Programming changes of hippocampal miR-134-5p/SOX2 signal mediate the susceptibility to depression in prenatal dexamethasone-exposed female offspring
Abstract
Depression is a neuropsychiatric disorder and has intrauterine developmental origins. This study aimed to confirm the depression susceptibility in offspring rats induced by prenatal dexamethasone exposure (PDE) and to further explore the intrauterine programming mechanism. Wistar rats were injected with dexamethasone (0.2 mg/kg·d) subcutaneously during the gestational days 9-20 and part of the offspring was given chronic stress at postnatal weeks 10-12. Behavioral results showed that the adult PDE female offspring was susceptible to depression, accompanied by increased hippocampal miR-134-5p expression and decreased sex-determining region Y-box 2 (SOX2) expression, as well as disorders of neural progenitor cells proliferation and hippocampal neurogenesis. The PDE female fetal rats presented consistent changes with the adult offspring, accompanied by the upregulation of glucocorticoid receptor (GR) expression and decreased sirtuin 1 (SIRT1) expression. We further found that the H3K9ac level of the miR-134-5p promoter was significantly increased in the PDE fetal hippocampus, as well as in adult offspring before and after chronic stress. In vitro, the changes of GR/SIRT1/miR-134-5p/SOX2 signal by dexamethasone were consistent with in vivo experiments, which could be reversed by GR receptor antagonist, SIRT1 agonist, and miR-134-5p inhibitor. This study confirmed that PDE led to an increased expression level as well as H3K9ac level of miR-134-5p by activating the GR/SIRT1 pathway in the fetal hippocampus and then inhibited the SOX2 expression. The programming effect mediated by the abnormal epigenetic modification could last from intrauterine to adulthood, which constitutes the intrauterine programming mechanism leading to hippocampal neurogenesis disorders and depression susceptibility in female offspring. Intrauterine programming mechanism for the increased depressive susceptibility in adult female offspring by prenatal dexamethasone exposure (PDE). GR, glucocorticoid receptor; SIRT1, sirtuin 1; SOX2, sex-determining region Y-box 2; NPCs, neuroprogenitor cells; H3K9ac, histone 3 lysine 9 acetylation; GRE, glucocorticoid response element.
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miR-335, miR-1202, miR-29b-3p, and miR-134-5p may regulate depression through inhibiting GRM4 expression, affecting Ca2+ influx into prefrontal cortex neurons and extracellular glutamate concentration.
“MiR-335, miR-1202, miR-29b-3p, and miR-134-5p may regulate depression through inhibiting the expression of GRM4 gene (Fig. 5), that in turn affect the influx of Ca2+ into the prefrontal cortex neurons and the extracellular concentration of glutamate.277–283”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [283]
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Wang, Y., Huang, Y., Luo, X., Lai, X., Yu, L., Zhao, Z., Zhang, A., Li, H., Huang, G., Li, Y., et al. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4879423
Prenatal Adverse Environment and Susceptibility to Fetal-Originated Disease
Tan, Y., & Chen, Y. (2024) · Springer eBooks · doi:10.1007/978-981-97-5730-5_1
Targets for Early Warning and Drug Intervention for Fetal-Originated Disease
Wang, H., Lu, X., & Peng, Y. (2024) · Springer eBooks · doi:10.1007/978-981-97-5730-5_22
Self-citationDevelopmental Toxicity of Dexamethasone and Related Fetal-Originated Disease
Xiao, H., & Liu, Y. (2024) · Springer eBooks · doi:10.1007/978-981-97-5730-5_10
Prednisone Exposure During Pregnancy Increases Susceptibility to Epilepsy in Adult Offspring Mice
Cheng, X.-L., Zeng, M., Wang, T.-T., Zhang, S., Luo, M., Zhou, X.-L., Wei, L.-Y., Wang, H., Xu, D., & Peng, B. (2026) · Neurochemical Research · doi:10.1007/s11064-026-04869-6
Self-citation
- Authors
- Jiang, T., Hu, S., Dai, S., Yi, Y., Wang, T., Li, X., Luo, M., Li, K., Chen, L., Wang, H., & Xu, D.
- Affiliations
- Wuhan University (CN)
- Zhongnan Hospital of Wuhan University (CN)
- Corresponding author
- Xu, Dan
- Venue
- Cell Biology and Toxicology
- Published
- 2021-02-22
- Volume
- 38
- Issue
- 1
- Pages
- 69-86
- ISSN
- 0742-2091 (ISSN-L)
- 1573-6822
- OpenAlex
- W3133091759
- Cited by
- 33
- References
- 72
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 9 · 2023: 10 · 2022: 3 · 2021: 7
- FWCI
- 4.64
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cell Biology and Toxicology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Health and Family Planning Commission of Hubei Province (WJ2019Q038)
- National Natural Science Foundation of China (81973405, 81671472, 81673524)
- Medical Science Advancement Program (Basic Medical Sciences) of Wuhan University (TFJC2018001)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Keywords
- depression vulnerability, prenatal dexamethasone exposure, intrauterine programming, glucocorticoid receptor, SIRT1, miR-134-5p, SOX2, hippocampal neurogenesis, neural progenitor cells, chronic stress, epigenetic modifications, H3K9ac, female offspring, developmental origins of health and disease, glucocorticoid response
- MeSH terms
- Adult, Animals, Depression, Dexamethasone, Female, Hippocampus, Humans, Pregnancy, Prenatal Exposure Delayed Effects, Receptors, Glucocorticoid, Rats, Wistar, MicroRNAs, Rats, SOXB1 Transcription Factors, Sirtuin 1
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