Long-Term Effects of Adverse Maternal Care on Hypothalamic-Pituitary-Adrenal (HPA) Axis Function of Juvenile and Adolescent Macaques.

IF 3.6 3区 生物学 Q1 BIOLOGY Biology-Basel Pub Date : 2025-02-15 DOI:10.3390/biology14020204
Kai McCormack, Sara Bramlett, Elyse L Morin, Erin R Siebert, Dora Guzman, Brittany Howell, Mar M Sanchez
{"title":"Long-Term Effects of Adverse Maternal Care on Hypothalamic-Pituitary-Adrenal (HPA) Axis Function of Juvenile and Adolescent Macaques.","authors":"Kai McCormack, Sara Bramlett, Elyse L Morin, Erin R Siebert, Dora Guzman, Brittany Howell, Mar M Sanchez","doi":"10.3390/biology14020204","DOIUrl":null,"url":null,"abstract":"<p><p>Early life adversity (ELA) is a known risk factor for psychopathology, including stress-related anxiety and depressive disorders. The underlying mechanisms and developmental changes remain poorly understood. A likely underpinning is the impact of ELA on the development of stress response systems, including the hypothalamic-pituitary-adrenal (HPA) axis. Our group studied a translational ELA model of spontaneous infant maltreatment by the mother in rhesus macaques, where we used a cross-fostering design to randomly assign infant macaques to either Control or Maltreating (MALT) foster mothers at birth to examine the impact of adverse caregiving on the development of the HPA axis, while controlling for the confounding effects of heritable and prenatal factors. We previously reported higher levels of plasma and hair cortisol (CORT) across the first 6 postnatal months (equivalent to the first 2 years of life in humans) in the MALT than in the Control infants. Here, we followed the same cohort of infants longitudinally to assess the long-term developmental impact of this adverse experience on HPA axis function during the juvenile (12, 18 months) and late adolescent (~5 years) periods. For this, we collected measurements of diurnal CORT rhythm and glucocorticoid negative feedback using the dexamethasone suppression test (DST). At 12 months, we found higher diurnal CORT secretion in MALT females compared to Control females, and impaired negative feedback in response to the DST in both sexes in the MALT group. However, ELA group differences in the HPA axis function disappeared by 18 months and late adolescence, while sex differences in diurnal CORT rhythm emerged or became stronger. These results suggest that infant maltreatment causes dysregulation of the HPA axis during the first year of life, with HPA axis function normalizing later, during the pre-pubertal juvenile period and adolescence. This suggests that the impact of maltreatment on HPA axis function may be transient, at least if the adverse experience stops. Our findings are consistent with human evidence of recalibration/normalization of HPA axis function during adolescence in children that switch from adverse/deprived environments to supportive adoptive families. This research has broad implications regarding the biological processes that translate ELA to psychopathology during development and the pathways to resiliency.</p>","PeriodicalId":48624,"journal":{"name":"Biology-Basel","volume":"14 2","pages":""},"PeriodicalIF":3.6000,"publicationDate":"2025-02-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11851656/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Biology-Basel","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.3390/biology14020204","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Early life adversity (ELA) is a known risk factor for psychopathology, including stress-related anxiety and depressive disorders. The underlying mechanisms and developmental changes remain poorly understood. A likely underpinning is the impact of ELA on the development of stress response systems, including the hypothalamic-pituitary-adrenal (HPA) axis. Our group studied a translational ELA model of spontaneous infant maltreatment by the mother in rhesus macaques, where we used a cross-fostering design to randomly assign infant macaques to either Control or Maltreating (MALT) foster mothers at birth to examine the impact of adverse caregiving on the development of the HPA axis, while controlling for the confounding effects of heritable and prenatal factors. We previously reported higher levels of plasma and hair cortisol (CORT) across the first 6 postnatal months (equivalent to the first 2 years of life in humans) in the MALT than in the Control infants. Here, we followed the same cohort of infants longitudinally to assess the long-term developmental impact of this adverse experience on HPA axis function during the juvenile (12, 18 months) and late adolescent (~5 years) periods. For this, we collected measurements of diurnal CORT rhythm and glucocorticoid negative feedback using the dexamethasone suppression test (DST). At 12 months, we found higher diurnal CORT secretion in MALT females compared to Control females, and impaired negative feedback in response to the DST in both sexes in the MALT group. However, ELA group differences in the HPA axis function disappeared by 18 months and late adolescence, while sex differences in diurnal CORT rhythm emerged or became stronger. These results suggest that infant maltreatment causes dysregulation of the HPA axis during the first year of life, with HPA axis function normalizing later, during the pre-pubertal juvenile period and adolescence. This suggests that the impact of maltreatment on HPA axis function may be transient, at least if the adverse experience stops. Our findings are consistent with human evidence of recalibration/normalization of HPA axis function during adolescence in children that switch from adverse/deprived environments to supportive adoptive families. This research has broad implications regarding the biological processes that translate ELA to psychopathology during development and the pathways to resiliency.

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
求助全文
约1分钟内获得全文 去求助
来源期刊
Biology-Basel
Biology-Basel Biological Science-Biological Science
CiteScore
5.70
自引率
4.80%
发文量
1618
审稿时长
11 weeks
期刊介绍: Biology (ISSN 2079-7737) is an international, peer-reviewed, quick-refereeing open access journal of Biological Science published by MDPI online. It publishes reviews, research papers and communications in all areas of biology and at the interface of related disciplines. Our aim is to encourage scientists to publish their experimental and theoretical results in as much detail as possible. There is no restriction on the length of the papers. The full experimental details must be provided so that the results can be reproduced. Electronic files regarding the full details of the experimental procedure, if unable to be published in a normal way, can be deposited as supplementary material.
期刊最新文献
The Role of tRNA-Derived Small RNAs (tsRNAs) in Regulating Cell Death of Cardiovascular Diseases. Effect of Fertilization on the Performance of Adult Pinus pinea Trees. Long-Term Engraftment of Cryopreserved Human Neurons for In Vivo Disease Modeling in Neurodegenerative Disease. CNPY2 in Solid Tumors: Mechanisms, Biomarker Potential, and Therapeutic Implications. Characterization of Exosome-like Nanoparticles from Saffron Tepals and Their Immunostimulatory Activity.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 联系我们:info@booksci.cn
Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。
Copyright © 2023 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1