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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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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
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Items 501–600 of 999
Breeding animals for quality products: not only genetics
Chavatte‐Palmer, P., Couturier‐Tarrade, A., Kiefer, H., Duranthon, V., & Jammes, H. (2015) · Reproduction Fertility and Development · doi:10.1071/rd15353 · Cited by 25
“Comparable changes in DNA methylation are also present in the brain of their own offspring and are associated with altered gene expression (Franklin et al. 2010).”
BackgroundStern, S., Snir, O., Mizrachi, E., Galili, M., Zaltsman, I., & Soen, Y. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.271445 · Cited by 22
“Additional mechanisms that have been shown to mediate transgenerational phenomena in various organisms include DNA methylation (Cubas et al. 1999; Morgan et al. 1999; Rakyan et al. 2002; Lane et al. 2003; Xing et al. 2007; Dunn & Bale, 2009; Franklin et al. 2010; Ng et al. 2010), histone modifications (Hammoud et al.”
BackgroundWilliams, Z. M. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.03.023 · Cited by 20
Behavioral Adaptations to Invasive Species
Langkilde, T. L., Thawley, C. J., & Robbins, T. R. (2017) · Advances in the study of behavior · doi:10.1016/bs.asb.2016.12.003 · Cited by 22
PARP Inhibitor Affects Long-term Heat-stress Response via Changes in DNA Methylation
Cramer, T., Rosenberg, T., Kisliouk, T., & Meiri, N. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.12.018 · Cited by 23
Batchelor, V., & Pang, T. Y. (2019) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2019.04.010 · Cited by 23
Demaili, A., Portugalov, A., Dudai, M., Maroun, M., Akirav, I., Braun, K., & Bock, J. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1129946 · Cited by 24
“Since the same methylation patterns were found in the cortex of F2 generation offspring, this indicates a possible transgenerational transmission of the stress-induced epigenetic changes (Franklin et al., 2010).”
BackgroundChamproux, A., Tang, Y., Dickson, D. A., Meng, A., Harrington, A. N., Liaw, L., Marzi, M. J., Nicassio, F., Schlaeger, T. M., & Feig, L. A. (2024) · Epigenetics · doi:10.1080/15592294.2024.2346694 · Cited by 25
Two Ways of Living through Postpartum Depression
Røseth, I., Binder, P., & Malt, U. F. (2011) · Journal of Phenomenological Psychology · doi:10.1163/156916211x599753 · Cited by 23
Vågerö, D., Aronsson, V., & Modin, B. (2017) · SSM - Population Health · doi:10.1016/j.ssmph.2017.11.006 · Cited by 22
“Of theoretical importance is the hypothesis that early experience can also cause epigenetic modification of germ-line DNA and potentially influence gene expression and longevity in the next generation (Franklin et al., 2010; Marsland, 2017; Rando, 2016; Sharma, 2017; Vaiserman, 2012).”
BackgroundDuffy, A. C. (2014) · Evidence-Based Mental Health · doi:10.1136/eb-2014-101993 · Cited by 21
“Epigenetic mechanisms, including DNA methylation and covalent histone modifications within gene promoters, have been shown to be responsive to the environment and in some cases these stable modifications are passed between generations.(6) Accruing evidence suggests that epigenetic mechanisms may in part explain the ‘m…”
BackgroundMigration modulates the prevalence of ASD and ADHD: a systematic review and meta-analysis
Gao, X., Zhao, Y., Wang, N., & Yang, L. (2022) · BMC Psychiatry · doi:10.1186/s12888-022-04037-4 · Cited by 26
“Early stress alters the profile of DNA methylation in the promoter of several candidate genes in the germline of male mice, and these alternations are also present in the brain of the offspring and correlated with changes in gene expression [69].”
BackgroundGómez‐Pinilla, F., & Thapak, P. (2024) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2024.04.237 · Cited by 24
Korgan, A. C., O’Leary, M. E., Bauer, J., Fortier, A., Weaver, I. C. G., & Perrot, T. S. (2016) · eNeuro · doi:10.1523/eneuro.0231-16.2016 · Cited by 22
“…et al., 2009, 2013), obesity (Ng et al., 2010; Fullston et al., 2013), enrichment (Mashoodh et al., 2012), and physiological/ psychological stress (Franklin et al., 2010; Dietz et al., 2011; Hoyer et al., 2013; Mychasiuk et al., 2013; Rodgers et al., 2013; Gapp et al., 2014; Wu et al., 2016) on…”
Cartier, J., Smith, T., Thomson, J. P., Rose, C. M., Khulan, B., Heger, A., Meehan, R. R., & Drake, A. J. (2018) · Genome biology · doi:10.1186/s13059-018-1422-4 · Cited by 21
“In other models, exposure to excess glucocorticoids as a consequence of stress in mice has been shown to produce small changes in DNA methylation at candidate genes in the male germline and behavioural changes in offspring [55, 56] and in rats, exposure to the fungicide vinclozolin leads to effects on male fertility w…”
BackgroundInter- and transgenerational inheritance of behavioral phenotypes
Jawaid, A., & Mansuy, I. M. (2019) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.12.004 · Cited by 21
Self-citationRyan, C. P., & Kuzawa, C. W. (2020) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.21828 · Cited by 21
Pruett, J. E., Addis, E. A., & Warner, D. A. (2019) · Animal Behaviour · doi:10.1016/j.anbehav.2019.04.010 · Cited by 20
Strober, M. A., Peris, T. S., & Steiger, H. (2014) · International Journal of Eating Disorders · doi:10.1002/eat.22322 · Cited by 20
Effects of Stress Across Generations: Why Sex Matters
Champagne, F. A. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.10.004 · Cited by 20
Champagne, F. A. (2019) · Functional Ecology · doi:10.1111/1365-2435.13411 · Cited by 23
“…are observed in the brain‐specific gamma isoform of protein kinase C (Prkcc), Mecp2, Cb1 and corticotropin‐releasing factor receptor 2 (Crfr2) genes in the sperm of F1‐exposed males and similar changes are observed in the brain of F2 offspring (Bohacek et al., 2015; Franklin et al., 2010).”
BackgroundInfluentialPacheco, H. A., Hernández, R. O., Chen, S., Neave, H. W., Pempek, J. A., & Brito, L. F. (2024) · Journal of Dairy Science · doi:10.3168/jds.2024-24953 · Cited by 20
King, S. E., Schatz, N. A., Babenko, O., Ilnytskyy, Y., Kovalchuk, I., & Metz, G. A. S. (2025) · Communications Biology · doi:10.1038/s42003-024-07444-3 · Cited by 23
“Moreover, ancestral stress can promote behavioral changes, such as increased anxiety-like behaviors 14,19,21 , risk taking 23,24 , depression-like phenotypes 15,16 and motor hyperactivity 25 .”
Environmental epigenetics: new horizons in redefining biological and health outcomes
Faraji, J., & Metz, G. A. S. (2026) · Environment International · doi:10.1016/j.envint.2026.110072 · Cited by 22
Varela, R. B., Cararo, J. H., Tye, S. J., Carvalho, A. F., Valvassori, S. S., Fries, G. R., & Quevedo, J. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104579 · Cited by 21
Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny
Valcarce, D. G., Riesco, M. F., Cuesta-Martín, L., Esteve‐Codina, A., Martínez, J. M., & Robles, V. (2023) · BMC Biology · doi:10.1186/s12915-023-01570-w · Cited by 18
Coelho, A. A., Bastos, S., Gobira, P. H., & Lisboa, S. F. D. S. (2023) · Neuronal Signaling · doi:10.1042/ns20220034 · Cited by 22
Faruk, M. O., Rahman, M. S., Rana, M. S., Mahmud, S., Neyma, M. A., Karim, M. S., & Alam, N. (2023) · PLoS ONE · doi:10.1371/journal.pone.0289220 · Cited by 21
Zhang, P., Li, G., Li, H., Tan, X., & Cheng, H. M. (2017) · Scientific Reports · doi:10.1038/s41598-017-13067-y · Cited by 22
“In our present study, we asked (1) whether circadian rhythm disturbance during the gestational period induces anhedonia- and depression-like behaviors in pregnant female mice, (2) whether in utero exposure to circadian rhythm disturbance leads to the development of these mood disorder-like behaviors in adolescent and…”
Maternal Trauma Exposure and Childhood Anxiety Outcomes: Examining Psychosocial Mechanisms of Risk
Robinson, B. A., Hendrix, C. L., Krakovsky, H. S., Smith, A. K., & Brennan, P. A. (2018) · Research on Child and Adolescent Psychopathology · doi:10.1007/s10802-018-0463-1 · Cited by 19
“Others have demonstrated that intergenerational transmission of trauma-related risk can be attributed to changes in the profile of DNA methylation of several candidate genes, which are then passed on to subsequent offspring (Franklin et al. 2010).”
BackgroundTransgenerational consequences of maternal immune activation
Pollak, D. D., & Weber‐Stadlbauer, U. (2019) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2019.06.006 · Cited by 20
Ambeskovic, M., Ilnytskyy, Y., Kiss, D., Currie, C. L., Montina, T., Kovalchuk, I., & Metz, G. A. S. (2020) · Aging · doi:10.18632/aging.102848 · Cited by 17
Gangisetty, O., Chaudhary, S., Palagani, A., & Sarkar, D. K. (2022) · PLoS ONE · doi:10.1371/journal.pone.0263340 · Cited by 22
“Postnatal trauma elicits depressive-like behavior for up to three generations [35].”
BackgroundFrom paramutation to human disease: RNA-mediated heredity
Rassoulzadegan, M., & Cuzin, F. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.08.007 · Cited by 19
Brew, B. K., Lundholm, C., Caffrey Osvald, E., Chambers, G., Öberg, S., Fang, F., & Almqvist, C. (2022) · American Journal of Epidemiology · doi:10.1093/aje/kwab236 · Cited by 19
“…separated from parents at birth to induce depression and anxiety; such studies have found a number of epigenetic changes increasing offspring disease risk and stress axis sensitivity, such as DNA methylation, populations of small noncoding RNAs, and posttranslational histone modifications (17, 18).”
Laricchiuta, D., Sciamanna, G., Gimenez, J., Termine, A., Fabrizio, C., Caioli, S., Balsamo, F., Panuccio, A., Bardi, M. D., Saba, L., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22020810 · Cited by 20
Convergent actions of stress and stimulants via epigenetic regulation of neural circuitry
Murphy, M. D., & Heller, E. A. (2022) · Trends in Neurosciences · doi:10.1016/j.tins.2022.10.001 · Cited by 20
Neurobiological disease etiology and inheritance: an epigenetic perspective
Saab, B. J., & Mansuy, I. M. (2013) · Journal of Experimental Biology · doi:10.1242/jeb.089995 · Cited by 18
“How this pathway is newly recruited is not known, but may involve persistent modifications such as DNA methylation, in a manner similar to how exposure to stressful conditions in early life leads to a hypermethylation and reduction of expression of the MeCP2 and CB1 genes (Franklin et al., 2010).”
BackgroundSelf-citationPre-Conception War Exposure and Mother and Child Adjustment 4 Years Later
Shachar-Dadon, A., Gueron‐Sela, N., Weintraub, Z., Maayan‐Metzger, A., & Leshem, M. (2016) · Research on Child and Adolescent Psychopathology · doi:10.1007/s10802-016-0153-9 · Cited by 25
“…of pre-conception stress effects via epigenetic alterations in stress substrates in the mother’s brain and ova, and subsequent alterations in offspring behavior, endocrine and brain microstructure (Bock et al. 2014; Franklin et al. 2010; Zaidan et al. 2013; Zaidan and Gaisler-Salomon 2015).”
BackgroundNeuroepigenetic mechanisms underlying fear extinction: emerging concepts
Marshall, P. R., & Bredy, T. W. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5084-4 · Cited by 18
“ory is not primarily contained within the synapse, a cognitive neuroepigenetic view leaves room for Lamarkianlike phenomena where information can be acquired in one generation and passed on to the next (Franklin et al. 2010; Fischer 2014).”
Christian, L. M. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.03.010 · Cited by 18
“Moreover, these differences in behavior and DNA methylation are, in part, transmitted to subsequent generations (Franklin et al., 2010).”
BackgroundMaternal High-Fat Diet Modulates Cnr1 Gene Expression in Male Rat Offspring
Gawliński, D., Gawlińska, K., & Smaga, I. (2021) · Nutrients · doi:10.3390/nu13082885 · Cited by 19
“protein 2 (MeCP2 gene), a transcriptional regulator that binds methylated DNA, was reported in the second-generation brain [13].”
BackgroundSocial Crowding during Development Causes Changes in GnRH1 DNA Methylation
Alvarado, S. G., Lenkov, K., Blake, W., & Fernald, R. D. (2015) · PLoS ONE · doi:10.1371/journal.pone.0142043 · Cited by 19
“Furthermore, unique signatures of DNA methylation accompany and mediate transgenerational effects underlying behaviors related to stress [18, 19] underlining their importance in generational adaptation to stress.”
BackgroundA Lexicon of DNA Modifications: Their Roles in Embryo Development and the Germline
Zhu, Q., Stöger, R. J., & Alberio, R. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00024 · Cited by 21
“…or multiple generations by diet (Holland et al., 2016), obesity (Donkin et al., 2016), drug addiction (Feng et al., 2015), stress/traumatic exposure (Franklin et al., 2010; Dias and Ressler, 2014; Gapp et al., 2014b), and toxins in the environment (Skinner et al., 2013; Nilsson and Skinner, 2015).”
BackgroundLi, W., Zhang, D., Zou, Q., Bose, A. P. H., Jordan, A. L., McCallum, E. S., Bao, J., & Duan, M. (2024) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2024.176336 · Cited by 17
Pembrey, M. E., Northstone, K., Gregory, S., Miller, L. L., & Golding, J. (2014) · BMJ Open · doi:10.1136/bmjopen-2014-005030 · Cited by 16
The Logic of Transgenerational Inheritance: Timescales of Adaptation
Sengupta, T., Kaletsky, R. L., & Murphy, C. T. (2023) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-020923-114620 · Cited by 18
Calling the question: what is mammalian transgenerational epigenetic inheritance?
Khatib, H., Townsend, J. A., Konkel, M. A., Conidi, G., & Hasselkus, J. A. (2024) · Epigenetics · doi:10.1080/15592294.2024.2333586 · Cited by 18
“The study conducted by Franklin et al. [46] examined the transmission of epigenetic effects of early stress through the F3 generation.”
Noll‐Hussong, M., Glaesmer, H., Herberger, S., Bernardy, K., Schönfeldt‐Lecuona, C., Lukas, A., Guendel, H. O., & Nikolaus, T. (2012) · Zeitschrift für Gerontologie und Geriatrie · doi:10.1007/s00391-012-0303-9 · Cited by 17
Xu, X., Weber, D. N., Martin, A., & Lone, D. (2015) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2015.11.003 · Cited by 17
“Animal studies with rodents have corroborated those findings that characteristics linked to early life experiences of the parents may be transmitted to subsequent generations (Benyshek et al. 2006; Franklin et al. 2010).”
BackgroundTransgenerational Effects of Variable Foraging Demand Stress in Female Bonnet Macaques
Kinnally, E. L., Feinberg, C., KIM, D., Ferguson, K., Coplan, J. D., & Mann, J. J. (2013) · American Journal of Primatology · doi:10.1002/ajp.22130 · Cited by 17
“Many studies have demonstrated intergenerational transmission of traits in same‐sex, but not necessarily opposite sex, offspring [Dunn et al., 2011; Fairbanks, 1989; Francis et al., 1999; Franklin et al., 2010; Maestripieri et al., 2005].”
BackgroundTransgenerational Epigenetics and Brain Disorders
Rachdaoui, N., & Sarkar, D. K. (2014) · International review of neurobiology · doi:10.1016/b978-0-12-801311-3.00002-0 · Cited by 18
Genome-Scale Assessment of Age-Related DNA Methylation Changes in Mouse Spermatozoa
Kobayashi, N., Okae, H., Hiura, H., Chiba, H., Shirakata, Y., Hara, K., Tanemura, K., & Arima, T. (2016) · PLoS ONE · doi:10.1371/journal.pone.0167127 · Cited by 17
“In spite of the stability, many studies have suggested that various environmental and physiological factors, including nutrition [10], exercise [11], psychological stress [12, 13] and advanced age [14–16], can alter DNA methylation patterns in spermatozoa.”
BackgroundLei, J., Nie, Q. H., & Chen, D. (2018) · Biology of Reproduction · doi:10.1093/biolre/ioy050 · Cited by 17
“Traumatic experience in early life and chronic social instability during adolescence and early adulthood are known to produce long-lasting effects for future psychiatric disorders and affect future generations [22,23].”
BackgroundEarly life stress and voluntary alcohol consumption in relation to Maoa methylation in male rats
Bendre, M., Granholm, L., Drennan, R., Meyer, A., Yan, L., Nilsson, K. W., Nylander, I., & Comasco, E. (2018) · Alcohol · doi:10.1016/j.alcohol.2018.11.001 · Cited by 18
Franco, L. O., de Carvalho, M. L., Costa, J., Ferreira, P. A., Guedes, J. R., Sousa, R. J. M., Edfawy, M., Seabra, C. M., Cardoso, A. L., & Peça, J. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0727-7 · Cited by 17
“This would be in line with a phenotypical manifestation of depression that is incompletely penetrant, prone to surface [21, 37] or not [38], depending on experimental variables or additional triggers [39].”
BackgroundMethodMañas-Ojeda, A., Ros‐Bernal, F., Olucha-Bordonau, F. E., & Castillo-Gómez, E. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165819 · Cited by 20
Premigration social adversity and autism spectrum disorder
Augereau, N., Lagdas, I., Kermarrec, S., Gicquel, L., Martin, V., Xavier, J., Cohen, D., Bouvet, M., Rolland, A.-C., & Tordjman, S. (2020) · BJPsych Open · doi:10.1192/bjo.2020.56 · Cited by 17
Serrano, A. R. D., Hughes, K. A., & Rodd, F. H. (2021) · Scientific Reports · doi:10.1038/s41598-021-83448-x · Cited by 17
Hickman, D. L., & Swan, M. P. (2011) · PubMed Central · Cited by 17
Biological Embedding of Psychosocial Stress Over the Life Course
Eachus, H., & Cunliffe, V. T. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-811060-7.00012-7 · Cited by 19
Early adversity and the regulation of gene expression: implications for prenatal health
Gillespie, S. L., Cole, S. W., & Christian, L. M. (2019) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2019.02.005 · Cited by 17
“CRFR2 [corticotropin-releasing factor 2] [67], NR3C1 [glucocorticoid receptor] [68–70], FKBP5 [affects glucocorticoid receptor sensitivity] [71], BDNF [nerve growth factor] [72]).”
DNA methylation in adolescents with anxiety disorder: A longitudinal study
Bortoluzzi, A., Salum, G. A., da Rosa, E. D., Chagas, V. D. S., Castro, M. A. A., & Manfro, G. G. (2018) · Scientific Reports · doi:10.1038/s41598-018-32090-1 · Cited by 16
Epigenetic programming for obesity and noncommunicable disease: From womb to tomb
Saavedra, L. P. J., Piovan, S., Moreira, V. M., Gonçalves, G. D., Ferreira, A. R. O., Ribeiro, M. V. G., Peres, M. N. C., Almeida, D. L., Raposo, S. R., da Silva, M. C., et al. (2023) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-023-09854-w · Cited by 20
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Holmes, L., Chinaka, C., Elmi, H., Deepika, K., Pelaez, L., Enwere, M., Akinola, O., & DABNEY, K. W. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph16214123 · Cited by 18
Houwing, D. J., Esquivel-Franco, D. C., Ramsteijn, A. S., Schuttel, K., Struik, E. L., Arling, C., de Boer, S. F., & Olivier, J. D. A. (2020) · Psychopharmacology · doi:10.1007/s00213-020-05535-7 · Cited by 16
Zaidan, H., Galiani, D., & Gaisler‐Salomon, I. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01220-1 · Cited by 19
Managing dingoes on Fraser Island: culling, conflict, and an alternative
O’Neill, A. J., Cairns, K. M., Kaplan, G., & Healy, E. (2016) · Pacific Conservation Biology · doi:10.1071/pc16026 · Cited by 16
Bidirectional Effects of Mother-Young Contact on the Maternal and Neonatal Brains
González‐Mariscal, G., & Melo, Á. I. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-62817-2_6 · Cited by 16
A Brief Guide to Studying Fear in Developing Rodents: Important Considerations and Common Pitfalls
Cowan, C. S. M., & Richardson, R. (2018) · Current Protocols in Neuroscience · doi:10.1002/cpns.44 · Cited by 17
“In fact, at least some of the effects of early-life manipulations are so strong that they can be observed across generations (Callaghan, Cowan, & Richardson, 2016; Francis et al., 1999; Franklin et al., 2010; for reviews, see Braun et al., in press; Cowan, Callaghan, Kan, & Richardson, 2016).”
BackgroundBeyond the maternal epigenetic legacy
Champagne, F. A. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0157-6 · Cited by 16
Social context influences the expression of DNA methyltransferase genes in the honeybee
Cardoso-Júnior, C. A. M., Eyer, M., Dainat, B., Hartfelder, K., & Dietemann, V. (2018) · Scientific Reports · doi:10.1038/s41598-018-29377-8 · Cited by 16
Preconception paternal mental disorders and child health: Mechanisms and interventions
Tan, X., Luo, J., Ding, X., & Li, H. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104976 · Cited by 16
Phillips, D. I. (2011) · World Journal of Diabetes · doi:10.4239/wjd.v2.i12.211 · Cited by 15
Chistiakov, D. A., & Chekhonin, V. P. (2017) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2017.1322714 · Cited by 16
“Increased expression of CRF and CRF2 leads to elevated production of adrenocorticotropic hormone (ACTH) by the pituitary gland, followed by up-regulation of the HPA axis.”
BackgroundLactobacillus reuteri effects on maternal separation stress in newborn mice
Park, E. S., Freeborn, J., Venna, V. R., Roos, S., Rhoads, J. M., & Liu, Y. (2021) · Pediatric Research · doi:10.1038/s41390-021-01374-0 · Cited by 15
Yao, Y., & Zhang, Y. (2022) · China Economic Review · doi:10.1016/j.chieco.2022.101914 · Cited by 15
Choi, Y., & Mango, S. E. (2014) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2014.05.011 · Cited by 15
“Grandchildren (F3) of F1 mice whowere raised under chronic stress from maternal separation exhibited depression-like behaviors, although they had not suffered from the same poormaternal care [34].”
BackgroundXiong, G.-J., Yang, Y., Cao, J., Mao, R., & Xu, L. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.12.026 · Cited by 16
“However, other studies suggested that transmission of abnormal behavioral traits can occur through both fathers (Franklin et al., 2010) and mothers (Weiss et al.”
BackgroundResultInfluentialEwen, B. M. (2015) · Trends in Neuroscience and Education · doi:10.1016/j.tine.2015.11.002 · Cited by 15
“Connections between epigenetics and stress-related symptoms have been studied in animal models [10,11,21,23,39,6].”
BackgroundPaternal transmission of early life traumatization through epigenetics: Do fathers play a role?
Rowold, E. D., Schulze, L. N., der Auwera, S. V., & Grabe, H. J. (2017) · Medical Hypotheses · doi:10.1016/j.mehy.2017.09.011 · Cited by 16
Zhang, S., Li, X., Wang, Z., Liu, Y., Gao, Y., Tan, L., Liu, E., Zhou, Q., Xu, C., Wang, X., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-01811-3 · Cited by 15
Zaidan, H., Wnuk, A., Aderka, I. M., Kajta, M., & Gaisler‐Salomon, I. (2023) · Stress · doi:10.1080/10253890.2023.2201325 · Cited by 15
“…the transgenerational impact of stress on behavioral, neuroendocrine and molecular phenotypes may be mediated by epigenetic changes in germ cells (Franklin et al., 2011, 2010; Gapp et al., 2014; van steenwyk et al., 2018). the present study also supports this possibility since changes to…”
BackgroundInfluentialRahia Mashoodh, A., Habrylo, I. B., Gudsnuk, K. M., & Champagne, F. A. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105357 · Cited by 15
Transgenerational effects of early life stress on the fecal microbiota in mice
Otaru, N., Kourouma, L., Pugin, B., Constancias, F., Braegger, C., Mansuy, I. M., & Lacroix, C. (2024) · Communications Biology · doi:10.1038/s42003-024-06279-2 · Cited by 15
“…withunpredictablematernalstress(MSUS)distinguishesitselffromother rodentmodelsofstressbyapplyingunpredictabilityastraumaticfactorand bycombiningstressofmothersandofpups(dailyunpredictableseparation for3handinadditionmothersarestressedunpredictablyduringseparation byrestraintorforcedswim) 22 .”
Self-citationArvind, A., Sreelekshmi, S., & Dubey, N. (2025) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-025-01549-x · Cited by 19
“…affecting the stress responses, where research has shown that epigenetic factors causing susceptibility are being transferred to the next generation (Nestler 2016); early stress alters DNA methylation in the stressed male germline and is observed in the subsequent generation (Franklin et al. 2010).”
The theory of RNA-mediated gene evolution
Morris, K. V. (2015) · Epigenetics · doi:10.1080/15592294.2014.995536 · Cited by 14
“Studies carried out in nematode, mouse, and pig model systems all suggest that transgenerational epigenetic inheritance involves non-coding RNAs.(12-14) There is also evidence for this phenomenon in humans, suggesting that some level of epigenetic inheritance is operative in the fabric of our existence.”
BackgroundLee, Y.-A., & Goto, Y. (2013) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2013.04.007 · Cited by 14
“Although inheritance of typical chromatin modification across generation has been confirmed in some studies (Franklin et al., 2010), it appears that miRNA transmitted across generation through gametes also plays significant role on this type of inheritance (Daxinger and”
InfluentialBehavioral Epigenetics: Perspectives Based on Experience-Dependent Epigenetic Inheritance
Pang, Y.-Y., Lu, R. J.-H., & Chen, P. (2019) · Epigenomes · doi:10.3390/epigenomes3030018 · Cited by 18
“In the field of behavioral epigenetics, exposure to adverse experiences during the postpartum period is often associated with aberrant methylation profiles of the genes encoding the glucocorticoid receptor (GCR) in both human and mouse models [7,8].”
BackgroundAlberry, B., Castellani, C. A., & Singh, S. M. (2020) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-020-09316-3 · Cited by 14
Sex-specific transgenerational effects of morphine exposure on reward and affective behaviors
Brynildsen, J. K., Sanchez, V., Yohn, N. L., Carpenter, M. D., & Blendy, J. A. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112842 · Cited by 14
“However, others have demonstrated that stress, toxins, and cocaine alter the germline epigenome through DNA methylation [20-25], histone acetylation [16], and potential non-coding RNA in the germline [26-28].”
BackgroundParents’ adulthood stress induces behavioral and hormonal alterations in male rat offspring
Niknazar, S., Nahavandi, A., Najafi, R., Danialy, S., Mehrjerdi, F. Z., & Karimi, M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.05.026 · Cited by 14
Vargas-Caraveo, A., Castillo-Michel, H. A., Mejía-Carmona, G. E., Pérez-Ishiwara, D. G., Cotte, M., & Martı́nez-Martı́nez, A. (2014) · Spectrochimica Acta Part A Molecular and Biomolecular Spectroscopy · doi:10.1016/j.saa.2014.02.148 · Cited by 14
Probing the germline-dependence of epigenetic inheritance using artificial insemination in mice
Bohacek, J., von Werdt, S., & Mansuy, I. M. (2016) · Current Zoology · doi:10.1093/eep/dvv015 · Cited by 14
Self-citationMolecular and Epigenetic Mechanisms Underlying Cognitive and Adaptive Responses to Stress
Trollope, A. F., Mifsud, K. R., Saunderson, E. A., & Reul, J. M. H. M. (2017) · Epigenomes · doi:10.3390/epigenomes1030017 · Cited by 13
“This research indicates that stress-related behaviors may be transmitted across generations and in sexspecific manner [99].”
BackgroundPreemptive Epigenetic Medicine Based on Fetal Programming
Kubota, T. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-5526-3_9 · Cited by 14
Paternal line effects of early experiences persist across three generations in rhesus macaques
Kinnally, E. L., Gonzalez, M. N., & Capitanio, J. P. (2018) · Developmental Psychobiology · doi:10.1002/dev.21771 · Cited by 14
Infant Emotion Development and Temperament
Aktar, E., & Pérez‐Edgar, K. E. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108351959.026 · Cited by 17
Duffy, H. B. D., & Roth, T. L. (2020) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2020.594244 · Cited by 15
Family centre in the Nordic Countries : A Meeting Point for Children and Families
Kekkonen, M., Montonen, M., & Viitala, R. (2012) · Diva portal (Dalarna University Library) · Cited by 14
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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