A single 24 h maternal separation at PND 9 promotes behavioral resilience of female C57BL/6J mice and the possible role of hippocampal Homer1a
Early life stress (ELS) has been thought to increase vulnerability to developing psychiatric disorders later in life, while some researchers have found that adversity early in life may promote stress resilience. Studies investigating the resilient effect of maternal separation (MS) are still relativ...
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2024-03-01
|
Series: | Heliyon |
Subjects: | |
Online Access: | http://www.sciencedirect.com/science/article/pii/S2405844024030688 |
_version_ | 1797259756202622976 |
---|---|
author | Yelu Hao Yujie Niu Fei Shi Lei Zhang Cheng Peng Zhiqiang Yan Xiaoyan Chen Hongyu Xu |
author_facet | Yelu Hao Yujie Niu Fei Shi Lei Zhang Cheng Peng Zhiqiang Yan Xiaoyan Chen Hongyu Xu |
author_sort | Yelu Hao |
collection | DOAJ |
description | Early life stress (ELS) has been thought to increase vulnerability to developing psychiatric disorders later in life, while some researchers have found that adversity early in life may promote stress resilience. Studies investigating the resilient effect of maternal separation (MS) are still relatively few, and the underlying mechanisms remain unknown. In the current study, the effect of a single 24 h MS paradigm at postnatal day 9 (PND 9) in female C57BL/6J mice was investigated by assessing behavioral performance in middle adolescence. We demonstrated that, mice in MS group displayed decreased anxiety-like behavior and increased exploratory behavior than controls in the open field test and elevated plus maze test. Furthermore, MS mice exhibited improved hippocampal-dependent spatial learning in the Morris water maze test. This performance indicated behavioral resilience to early life stress. The protein expression levels of Homer1 isoforms, which are implicated in a variety of neuropsychiatric disorders, were evaluated using Western blot analysis. A significant increase in hippocampal Homer1a protein expression was observed immediately after MS, which subsequently decreased until adolescence (PND 27–42), when a significant increase was observed again. This distinctive change of hippocampal Homer1a protein expression pattern indicated that hippocampal Homer1a might play a role in behavioral resilience to MS in female C57BL/6J mice. In conclusion, this study demonstrated that exposure to a single 24 h MS at PND 9 promoted behavioral resilience of female C57BL/6J mice in middle adolescence. This behavioral resilience might be related to increased expression of hippocampal Homer1a. |
first_indexed | 2024-03-07T18:35:51Z |
format | Article |
id | doaj.art-0662143a2ea444ce8645d46bd2736dc3 |
institution | Directory Open Access Journal |
issn | 2405-8440 |
language | English |
last_indexed | 2024-04-24T23:14:29Z |
publishDate | 2024-03-01 |
publisher | Elsevier |
record_format | Article |
series | Heliyon |
spelling | doaj.art-0662143a2ea444ce8645d46bd2736dc32024-03-17T07:57:09ZengElsevierHeliyon2405-84402024-03-01105e27037A single 24 h maternal separation at PND 9 promotes behavioral resilience of female C57BL/6J mice and the possible role of hippocampal Homer1aYelu Hao0Yujie Niu1Fei Shi2Lei Zhang3Cheng Peng4Zhiqiang Yan5Xiaoyan Chen6Hongyu Xu7Department of Neurosurgery, Xijing Hospital, Fourth Military Medical University, Xi'an, Shaanxi, China; Department of Neurosurgery, The 940 Hospital of PLA Joint Logistic Support Force, Lanzhou, Gansu, ChinaDepartment of Hematology, The First Affiliated Hospital of Lanzhou University, Lanzhou, Gansu, ChinaThe Key Laboratory of Aerospace Medicine, Ministry of Education, Fourth Military Medical University, Xi'an, Shaanxi, ChinaDepartment of Neurosurgery, Xijing Hospital, Fourth Military Medical University, Xi'an, Shaanxi, ChinaDepartment of Neurosurgery, The 984 Hospital of PLA Joint Logistic Support Force, Beijing, ChinaDepartment of Neurosurgery, Xijing Hospital, Fourth Military Medical University, Xi'an, Shaanxi, ChinaDepartment of Neurosurgery, Xijing Hospital, Fourth Military Medical University, Xi'an, Shaanxi, ChinaCollege of Science and Technology, Wenzhou-Kean University, Wenzhou, Zhejiang, China; Wenzhou Municipal Key Lab of Applied Biomedical and Biopharmaceutical Informatics, Wenzhou-Kean University, Wenzhou, Zhejiang, China; Zhejiang Bioinformatics International Science and Technology Cooperation Center, Wenzhou-Kean University, Wenzhou, Zhejiang, China; Dorothy and George Hennings College of Science, Mathematics and Technology, Kean University, 1000 Morris Ave, Union, NJ, 07083, USA; Corresponding author. College of Science and Technology, Wenzhou-Kean University, Wenzhou, Zhejiang, China.Early life stress (ELS) has been thought to increase vulnerability to developing psychiatric disorders later in life, while some researchers have found that adversity early in life may promote stress resilience. Studies investigating the resilient effect of maternal separation (MS) are still relatively few, and the underlying mechanisms remain unknown. In the current study, the effect of a single 24 h MS paradigm at postnatal day 9 (PND 9) in female C57BL/6J mice was investigated by assessing behavioral performance in middle adolescence. We demonstrated that, mice in MS group displayed decreased anxiety-like behavior and increased exploratory behavior than controls in the open field test and elevated plus maze test. Furthermore, MS mice exhibited improved hippocampal-dependent spatial learning in the Morris water maze test. This performance indicated behavioral resilience to early life stress. The protein expression levels of Homer1 isoforms, which are implicated in a variety of neuropsychiatric disorders, were evaluated using Western blot analysis. A significant increase in hippocampal Homer1a protein expression was observed immediately after MS, which subsequently decreased until adolescence (PND 27–42), when a significant increase was observed again. This distinctive change of hippocampal Homer1a protein expression pattern indicated that hippocampal Homer1a might play a role in behavioral resilience to MS in female C57BL/6J mice. In conclusion, this study demonstrated that exposure to a single 24 h MS at PND 9 promoted behavioral resilience of female C57BL/6J mice in middle adolescence. This behavioral resilience might be related to increased expression of hippocampal Homer1a.http://www.sciencedirect.com/science/article/pii/S2405844024030688Early life stress (ELS)Maternal separation (MS)Behavioral resilienceHippocampusHomer1a |
spellingShingle | Yelu Hao Yujie Niu Fei Shi Lei Zhang Cheng Peng Zhiqiang Yan Xiaoyan Chen Hongyu Xu A single 24 h maternal separation at PND 9 promotes behavioral resilience of female C57BL/6J mice and the possible role of hippocampal Homer1a Heliyon Early life stress (ELS) Maternal separation (MS) Behavioral resilience Hippocampus Homer1a |
title | A single 24 h maternal separation at PND 9 promotes behavioral resilience of female C57BL/6J mice and the possible role of hippocampal Homer1a |
title_full | A single 24 h maternal separation at PND 9 promotes behavioral resilience of female C57BL/6J mice and the possible role of hippocampal Homer1a |
title_fullStr | A single 24 h maternal separation at PND 9 promotes behavioral resilience of female C57BL/6J mice and the possible role of hippocampal Homer1a |
title_full_unstemmed | A single 24 h maternal separation at PND 9 promotes behavioral resilience of female C57BL/6J mice and the possible role of hippocampal Homer1a |
title_short | A single 24 h maternal separation at PND 9 promotes behavioral resilience of female C57BL/6J mice and the possible role of hippocampal Homer1a |
title_sort | single 24 h maternal separation at pnd 9 promotes behavioral resilience of female c57bl 6j mice and the possible role of hippocampal homer1a |
topic | Early life stress (ELS) Maternal separation (MS) Behavioral resilience Hippocampus Homer1a |
url | http://www.sciencedirect.com/science/article/pii/S2405844024030688 |
work_keys_str_mv | AT yeluhao asingle24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT yujieniu asingle24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT feishi asingle24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT leizhang asingle24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT chengpeng asingle24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT zhiqiangyan asingle24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT xiaoyanchen asingle24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT hongyuxu asingle24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT yeluhao single24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT yujieniu single24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT feishi single24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT leizhang single24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT chengpeng single24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT zhiqiangyan single24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT xiaoyanchen single24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a AT hongyuxu single24hmaternalseparationatpnd9promotesbehavioralresilienceoffemalec57bl6jmiceandthepossibleroleofhippocampalhomer1a |