mutant mice were used to classify individuals into two clusters, one of which contained 16 of 18 schizophrenic patients. Nearly half of the differentially-expressed probes in the schizophrenia-enriched cluster encoded genes that are involved in neurogenesis or in neuronal migration/maturation, including calbindin, a marker for mature DG neurons. Based on these results, we propose that an "immature DG" in adulthood might induce alterations in behavior and serve as a promising candidate endophenotype of schizophrenia and other human psychiatric disorders. Elucidating the neural and genetic factors underlying psychiatric illness is hampered by current methods of clinical diagnosis. The identification and investigation of clinical endophenotypes may be one solution, but represents a considerable challenge in human subjects. Here we report that mice heterozygous for a null mutation of the alpha-isoform of calcium/calmodulin-dependent protein kinase II (alpha-CaMKII+/-) have profoundly dysregulated behaviours and impaired neuronal development in the dentate gyrus (DG). The behavioral abnormalities include a severe working memory deficit and an exaggerated infradian rhythm, which are similar to symptoms seen in schizophrenia, bipolar mood disorder and other psychiatric disorders. Transcriptome analysis of the hippocampus of these mutants revealed that the expression levels of more than 2000 genes were significantly changed. Strikingly, among the 20 most downregulated genes, 5 had highly selective expression in the DG. Whereas BrdU incorporated cells in the mutant mouse DG was increased by more than 50 percent, the number of mature neurons in the DG was dramatically decreased. Morphological and physiological features of the DG neurons in the mutants were strikingly similar to those of immature DG neurons in normal rodents. Moreover, c-Fos expression in the DG after electric footshock was almost completely and selectively abolished in the mutants. Statistical clustering of human post-mortem brains using 10 genes differentially-expressed in the mutant mice were used to classify individuals into two clusters, one of which contained 16 of 18 schizophrenic patients. Nearly half of the differentially-expressed probes in the schizophrenia-enriched cluster encoded genes that are involved in neurogenesis or in neuronal migration/maturation, including calbindin, a marker for mature DG neurons. Based on these results, we propose that an "immature DG" in adulthood might induce alterations in behavior and serve as a promising candidate endophenotype of schizophrenia and other human psychiatric disorders.Elucidating the neural and genetic factors underlying psychiatric illness is hampered by current methods of clinical diagnosis. The identification and investigation of clinical endophenotypes may be one solution, but represents a considerable challenge in human subjects. Here we report that mice heterozygous for a null mutation of the alpha-isoform of calcium/calmodulin-dependent protein kinase II (alpha-CaMKII+/-) have profoundly dysregulated behaviours and impaired neuronal development in the dentate gyrus (DG). The behavioral abnormalities include a severe working memory deficit and an exaggerated infradian rhythm, which are similar to symptoms seen in schizophrenia, bipolar mood disorder and other psychiatric disorders. Transcriptome analysis of the hippocampus of these mutants revealed that the expression levels of more than 2000 genes were significantly changed. Strikingly, among the 20 most downregulated genes, 5 had highly selective expression in the DG. Whereas BrdU incorporated cells in the mutant mouse DG was increased by more than 50 percent, the number of mature neurons in the DG was dramatically decreased. Morphological and physiological features of the DG neurons in the mutants were strikingly similar to those of immature DG neurons in normal rodents. Moreover, c-Fos expression in the DG after electric footshock was almost completely and selectively abolished in the mutants. Statistical clustering of human post-mortem brains using 10 genes differentially-expressed in the mutant mice were used to classify individuals into two clusters, one of which contained 16 of 18 schizophrenic patients. Nearly half of the differentially-expressed probes in the schizophrenia-enriched cluster encoded genes that are involved in neurogenesis or in neuronal migration/maturation, including calbindin, a marker for mature DG neurons. Based on these results, we propose that an "immature DG" in adulthood might induce alterations in behavior and serve as a promising candidate endophenotype of schizophrenia and other human psychiatric disorders. Abstract Elucidating the neural and genetic factors underlying psychiatric illness is hampered by current methods of clinical diagnosis. The identification and investigation of clinical endophenotypes may be one solution, but represents a considerable challenge in human subjects. Here we report that mice heterozygous for a null mutation of the alpha-isoform of calcium/calmodulin-dependent protein kinase II (alpha-CaMKII+/-) have profoundly dysregulated behaviours and impaired neuronal development in the dentate gyrus (DG). The behavioral abnormalities include a severe working memory deficit and an exaggerated infradian rhythm, which are similar to symptoms seen in schizophrenia, bipolar mood disorder and other psychiatric disorders. Transcriptome analysis of the hippocampus of these mutants revealed that the expression levels of more than 2000 genes were significantly changed. Strikingly, among the 20 most downregulated genes, 5 had highly selective expression in the DG. Whereas BrdU incorporated cells in the mutant mouse DG was increased by more than 50 percent, the number of mature neurons in the DG was dramatically decreased. Morphological and physiological features of the DG neurons in the mutants were strikingly similar to those of immature DG neurons in normal rodents. Moreover, c-Fos expression in the DG after electric footshock was almost completely and selectively abolished in the mutants. Statistical clustering of human post-mortem brains using 10 genes differentially-expressed in the mutant mice were used to classify individuals into two clusters, one of which contained 16 of 18 schizophrenic patients. Nearly half of the differentially-expressed probes in the schizophrenia-enriched cluster encoded genes that are involved in neurogenesis or in neuronal migration/maturation, including calbindin, a marker for mature DG neurons. Based on these results, we propose that an "immature DG" in adulthood might induce alterations in behavior and serve as a promising candidate endophenotype of schizophrenia and other human psychiatric disorders.
ArticleNumber	6
Audience	Academic
Author	Maekawa, Motoko Kanzaki, Kouji Sudo, Yusuke Suzuki, Hidenori Yamasaki, Nobuyuki Kobayashi, Katsunori Tanda, Koichi Ozaki, Norio Higuchi, Makoto Toyama, Keiko Maeda, Jun Ikeda, Masashi Ohira, Koji Fukunaga, Kohji Soma, Miho Suhara, Tetsuya Yuasa, Shigeki Takao, Keizo Iwata, Nakao Miyakawa, Tsuyoshi Ichinose, Hiroshi Kajii, Yasushi
AuthorAffiliation	4 Japan Science and Technology Agency, BIRD, Saitama, Japan 3 Japan Science and Technology Agency, CREST, Saitama, Japan 12 Graduate School of Medicine, Fujita Health University, 1-98 Dengakugakubo, Kutsukake-cho, Toyoake, Japan 2 Department of Psychiatry, Kyoto University Graduate School of Medicine, 54 Shogoin-Kawahara-cho, Sakyo-ku, Kyoto, Japan 14 Center for Genetic Analysis of Behavior, National Institute for Physiological Sciences, Myodaiji, Okazaki, Japan 5 Department of Ultrastructural Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, 4-1-1 Ogawa-higashi, Kodaira, Tokyo, Japan 13 Graduate School of Medicine, Nagoya University, 65 Tsuruma-cho, Showa-ku, Nagoya, Japan 7 Mitsubishi Tanabe Pharma Corporation, 1000 Kamoshida-cho, Aoba-ku, Yokohama, Japan 10 Graduate School of Pharmaceutical Sciences, Tohoku University, Aramaki, Aoba-ku, Sendai, Japan 8 Department of Molecular Neuroimaging, Molecular Imaging Center, National Institute of Radiological S
AuthorAffiliation_xml	– name: 9 Division of Systems Medicine, Institute for Comprehensive Medical Science, Fujita Health University, 1-98 Dengakugakubo, Kutsukake-cho, Toyoake, Japan – name: 1 Genetic Engineering and Functional Genomics Group, Frontier Technology Center, Kyoto University Graduate School of Medicine, Yoshida-Konoe-cho, Sakyo-ku, Kyoto, Japan – name: 2 Department of Psychiatry, Kyoto University Graduate School of Medicine, 54 Shogoin-Kawahara-cho, Sakyo-ku, Kyoto, Japan – name: 6 Department of Pharmacology, Nippon Medical School, 1-1-5 Sendagi, Bunkyo-ku, Tokyo, Japan – name: 12 Graduate School of Medicine, Fujita Health University, 1-98 Dengakugakubo, Kutsukake-cho, Toyoake, Japan – name: 5 Department of Ultrastructural Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, 4-1-1 Ogawa-higashi, Kodaira, Tokyo, Japan – name: 14 Center for Genetic Analysis of Behavior, National Institute for Physiological Sciences, Myodaiji, Okazaki, Japan – name: 8 Department of Molecular Neuroimaging, Molecular Imaging Center, National Institute of Radiological Sciences, 4-9-1 Anagawa, Inage-ku, Chiba, Japan – name: 3 Japan Science and Technology Agency, CREST, Saitama, Japan – name: 10 Graduate School of Pharmaceutical Sciences, Tohoku University, Aramaki, Aoba-ku, Sendai, Japan – name: 13 Graduate School of Medicine, Nagoya University, 65 Tsuruma-cho, Showa-ku, Nagoya, Japan – name: 7 Mitsubishi Tanabe Pharma Corporation, 1000 Kamoshida-cho, Aoba-ku, Yokohama, Japan – name: 4 Japan Science and Technology Agency, BIRD, Saitama, Japan – name: 11 Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, 4259 Nagatsuta-cho, Midori-ku, Yokohama, Japan
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givenname: Yusuke surname: Sudo fullname: Sudo, Yusuke organization: Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology – sequence: 14 givenname: Hiroshi surname: Ichinose fullname: Ichinose, Hiroshi organization: Japan Science and Technology Agency, CREST, Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology – sequence: 15 givenname: Masashi surname: Ikeda fullname: Ikeda, Masashi organization: Japan Science and Technology Agency, CREST, Graduate School of Medicine, Fujita Health University, Graduate School of Medicine, Nagoya University – sequence: 16 givenname: Nakao surname: Iwata fullname: Iwata, Nakao organization: Japan Science and Technology Agency, CREST, Graduate School of Medicine, Fujita Health University – sequence: 17 givenname: Norio surname: Ozaki fullname: Ozaki, Norio organization: Japan Science and Technology Agency, CREST, Graduate School of Medicine, Nagoya University – sequence: 18 givenname: Hidenori surname: 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Japan Science and Technology Agency, CREST, Japan Science and Technology Agency, BIRD, Division of Systems Medicine, Institute for Comprehensive Medical Science, Fujita Health University, Center for Genetic Analysis of Behavior, National Institute for Physiological Sciences
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/18803808$$D View this record in MEDLINE/PubMed
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Snippet	Elucidating the neural and genetic factors underlying psychiatric illness is hampered by current methods of clinical diagnosis. The identification and... Abstract Elucidating the neural and genetic factors underlying psychiatric illness is hampered by current methods of clinical diagnosis. The identification and...
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SubjectTerms	Adult Animals Biomarkers - metabolism Biomedical and Life Sciences Biomedicine Calcium-Calmodulin-Dependent Protein Kinase Type 2 - deficiency Calcium-Calmodulin-Dependent Protein Kinase Type 2 - metabolism Cluster Analysis Dentate gyrus Dentate Gyrus - enzymology Dentate Gyrus - pathology Dentate Gyrus - physiopathology Dentate Gyrus - ultrastructure Endophenotypes Female Genetic aspects Humans Male Memory Disorders - complications Memory Disorders - physiopathology Mental Disorders - complications Mental Disorders - enzymology Mental Disorders - physiopathology Mental illness Mice Middle Aged Mossy Fibers, Hippocampal - physiopathology Mossy Fibers, Hippocampal - ultrastructure Neurology Neurosciences Physiological aspects Postmortem Changes Protein kinases Psychopharmacology Risk factors Synaptic Transmission - physiology
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Title	Alpha-CaMKII deficiency causes immature dentate gyrus, a novel candidate endophenotype of psychiatric disorders
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