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      A postpartum enriched environment rescues impaired cognition and oxidative markers in aged mice with gestational inflammation

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          Abstract

          Introduction

          Previous studies have shown that gestational inflammation can accelerate age‐associated cognitive decline (AACD) in maternal mice; enriched environments (EEs) have been reported to protect normally aging mice from AACD and improve mitochondrial function. However, it is unclear whether the nitrosative stress‐related proteins tet methylcytosine dioxygenase 1 (TET1) and S‐nitrosoglutathione reductase (GSNOR) are involved in the accelerated aging process of gestational inflammation and whether EEs can slow this process.

          Methods

          In this study, CD‐1 female mice on the 15th day of pregnancy were injected with bacterial lipopolysaccharide (50 μg/kg; LPS group) or an equivalent amount of normal saline (CON group) from the abdominal cavity for 4 consecutive days. Twenty‐one days after delivery, half of the LPS‐treated mice were randomly selected for EE until the end of the behavioral experiment (LPS‐E group). When the female rats were raised to 6 months and 18 months of age, the Morris water maze (MWM) was used to detect spatial learning and memory ability; RT‐PCR and Western blots were used to measure the mRNA and protein levels of hippocampal TET1 and GSNOR.

          Results

          As for the control group, compared with 6‐month‐old mice, the spatial learning and memory ability of 18‐month‐old mice decreased, and the hippocampal TET1 and GSNOR mRNA and protein levels were decreased. Gestational inflammation exacerbated these age‐related changes, but an EE alleviated the effects. Pearson's correlation analysis indicated that performance during the learning and memory periods in the MWM correlated with the levels of hippocampal TET1 and GSNOR.

          Conclusions

          Our findings suggest that gestational inflammation accelerates age‐related learning and memory impairments and that postpartum EE exposure could alleviate these changes. These effects may be related to hippocampal TET1 and GSNOR expression.

          Abstract

          Protein cysteine residues can be oxidized by nitric oxide (NO) to form protein S‐nitrosothiols (SNOs) in a process called S‐nitrosylation. S‐nitrosoglutathione reductase (GSNOR) is a highly specific denitrase for GSNO; it controls the intracellular levels of GSNO and protein SNOs and protects the body from nitrosative stress.

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          Most cited references53

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          Oxidative Stress

          Oxidative stress is two sided: Whereas excessive oxidant challenge causes damage to biomolecules, maintenance of a physiological level of oxidant challenge, termed oxidative eustress, is essential for governing life processes through redox signaling. Recent interest has focused on the intricate ways by which redox signaling integrates these converse properties. Redox balance is maintained by prevention, interception, and repair, and concomitantly the regulatory potential of molecular thiol-driven master switches such as Nrf2/Keap1 or NF-κB/IκB is used for system-wide oxidative stress response. Nonradical species such as hydrogen peroxide (H2O2) or singlet molecular oxygen, rather than free-radical species, perform major second messenger functions. Chemokine-controlled NADPH oxidases and metabolically controlled mitochondrial sources of H2O2 as well as glutathione- and thioredoxin-related pathways, with powerful enzymatic back-up systems, are responsible for fine-tuning physiological redox signaling. This makes for a rich research field spanning from biochemistry and cell biology into nutritional sciences, environmental medicine, and molecular knowledge-based redox medicine.
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            Mitochondria, oxidants, and aging.

            The free radical theory of aging postulates that the production of intracellular reactive oxygen species is the major determinant of life span. Numerous cell culture, invertebrate, and mammalian models exist that lend support to this half-century-old hypothesis. Here we review the evidence that both supports and conflicts with the free radical theory and examine the growing link between mitochondrial metabolism, oxidant formation, and the biology of aging.
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              Enriched environments, experience-dependent plasticity and disorders of the nervous system.

              Behavioural, cellular and molecular studies have revealed significant effects of enriched environments on rodents and other species, and provided new insights into mechanisms of experience-dependent plasticity, including adult neurogenesis and synaptic plasticity. The demonstration that the onset and progression of Huntington's disease in transgenic mice is delayed by environmental enrichment has emphasized the importance of understanding both genetic and environmental factors in nervous system disorders, including those with Mendelian inheritance patterns. A range of rodent models of other brain disorders, including Alzheimer's disease and Parkinson's disease, fragile X and Down syndrome, as well as various forms of brain injury, have now been compared under enriched and standard housing conditions. Here, we review these findings on the environmental modulators of pathogenesis and gene-environment interactions in CNS disorders, and discuss their therapeutic implications.
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                Author and article information

                Contributors
                y1520989@163.com
                caolei0531@163.com
                Journal
                Brain Behav
                Brain Behav
                10.1002/(ISSN)2157-9032
                BRB3
                Brain and Behavior
                John Wiley and Sons Inc. (Hoboken )
                2162-3279
                21 November 2022
                December 2022
                : 12
                : 12 ( doiID: 10.1002/brb3.v12.12 )
                : e2817
                Affiliations
                [ 1 ] Department of Neurology (Sleep Disorders) the Affiliated Chaohu Hospital of Anhui Medical University Hefei (Chaohu) Anhui P. R. China
                [ 2 ] Department of Neurology the Second Affiliated Hospital of Anhui Medical University Hefei Anhui Province P. R. China
                [ 3 ] Department of Neurology Bengbu Second People's Hospital Bengbu Anhui Province P. R. China
                [ 4 ] Department of Neurology The First Affiliated Hospital of Anhui University of Science and Technology Huainan Anhui Province P. R. China
                [ 5 ] Department of Neurology the First Affiliated Hospital of Anhui Medical University Hefei Anhui Province P. R. China
                Author notes
                [*] [* ] Correspondence

                Gui‐Hai Chen, Department of Neurology (Sleep Disorders), the Affiliated Chaohu Hospital of Anhui Medical University, Hefei (Chaohu) 238000, Anhui, P. R. China.

                Email: y1520989@ 123456163.com

                Lei Cao, Department of Neurology, the Second Affiliated Hospital of Anhui Medical University, Hefei 230601, Anhui Province, P. R. China.

                caolei0531@ 123456163.com

                Author information
                https://orcid.org/0000-0002-1277-6143
                Article
                BRB32817
                10.1002/brb3.2817
                9759132
                36409568
                e37b04b7-d720-4dd3-809a-9bbe36eb3e64
                © 2022 The Authors. Brain and Behavior published by Wiley Periodicals LLC.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 16 October 2022
                : 18 December 2021
                : 22 October 2022
                Page count
                Figures: 4, Tables: 2, Pages: 12, Words: 8384
                Funding
                Funded by: National Natural Science Foundation of China , doi 10.13039/501100001809;
                Award ID: 81370444
                Award ID: 81671316
                Funded by: Natural Science Foundation for the Youth of Anhui Province
                Award ID: 1708085QH182
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                December 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.2.3 mode:remove_FC converted:17.12.2022

                Neurosciences
                aging,enriched environment,lipopolysaccharide,memory,s‐nitrosoglutathione reductase (gsnor),tet methylcytosine dioxygenase 1 (tet1)

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