Enriched environment improves sevoflurane-induced cognitive impairment during late-pregnancy via hippocampal histone acetylation

Yu, Zhiqiang; Zhang, Peijun; Wang, Jianbo; Cui, Jian; Wang, Haiyun

doi:10.1590/1414-431x20209861

Cited by 11 publications

(9 citation statements)

References 28 publications

(30 reference statements)

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“…The present results showed that MSD decreased the protein expression levels of BDNF and TrkB in the elderly offspring, which further supports that decreased expression of BDNF and TrkB may be a potential cause of depression and cognitive impairment. A previous study showed that the downregulation of BDNF expression induced by maternal sevoflurane exposure was reversed by EE through increasing the level of histone acetylation ( Yu et al, 2020b ). Consistently, we found that EE reversed the MSD-induced downregulation of the BDNF/TrkB signaling pathway to improve depression and cognitive impairment.…”

Section: Discussionmentioning

confidence: 99%

Long-term environmental enrichment overcomes depression, learning, and memory impairment in elderly CD-1 mice with maternal sleep deprivation exposure

Zhang

Wei

et al. 2023

Front. Aging Neurosci.

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Early-life stress disrupts central nervous system development and increases the risk of neuropsychiatric disorder in offspring based on rodent studies. Maternal sleep deprivation (MSD) in rodents has also been associated with depression and cognitive decline in adult offspring. However, it is not known whether these issues persist into old age. Environmental enrichment is a non-pharmacological intervention with proven benefits in improving depression and cognitive impairment; however, it is unclear whether these benefits hold for aging mice following MSD exposure. The aim of this study was to explore the effects of MSD on depression and cognition in elderly offspring CD-1 mice and to determine whether long-term environmental enrichment could alleviate these effects by improving neuroinflammation and synaptic plasticity. The offspring mice subjected to MSD were randomly assigned to either a standard environment or an enriched environment. At 18 months of age, the forced swimming and tail suspension tests were used to evaluated depression-like behaviors, and the Morris water maze test was used to evaluate cognitive function. The expression levels of hippocampal proinflammatory cytokines and synaptic plasticity-associated proteins were also measured. MSD increased depression-like behaviors and impaired cognition function in aging CD-1 offspring mice. These effects were accompanied by upregulated interleukin (IL)-1β, IL-6, and tumor necrosis factor-α expression, and downregulated brain-derived neurotrophic factor, tyrosine kinase receptor B, postsynaptic density-95, and synaptophysin expression in the hippocampus. All of these changes were reversed by long-term exposure to an enriched environment. These findings suggest that MSD exerts long-term effects on the behaviors of offspring in mice, leading to depression and cognitive impairment in older age. Importantly, long-term environmental enrichment could counteract the behavior difficulties induced by MSD through improving hippocampal proinflammatory cytokines and synaptic plasticity-associated proteins.

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Section: Discussionmentioning

confidence: 99%

Long-term environmental enrichment overcomes depression, learning, and memory impairment in elderly CD-1 mice with maternal sleep deprivation exposure

Zhang

Wei

et al. 2023

Front. Aging Neurosci.

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“…The concept of an enriched environment (EE) was proposed by Hebb in 1947 and is a simple and effective method to improve cognitive deficits (Alwis and Rajan, 2014 ). EE is an experimental paradigm that allows mice to receive sensory, motor, and social stimulation by placing them in larger devices equipped with a variety of toys and running wheels (Yu et al, 2020 ; Zhang et al, 2021 ). EE has been found to affect cell survival, neurogenesis, synaptogenesis, and dendritic morphology in the hippocampus (Wang et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Environmental Enrichment Reverses Maternal Sleep Deprivation-Induced Anxiety-Like Behavior and Cognitive Impairment in CD-1 Mice

Zhang

Cheng

Wang

et al. 2022

Front. Behav. Neurosci.

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Preclinical studies have clearly indicated that offspring of mothers who suffered sleep deprivation during pregnancy exhibit anxiety, depression-like behaviors, and cognitive deficits. The cognitive impairment induced by maternal sleep deprivation (MSD) is currently poorly treated. Growing evidence indicates that an enriched environment (EE) improves cognition function in models of Alzheimer’s disease, schizophrenia, and lipopolysaccharide. However, the effects of EE on hippocampal-dependent learning and memory, as well as synaptic plasticity markers changes induced by MSD, are unclear. In the present study, pregnant CD-1 mice were randomly divided into a control group, MSD group, and MSD+EE group. Two different living environments, including standard environment and EE, were prepared. When male and female offspring were 2 months, the open field test and elevated plus maze were used to assess anxiety-like behavior, and the Morris water maze was used to evaluate hippocampal learning and memory. Western blotting and real-time fluorescence quantitative polymerase chain reaction were used to detect the expression of brain-derived neurotrophic factor and Synaptotagmin-1 in the hippocampus of offspring. The results revealed that MSD-induced offspring showed anxiety-like behaviors and cognitive impairment, while EE alleviated anxiety-like behavior and cognitive impairment in offspring of the MSD+EE group. The cognitive impairment induced by MSD was associated with a decreased brain-derived neurotrophic factor and an increased Synaptotagmin-1, while EE increased and decreased brain-derived neurotrophic factor and Synaptotagmin-1 in the hippocampus of mice from the MSD+EE group, respectively. Taken together, we can conclude that EE has beneficial effects on MSD-induced synaptic plasticity markers changes and can alleviate anxiety-like behaviors and cognitive impairment.

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“…Sevoflurane is often used for anesthesia during pregnancy, and many studies have begun to preliminarily explore whether and how sevoflurane may have lasting harmful effects on the brains of gestationally exposed offspring. Multiple mechanisms are involved in neuronal damage to offspring, for example neuronal apoptosis [ 16 ], synaptic plasticity [ 17 ], and BDNF-related pathways [ 18 , 19 ]. Chai et al [ 20 ] reviewed the fundamentals of fetal toxicity related to gestational sevoflurane exposure and demonstrated that the pathology associated with fetal toxicity involves oxidative stress, neuroinflammation, neuronal apoptosis, and alteration of synaptic properties.…”

Section: Discussionmentioning

confidence: 99%

Effects of sevoflurane exposure during different stages of pregnancy on the brain development of rat offspring

Cui

et al. 2021

J Anesth

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Objective This study explored the effects of sevoflurane exposure during different stages of pregnancy on the brain development of offspring. Methods Thirty-six pregnant SD rats were randomly divided into 4 groups: control, sevoflurane exposure in early (S1) pregnancy, sevoflurane exposure in middle (S2) pregnancy, and sevoflurane exposure in late (S3) pregnancy. After natural birth, the learning and memory capacity of offspring rats was analyzed using the Morris water maze experiment. The hippocampi of offspring rats were collected. The levels of interleukin (IL)-1β, IL-6, and tumor necrosis factor (TNF)-α in the hippocampus were measured by ELISA. Additionally, the Nissl bodies in the hippocampus were analyzed using Nissl staining. Immunohistochemistry was used to examine the expression of BDNF and CPEB2 in the hippocampus of offspring. Proteins related to the NR4A1/NF-κB pathway were analyzed using western blotting. Results The memory and learning capacity of offspring rats was significantly reduced in the S1 and S2 groups compared to the control group (p < 0.05), while there was no obvious difference between the control and S3 groups (p > 0.05). The level of IL-1β was significantly increased (p < 0.05) in the S1 group compared with the control group. Sevoflurane anesthesia received in early and middle pregnancy could significantly affect the formation of Nissl bodies in the hippocampi of offspring rats. In addition, the expression of BDNF and CPEB2 in the hippocampi of offspring rats was greatly decreased in the S1 group compared with the control group (p < 0.05). The expression of NR4A1 in the hippocampi of rat offspring was significantly decreased in the S1 and S2 groups compared with the control group (p < 0.05). The expression of proteins related to the NF-κB pathway was increased in the S1 group compared to the control group (p < 0.05). Conclusions The neurotoxic effect of maternal sevoflurane anesthesia on the brain development of offspring is higher when the exposure occurs in early pregnancy than in late pregnancy, and its mechanism might involve the NR4A1/NF-κB pathway to increase the secretion of inflammatory cytokines.

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Enriched environment improves sevoflurane-induced cognitive impairment during late-pregnancy via hippocampal histone acetylation

Cited by 11 publications

References 28 publications

Long-term environmental enrichment overcomes depression, learning, and memory impairment in elderly CD-1 mice with maternal sleep deprivation exposure

Long-term environmental enrichment overcomes depression, learning, and memory impairment in elderly CD-1 mice with maternal sleep deprivation exposure

Environmental Enrichment Reverses Maternal Sleep Deprivation-Induced Anxiety-Like Behavior and Cognitive Impairment in CD-1 Mice

Effects of sevoflurane exposure during different stages of pregnancy on the brain development of rat offspring

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