Combined effect of neonatal immune activation and mutant DISC1 on phenotypic changes in adulthood

Ibi, Daisuke; Nagai, Taku; Koike, Hiroyuki; Kitahara, Yuko; Mizoguchi, Hiroyuki; Niwa, Minae; Jaaro-Peled, Hanna; Nitta, Atsumi; Yoneda, Yukio; Nabeshima, Toshitaka

doi:10.1016/j.bbr.2009.08.027

Cited by 137Schizophrenia research and treatmentTryptophan and brain disordersNeurotransmitter Receptor Influence on Behavior

Combined effect of neonatal immune activation and mutant DISC1 on phenotypic changes in adulthood

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Ibi, Daisuke, Nagai, Taku, Koike, Hiroyuki, Kitahara, Yuko, Mizoguchi, Hiroyuki, Niwa, Minae, Jaaro-Peled, Hanna, Nitta, Atsumi +2 more·2010·Behavioural Brain Research

DOI 10.1016/j.bbr.2009.08.027PMC PMC2846597

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Abstract

Gene-environment interaction may play a role in the etiology of schizophrenia. Transgenic mice expressing dominant-negative DISC1 (DN-DISC1 mice) show some histological and behavioral endophenotypes relevant to schizophrenia. Viral infection during neurodevelopment provides a major environmental risk for schizophrenia. Neonatal injection of polyriboinosinic-polyribocytidylic acid (polyI:C), which mimics innate immune responses elicited by viral infection, leads to schizophrenia-like behavioral alteration in mice after puberty. To study how gene-environmental interaction during neurodevelopment results in phenotypic changes in adulthood, we treated DN-DISC1 mice or wild-type littermates with injection of polyI:C during the neonatal stage, according to the published method, respectively, and the behavioral and histological phenotypes were examined in adulthood. We demonstrated that neonatal polyI:C treatment in DN-DISC1 mice resulted in the deficits of short-term, object recognition, and hippocampus-dependent fear memories after puberty, although polyI:C treatment by itself had smaller influences on wild-type mice. Furthermore, polyI:C-treated DN-DISC1 mice exhibited signs of impairment of social recognition and interaction, and augmented susceptibility to MK-801-induced hyperactivity as compared with vehicle-treated wild-type mice. Of most importance, additive effects of polyI:C and DN-DISC1 were observed by a marked decrease in parvalbumin-positive interneurons in the medial prefrontal cortex. These results suggest that combined effect of neonatal polyI:C treatment and DN-DISC1 affects some behavioral and histological phenotypes in adulthood.

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Antioxidant therapy with NAC reduces the pathological and behavioural consequences of maternal LPS treatment and reduces foetal proinflammatory cytokine production.
“Activated innate immune cells both produce and are activated by ROS: antioxidant therapy with NAC reduces the pathological and behavioural consequences of maternal LPS treatment and reduces foetal proinflammatory cytokine production 92,93 .”
From Linking early-life NMDAR hypofunction and oxidative stress in schizophrenia pathogenesis (2016) · cites this paper as [93]

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Involvement of Genetic an d Environmental Factors in the Onset of Depression
Nabeshima, T., & Kim, H. (2013) · Experimental Neurobiology · doi:10.5607/en.2013.22.4.235 · Cited by 79 · see citing works
“The question of what happens when mice that possess an abnormal DISC1 gene (G) are subjected to this low stress (E) was investigated [47].”
BackgroundInfluentialSelf-citation
Developmental disruption of perineuronal nets in the medial prefrontal cortex after maternal immune activation
Paylor, J. W., Lins, B. R., Greba, Q., Moen, N., de Moraes, R. S., Howland, J. G., & Winship, I. R. (2016) · Scientific Reports · doi:10.1038/srep37580 · Cited by 79 · see citing works
Selective loss of parvalbumin-positive GABAergic interneurons in the cerebral cortex of maternally stressed Gad1-heterozygous mouse offspring
Uchida, T., Furukawa, T., Iwata, S., Yanagawa, Y., & Fukuda, A. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.13 · Cited by 73 · see citing works
Utility and validity of DISC1 mouse models in biological psychiatry
Tomoda, T., Sumitomo, A., Jaaro-Peled, H., & Sawa, A. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2015.12.061 · Cited by 68 · see citing works
“…2013), neonatal immune activation by polyI:C injection at postnatal days 2–6, which corresponds to the second trimester of human brain development (Ibi et al., 2010; Nagai et al., 2011), chronic social defeat (Haque et al., 2012), and adolescent social isolation stress (Niwa et al., 2013), as…”
BackgroundSelf-citation
Roles of glial cells in schizophrenia: Possible targets for therapeutic approaches
Takahashi, N., & Sakurai, T. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.11.001 · Cited by 67 · see citing works
Gene–environment interactions and construct validity in preclinical models of psychiatric disorders
Burrows, E. L., McOmish, C. E., & Hannan, A. J. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2010.12.011 · Cited by 63 · see citing works
“…illustration of this approach is seen in a recent study investigating the interaction of the schizophrenia candidate gene DISC1 (Muir et al., 2008; Roberts, 2007), with neonatal exposure to viral infection and the behavioral and pathological consequences of such an interaction (Ibi et al., 2010).”
Astroglial major histocompatibility complex class I following immune activation leads to behavioral and neuropathological changes
Sobue, A., Ito, N., Nagai, T., Wei, S., Hada, K., Nakajima, A., Murakami, Y., Mouri, A., Yamamoto, Y., Nabeshima, T., et al. (2018) · Glia · doi:10.1002/glia.23299 · Cited by 58 · see citing works
“The Y-maze test was performed as described previously (Ibi et al., 2010).”
MethodSelf-citation
Disrupted-In-Schizophrenia-1 (DISC1) interactome and mental disorders: Impact of mouse models
Lipina, T. V., & Roder, J. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.07.001 · Cited by 57 · see citing works
“The polyI:C approach was applied to CaMK-DN-DISC1 mice (Abazyan et al., 2010) and DISC1 point mutants (Lipina et al., 2013c) at E9, and at the neonatal period (postnatal days 2-6) to CaMK-DN-DISC1 pups (Ibi et al., 2010; Nagai et al., 2011).”
Social defeat interacts with Disc1 mutations in the mouse to affect behavior
Haque, F. N., Lipina, T. V., Roder, J., & Wong, A. H. C. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.05.037 · Cited by 53 · see citing works
Mouse models of gene-environment interactions in schizophrenia
Kannan, G., Sawa, A., & Pletnikov, M. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2013.05.012 · Cited by 59 · see citing works
Subcortical dopaminergic deficits in a DISC1 mutant model: a study in direct reference to human molecular brain imaging.
Jaaro-Peled, H., Niwa, M., Foss, C., Murai, R., Reyes, S. D. L., Kamiya, A., Mateo, Y., O'Donnell, P., Cascella, N., Nabeshima, T., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt007 · Cited by 56 · see citing works
“However, previous studies with this model have not addressed potential dysfunction of the dopaminergic system (16,23,24).”
ResultSelf-citation
Heterozygous Disruption of Autism susceptibility candidate 2 Causes Impaired Emotional Control and Cognitive Memory
Hori, K., Nagai, T., Shan, W., Sakamoto, A., Abe, M., Yamazaki, M., Sakimura, K., Yamada, K., & Hoshino, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0145979 · Cited by 47 · see citing works
“The fear-conditioning test was carried out as described previously [21].”
MethodSelf-citation
From Shortage to Surge: A Developmental Switch in Hippocampal–Prefrontal Coupling in a Gene–Environment Model of Neuropsychiatric Disorders
Hartung, H., Cichon, N. B., Feo, V. D., Riemann, S., Schildt, S., Lindemann, C., Mulert, C., Gogos, J. A., & Hanganu‐Opatz, I. L. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw274 · Cited by 47 · see citing works
“ment throughout the life span, altered cognitive and social behavior, anxiety, and hyperactivity being detected at adult age (Abazyan et al. 2010; Ibi et al. 2010; Lipina et al. 2013).”
BackgroundInfluential
Genetic and animal model analyses reveal the pathogenic role of a novel deletion of RELN in schizophrenia
Sobue, A., Kushima, I., Nagai, T., Shan, W., Kohno, T., Aleksić, B., Aoyama, Y., Mori, D., Arioka, Y., Kawano, N., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-31390-w · Cited by 48 · see citing works
Self-citation
Effects of antipsychotics on the behavioral deficits in human dominant-negative DISC1 transgenic mice with neonatal polyI:C treatment
Nagai, T., Kitahara, Y., Ibi, D., Nabeshima, T., Sawa, A., & Yamada, K. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.07.049 · Cited by 47 · see citing works
Self-citation
DISC1 mouse models as a tool to decipher gene-environment interactions in psychiatric disorders
Cash-Padgett, T. V., & Jaaro-Peled, H. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00113 · Cited by 46 · see citing works
Self-citation
BDNF overexpression prevents cognitive deficit elicited by adolescent cannabis exposure and host susceptibility interaction
Segal‐Gavish, H., Gazit, N., Barhum, Y., Ben‐Zur, T., Taler, M., Hornfeld, S. H., Gil‐Ad, I., Weizman, A., Slutsky, I., Niwa, M., et al. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx139 · Cited by 45 · see citing works
Self-citation
Different Paths to Core Pathology: The Equifinal Model of the Schizophrenia Syndrome
Green, I. W., & Glausier, J. R. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv136 · Cited by 44 · see citing works
DISC1 as a therapeutic target for mental illnesses
Hikida, T., Gamo, N. J., & Sawa, A. (2012) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2012.719879 · Cited by 43 · see citing works
“innate immune activation, augments the behavioral and histological phenotype of Disc1 mutant mice [102,113].”
Background
Sensorimotor gating deficits in “two-hit” models of schizophrenia risk factors
Khan, A., & Powell, S. B. (2017) · Schizophrenia Research · doi:10.1016/j.schres.2017.10.009 · Cited by 43 · see citing works
Adolescent cannabis exposure interacts with mutant DISC1 to produce impaired adult emotional memory
Ballinger, M. D., Saito, A., Abazyan, B. N., Taniguchi, Y., Huang, C.-H., Ito, K., Zhu, X., Segal‐Gavish, H., Jaaro-Peled, H., Sawa, A., et al. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.06.006 · Cited by 42 · see citing works
Self-citation
Behavioral phenotypes in schizophrenic animal models with multiple combinations of genetic and environmental factors.
Hida, H., Mouri, A., & Noda, Y. (2013) · Journal of Pharmacological Sciences · doi:10.1254/jphs.12r15cp · Cited by 40 · see citing works
Genetic disruption of the autism spectrum disorder risk gene PLAUR induces GABAA receptor subunit changes
Eagleson, K. L., Gravielle, M. C., Schlueter, L. J., Russek, S. J., Farb, D. H., & Levitt, P. R. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.03.066 · Cited by 41 · see citing works
“…IH -PA Author M anuscript 2008, Wallis et al., 2008, Barber et al., 2009, Batista-Brito et al., 2009, Bond et al., 2009, Canty et al., 2009, Ibi et al., 2009, Mao et al., 2009, Price et al., 2009, Sakata et al., 2009), the impact of altered interneuron development on the long-term…”
Background
Perinatal complications and schizophrenia: involvement of the immune system
Jenkins, T. A. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00110 · Cited by 41 · see citing works
“Findings from epidemiological studies provide evidence that perinatal factors including environment, parental influence on the foetus during pregnancy and obstetric complications contribute to the risk of developing schizophrenia.”
Background
DISC1
Narayan, S., Nakajima, K., & Sawa, A. (2013) · The Neuroscientist · doi:10.1177/1073858412470168 · Cited by 37 · see citing works
Progress in defining the biological causes of schizophrenia
Pickard, B. S. (2011) · Expert Reviews in Molecular Medicine · doi:10.1017/s1462399411001955 · Cited by 38 · see citing works
“Molecular Psychiatry 177 Ibi, D. et al. (2010) Combined effect of neonatal”
Background
JNK signalling mediates aspects of maternal immune activation: importance of maternal genotype in relation to schizophrenia risk
Openshaw, R. L., Kwon, J., McColl, A., Penninger, J. M., Cavanagh, J., Pratt, J. A., & MORRIS, B. J. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1408-5 · Cited by 38 · see citing works
Animal models of schizophrenia for molecular and pharmacological intervention and potential candidate molecules
Mouri, A., Nagai, T., Ibi, D., & Yamada, K. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.10.025 · Cited by 36 · see citing works
Self-citation
A Methionine-Induced Animal Model of Schizophrenia: Face and Predictive Validity
Wang, L., Alachkar, A., Sanathara, N. M., Belluzzi, J. D., Wang, Z., & Civelli, O. (2015) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyv054 · Cited by 37 · see citing works
Neuregulin 1: a prime candidate for research into gene-environment interactions in schizophrenia? Insights from genetic rodent models
Karl, T. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00106 · Cited by 36 · see citing works
“Researchers should focus on models with significant relevance to schizophrenia including, for example, cannabis abuse (discussed above) and maternal immunization (Ibi et al., 2010; Giovanoli et al., 2013) and consider not only Nrg1 but also other genetic candidates for GxE interactions.”
Background
Animal Model for Schizophrenia That Reflects Gene-Environment Interactions
Nagai, T., Ibi, D., & Yamada, K. (2011) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.34.1364 · Cited by 36 · see citing works
Self-citation
Disrupted-in-Schizophrenia-1 is essential for normal hypothalamic-pituitary-interrenal (HPI) axis function
Eachus, H., Bright, C., Cunliffe, V. T., Placzek, M., Wood, J., & Watt, P. J. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx076 · Cited by 34 · see citing works
“These studies have utilised either mice with Disc1 point mutations (27), mice carrying a naturally occurring 25 base-pair deletion in Disc1 (29,30), or transgenic mice expressing a truncated form of human DISC1 (24,28,31).”
Background
Sonic hedgehog functions upstream ofdisrupted-in-schizophrenia 1(disc1): implications for mental illness
Boyd, P. J., Cunliffe, V. T., Roy, S., & Wood, J. (2015) · Biology Open · doi:10.1242/bio.012005 · Cited by 34 · see citing works
“Moreover, interactions between DISC1 and environmental factors have been shown to modulate behaviour (Abazyan et al., 2010; Haque et al., 2012; Ibi et al., 2010; Niwa et al., 2013).”
Background
Modulation of schizophrenia-related genes in the forebrain of adolescent and adult rats exposed to maternal immune activation
Hemmerle, A. M., Ahlbrand, R. A., Bronson, S. L., Lundgren, K. H., Richtand, N. M., & Seroogy, K. B. (2015) · Schizophrenia Research · doi:10.1016/j.schres.2015.07.006 · Cited by 33 · see citing works
“Evidence supporting this gene/environment interaction has also been demonstrated in other rodent animal models, where activation of the prenatal and neonatal immune system by Poly I:C in DISC1 mutant mice results in offspring with behavior and cellular effects worsened compared to mutant animals alone (Abazyan et al.,…”
BackgroundResult
Paternal valproic acid exposure in mice triggers behavioral alterations in offspring
Ibi, D., Fujiki, Y., Koide, N., Nakasai, G., Takaba, R., & Hiramatsu, M. (2019) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2019.106837 · Cited by 33 · see citing works
Self-citation
Immune activation in lactating dams alters sucklings' brain cytokines and produces non-overlapping behavioral deficits in adult female and male offspring: A novel neurodevelopmental model of sex-specific psychopathology
Arad, M., Piontkewitz, Y., Albelda, N., Shaashua, L., & Weiner, I. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.01.015 · Cited by 33 · see citing works
Phenotypic characterization of C57BL/6J mice carrying the Disc1 gene from the 129S6/SvEv strain
Juan, L.-W., Liao, C., Lai, W., Chang, C., Pei, J.-C., Wong, W.-R., Liu, C., Hwu, H., & Lee, L. (2013) · Brain Structure and Function · doi:10.1007/s00429-013-0577-8 · Cited by 31 · see citing works
“The interplays and consequences of genetic and environmental factors in the pathogenesis of mental disorders such as schizophrenia (Abazyan et al. 2010; Ibi et al. 2010) could be further investigated using this Disc1 mutant model.”
Effect of AceK (acesulfame potassium) on brain function under dietary restriction in mice.
Ibi, D., Suzuki, F., & Hiramatsu, M. (2018) · Physiology and Behavior · doi:10.1016/j.physbeh.2018.02.024 · Cited by 26 · see citing works
Self-citation
Neurobiology and treatment of social cognition in schizophrenia: Bridging the bed-bench gap
Kimoto, S., Makinodan, M., & Kishimoto, T. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.10.022 · Cited by 30 · see citing works
Season of birth in schizophrenia: a maternal-fetal chronobiological hypothesis.
Schwartz, P. (2011) · Medical Hypotheses · doi:10.1016/j.mehy.2011.02.019 · Cited by 32 · see citing works
“ventral hippocampal lesion model [13] as well as inflammatory models in neonatal mice [14,15] or rats [16] have also produced”
Background
Transient Knock-Down of Prefrontal DISC1 in Immune-Challenged Mice Causes Abnormal Long-Range Coupling and Cognitive Dysfunction throughout Development
Xu, X., Chini, M., Bitzenhofer, S. H., & Hanganu‐Opatz, I. L. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2170-18.2018 · Cited by 28 · see citing works
Role for neonatal D-serine signaling: prevention of physiological and behavioral deficits in adult Pick1 knockout mice
Nomura, J., Jaaro-Peled, H., Lewis, E. M., Núñez-Abades, P., Huppé-Gourgues, F., Cash-Padgett, T., Emiliani, F. E., Kondo, M. A., Furuya, A., Landek-Salgado, M. A., et al. (2015) · Molecular Psychiatry · doi:10.1038/mp.2015.61 · Cited by 23 · see citing works
Self-citation
Intra-nasal dopamine alleviates cognitive deficits in tgDISC1 rats which overexpress the human DISC1 gene
Wang, A., Fazari, B., Chao, O. Y.-H., Nikolaus, S., Trossbach, S. V., Korth, C., Sialana, F. J., Lübec, G., Huston, J. P., Mattern, C., et al. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.10.015 · Cited by 26 · see citing works
Tumour necrosis factor-mediated homeostatic synaptic plasticity in behavioural models: testing a role in maternal immune activation
Konefal, S., & Stellwagen, D. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0160 · Cited by 25 · see citing works
Exposure to acrylamide decreases noradrenergic axons in rat brain
Zhang, L., Hara, S., Ichinose, H., Nagashima, D., Morita, K., Sakurai, T., Ichihara, S., & Ichihara, G. (2020) · NeuroToxicology · doi:10.1016/j.neuro.2020.03.001 · Cited by 25 · see citing works
DISC1 Pathway in Brain Development: Exploring Therapeutic Targets for Major Psychiatric Disorders
Kamiya, A., Sedlak, T. W., & Pletnikov, M. V. (2012) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2012.00025 · Cited by 24 · see citing works
“However, recently, there have been several reports on developing and characterizing animal models based on combining prenatal immune activation with genetic mutations relevant to schizophrenia (Ibi et al., 2010; Ehninger et al., 2012).”
Background
Disrupted-in-Schizophrenia 1 (DISC1) Overexpression and Juvenile Immune Activation Cause Sex-Specific Schizophrenia-Related Psychopathology in Rats
Uzuneser, T. C., Speidel, J., Kogias, G., Wang, A., Silva, M. A. D. S., Huston, J. P., Zoicas, I., von Hörsten, S., Kornhuber, J., Korth, C., et al. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00222 · Cited by 24 · see citing works
“LPS, lipopolysaccharide; SD, social discrimination; NOR, novel object recognition; SNP, spatial novelty preference; OF, open field; PPI, prepulse inhibition; PND, postnatal day.”
BackgroundInfluential
Parvalbumin Interneuron Dysfunction in a Thalamo-Prefrontal Cortical Circuit in Disc1 Locus Impairment Mice
Delevich, K. M., Jaaro-Peled, H., Penzo, M. A., Sawa, A., & Li, B. (2020) · eNeuro · doi:10.1523/eneuro.0496-19.2020 · Cited by 25 · see citing works
“Furthermore, a variety of Disc1 mouse models exhibit reduced prefrontal PV expression (Hikida et al., 2007; Shen et al., 2008; Ibi et al., 2010; Niwa et al., 2010; Ayhan et al., 2011; Lee et al., 2013).”
BackgroundSelf-citation
Peripheral immune challenge with viral mimic during early postnatal period robustly enhances anxiety-like behavior in young adult rats
Konat, G. W., Lally, B. E., Toth, A. A., & Salm, A. K. (2011) · Metabolic Brain Disease · doi:10.1007/s11011-011-9244-z · Cited by 23 · see citing works
“Subsequent studies from this laboratory (Ibi et al. 2010) showed PIC treatment to precipitate and/or potentiate behavioral deficits in transgenic mice deficient in the disrupted-in-schizophrenia 1 (DISC1) gene.”
Background
Administration of molecular hydrogen during pregnancy improves behavioral abnormalities of offspring in a maternal immune activation model
Imai, K., Kotani, T., Tsuda, H., Nakano, T., Ushida, T., Iwase, A., Nagai, T., Toyokuni, S., Suzumura, A., & Kikkawa, F. (2018) · Scientific Reports · doi:10.1038/s41598-018-27626-4 · Cited by 22 · see citing works
Self-citation
Gene-environment interactions in cortical interneuron development and dysfunction: A review of preclinical studies
Ansen-Wilson, L. J., & Lipinski, R. J. (2016) · NeuroToxicology · doi:10.1016/j.neuro.2016.12.002 · Cited by 22 · see citing works
“…unique transcriptional cascades have been identified, they do not completely account for the observed biological complexity (Peyre et al., 2015; Xu et al., 2004; Butt et al., 2005, 2008; Flames et al., 2007; Miyoshi et al., 2007; Wonders et al., 2008; Welagen and Anderson, 2011; Inan et al., 2012).”
A Classification of Sociomedical Health Indicators: Perspectives for Health Administrators and Health Planners
Siegmann, A. E. (1976) · International Journal of Health Services · doi:10.2190/my7u-4bgm-9qfy-n0tn · Cited by 22 · see citing works
No association of Disrupted-in-Schizophrenia-1 variation with prefrontal function in patients with schizophrenia and bipolar disorder
Prata, D. P., Mechelli, A., Picchioni, M., Fu, C. H. Y., Kane, F., Kalidindi, S., McDonald, C., Kravariti, E., Toulopoulou, T., Bramon, E., et al. (2010) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2010.00665.x · Cited by 21 · see citing works
“…protein zeta-1 (FEZ1), pericentriolar material 1 (PCM1) and DISC1-binding zinc finger protein (DBZ)] (Burdick et al. 2008; Eastwood et al. 2010; Millar et al. 2000; Ming & Song 2009; Miyoshi et al. 2003; Nicodemus et al. 2007; Taya et al. 2007) and gene × environment interactions (Ibi et al. 2010).”
Background
Predicting Risk and the Emergence of Schizophrenia
Clarke, M. C., Kelleher, I., Clancy, M., & Cannon, M. D. (2012) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2012.06.003 · Cited by 21 · see citing works
Combination of neonatal PolyI:C and adolescent phencyclidine treatments is required to induce behavioral abnormalities with overexpression of GLAST in adult mice
Hida, H., Mouri, A., Ando, Y., Mori, K., Mamiya, T., Iwamoto, K., Ozaki, N., Yamada, K., Nabeshima, T., & Noda, Y. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.09.026 · Cited by 19 · see citing works
Self-citation
A Role for the Transcription Factor Nk2 Homeobox 1 in Schizophrenia: Convergent Evidence from Animal and Human Studies
Malt, E. A., Juhasz, K., Malt, U. F., & Naumann, T. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00059 · Cited by 19 · see citing works
“When exposed to an immune challenge corresponding to viral infection during the neonatal period, the transgenic mice exhibited impaired Nkx2-1-associated behaviors, such as fear memory, social recognition, and social interaction (Ibi et al., 2010).”
Background
Experimental Schizophrenia Models in Rodents Established with Inflammatory Agents and Cytokines
Nawa, H., & Yamada, K. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-458-2_28 · Cited by 18 · see citing works
Innate immune activation of astrocytes impairs neurodevelopment via upregulation of follistatin-like 1 and interferon-induced transmembrane protein 3
Yamada, S., Itoh, N., Nagai, T., NAKAI, T., Ibi, D., Nakajima, A., Nabeshima, T., & Yamada, K. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1332-0 · Cited by 18 · see citing works
Self-citation
Evaluating negative-symptom-like behavioural changes in developmental models of schizophrenia
Moser, P. C. (2013) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2013.11.004 · Cited by 16 · see citing works
“One series of studies used post-natal polyI:C administration (PD2-6) in a Disrupted-in-schizophrenia-1 (DISC-1) transgenic mouse (Ibi et al., 2010; Nagai et al., 2011) and demonstrated deficits in various tests including tests for cognition and social interaction in DISC-1 mice exposed to polyI:C.”
Adolescent Isolation Interacts With DISC1 Point Mutation to Impair Adult Social Memory and Synaptic Functions in the Hippocampus
Li, N., Cui, L., Song, G., Guo, L., Gu, H., Cao, H., Li, G.-D., & Zhou, Y. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00238 · Cited by 16 · see citing works
“Gene × environment studies have been done with both DISC1 transgenic mice (Abazyan et al., 2010; Ibi et al., 2010; Nagai et al., 2011; Niwa et al., 2013) and DISC1 point mutation (L100P and Q31L) heterozygotes (Haque et al.”
Background
Adolescent stress leads to glutamatergic disturbance through dopaminergic abnormalities in the prefrontal cortex of genetically vulnerable mice
Matsumoto, Y., Niwa, M., Mouri, A., Noda, Y., Fukushima, T., Ozaki, N., & Nabeshima, T. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4704-8 · Cited by 15 · see citing works
“…2011; Callicott et al. 2005; Furukubo-Tokunaga et al. 2016; Hamshere et al. 2005; Hashimoto et al. 2006; Hennah et al. 2003; Hodgkinson et al. 2004; Ibi et al. 2010; Ishizuka et al. 2011; Jaaro-Peled et al. 2016; Jaaro-Peled et al. 2013; Kamiya et al. 2005; Kilpinen et al. 2008; Nagai et al. 2011;…”
Self-citation
Spared motivational modulation of cognitive effort in a maternal immune activation model of schizophrenia risk
Bates, V., Maharjan, A., Millar, J., Bilkey, D. K., & Ward, R. D. (2018) · Behavioral Neuroscience · doi:10.1037/bne0000230 · Cited by 15 · see citing works
Cerebral Response to Peripheral Challenge with a Viral Mimetic
Konat, G. W. (2015) · Neurochemical Research · doi:10.1007/s11064-015-1746-3 · Cited by 14 · see citing works
“PIC challenge also exacerbated behavioral deficits in transgenic mice deficient in the disrupted-in-schizophrenia 1 (DISC1) gene [130].”
Background
Molecular Genetic Models Related to Schizophrenia and Psychotic Illness: Heuristics and Challenges
O’Tuathaigh, C. M. P., Desbonnet, L., Moran, P. M., Kirby, B. P., & Waddington, J. L. (2011) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_111 · Cited by 13 · see citing works
Application of animal experimental models in the research of schizophrenia
Wang, P., Li, M., Zhao, A., & Ma, J. (2021) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32863 · Cited by 13 · see citing works
“The animals with a Disc1 gene combined with PolyI:C and other environmental factors are used for their schizophrenia-like phenotypes, such as loss of object recognition and hippocampal-dependent fear memory (Ibi et al., 2010; Nagai, Ibi, & Yamada, 2011).”
Background
Schizophrenia-related dysbindin-1 gene is required for innate immune response and homeostasis in the developing subventricular zone
Al‐Shammari, A. R., Bhardwaj, S. K., Musaelyan, K., Srivastava, L. K., & Szele, F. G. (2018) · Schizophrenia · doi:10.1038/s41537-018-0057-5 · Cited by 12 · see citing works
Knock-Down of Hippocampal DISC1 in Immune-Challenged Mice Impairs the Prefrontal–Hippocampal Coupling and the Cognitive Performance Throughout Development
Xu, X., Song, L., & Hanganu‐Opatz, I. L. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa291 · Cited by 12 · see citing works

[PolyI:C-induced neurodevelopmental animal model for schizophrenia].
Ibi, D., Nagai, T., Nabeshima, T., & Yamada, K. (2011) · PubMed · Cited by 10 · see citing works
Self-citation
Animal Model for Schizophrenia That Reflects Gene-Environment Interactions
Nagai, T., Ibi, D., & Yamada, K. (2011) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.34.1364 · Cited by 36 · see citing works
Self-citation
Neonatal polyI:C treatment in mice results in schizophrenia-like behavioral and neurochemical abnormalities in adulthood
Ibi, D., Nagai, T., Kitahara, Y., Mizoguchi, H., Koike, H., Shiraki, A., Takuma, K., Kamei, H., Noda, Y., Nitta, A., et al. (2009) · Neuroscience Research · doi:10.1016/j.neures.2009.03.015 · Cited by 135 · see citing works
Self-citation
Maternal Immune Activation during Gestation Interacts withDisc1Point Mutation to Exacerbate Schizophrenia-Related Behaviors in Mice
Lipina, T. V., Zai, C. C. H., Hlousek, D., Roder, J., & Wong, A. H. C. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0091-13.2013 · Cited by 146 · see citing works
Prenatal interaction of mutant DISC1 and immune activation produces adult psychopathology
Abazyan, B., Nomura, J., Kannan, G., Ishizuka, K., Tamashiro, K. L., Nucifora, F., Pogorelov, V., Ladenheim, B., Yang, C., Krasnova, I. N., et al. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.09.022 · Cited by 255 · see citing works

Authors: Ibi, D., Nagai, T., Koike, H., Kitahara, Y., Mizoguchi, H., Niwa, M., Jaaro-Peled, H., Nitta, A., Yoneda, Y., & Nabeshima, T.
Affiliations: Nagoya University Hospital (JP)
Nagoya University (JP)
Kanazawa University (JP)
Research Institute of Environmental Medicine, Nagoya University (JP)
Johns Hopkins University (US)
Meijo University (JP)
ORCID: Nagai, Taku
Mizoguchi, Hiroyuki
Niwa, Minae
Jaaro-Peled, Hanna
Nitta, Atsumi
Yoneda, Yukio
Nabeshima, Toshitaka
Venue: Behavioural Brain Research
Publisher: Elsevier BV
Published: 2010-01-05
Volume: 206
Issue: 1
Pages: 32-37
ISSN: 0166-4328 (ISSN-L)
DOI: 10.1016/j.bbr.2009.08.027
PMC: PMC2846597
OpenAlex: W1988682809
Cited by: 137
References: 26
Citations by year: 2026: 1 · 2025: 4 · 2024: 3 · 2023: 1 · 2022: 5 · 2021: 3 · 2020: 3 · 2019: 5 · 2018: 10 · 2017: 12 · 2016: 9 · 2015: 15 · 2014: 12 · 2013: 17 · 2012: 11
FWCI: 7.42
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Behavioural Brain Research (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (P20MH084018, R01MH069853)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: schizophrenia, gene-environment interaction, DISC1, poly(I:C), viral infection, brain development, object recognition, social recognition, fear memory, hippocampus, parvalbumin interneurons, medial prefrontal cortex, transgenic mice
MeSH terms: Analysis of Variance, Animals, Animals, Newborn, Behavior, Animal, Conditioning, Classical, Fear, Female, Hippocampus, Hyperkinesis, Immunohistochemistry, Interferon Inducers, Male, Memory, Short-Term, Mice, Transgenic, Nerve Tissue Proteins, Parvalbumins, Phenotype, Poly I-C, Social Behavior, Staining and Labeling, Reflex, Startle, Dizocilpine Maleate, Ki-67 Antigen, Recognition, Psychology, Freezing Reaction, Cataleptic, Cell Proliferation, Mice, Sensory Gating

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Combined effect of neonatal immune activation and mutant DISC1 on phenotypic changes in adulthood

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