The DOI matches its Crossref record; 37 of the 37 references it cites were found in a registry or an index.
Glucocorticoid exposure during hippocampal neurogenesis primes future stress response by inducing changes in DNA methylation
Open accessAbstract
Significance: Prenatal stress exposure is associated with a wide range of health problems later in life. This may be mediated in part via glucocorticoid (GC) exposure during fetal development known to impact neurogenesis and induce epigenetic changes. Using a human fetal hippocampal progenitor cell line to assess the effects of GCs, we observe that exposure to GCs early during neurogenesis results in lasting changes in DNA methylation (DNAm). Lasting DNAm alterations are associated with significantly enhanced transcriptional response to a subsequent GC exposure. Our data suggest that early exposure to GCs changes the set point of future transcriptional responses to stress by inducing lasting DNAm changes. Such altered set points may relate to differential vulnerability to stress exposure later in life.
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In the citing paper
“Such lasting changes in DNAm result in an altered set-point for transcriptional changes of FKBP5 upon subsequent GR activation. 55 , 69 , 72”
From Epigenetics and depression (2019) · cites this paper as [55]
In the citing paper
“Subsequent post-differentiation exposure to GCs resulted in robust transcriptional changes in the HPCs that were initially treated during proliferation and differentiation, indicating that GC induced DNAm changes are long-lasting and prime the stress response for future exposure.”
From Epigenetics and depression (2019) · cites this paper as [55]
In the citing paper
“Furthermore, the DMRs were enriched for the binding motif of the glucocorticoid receptor (GR), a key modulator of the hypothalamus-pituitary-adrenal (HPA) axis.”
From Epigenetics and depression (2019) · cites this paper as [55]
In the citing paper
“In a model of stress using a human hippocampal progenitor cell line (HPCs), exposure to glucocorticoids (GCs) during differentiation and proliferation induced long-lasting DNAm changes.”
From Epigenetics and depression (2019) · cites this paper as [55]
In the citing paper
“In human models, there is also evidence of environmental factors inducing epigenetic changes. 55”
From Epigenetics and depression (2019) · cites this paper as [55]
In the citing paper
“However, as shown in a human hippocampal progenitor cell line, GR-induced demethylation can become stable when initiated during certain early developmental periods. 55”
From Epigenetics and depression (2019) · cites this paper as [55]
In the citing paper
“The DMRs with GR binding motifs were more commonly demethylated than hypermethylated.”
From Epigenetics and depression (2019) · cites this paper as [55]
Citations
Cites
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Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys
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Impact of Maternal Stress, Depression and Anxiety on Fetal Neurobehavioral Development
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Glucocorticoid-Related Molecular Signaling Pathways Regulating Hippocampal Neurogenesis
Anacker, C., Cattaneo, A., Luoni, A., Musaelyan, K., Zunszain, P. A., Milanesi, E., Rybka, J., Berry, A., Cirulli, F., Thuret, S., et al. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.253 · Cited by 331
Self-citationAnacker, C., Cattaneo, A., Musaelyan, K., Zunszain, P. A., Horowitz, M., Molteni, R., Luoni, A., Calabrese, F., Tansey, K., Gennarelli, M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300886110 · Cited by 319
Self-citation
Research works printed but not linked: 1
- N. Provencal . Glucocorticoid exposure during hippocampal neurogenesis primes future stress response by inducing long-lasting changes in DNA methylation. Gene Expression Omnibus. https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE119847. Deposited 12 September 2018.
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Mikulska, J., Juszczyk, G., Gawrońska-Grzywacz, M., & Herbet, M. (2021) · Brain Sciences · doi:10.3390/brainsci11101298 · Cited by 450
Biological embedding of experience: a primer on epigenetics
Aristizabal, M. J., Anreiter, I., Halldorsdottir, T., Odgers, C. L., McDade, T. W., Goldenberg, A., Mostafavi, S., Kobor, M. S., Binder, E. B., Sokolowski, M. B., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820838116 · Cited by 268
Self-citationPenner-Goeke, S., & Binder, E. B. (2019) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2019.21.4/ebinder · Cited by 254
Self-citationEarly life adversity shapes neural circuit function during sensitive postnatal developmental periods
Malave, L., van Dijk, M. T., & Anacker, C. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02092-9 · Cited by 177
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Metadata
- Authors
- Provençal, N., Arloth, J., Cattaneo, A., Anacker, C., Cattane, N., Wiechmann, T., Röh, S., Ködel, M., Klengel, T., Czamara, D., Müller, N. S., Lahti, J., PREDO team, Räikkönen, K., Pariante, C. M., Binder, E. B., Kajantie, E., Hämäläinen, E., Villa, P., & Laivuori, H.
- Affiliations
- Simon Fraser University (CA)
- Helmholtz Munich (DE)
- King's College London (GB)
- Research Foundation For Mental Hygiene (US)
- Centro San Giovanni di Dio Fatebenefratelli (IT)
- Max Planck Institute of Psychiatry (DE)
- Harvard University (US)
- University of Helsinki (FI)
- Emory University (US)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2019-08-09
- Volume
- 117
- Issue
- 38
- Pages
- 23280-23285
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC7519233
- OpenAlex
- W2968811349
- Cited by
- 209
- References
- 37
- Citations by year
- 2026: 16 · 2025: 22 · 2024: 32 · 2023: 34 · 2022: 28 · 2021: 46 · 2020: 24 · 2019: 7
- FWCI
- 10.17
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
- Työväentutkimus Vuosikirja (submittedVersion)
- Site cant be reached (submittedVersion, other-oa)
- GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
- Funders
- National Institute for Health and Care Research (NIHR201376, NF-SI-0616-10074)
- Canadian Institutes of Health Research
- Medical Research Council (MR/N029488/1)
- National Institute of Mental Health (K99MH108719, R00MH108719)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R21HD088931)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- glucocorticoids, prenatal stress, hippocampal neurogenesis, DNA methylation, epigenetics, hippocampal progenitor cells, stress response, differentially methylated sites, umbilical cord blood, mental illness, fetal brain development
- MeSH terms
- Female, Gene Expression Regulation, Glucocorticoids, Hippocampus, Humans, Male, Pregnancy, Prenatal Exposure Delayed Effects, Stress, Physiological, Cohort Studies, DNA Methylation, Neurogenesis
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