Social isolation rearing‐induced impairment of the hippocampal neurogenesis is associated with deficits in spatial memory and emotion‐related behaviors in juvenile mice

Ibi, Daisuke; Takuma, Kazuhiro; Koike, Hiroyuki; Mizoguchi, Hideaki; Tsuritani, Katsuki; Kuwahara, Yusuke; Kamei, Hiroyuki; Nagai, Taku; Yoneda, Yukio; Nabeshima, Toshitaka; Yamada, Kiyofumi

doi:10.1111/j.1471-4159.2007.05207.x

Cited by 223 publications

(183 citation statements)

References 56 publications

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“…Lin et al (13) have reported that NPAS4 regulates the development of GABAergic inhibitory synapses in an activity-dependent manner and suggested its homeostatic role in the balance between excitatory and inhibitory neuronal activities in the brain. We previously reported that reduced Npas4 mRNA levels may contribute to impairments in adult neurogenesis in the hippocampus, memory and emotional behaviors induced by social isolation or restriction stress (16,17). Recent studies (18,19) revealed that NPAS4 is important in memory formation and consolidation.…”

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confidence: 99%

Neuronal Per Arnt Sim (PAS) Domain Protein 4 (NPAS4) Regulates Neurite Outgrowth and Phosphorylation of Synapsin I

Yun

Nagai

Furukawa‐Hibi

et al. 2013

Journal of Biological Chemistry

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Background: NPAS4 is involved in memory formation, but its roles in neuronal function remain to be fully elucidated. Results: NPAS4 increased CDK5-dependent phosphorylation of synapsin I that was associated with neurite elongation. Conclusion: NPAS4 induced CDK5-dependent phosphorylation of synapsin I to facilitate neurite outgrowth. Significance: NPAS4 plays an important role in the structural and functional plasticity of neurons.

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confidence: 99%

Neuronal Per Arnt Sim (PAS) Domain Protein 4 (NPAS4) Regulates Neurite Outgrowth and Phosphorylation of Synapsin I

Yun

Nagai

Furukawa‐Hibi

et al. 2013

Journal of Biological Chemistry

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“…At a cellular level, EE triggers an increase in the generation and integration of adult-born neurons into the granule cell layer (GCL) of the hippocampus and increases dendritic branching complexity and synapse formation in excitatory neurons of the hippocampus (Kempermann et al 1997(Kempermann et al , 1998van Praag et al 2000;Faherty et al 2003). Further, reduced sensory stimulation leads to a decrease in progenitor proliferation and dendrite branch patterns, which likely results in the wellcharacterized increase in depression and reduced cognitive capacity (Silva-Gomez et al 2003;Bianchi et al 2006;Ibi et al 2008). Importantly, retrospective analysis of humans exposed to psychosocial or behavioral enrichment appears to support the findings of animal studies (Cotman and Berchtold 2002;Agrigoroaei and Lachman 2011;Erickson et al 2011).…”

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confidence: 99%

MSK1 regulates environmental enrichment-induced hippocampal plasticity and cognitive enhancement

et al. 2012

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Environmental enrichment (EE) has marked beneficial effects on cognitive capacity. Given the possibility that this form of neuronal plasticity could function via the actuation of the same cellular signaling pathways that underlie learning/memory formation, we examined whether the MAPK cascade effector, mitogen/stress-activated kinase 1 (MSK1), could play a role in this process. MSK1 functions as a key signaling intermediate that couples changes in neuronal activity into inducible gene expression, neuronal plasticity, and learning/memory. Here, we show that MSK1 is expressed in excitatory cell layers of the hippocampus, progenitor cells of the subgranular zone (SGZ), and adult-born immature neurons. MSK1 2/2 mice exhibit reduced spinogenesis and decreased dendritic branching complexity in hippocampal neurons, compared with WT mice. Further, in MSK1 2/2 mice, progenitor cell proliferation within the SGZ was significantly reduced and, correspondingly, the number of immature neurons within the dentate gyrus was significantly reduced. Consistent with prior work, MSK1 2/2 mice displayed deficits in both spatial and recognition memory tasks. Strikingly, cognitive enhancement resulting from a 40-d period of EE was markedly reduced in MSK1 2/2 animals. MSK1 2/2 mice exhibited reduced levels of EE-induced spinogenesis and SGZ progenitor proliferation. Taken together, these data reveal that MSK1 serves as a critical regulator of hippocampal physiology and function and that MSK1 serves as a key conduit by which enriching stimuli augment cellular plasticity and cognition.

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“…[11][12][13][14][15][16] Generally, SI stress impairs neuronal precursor cells at multiple steps, including the mitotic and survival phases of neurogenesis. 17 SI also suppresses the expression of glutamate receptor, 18 which functions in learning and memory. 19 In contrast, SI-induced abnormalities can be rescued by environmental enrichment, 14 and fluoxetine, an antidepressant that selectively inhibits serotonin re-uptake.…”

Section: Introductionmentioning

confidence: 99%

“…19 In contrast, SI-induced abnormalities can be rescued by environmental enrichment, 14 and fluoxetine, an antidepressant that selectively inhibits serotonin re-uptake. 17,20 Interestingly, environmental enrichment ameliorates SIinduced defects at both the mitotic and post-mitotic phases of hippocampal neurogenesis, 21 whereas fluoxetine mainly protects against the SI-induced downregulation of cell proliferation. 17 To investigate the physiological roles of L1-RTP in the CNS, we first examined L1 copy numbers in the hippocampus genome of mice at different ages.…”

Section: Introductionmentioning

confidence: 99%

“…17,20 Interestingly, environmental enrichment ameliorates SIinduced defects at both the mitotic and post-mitotic phases of hippocampal neurogenesis, 21 whereas fluoxetine mainly protects against the SI-induced downregulation of cell proliferation. 17 To investigate the physiological roles of L1-RTP in the CNS, we first examined L1 copy numbers in the hippocampus genome of mice at different ages. Interestingly, we found that L1 copy numbers in the hippocampus were higher in 8-week-old mice than in 3-week-old mice.…”

Section: Introductionmentioning

confidence: 99%

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Modulation of long interspersed nuclear element-1 in the mouse hippocampus during maturation

Ueno

Okamura²,

Mishina

et al. 2016

Mobile Genetic Elements

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Background: Retrotransposition of long interspersed nuclear element-1 (L1-RTP) is proposed to contribute to central nervous system (CNS) plasticity by inducing mosaicism of neuronal cells. Clinical studies have identified increased L1 copy numbers in the brains of patients with psychiatric disorders. These observations implicate that L1-RTP is important for neurogenesis and that its deregulation represents a risk factor for mental disorders. However, no supportive evidence is available for understanding the importance of L1-RTP in CNS function. Findings: To explore the physiological role of L1-RTP in CNS, we examined the L1 copy number during maturation. Interestingly, the L1 copy number increased after birth in the mouse hippocampus, but not the frontal lobe, with maximal copy numbers found in 8-week-old mice. This age-dependent L1 increase was abolished by administration of a reverse-transcriptase inhibitor, stavudine (d4T), which showed no toxic effects. Notably, the age-dependent L1 increase was attenuated by post-weaning social isolation (SI) stress, a well-known intervention for inducing psychiatric disorders in mice, or deletion of the NR2A gene that encodes a subunit of the glutamate receptor. Moreover, the negative effects of SI stress on L1-RTP were partially restored by environmental enrichment with voluntary running, but not by fluoxetine, a commonly used antipsychiatric drug. Finally, behavioral experiments revealed that learning memory was defective in d4T-treated mice, which was similarly observed in mice raised under SI stress. Conclusion: We detected the modulation of L1-RTP in the hippocampus during maturation of the CNS. In a recent study, we demonstrated that stimulants such as methamphetamine and cocaine were active in the induction of L1-RTP in neuronal cells, and previous studies have shown that NR2A-deficient mice are susceptible to mental abnormality. Herein, our data support the notion that the age-dependent modulation of L1-RTP is involved in genome differentiation in the hippocampus, and that modulation defects are linked to the development of psychiatric disorders.

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Social isolation rearing‐induced impairment of the hippocampal neurogenesis is associated with deficits in spatial memory and emotion‐related behaviors in juvenile mice

Cited by 223 publications

References 56 publications

Neuronal Per Arnt Sim (PAS) Domain Protein 4 (NPAS4) Regulates Neurite Outgrowth and Phosphorylation of Synapsin I

Neuronal Per Arnt Sim (PAS) Domain Protein 4 (NPAS4) Regulates Neurite Outgrowth and Phosphorylation of Synapsin I

MSK1 regulates environmental enrichment-induced hippocampal plasticity and cognitive enhancement

Modulation of long interspersed nuclear element-1 in the mouse hippocampus during maturation

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