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Epigenetic Transmission of the Impact of Early Stress Across Generations
Open accessAbstract
Background Traumatic experiences in early life are risk factors for the development of behavioral and emotional disorders. Such disorders can persist through adulthood and have often been reported to be transmitted across generations.Methods To investigate the transgenerational effect of early stress, mice were exposed to chronic and unpredictable maternal separation from postnatal day 1 to 14.Results We show that chronic and unpredictable maternal separation induces depressive-like behaviors and alters the behavioral response to aversive environments in the separated animals when adult. Most of the behavioral alterations are further expressed by the offspring of males subjected to maternal separation, despite the fact that these males are reared normally. Chronic and unpredictable maternal separation also alters the profile of DNA methylation in the promoter of several candidate genes in the germline of the separated males. Comparable changes in DNA methylation are also present in the brain of the offspring and are associated with altered gene expression.Conclusions These findings highlight the negative impact of early stress on behavioral responses across generations and on the regulation of DNA methylation in the germline.
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“Multigenerational early-life stress models demonstrate enduring regulatory and behavioral variation, including depressive-like behaviors and altered responses to environmental novelty (64).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [64]
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“These findings include epigenetic modulation of genes involved in synaptic and stress signaling, including Mecp2, CB1, and CRFR2, with methylation differences observed in both germline and neural tissues (64).”
From Epigenetic changes associated with multi-generational trauma: characterization, mechanisms, and therapeutics (2026) · cites this paper as [64]
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“Enduring behavioral responses to stress and epigenetic alterations in adult offspring have been demonstrated to be mediated by changes in gametes (10)(11)(12)(13), in utero effects (14), variations in early postnatal care (15,16), and/or other early life experiences (17) that are influenced by parental exposure (18).”
From Holocaust Exposure Induced Intergenerational Effects on FKBP5 Methylation (2016) · cites this paper as [12]
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“Epigenetic effects in maternal or paternal gametes are a potential explanation for epigenetic effects in offspring (10-13), but blood samples will not permit ascertainment of gamete-dependent transmission.”
From Holocaust Exposure Induced Intergenerational Effects on FKBP5 Methylation (2016) · cites this paper as [12]
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“early-life postnatal adversity in animal models can persistently affect behavior across generations and DNA methylation in the germline.”
From Gene × Environment Interactions in Autism Spectrum Disorders: Role of Epigenetic Mechanisms (2014) · cites this paper as [163]
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Lyons, E. R., Wells, J. N., Scholtes, C. M., Mintz, B., Giuliano, R. J., & Skowron, E. A. (2018) · Developmental Psychobiology · doi:10.1002/dev.21815 · Cited by 8
Rachwani, J., Hoch, J. E., & Adolph, K. E. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.017 · Cited by 9
The impact of maternal neglect on genetic hyperactivity
Majdak, P., Grogan, E. L., Gogola, J. V., Sorokina, A., Tse, S., & Rhodes, J. S. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.07.033 · Cited by 8
State of the Science: Using Telomeres as Biomarkers During the First 1,000 Days of Life
Oerther, S. E., & Lorenz, R. A. (2018) · Western Journal of Nursing Research · doi:10.1177/0193945918762806 · Cited by 8
“Researchers have also found differences in memory and synaptic functioning in human infants who were maternal deprived (Chen et al., 2012; Franklin et al., 2010).”
BackgroundInfant Object Manipulation and Play
Tamis‐LeMonda, C. S., & Lockman, J. J. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.019 · Cited by 8
Rahia Mashoodh, A., Sarkies, P., Westoby, J., & Kilner, R. M. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.03.25.436923 · Cited by 8
Wu, Y., Zhu, Y., Zheng, S., & Mingxing, D. (2025) · Future Science OA · doi:10.1080/20565623.2025.2463852 · Cited by 9
“…life, to deal with environmental stress, epigenetic mechanisms are activated to regulate the expression and function of certain important genes [33,34]. of these epigenetic factors, sirtuins family (Sirts, nad + -dependent deacylases), the class iii histone deacetylases, has aroused interest…”
Epigenetic Effect of Environmental Factors on Neurodevelopmenal Disorders
Kubota, T. (2016) · Nippon Eiseigaku Zasshi (Japanese Journal of Hygiene) · doi:10.1265/jjh.71.200 · Cited by 7
Kretschmer, M., Fischer, V., & Gapp, K. (2023) · Biomolecules · doi:10.3390/biom13121750 · Cited by 7
“For instance, studies using the MSUS model reported changes in methylation levels at the promoters of several candidate genes in the sperm of the F0 generation (three up-regulated, two down-regulated, and two unaltered) [58,60,82].”
BackgroundInfluentialHypothesis: epigenetic effects will require a review of the genetics of child development
Kosztolányi, G. (2011) · Journal of Community Genetics · doi:10.1007/s12687-011-0044-2 · Cited by 7
“Recent research discovered that male mice made depressed by early stress and lack of maternal care appeared to pass this behavior and anxiety on to their offspring, suggesting that the impact of stress may be passed on from one generation to the next, presumably through epigenetic marks on sperm cells (Franklin et al.…”
Transgenerational Epigenetic Inheritance
Jablonka, E., & Lamb, M. J. (2010) · The MIT Press eBooks · doi:10.7551/mitpress/8278.003.0012 · Cited by 101
L’épigénétique comme partenaire de la psychiatrie : vers une approche personnalisée du patient
Kular, S., & Kular, L. (2018) · L Évolution Psychiatrique · doi:10.1016/j.evopsy.2018.05.003 · Cited by 7
Dairy cows – an opportunity in the research field of non-genetic inheritance?
Engmann, O. (2018) · Current Zoology · doi:10.1093/eep/dvy014 · Cited by 7
Strachan, E. D., Zhao, J., Roy‐Byrne, P., Fowler, E., & Bacus, T. J. (2018) · Twin Research and Human Genetics · doi:10.1017/thg.2018.64 · Cited by 7
“The questionnaire packet also included measures of lifetime exposure to stressful events that may influence epigenetic variations leading to disease (Franklin et al., 2010; Waterland, 2009).”
BackgroundThe (not so) Controversial Role of DNA Methylation in Epigenetic Inheritance Across Generations
Irmler, M., Kaspar, D., de Angelis, M. H., & Beckers, J. (2020) · Springer eBooks · doi:10.1007/978-3-030-35213-4_10 · Cited by 7
Involvement of early embryonic miR‐409‐3p in the establishment of anxiety levels in female mice
Dickson, D. A., Stohn, J. P., Saavedra-Rodríguez, L., Hernández, A., Harrington, A. N., Liaw, L., & Feig, L. A. (2020) · Developmental Neurobiology · doi:10.1002/dneu.22756 · Cited by 7
“…defeat (Dietz et al., 2011), chronic physical restraint (He et al., 2016), multiple variable stressors (Rodgers, Morgan, Bronson, Revello, & Bale, 2013) early maternal separation (Franklin et al., 2010), and chronic social instability (CSI)(Dickson et al., 2018; Saavedra-Rodriguez & Feig, 2013).”
BackgroundHossin, M. Z., Falkstedt, D., Allebeck, P., Mishra, G. D., & Koupil, I. (2021) · Social Science & Medicine · doi:10.1016/j.socscimed.2021.113811 · Cited by 8
Manoni, G., Puzzo, C., Gigantesco, A., & Adriani, W. (2022) · Brain Sciences · doi:10.3390/brainsci12040469 · Cited by 7
Kumar, J. A., Balaji, T., Sekaran, S. P. C., Patil, S. A., Poojari, M., & Subramanian, M. (2022) · Morphologie · doi:10.1016/j.morpho.2022.05.001 · Cited by 7
Bolhuis, K., Steenkamp, L. R., Tiemeier, H. W., Blanken, L. M. E., Pingault, J., Cecil, C. A. M., & Marroun, H. E. (2022) · Schizophrenia Bulletin · doi:10.1093/schbul/sbac195 · Cited by 9
“Six items were used to evaluate 6 different types of delusional experiences: (1) Have other people ever read your thoughts? (2) Have you ever believed that you were being sent special messages through television or radio? (3) Have you ever thought you were being followed or spied on? (4) Have you ever felt as though y…”
MethodPrefrontal cortical dopamine from an evolutionary perspective
Lee, Y., & Goto, Y. (2015) · Neuroscience Bulletin · doi:10.1007/s12264-014-1499-z · Cited by 8
Metadata
- Authors
- Franklin, T. B., Russig, H., Weiss, I. C., Gräff, J., Linder, N., Michalon, A., Vizi, S., & Mansuy, I. M.
- Affiliations
- University of Zurich (CH)
- Massachusetts Institute of Technology (US)
- F. Hoffmann-La Roche AG (CH)
- Corresponding author
- Mansuy, Isabelle M.
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2010-09
- Volume
- 68
- Issue
- 5
- Pages
- 408-415
- ISSN
- 0006-3223 (ISSN-L)
- OpenAlex
- W2035616108
- Cited by
- 1,125
- References
- 68
- Citations by year
- 2026: 35 · 2025: 43 · 2024: 39 · 2023: 63 · 2022: 48 · 2021: 63 · 2020: 115 · 2019: 75 · 2018: 96 · 2017: 79 · 2016: 89 · 2015: 88 · 2014: 95 · 2013: 82 · 2012: 66
- FWCI
- 25.65
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Funders
- University of Zürich
- Swiss Federal Institute of Technology
- Swiss National Science Foundation
- National Center for Competence in Research “Neural Plasticity and Repair,”
- Human Frontier Science Program
- Borderline Personality Disorder Research Foundation
- Roche
- European Molecular Biology Organization Young Investigator Program
- Novartis Research Foundation
- 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 › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Keywords
- transgenerational transmission, early life stress, maternal separation, chronic unpredictable mild stress, depression-like behavior, DNA methylation, offspring behavior, gene expression
- MeSH terms
- Age Factors, Animals, Behavior, Animal, Mental Disorders, Brain, Female, Humans, Male, Maternal Deprivation, Sex Factors, Stress, Psychological, Gene Expression, DNA Methylation, Models, Animal, Epigenesis, Genetic, Mice
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