Maternal sleep deprivation inhibits hippocampal neurogenesis associated with inflammatory response in young offspring rats

Although sleep complaints are very common among pregnant women, the potential adverse effects of sleep disturbance on the offspring are not well studied. Growing evidence suggests that maternal stress can induce an inflammatory environment on the fetal development. But people are not sure about the...

Full description

Bibliographic Details
Main Authors: Qiuying Zhao, Cheng Peng, Xiaohui Wu, Yubo Chen, Cheng Wang, Zili You
Format: Article
Language:English
Published: Elsevier 2014-08-01
Series:Neurobiology of Disease
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0969996114000977
_version_ 1818742097414455296
author Qiuying Zhao
Cheng Peng
Xiaohui Wu
Yubo Chen
Cheng Wang
Zili You
author_facet Qiuying Zhao
Cheng Peng
Xiaohui Wu
Yubo Chen
Cheng Wang
Zili You
author_sort Qiuying Zhao
collection DOAJ
description Although sleep complaints are very common among pregnant women, the potential adverse effects of sleep disturbance on the offspring are not well studied. Growing evidence suggests that maternal stress can induce an inflammatory environment on the fetal development. But people are not sure about the consequences of prenatal stress such as the inflammatory responses induced by maternal sleep deprivation (MSD). In the present study, we investigated the effects of MSD on long-term behavioral and cognitive consequences in offspring and its underlying inflammatory response pathway. The pregnant Wistar rats received prolonged sleep deprivation (72 h) on gestational day (GD) 4, 9, and 18, respectively. The post-natal day (PND) 21 offspring showed impaired hippocampus-dependent spatial learning and memory in the Morris Water Maze task and anhedonia in sucrose preference experiment. Quantification of BrdU+ and DCX+ cells revealed a significant decrease in hippocampus neurogenesis in prepuberty offspring, especially for the late MSD (GD 18) group. Real-time RT-PCR showed that after MSD, the expression of pro-inflammatory cytokines (IL-1β, IL-6 and TNFα) increased in the hippocampus of offspring on PND 1, 7, 14 and 21, whereas anti-inflammatory cytokine IL-10 reduced at the same time. Immunofluorescence found that the cells of activated microglia were higher in the brains of MSD offspring. Taken together, these results suggested that the MSD-induced inflammatory response is an important factor for neurogenesis impairment and neurobehavioral outcomes in prepuberty offspring.
first_indexed 2024-12-18T02:07:06Z
format Article
id doaj.art-b40cfdfa84de4728b1e92f0298ec9407
institution Directory Open Access Journal
issn 1095-953X
language English
last_indexed 2024-12-18T02:07:06Z
publishDate 2014-08-01
publisher Elsevier
record_format Article
series Neurobiology of Disease
spelling doaj.art-b40cfdfa84de4728b1e92f0298ec94072022-12-21T21:24:34ZengElsevierNeurobiology of Disease1095-953X2014-08-01685765Maternal sleep deprivation inhibits hippocampal neurogenesis associated with inflammatory response in young offspring ratsQiuying Zhao0Cheng Peng1Xiaohui Wu2Yubo Chen3Cheng Wang4Zili You5School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 610054, ChinaState Key Laboratory Breeding Base of Systematic Research, Development and Utilization of Chinese Medicine Resources, Pharmacy College, Chengdu University of Traditional Chinese Medicine, Chengdu 610075, ChinaSchool of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 610054, ChinaSchool of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 610054, ChinaSchool of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 610054, ChinaSchool of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 610054, China; Corresponding author. Fax: +86 28 83208838.Although sleep complaints are very common among pregnant women, the potential adverse effects of sleep disturbance on the offspring are not well studied. Growing evidence suggests that maternal stress can induce an inflammatory environment on the fetal development. But people are not sure about the consequences of prenatal stress such as the inflammatory responses induced by maternal sleep deprivation (MSD). In the present study, we investigated the effects of MSD on long-term behavioral and cognitive consequences in offspring and its underlying inflammatory response pathway. The pregnant Wistar rats received prolonged sleep deprivation (72 h) on gestational day (GD) 4, 9, and 18, respectively. The post-natal day (PND) 21 offspring showed impaired hippocampus-dependent spatial learning and memory in the Morris Water Maze task and anhedonia in sucrose preference experiment. Quantification of BrdU+ and DCX+ cells revealed a significant decrease in hippocampus neurogenesis in prepuberty offspring, especially for the late MSD (GD 18) group. Real-time RT-PCR showed that after MSD, the expression of pro-inflammatory cytokines (IL-1β, IL-6 and TNFα) increased in the hippocampus of offspring on PND 1, 7, 14 and 21, whereas anti-inflammatory cytokine IL-10 reduced at the same time. Immunofluorescence found that the cells of activated microglia were higher in the brains of MSD offspring. Taken together, these results suggested that the MSD-induced inflammatory response is an important factor for neurogenesis impairment and neurobehavioral outcomes in prepuberty offspring.http://www.sciencedirect.com/science/article/pii/S0969996114000977Sleep deprivationPregnancyOffspringNeurogenesisMicroglial activationInflammatory response
spellingShingle Qiuying Zhao
Cheng Peng
Xiaohui Wu
Yubo Chen
Cheng Wang
Zili You
Maternal sleep deprivation inhibits hippocampal neurogenesis associated with inflammatory response in young offspring rats
Neurobiology of Disease
Sleep deprivation
Pregnancy
Offspring
Neurogenesis
Microglial activation
Inflammatory response
title Maternal sleep deprivation inhibits hippocampal neurogenesis associated with inflammatory response in young offspring rats
title_full Maternal sleep deprivation inhibits hippocampal neurogenesis associated with inflammatory response in young offspring rats
title_fullStr Maternal sleep deprivation inhibits hippocampal neurogenesis associated with inflammatory response in young offspring rats
title_full_unstemmed Maternal sleep deprivation inhibits hippocampal neurogenesis associated with inflammatory response in young offspring rats
title_short Maternal sleep deprivation inhibits hippocampal neurogenesis associated with inflammatory response in young offspring rats
title_sort maternal sleep deprivation inhibits hippocampal neurogenesis associated with inflammatory response in young offspring rats
topic Sleep deprivation
Pregnancy
Offspring
Neurogenesis
Microglial activation
Inflammatory response
url http://www.sciencedirect.com/science/article/pii/S0969996114000977
work_keys_str_mv AT qiuyingzhao maternalsleepdeprivationinhibitshippocampalneurogenesisassociatedwithinflammatoryresponseinyoungoffspringrats
AT chengpeng maternalsleepdeprivationinhibitshippocampalneurogenesisassociatedwithinflammatoryresponseinyoungoffspringrats
AT xiaohuiwu maternalsleepdeprivationinhibitshippocampalneurogenesisassociatedwithinflammatoryresponseinyoungoffspringrats
AT yubochen maternalsleepdeprivationinhibitshippocampalneurogenesisassociatedwithinflammatoryresponseinyoungoffspringrats
AT chengwang maternalsleepdeprivationinhibitshippocampalneurogenesisassociatedwithinflammatoryresponseinyoungoffspringrats
AT ziliyou maternalsleepdeprivationinhibitshippocampalneurogenesisassociatedwithinflammatoryresponseinyoungoffspringrats