The DOI matches its Crossref record; 68 of the 68 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The cited source says what the claim attributes to it.
In the citing paper
“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]
The cited source says what the claim attributes to it.
In the citing paper
“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]
The cited source says what the claim attributes to it.
In the citing paper
“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]
The cited source says what the claim attributes to it.
In the citing paper
“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]
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177
Common polygenic variation contributes to risk of schizophrenia and bipolar disorder
The International Schizophrenia Consortium (2009) · Nature · doi:10.1038/nature08185 · Cited by 4,821
Depression: a new animal model sensitive to antidepressant treatments
PORSOLT, R. D., LE PICHON, M., & JALFRE, M. (1977) · Nature · doi:10.1038/266730a0 · Cited by 4,451
CpG Islands in vertebrate genomes
Gardiner‐Garden, M., & Frommer, M. (1987) · Journal of Molecular Biology · doi:10.1016/0022-2836(87)90689-9 · Cited by 3,417
DNA methylation and human disease
Robertson, K. D. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1655 · Cited by 2,864
Epigenetic Transgenerational Actions of Endocrine Disruptors and Male Fertility
Anway, M. D., Cupp, A. S., Uzumcu, M., & Skinner, M. K. (2005) · Science · doi:10.1126/science.1108190 · Cited by 2,563
Genomic DNA methylation: the mark and its mediators.
Klose, R. J., & Bird, A. P. (2006) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2005.12.008 · Cited by 2,501
Environmental epigenomics and disease susceptibility
Jirtle, R. L., & Skinner, M. K. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2045 · Cited by 2,492
Weber, M., Hellmann, I., Stadler, M. B., Ramos, L., Pääbo, S., Rebhan, M., & Schübeler, D. (2007) · Nature Genetics · doi:10.1038/ng1990 · Cited by 2,297
The link between childhood trauma and depression: insights from HPA axis studies in humans
Heim, C., Newport, D. J., Mletzko, T., Miller, A. H., & Nemeroff, C. B. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.03.008 · Cited by 1,704
Research works printed but not linked: 1
- Weaver, 2004, Epigenetic programming by maternal behavior, Nat Neurosci, 7, 847, 10.1038/nn1276 · DOI · Paper page
Cited by
Sorted by citations
Items 801–900 of 999
Dimeji, I. Y., Sanni, M. O., Abass, K. S., Samson, A. O., & Harrath, A. H. (2026) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2026.1791177 · Cited by 3
Lalrinawma, T. S. K., Sangma, J. T., Renthlei, Z., & Trivedi, A. K. (2024) · Molecular Biology Reports · doi:10.1007/s11033-024-09224-y · Cited by 3
“It has been reported that the transmission of stress affected behavior across generations and that some traits, although not exhibited by the parents, can be expressed in the next generation, suggesting that mice can be silent carriers of specific behavioral alterations [68].”
El‐Kadi, R. A., Sedeek, M. S., Abdelkader, N. F., Zaki, H. F., & Kamel, A. S. E. D. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-04911-8 · Cited by 4
Clinical Aspects of Transgenerational Epigenetics
Versmissen, J., van Lennep, J. E. R., & Sijbrands, E. J. G. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405944-3.00025-8 · Cited by 3
The Biosocial Bases of Aggressivity and Aggressive Behavior
Львович, М. А. (2018) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-018-0558-8 · Cited by 3
“…et al., 2010], the corticotropin-releasing hormone (Crh) [Elliott et al., 2010], and the type 2 corticotropin-releasing hormone receptor (Crhr2) [Franklin et al., 2010] genes, and, fi nally, the glutamate decarboxylase 1 (Gad 1) [Zhang et al., 2010] and the olfactory receptor 151 (Olfr151)…”
InfluentialZammatteo, N., & Botman, M. (2018) · European Journal of Trauma & Dissociation · doi:10.1016/j.ejtd.2018.06.003 · Cited by 3
Developmental Programming During Psychological Stress in Pregnancy: A Neurobiological Perspective
Aboustate, N., & Baune, B. T. (2020) · Progress in inflammation research · doi:10.1007/978-3-030-39335-9_2 · Cited by 3
Jayaraman, S., & Smith, L. B. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.020 · Cited by 2
The potential role of stress and sex steroids in heritable effects of sevoflurane
Martynyuk, A. E., Ju, L.-S., & Morey, T. E. (2021) · Biology of Reproduction · doi:10.1093/biolre/ioab129 · Cited by 3
Traumatic progression: psychoanalytic and neuroscientific dimensions
Miller, C. W. T. (2021) · The Scandinavian Psychoanalytic Review · doi:10.1080/01062301.2022.2030084 · Cited by 3
“genes controlling stress hormone release (Franklin et al., 2010).”
BackgroundMaurer, D. M. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.006 · Cited by 3
de Lisenko, N. R., Gray, H. L., & Bohn, J. (2022) · Maternal and Child Health Journal · doi:10.1007/s10995-022-03503-5 · Cited by 4
“, 2017), transgenerational trauma (Chen & Baram, 2016; Franklin et al., 2010; Racine et al., 2018; Scully et al., 2020; Yehuda & Lehrner, 2018), and environmental trauma (Dove-Medows et al.”
BackgroundSánchez-Lafuente, C. L., Reive, B. S., Kalynchuk, L. E., & Caruncho, H. J. (2022) · Biomedicines · doi:10.3390/biomedicines10123213 · Cited by 3
“Moreover, stress has transgenerational effects that can be passed via epigenetic modifications into the offspring [19,20].”
BackgroundEpigenetic Advances in Behavioral and Brain Sciences Have Relevance for Public Policy
Roth, T. L. (2017) · Policy Insights from the Behavioral and Brain Sciences · doi:10.1177/2372732217719091 · Cited by 3
“…2016; Peña, Neugut, & Champagne, 2013; Weaver et al., 2004) or have been experimentally manipulated (Blaze & Roth, 2017; Doherty, Forster, & Roth, 2016; Franklin et al., 2010; Kosten & Nielsen, 2014) have provided direct evidence that these particular factors change methylation states in the brain.”
BackgroundRadiation induces stress and transgenerational impacts in the cricket, Acheta domesticus
Li, X., & Rollo, C. D. (2021) · International Journal of Radiation Biology · doi:10.1080/09553002.2021.1872816 · Cited by 3
“In humans, offspring of parents with early-life dietary stress can express a similar obesity syndrome as their parent, even if they never experienced the stress (Franklin et al. 2010; Curley et al. 2011; Skinner 2014).”
BackgroundNaidoo, V., Martínez-Iglesias, O. A., & Cacabelos, R. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-823039-8.00012-5 · Cited by 3
Effects of cross-fostering experience on emotion in adolescent Kunming mice
Zhu, Y., Wang, Y., Wang, Y., Feng, Y., Wang, Q., Wang, Q., Tian, Y., Tai, F., & Jia, R. (2023) · Behaviour · doi:10.1163/1568539x-bja10200 · Cited by 3
Brain plasticity as a convergence of intrapsychic and intersubjective
Flordellis, C. S., & Kyriazis, D. (2012) · International Forum of Psychoanalysis · doi:10.1080/0803706x.2012.661876 · Cited by 3
“The perception of a stimulus expresses not its nature, but its significance for the individual (Freeman, 2000).”
BackgroundHPA Axis Function During the Perinatal Period in Patients with Affective Disorders
Leff, P., Cruz-Fuentes, C. S., Reyes‐Grajeda, J. P., Mancilla‐Herrera, I., López‐Martínez, M., Bustos, R. G., Gomez, M. L. M., & Flores‐Ramos, M. (2015) · Current Psychiatry Reviews · doi:10.2174/1573400511666150407224518 · Cited by 3
Complex Phenotypes: Epigenetic Manifestation of Environmental Exposures
Faulk, C. D., & Dolinoy, D. C. (2013) · Epigenetics and human health · doi:10.1007/978-3-642-23380-7_4 · Cited by 3
Bolm, T. (2015) · DNP - Der Neurologe und Psychiater · doi:10.1007/s15202-015-0816-3 · Cited by 3
Hollingshaus, M. (2016) · J. Willard Marriott Library · doi:10.26053/0h-asx8-4900 · Cited by 3
Rajaleid, K., & Vågerö, D. H. (2019) · SSM - Population Health · doi:10.1016/j.ssmph.2019.100429 · Cited by 3
“In animal experiments there is evidence that psychological trauma can be transmitted from traumatized males to their offspring, with methylation of genes which are expressed both in germ cells and in the brain of offspring (Franklin et al., 2010).”
BackgroundInfant Learning in the Digital Age
Rusnak, S. N., & Barr, R. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.016 · Cited by 3
Mullola, S., Jeanne Brooks-gunn, B., Elovainio, M. J., Hakulinen, C. A., Schneper, L. M., & Notterman, D. A. (2020) · Journal of Affective Disorders · doi:10.1016/j.jad.2020.11.026 · Cited by 3
“For example, Franklin and co-workers (Franklin et al., 2010) observed a depressivelike phenotype in the offspring of parents who had been subjected to stress in early life (maternal separation), and found that such stress altered the DNA methylation profile in the promoter of several candidate genes in the germline of…”
BackgroundRisiko, Vulnerabilität, Resilienz und Prävention
Fegert, J. M., & Resch, F. (2011) · Springer eBooks · doi:10.1007/978-3-642-19846-5_5 · Cited by 3
Epigenetics in Posttraumatic Stress Disorder
Hunter, R. G. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-417114-5.00016-4 · Cited by 3
Unconscious ties that bind – attending to complexes in the classroom: part 2
Fidyk, A. L. (2016) · International Journal of Jungian Studies · doi:10.1080/19409052.2016.1195426 · Cited by 3
Hannan, A. J. (2020) · The EMBO Journal · doi:10.15252/embj.2020107014 · Cited by 3
“…separation combined with unpredictable maternal stress (MSUS), with male mice exposed to this early-life stress (versus non-stressed controls) used for studies of paternally modulated sperm epigenetics and offspring phenotypes (Franklin et al , 2010; Gapp et al , 2014; van Steenwyk et al , 2018).”
Jablonka, E., & Bronfman, Z. Z. (2015) · Oxford University Press eBooks · doi:10.1093/obo/9780199941728-0063 · Cited by 3
Hayne, H., & Herbert, J. S. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.012 · Cited by 1
Calado, C. M. S. D. S., Manhães‐de‐Castro, R., Gouveia, H. J. C. B., Nogueira, R. M. T. B. L., Souza, V. D. S., de Lira, A. V. S. M., Merencio, S. M. D. A., Lima, B. M. P., de Oliveira, M. V. P., & Toscano, A. E. (2025) · Brain Research · doi:10.1016/j.brainres.2025.149924 · Cited by 3
Rivera, M. A. P., Deddens, V., Fortuin, A. M. J., Wever, K. E., & Olivier, J. D. A. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106388 · Cited by 2
Merhi, A. A., Sivan, V., Koueik, J., Walsh, A. J., Papale, L. A., Alisch, R. S., Hogan, K. J., & Iskandar, B. J. (2025) · Neurochemistry International · doi:10.1016/j.neuint.2025.106088 · Cited by 2
Anisman, H., Bombay, A., & Matheson, K. (2025) · Frontiers in Environmental Health · doi:10.3389/fenvh.2025.1720326 · Cited by 4
Rethinking ADHD as a neurointestinal syndrome: a gut–brain–parasite hypothesis
Demas, A. (2026) · Frontiers in Neuroscience · doi:10.3389/fnins.2025.1694628 · Cited by 2
“…production (IL-6, IL-10), serotonergic signaling (SLC6A4, TPH1), and HPA axis regulation (NR3C1), which are then partially transmitted to offspring, who show altered stress responsivity and gut physiology (Hooper et al., 2012; Tamara et al., 2010; Kundakovic and Champagne, 2015; Del Giudice, 2018).”
Pipelias, P., Kanaka‐Gantenbein, C., & Pervanidou, P. (2026) · Children · doi:10.3390/children13060802 · Cited by 4
“Early life paternal adversity has been linked to long-term changes in offspring stress physiology and emotional regulation [116,117].”
From animal to human epigenetics
Berretta, E., Cutuli, D., Laricchiuta, D., & Petrosini, L. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-819262-7.00002-7 · Cited by 2
Epigenética: Alterações hereditárias em decorrência aos medicamentos ansiolíticos e antidepressivos
de Oliveira, H. L. A., Nobre, N. K. D. S., & Magalhães-Padilha, D. M. (2022) · Research Society and Development · doi:10.33448/rsd-v11i17.38961 · Cited by 2
“Autor (es) Ano Tipo de estudo Critérios de exclusão Franklin et al. 2010 Estudo experimental Transmissão epigenética do estresse nas gerações Deans & Maggert 2015 Artigo de revisão Definição da epigenética Liberman, Wang, & Greer 2019 Artigo de revisão Herança epigenética e mecanismos…”
BackgroundArogundade, T. T., Gbadamosi, I., & Enaibe, B. U. (2023) · Nutritional Neuroscience · doi:10.1080/1028415x.2023.2166804 · Cited by 3
“Epigenetic marks drive biological processes and features as diverse as memory, growth, development, and disease susceptibility; consequently, the nurturing component of nature/nurture interaction makes a signi fi cant contribution to our body and behaviors [3 – 5].”
BackgroundParental enriched environment: A look through key temporary windows
Mir, F. R., Renard, G. M., & Rivarola, M. A. (2023) · Journal of Neuroendocrinology · doi:10.1111/jne.13308 · Cited by 4
Jefferson, J. (2023) · Health and Society · doi:10.51249/hs.v3i04.1474 · Cited by 2
Jefferson, J. (2023) · Health and Society · doi:10.51249/hs.v3i04.1473 · Cited by 2
“Todos os três traços da Tríade Sombria estão associados à insensibilidade (Franklin et al., 2010; Jonason, Koenig e Tost, 2010; Jonason e Tost, 2010), tendências a crimes fi nanceiros (Johnson et al., 2013) e vários tipos de manipulação ((Jonason e Webster, 2010; Murphy et al., 2012).”
BackgroundDifferential susceptibility of male and female germ cells to glucocorticoid-mediated signaling
Cincotta, S. A., Richardson, N., Foecke, M. H., & Laird, D. J. (2024) · eLife · doi:10.7554/elife.90164.3 · Cited by 2
Filošević, A., Matić, I. S., Martinović, L. S., & Pavlić, S. D. (2024) · Future Pharmacology · doi:10.3390/futurepharmacol4010009 · Cited by 2
“…it is important that it can be altered at speci fi c loci in germ cells by exposure to environmental factors such as toxins [101] and stress [102], and can therefore be inherited by o ff spring over multiple generations. methylation increases the gene transcription, while lysine (K)…”
BackgroundThe Impact of Social Concepts on Adventure Tourism Participation: A Mixed Method Study
Pranoto, P., Sukrisno, S., Supriyanto, S., Listyorini, H., Soehari, H., & Kundori, K. (2024) · Journal of Management and Business Review · doi:10.34149/jmbr.v21i2.652 · Cited by 2
“This study focuses on self-identity as a key driver, given how self-identity influences attitudes and intentions, particularly among young traveler consumers (Franklin et al. , 2010; Gardiner et al. , 2013; Gardiner et al., 2023).”
BackgroundEpigenetic Modulations by Microbiome in Breast Cancer
Zhao, Y., & Bhatnagar, S. (2024) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-66686-5_4 · Cited by 2
Ambeskovic, M., Truica, S., McCreary, J. K., Faraji, J., Fang, X., Olson, D. M., & Metz, G. A. S. (2025) · Brain Behavior and Immunity Integrative · doi:10.1016/j.bbii.2025.100104 · Cited by 2
Understanding human behavior: What social workers need to know about animal research
Strong, J., & Combs-Orme, T. D. (2018) · Journal of Human Behavior in the Social Environment · doi:10.1080/10911359.2018.1461165 · Cited by 2
“Recent research on trauma and chronic stress also have benefited from this feature, as pre-clinical research using mice has demonstrated transgenerational effects of traumatic maternal separation on subsequent generations (Franklin et al., 2010).”
BackgroundMalysheva, O. V., Пивина, С. Г., Ponomareva, E. N., & Ordyan, N. E. (2023) · Tsitologiya · doi:10.31857/s0041377123010078 · Cited by 2
Epigenetic Inheritance in Mammals
Bohacek, J., & Mansuy, I. M. (2012) · Research and perspectives in neurosciences · doi:10.1007/978-3-642-27913-3_5 · Cited by 2
Self-citationEpigenetic Modifications: Genetic Basis of Environmental Stress Response
Kubota, T., Miyake, K., & Hirasaw, T. (2011) · InTech eBooks · doi:10.5772/20952 · Cited by 2
“Hence, the altered epigenetic code can be transmitted to the next generation, escaping the erasure of epigenetic marks that typically occurs during gametogenesis (Franklin et al., 2010).”
BackgroundLegato, M. J. (2014) · Academic Emergency Medicine · doi:10.1111/acem.12533 · Cited by 2
Traces épigénétiques des carences affectives précoces
Ladha, K., Monhonval, P., & Lotstra, F. (2013) · Cahiers critiques de thérapie familiale et de pratiques de réseaux · doi:10.3917/ctf.049.0205 · Cited by 2
Transgenerational Transmission of Stress Pathology
Bolten, M. I. (2015) · Zeitschrift für Psychologie · doi:10.1027/2151-2604/a000219 · Cited by 3
Challenge of Developing a Validated Animal Model of PTSD – Focus on Juvenile Stress Model
Richter‐Levin, G., Kehat, O., Shtoots, L., & Ruchi, A. (2015) · Springer eBooks · doi:10.1007/978-3-319-08613-2_121-1 · Cited by 2
Epigenetics in Childhood Health and Disease
Hussain, N. (2014) · Springer eBooks · doi:10.1007/978-1-4939-0706-9_1 · Cited by 2
Early-Life Exposures and the Epigenome: Interactions between Nutrients and the Environment
Marchlewicz, E. H., Anderson, O. S., & Dolinoy, D. C. (2014) · Oxidative stress and disease · doi:10.1201/b17530-3 · Cited by 2
Epigenetics of Psychiatric Disorders
Kundaković, M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803239-8.00019-3 · Cited by 3
Walter, J., & Hümpel, A. (2017) · Nomos Verlagsgesellschaft mbH & Co. KG eBooks · doi:10.5771/9783845270838 · Cited by 1
Kimura, R., & Tefera, S. (2018) · Pastoralism Research Policy and Practice · doi:10.1186/s13570-018-0126-4 · Cited by 2
The History of Horses and Their Relationship to Humans
Beaver, B. V. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-812106-1.00001-2 · Cited by 2
The Importance of the Epigenome for Social-Related Neural Circuits
Wheeler, R. V., & Franklin, T. B. (2019) · Epigenomics · doi:10.2217/epi-2019-0255 · Cited by 2
Self-citationEmbodied Brain Model for Understanding Functional Neural Development of Fetuses and Infants
Yamada, Y., Kanazawa, H., & Kuniyoshi, Y. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.001 · Cited by 3
Transgenerational epigenetics and psychiatric disorders
Gapp, K., & Franklin, T. B. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-823577-5.00026-x · Cited by 4
Self-citationAn Enactive Approach to Causes, Diagnosis, and Treatment of Psychiatric Disorders
de Haan, S. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108685214.009 · Cited by 2
The epigenetics of suicide: The critical impact of environment on epigenetic regulation in suicide
Lutz, P.-É., Turecki, G., & Labonté, B. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-823577-5.00010-6 · Cited by 2
What Every Rabbit and Rodent Owner Needs to Know
Magnus, E., & McBride, A. (2022) · CABI eBooks · doi:10.1079/9781800621312.0010 · Cited by 2
Malysheva, O. V., Пивина, С. Г., Ponomareva, E. N., & Ordyan, N. E. (2023) · Cell and Tissue Biology · doi:10.1134/s1990519x23030070 · Cited by 2
How trauma 'gets under the skin': Biological and cognitive processes of child maltreatment
VanZomeren‐Dohm, A., Ng, R., Howard, K., Kenney, M., Cyr, L. R., Gourneau, J., & Michaels, C. (2013) · University of Minnesota Digital Conservancy (University of Minnesota) · Cited by 2
Dias, B. G. (2016) · International Journal of Epidemiology · doi:10.1093/ije/dyw031 · Cited by 2
Zannas, A. S., Binder, E. B., & Mehta, D. (2016) · Wiley eBooks · doi:10.1002/9781118356142.ch10 · Cited by 2
Alberry, B., Castellani, C. A., & Singh, S. M. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/685586 · Cited by 2
Khodamoradi, K., Khosravizadeh, Z., Amini-Khoei, H., Hosseini, S. R., Dehpour, A. R., & Hassanzadeh, G. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.02.26.966192 · Cited by 2
Adverse Childhood Experiences: A New Framework for Infant Mental Health
Hays-Grudo, J., Ratliff, E. L., & Morris, A. S. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.23592-x · Cited by 2
Boar welfare influence the quality of the gametes
Bernardino, T. (2021) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.10.2021.tde-15032022-145834 · Cited by 2
Steklis, H. D., & Steklis, N. G. (2011) · Human Ethology · doi:10.22330/001c.89870 · Cited by 2
Kac, E., Qi, Q., & Ryznar, R. (2026) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2026.1769422 · Cited by 1
“These fi ndings 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).”
Nature (Genes), Nurture (Epigenetics), and Brain Development
Perna, R. B. (2017) · Journal of Pediatrics & Neonatal Care · doi:10.15406/jpnc.2017.06.00238 · Cited by 1
The Development of Touch Perception and Body Representation
Bremner, A. J. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.009 · Cited by 3
de Haan, S. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108685214.008 · Cited by 1
Bolhuis, E., Scher, A., Ohana, H., Ad-Epsztein, R., Leshem, M., & Beijers, R. (2023) · International Journal of Behavioral Development · doi:10.1177/01650254231215063 · Cited by 3
“However, it is not always the female sex that experiences the most consequences of pre-conception stress (Bock et al., 2016; Franklin et al., 2010; Jenkins et al., 2022; Zaidan et al., 2013).”
BackgroundMethodInfluentialPérez‐Garnelo, S. S., Utrilla, M. J., Fernández-Novo, A., Revilla‐Ruiz, Á., Villagrá, A., & Astiz, S. (2024) · Springer eBooks · doi:10.1007/978-3-031-73079-5_6 · Cited by 4
Transpersonal aspects of venous disease, an opportunity to improve its management
Rasgado, F. V., & Rasgado, L. A. V. (2025) · Acta Phlebologica · doi:10.23736/s1593-232x.24.00636-2 · Cited by 1
Agu, P. C., & Aja, P. M. (2025) · Toxicological & Environmental Chemistry Reviews · doi:10.1080/02772248.2025.2527656 · Cited by 1
Zhao, X., Wang, Z., Xia, Z., Chen, H., Zhu, Y., Wang, S., Bao, Y., Liu, Y., Wang, H., & Ao, Y. (2025) · Cell Communication and Signaling · doi:10.1186/s12964-025-02346-1 · Cited by 1
“For example, in the model of early separation from the mother after birth, male F1-F2 offspring mice showed more depressive-like behaviors in adulthood, whereas no changes were observed in females [67].”
Epigenetics of Aggression: Recent Advances and Perspectives on Animal Models
Dudko, N. A., Nurieva, G. N., Станиславовна, К. С., & Kuznetsova, I. L. (2025) · Russian Journal of Genetics · doi:10.1134/s1022795425700711 · Cited by 2
“…of genes such as Nr3c1 (glucocorticoid receptor), Mecp2 (methyl-CpG-binding protein 2), Crfr2 (corti-cotropin releasing factor receptor), and Cb1 (cannabinoid receptor 1), which in turn affects their expression in the brain and may increase the risk of developing aggressive behavior [64–66].”
Maldonado, M. B. C., de Lima, C. B., Oudihat, M., Block, J., Sagheer, M., Cuellar, C. J., Yu, F., Zhang, Y., Haimon, M. L. J., Bromfield, J. J., et al. (2026) · Biology of Reproduction · doi:10.1093/biolre/ioag013 · Cited by 1
Female-biased vulnerability to transgenerational impact of paternal early-life stress
Ishikawa, I., Ohta, K.-I., Imai, M., Ishikawa, M., Kumei, H., Kashima, M., Fugo, U., Suzuki, S., Otabi, H., Miki, T., et al. (2026) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2026.107773 · Cited by 1
Stress-induced epigenome changes as a risk factor in the onset of mental disorders
Shkarina, L., Дмитриевич, Б. К., Станиславович, Д. С., Primak, A. L., Tkachuk, V., Chaika, Y. A., Neyfeld, E. A., & Karagyaur, M. N. (2026) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2026.1764368 · Cited by 2
Mindfulness Intervention for Parent Stress and Childhood Obesity Risk: A Randomized Trial
Fogelman, N., Bernstein, H. M., Bautista, T. G., Savoye, M., Chaplin, T. M., Silverman, W. K., Jastreboff, A. M., & Sinha, R. (2026) · PEDIATRICS · doi:10.1542/peds.2025-072230 · Cited by 1
Abu-Moch, M., Azab, A. N., Yousef, M., & Agam, G. (2026) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2026.119356 · Cited by 1
Early life adversity, oxytocin system alterations, and addiction vulnerability: a narrative review
Saboory, E., Ahmadian-Moghadam, S., & Mehranfard, N. (2026) · Psychopharmacology · doi:10.1007/s00213-026-07027-6 · Cited by 2
Epigenomic and Noncoding RNA Regulation in Addictive Processes
Satterlee, J. S. (2013) · Epigenetics and human health · doi:10.1007/978-3-642-36827-1_7 · Cited by 1
Biofeedback: Messverfahren und Trainingsmethoden
Pirker-Binder, I. (2016) · Springer eBooks · doi:10.1007/978-3-662-48619-1_11 · Cited by 1
The Epigenetics of Parental Effects
Zhang, T., Caldji, C., Diorio, J. C., Dhir, S. K., Turecki, G., & Meaney, M. J. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-391494-1.00004-5 · Cited by 1
Mental Disorders and Transgenerational Epigenetics
Kubota, T., Hirasawa, T., & Miyake, K. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405944-3.00024-6 · Cited by 1
Epigenetic Modulation of Human Neurobiological Disorders
Kubota, T., Miyake, K., Hirasawa, T., Onaka, T., & Yamasue, H. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-388415-2.00010-x · Cited by 1
Nature or Nurture – Will Epigenomics Solve the Dilemma?
Płonka, B. K. (2016) · Studia Humana · doi:10.1515/sh-2016-0007 · Cited by 1
“Early life stress due to maternal separation induces alteration of some behavior (risk assessment, novelty response, social behavior) across three generations in mice [61, 204], but the effect can be diminished by environmental enrichment [67].”
BackgroundHandlung zwischen Automatismus, Bauchgefühl und Erinnerung
Markowitsch, H. J., & Staniloiu, A. (2017) · Springer eBooks · doi:10.1007/978-3-658-16891-9_5 · Cited by 1
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review