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Effects of early postnatal exposure to fine particulate matter on emotional and cognitive development and structural synaptic plasticity in immature and mature rats

INTRODUCTION: Fine particulate matter (PM2.5) is closely associated with many neurological disorders including neurodegenerative disease, stroke, and brain tumors. However, the toxic effects of PM2.5 on neurodevelopment remain unclear. In this study, we aimed to determine the neurotoxic effects of e...

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Autores principales: Liu, Jie, Yang, Chen, Yang, Jing, Song, Xiaojie, Han, Wei, Xie, Mingdan, Cheng, Li, Xie, Lingling, Chen, Hengsheng, Jiang, Li
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6908876/
https://www.ncbi.nlm.nih.gov/pubmed/31709780
http://dx.doi.org/10.1002/brb3.1453
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author Liu, Jie
Yang, Chen
Yang, Jing
Song, Xiaojie
Han, Wei
Xie, Mingdan
Cheng, Li
Xie, Lingling
Chen, Hengsheng
Jiang, Li
author_facet Liu, Jie
Yang, Chen
Yang, Jing
Song, Xiaojie
Han, Wei
Xie, Mingdan
Cheng, Li
Xie, Lingling
Chen, Hengsheng
Jiang, Li
author_sort Liu, Jie
collection PubMed
description INTRODUCTION: Fine particulate matter (PM2.5) is closely associated with many neurological disorders including neurodegenerative disease, stroke, and brain tumors. However, the toxic effects of PM2.5 on neurodevelopment remain unclear. In this study, we aimed to determine the neurotoxic effects of early postnatal exposure to PM2.5 in immature and mature rats. METHODS: We exposed neonatal rats to PM2.5 (2 or 10 mg/kg body weight) through intranasal instillation from postnatal day (PND) 3–15, once a day. Emotional and cognitive development were evaluated using the elevated plus maze, forced swimming, and Morris water maze tests. Hippocampal tissue was collected and subjected to transmission electron microscopy observation and western blot analysis. RESULTS: Rats had lower body weight after exposure to high dose of PM2.5. The behavioral test results indicated that high‐dose PM2.5 exposure led to increased anxiety‐like symptoms in immature and mature rats, apparent depressive‐like behaviors in mature rats, and impaired spatial learning and memory abilities in immature rats, and low‐dose PM2.5 exposure increased anxiety‐like behaviors in immature rats. Further, high‐dose PM2.5 exposure contributed to fewer synapses, thinner postsynaptic density, and shorter active zone in immature and mature rats, and also decreased expressions of synaptophysin (SYP), growth associated protein‐43 (GAP43), and postsynaptic density‐95 (PSD95) in immature rats, SYP and PSD95 in mature rats. Moreover, low‐dose PM2.5 exposure diminished the expression of PSD95 in immature rats. In addition, high‐dose PM2.5 exposure reduced brain‐derived neurotrophic factor (BDNF) expression and cAMP response element binding protein (CREB) phosphorylation in both immature and mature rats, and low‐dose PM2.5 exposure lessened BDNF expression and CREB phosphorylation in immature rats. CONCLUSIONS: Our findings indicate that PM2.5 impairs emotional and cognitive development by disrupting structural synaptic plasticity, possibly via the CREB/BDNF signaling pathway.
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spelling pubmed-69088762019-12-20 Effects of early postnatal exposure to fine particulate matter on emotional and cognitive development and structural synaptic plasticity in immature and mature rats Liu, Jie Yang, Chen Yang, Jing Song, Xiaojie Han, Wei Xie, Mingdan Cheng, Li Xie, Lingling Chen, Hengsheng Jiang, Li Brain Behav Original Research INTRODUCTION: Fine particulate matter (PM2.5) is closely associated with many neurological disorders including neurodegenerative disease, stroke, and brain tumors. However, the toxic effects of PM2.5 on neurodevelopment remain unclear. In this study, we aimed to determine the neurotoxic effects of early postnatal exposure to PM2.5 in immature and mature rats. METHODS: We exposed neonatal rats to PM2.5 (2 or 10 mg/kg body weight) through intranasal instillation from postnatal day (PND) 3–15, once a day. Emotional and cognitive development were evaluated using the elevated plus maze, forced swimming, and Morris water maze tests. Hippocampal tissue was collected and subjected to transmission electron microscopy observation and western blot analysis. RESULTS: Rats had lower body weight after exposure to high dose of PM2.5. The behavioral test results indicated that high‐dose PM2.5 exposure led to increased anxiety‐like symptoms in immature and mature rats, apparent depressive‐like behaviors in mature rats, and impaired spatial learning and memory abilities in immature rats, and low‐dose PM2.5 exposure increased anxiety‐like behaviors in immature rats. Further, high‐dose PM2.5 exposure contributed to fewer synapses, thinner postsynaptic density, and shorter active zone in immature and mature rats, and also decreased expressions of synaptophysin (SYP), growth associated protein‐43 (GAP43), and postsynaptic density‐95 (PSD95) in immature rats, SYP and PSD95 in mature rats. Moreover, low‐dose PM2.5 exposure diminished the expression of PSD95 in immature rats. In addition, high‐dose PM2.5 exposure reduced brain‐derived neurotrophic factor (BDNF) expression and cAMP response element binding protein (CREB) phosphorylation in both immature and mature rats, and low‐dose PM2.5 exposure lessened BDNF expression and CREB phosphorylation in immature rats. CONCLUSIONS: Our findings indicate that PM2.5 impairs emotional and cognitive development by disrupting structural synaptic plasticity, possibly via the CREB/BDNF signaling pathway. John Wiley and Sons Inc. 2019-11-11 /pmc/articles/PMC6908876/ /pubmed/31709780 http://dx.doi.org/10.1002/brb3.1453 Text en © 2019 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Original Research
Liu, Jie
Yang, Chen
Yang, Jing
Song, Xiaojie
Han, Wei
Xie, Mingdan
Cheng, Li
Xie, Lingling
Chen, Hengsheng
Jiang, Li
Effects of early postnatal exposure to fine particulate matter on emotional and cognitive development and structural synaptic plasticity in immature and mature rats
title Effects of early postnatal exposure to fine particulate matter on emotional and cognitive development and structural synaptic plasticity in immature and mature rats
title_full Effects of early postnatal exposure to fine particulate matter on emotional and cognitive development and structural synaptic plasticity in immature and mature rats
title_fullStr Effects of early postnatal exposure to fine particulate matter on emotional and cognitive development and structural synaptic plasticity in immature and mature rats
title_full_unstemmed Effects of early postnatal exposure to fine particulate matter on emotional and cognitive development and structural synaptic plasticity in immature and mature rats
title_short Effects of early postnatal exposure to fine particulate matter on emotional and cognitive development and structural synaptic plasticity in immature and mature rats
title_sort effects of early postnatal exposure to fine particulate matter on emotional and cognitive development and structural synaptic plasticity in immature and mature rats
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6908876/
https://www.ncbi.nlm.nih.gov/pubmed/31709780
http://dx.doi.org/10.1002/brb3.1453
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