Cognitive impairment following maternal separation in rats mediated by the NAD+/SIRT3 axis via modulation of hippocampal synaptic plasticity

Abstract Maternal separation (MS) during early life can induce behaviors in adult animals that resemble those seen in schizophrenia, manifesting cognitive deficits. These cognitive deficits may be indicative of oxidative stress linked to mitochondrial dysfunction. However, there is limited understan...

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Main Authors: Keke Hao, Fashuai Chen, Shilin Xu, Ying Xiong, Rui Xu, Huan Huang, Chang Shu, Yisheng Lv, Gaohua Wang, Huiling Wang
Format: Article
Language:English
Published: Nature Publishing Group 2025-03-01
Series:Translational Psychiatry
Online Access:https://doi.org/10.1038/s41398-025-03318-2
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author Keke Hao
Fashuai Chen
Shilin Xu
Ying Xiong
Rui Xu
Huan Huang
Chang Shu
Yisheng Lv
Gaohua Wang
Huiling Wang
author_facet Keke Hao
Fashuai Chen
Shilin Xu
Ying Xiong
Rui Xu
Huan Huang
Chang Shu
Yisheng Lv
Gaohua Wang
Huiling Wang
author_sort Keke Hao
collection DOAJ
description Abstract Maternal separation (MS) during early life can induce behaviors in adult animals that resemble those seen in schizophrenia, manifesting cognitive deficits. These cognitive deficits may be indicative of oxidative stress linked to mitochondrial dysfunction. However, there is limited understanding of the molecular mechanisms regulating mitochondria in neural circuits that govern cognitive impairment relevant to schizophrenia, and their impact on neuronal structure and function. A 24-h MS rat model was utilized to simulate features associated with schizophrenia. Schizophrenia-associated behaviors and cognitive impairment were assessed using the open field test, pre-pulse inhibition, novel object recognition test, and Barnes maze test. The levels of mitochondrial proteins were measured using western blot analysis. Additionally, alterations in mitochondrial morphology, reduced hippocampal neuronal spine density, and impaired LTP in the hippocampus were observed. Nicotinamide (NAM) supplementation, administration of honokiol (HNK) (a SIRT3 activator), or overexpression of SIRT3 could inhibit cognitive deficits and cellular dysfunction. Conversely, administration of 3-TYP (a SIRT3 inhibitor) or knocking down SIRT3 expression in control rats led to deficits in behavioral and hippocampal neuronal phenotype. Our results suggest a causal role for the NAD+/SIRT3 axis in modulating cognitive behaviors via effects on hippocampal neuronal synaptic plasticity. The NAD+/SIRT3 axis could be a promising therapeutic target for addressing cognitive dysfunctions, such as those seen in schizophrenia.
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spelling doaj-art-d9bdc3d6d7fa4a9fa9a84db594a7d6032025-08-20T02:10:22ZengNature Publishing GroupTranslational Psychiatry2158-31882025-03-0115111010.1038/s41398-025-03318-2Cognitive impairment following maternal separation in rats mediated by the NAD+/SIRT3 axis via modulation of hippocampal synaptic plasticityKeke Hao0Fashuai Chen1Shilin Xu2Ying Xiong3Rui Xu4Huan Huang5Chang Shu6Yisheng Lv7Gaohua Wang8Huiling Wang9Department of Psychiatry, Renmin Hospital of Wuhan UniversityDepartment of Psychiatry, Renmin Hospital of Wuhan UniversityDepartment of Psychiatry, Renmin Hospital of Wuhan UniversityDepartment of Psychiatry, Renmin Hospital of Wuhan UniversityDepartment of Psychiatry, Renmin Hospital of Wuhan UniversityDepartment of Psychiatry, Renmin Hospital of Wuhan UniversityDepartment of Psychiatry, Renmin Hospital of Wuhan UniversityDepartment of Physiology, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and TechnologyDepartment of Psychiatry, Renmin Hospital of Wuhan UniversityDepartment of Psychiatry, Renmin Hospital of Wuhan UniversityAbstract Maternal separation (MS) during early life can induce behaviors in adult animals that resemble those seen in schizophrenia, manifesting cognitive deficits. These cognitive deficits may be indicative of oxidative stress linked to mitochondrial dysfunction. However, there is limited understanding of the molecular mechanisms regulating mitochondria in neural circuits that govern cognitive impairment relevant to schizophrenia, and their impact on neuronal structure and function. A 24-h MS rat model was utilized to simulate features associated with schizophrenia. Schizophrenia-associated behaviors and cognitive impairment were assessed using the open field test, pre-pulse inhibition, novel object recognition test, and Barnes maze test. The levels of mitochondrial proteins were measured using western blot analysis. Additionally, alterations in mitochondrial morphology, reduced hippocampal neuronal spine density, and impaired LTP in the hippocampus were observed. Nicotinamide (NAM) supplementation, administration of honokiol (HNK) (a SIRT3 activator), or overexpression of SIRT3 could inhibit cognitive deficits and cellular dysfunction. Conversely, administration of 3-TYP (a SIRT3 inhibitor) or knocking down SIRT3 expression in control rats led to deficits in behavioral and hippocampal neuronal phenotype. Our results suggest a causal role for the NAD+/SIRT3 axis in modulating cognitive behaviors via effects on hippocampal neuronal synaptic plasticity. The NAD+/SIRT3 axis could be a promising therapeutic target for addressing cognitive dysfunctions, such as those seen in schizophrenia.https://doi.org/10.1038/s41398-025-03318-2
spellingShingle Keke Hao
Fashuai Chen
Shilin Xu
Ying Xiong
Rui Xu
Huan Huang
Chang Shu
Yisheng Lv
Gaohua Wang
Huiling Wang
Cognitive impairment following maternal separation in rats mediated by the NAD+/SIRT3 axis via modulation of hippocampal synaptic plasticity
Translational Psychiatry
title Cognitive impairment following maternal separation in rats mediated by the NAD+/SIRT3 axis via modulation of hippocampal synaptic plasticity
title_full Cognitive impairment following maternal separation in rats mediated by the NAD+/SIRT3 axis via modulation of hippocampal synaptic plasticity
title_fullStr Cognitive impairment following maternal separation in rats mediated by the NAD+/SIRT3 axis via modulation of hippocampal synaptic plasticity
title_full_unstemmed Cognitive impairment following maternal separation in rats mediated by the NAD+/SIRT3 axis via modulation of hippocampal synaptic plasticity
title_short Cognitive impairment following maternal separation in rats mediated by the NAD+/SIRT3 axis via modulation of hippocampal synaptic plasticity
title_sort cognitive impairment following maternal separation in rats mediated by the nad sirt3 axis via modulation of hippocampal synaptic plasticity
url https://doi.org/10.1038/s41398-025-03318-2
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