Transgenerational inheritance of behavioral and metabolic effects of paternal exposure to traumatic stress in early postnatal life: evidence in the 4th generation
Open accessAbstract
In the past decades, evidence supporting the transmission of acquired traits across generations has reshaped the field of genetics and the understanding of disease susceptibility. In humans, pioneer studies showed that exposure to famine, endocrine disruptors or trauma can affect descendants, and has led to a paradigm shift in thinking about heredity. Studies in humans have however been limited by the low number of successive generations, the different conditions that can be examined, and the lack of mechanistic insight they can provide. Animal models have been instrumental to circumvent these limitations and allowed studies on the mechanisms of inheritance of environmentally induced traits across generations in controlled and reproducible settings. However, most models available today are only intergenerational and do not demonstrate transmission beyond the direct offspring of exposed individuals. Here, we report transgenerational transmission of behavioral and metabolic phenotypes up to the 4th generation in a mouse model of paternal postnatal trauma (MSUS). Based on large animal numbers (up to 124 per group) from several independent breedings conducted 10 years apart by different experimenters, we show that depressive-like behaviors are transmitted to the offspring until the third generation, and risk-taking and glucose dysregulation until the fourth generation via males. The symptoms are consistent and reproducible, and persist with similar severity across generations. These results provide strong evidence that adverse conditions in early postnatal life can have transgenerational effects, and highlight the validity of MSUS as a solid model of transgenerational epigenetic inheritance.
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In animal studies, there has been some evidence that paternal postnatal trauma can have behavioral effects on or up to the fourth generation.
“In animal studies, there has also been some evidence that paternal postnatal trauma can have behavioral effects on or up to, the fourth generation [66].”
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Cites
Diagnostic and Statistical Manual of Mental Disorders
American Psychiatric Association (2013) · doi:10.1176/appi.books.9780890425596 · Cited by 116,369 · see citing works
Finding the missing heritability of complex diseases
Manolio, T. A., Collins, F. S., Cox, N. J., Goldstein, D. B., Hindorff, L. A., Hunter, D. J., McCarthy, M. I., Ramos, E. M., Cardon, L. R., Chakravarti, A., et al. (2009) · Nature · doi:10.1038/nature08494 · Cited by 8,336 · see citing works
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 · see citing works
Epigenetic inheritance at the agouti locus in the mouse
Morgan, H. D., Sutherland, H. G. E., Martin, D. I. K., & Whitelaw, E. (1999) · Nature Genetics · doi:10.1038/15490 · Cited by 1,476 · see citing works
Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder
Chen, Q., Yan, M., Cao, Z., Li, X., Zhang, Y., Shi, J., Feng, G.-H., Peng, H., Zhang, X., Zhang, Y., et al. (2016) · Science · doi:10.1126/science.aad7977 · Cited by 1,470 · see citing works
Parental olfactory experience influences behavior and neural structure in subsequent generations
Dias, B. G., & Ressler, K. J. (2014) · Nature Neuroscience · doi:10.1038/nn.3594 · Cited by 1,338 · see citing works
Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice
Gapp, K., Jawaid, A., Sarkies, P., Bohacek, J., Pelczar, P., Prados, J., Farinelli, L., Miska, E., & Mansuy, I. M. (2014) · Nature Neuroscience · doi:10.1038/nn.3695 · Cited by 1,306 · see citing works
Self-citationEpigenetic transmission of the impact of early stress across generations
Franklin, T. B., Russig, H., Weiss, I. C., Gräff, J., Linder, N., Michalon, A., Vizi, S., & Mansuy, I. M. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.05.036 · Cited by 1,125 · see citing works
Self-citationZanarini, M. C., Williams, A. A., Lewis, R. E., Reich, R., Vera, S. C., Marino, M. F., Levin, A., Yong, L., & Frankenburg, F. R. (1997) · American Journal of Psychiatry · doi:10.1176/ajp.154.8.1101 · Cited by 717 · see citing works
Fullston, T., Teague, E. M. C. O., Palmer, N. O., DeBlasio, M. J., Mitchell, M., Corbett, M., Print, C. G., Owens, J. A., & Lane, M. (2013) · The FASEB Journal · doi:10.1096/fj.12-224048 · Cited by 600 · see citing works
Epigenetic inheritance of acquired traits through sperm RNAs and sperm RNA modifications
Chen, Q., Yan, W., & Duan, E. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.106 · Cited by 576 · see citing works
de Castro Barbosa, T., Ingerslev, L. R., Alm, P. S., Versteyhe, S., Massart, J., Rasmussen, M., Donkin, I., Sjögren, R., Mudry, J. M., Vetterli, L., et al. (2016) · Molecular Metabolism · doi:10.1016/j.molmet.2015.12.002 · Cited by 417 · see citing works
RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders
Grandjean, V., Fourré, S., de Abreu, D. A. F., Derieppe, M., Rémy, J., & Rassoulzadegan, M. (2015) · Scientific Reports · doi:10.1038/srep18193 · Cited by 417 · see citing works
Soares, A. R., Martins‐Marques, T., Ribeiro‐Rodrigues, T., Ferreira, J. V., Catarino, S., Pinho, M. J., Zuzarte, M., Anjo, S. I., Manadas, B. J., Sluijter, J. P. G., et al. (2015) · Scientific Reports · doi:10.1038/srep14888 · Cited by 405 · see citing works
Skinner, M., Manikkam, M., Tracey, R., Guerrero-Bosagna, C., Haque, M., & Nilsson, E. (2013) · BMC Medicine · doi:10.1186/1741-7015-11-228 · Cited by 401 · see citing works
CHILDHOOD EXPERIENCES ASSOCIATED WITH THE DEVELOPMENT OF BORDERLINE PERSONALITY DISORDER
Zanarini, M. C. (2000) · Psychiatric Clinics of North America · doi:10.1016/s0193-953x(05)70145-3 · Cited by 377 · see citing works
Epigenetic germline inheritance of diet-induced obesity and insulin resistance
Huypens, P., Sass, S., Wu, M., Dyckhoff, D., Tschöp, M., Theis, F., Marschall, S., de Angelis, M. H., & Beckers, J. (2016) · Nature Genetics · doi:10.1038/ng.3527 · Cited by 366 · see citing works
Kassaar, O., Morais, M. P. P., Xu, S., Adam, E. L., Chamberlain, R. C., Jenkins, B., James, T. D., Francis, P. T., Ward, S. G., Williams, R. J., et al. (2017) · Scientific Reports · doi:10.1038/srep45417 · Cited by 329 · see citing works
Pembrey, M., Saffery, R., Bygren, L. O., & Network in Epigenetic Epidemiology (2014) · Journal of Medical Genetics · doi:10.1136/jmedgenet-2014-102577 · Cited by 325 · see citing works
Molecular insights into transgenerational non-genetic inheritance of acquired behaviours
Bohacek, J., & Mansuy, I. M. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3964 · Cited by 318 · see citing works
Self-citationDevelopment of Maladaptive Coping: A Functional Adaptation to Chronic, Uncontrollable Stress
Wadsworth, M. (2015) · Child Development Perspectives · doi:10.1111/cdep.12112 · Cited by 289 · see citing works
Chromatin States in Mouse Sperm Correlate with Embryonic and Adult Regulatory Landscapes
Jung, Y. H., Sauria, M. E. G., Lyu, X., Cheema, M. S., Ausió, J., Taylor, J., & Corces, V. G. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.01.034 · Cited by 288 · see citing works
Multigenerational epigenetic adaptation of the hepatic wound-healing response
Zeybel, M., Hardy, T., Wong, Y. K., Mathers, J. C., Fox, C. R., Gackowska, A., Oakley, F., Burt, A. D., Wilson, C. L., Anstee, Q. M., et al. (2012) · Nature Medicine · doi:10.1038/nm.2893 · Cited by 279 · see citing works
The neuropsychology of borderline personality disorder: A meta-analysis and review
Ruocco, A. C. (2005) · Psychiatry Research · doi:10.1016/j.psychres.2005.07.004 · Cited by 274 · see citing works
Saben, J. L., Boudoures, A. L., Shyr, Z. A., Thompson, A. S., Drury, A. M., Zhang, W., Chi, M. M.-Y., Cusumano, A., Scheaffer, S. M., & Moley, K. H. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.05.065 · Cited by 266 · see citing works
Manikkam, M., Haque, M. M., Guerrero‐Bosagna, C., Nilsson, E. E., & Skinner, M. K. (2014) · PLoS ONE · doi:10.1371/journal.pone.0102091 · Cited by 247 · see citing works
Padmanabhan, N., Jia, D., Geary-Joo, C., Wu, X., Ferguson‐Smith, A. C., Fung, E., Bieda, M. C., Snyder, F. F., Gravel, R. A., Cross, J. C., et al. (2013) · Cell · doi:10.1016/j.cell.2013.09.002 · Cited by 245 · see citing works
Govorko, D., Bekdash, R. A., Zhang, C., & Sarkar, D. K. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.04.006 · Cited by 244 · see citing works
Epigenetic Mechanisms of Transmission of Metabolic Disease across Generations
Sales, V., Ferguson‐Smith, A. C., & Patti, M. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.02.016 · Cited by 242 · see citing works
Influence of Early Stress on Social Abilities and Serotonergic Functions across Generations in Mice
Franklin, T. B., Linder, N., Russig, H., Thöny, B., & Mansuy, I. M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021842 · Cited by 207 · see citing works
Self-citationBorderline Personality Disorder in Primary Care
Gross, R., Olfson, M., Gameroff, M. J., Shea, S. A., Feder, A., Fuentes, M. A., Lantigua, R., & Weissman, M. M. (2002) · Archives of Internal Medicine · doi:10.1001/archinte.162.1.53 · Cited by 197 · see citing works
Genetics of borderline personality disorder: Systematic review and proposal of an integrative model
Amad, A., Ramoz, N., Thomas, P., Jardri, R., & Gorwood, P. A. P. M. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.01.003 · Cited by 190 · see citing works
Epigenetic transgenerational inheritance
Skinner, M. K. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.206 · Cited by 184 · see citing works
Potential of Environmental Enrichment to Prevent Transgenerational Effects of Paternal Trauma
Gapp, K., Bohacek, J., Grossmann, J., Brunner, A. M., Manuella, F., Nanni, P., & Mansuy, I. M. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.87 · Cited by 172 · see citing works
Self-citationEarly life stress in fathers improves behavioural flexibility in their offspring
Gapp, K., Soldado-Magraner, S., Álvarez-Sánchez, M., Bohacek, J., Vernaz, G., Shu, H., Franklin, T. B., Wolfer, D. P., & Mansuy, I. M. (2014) · Nature Communications · doi:10.1038/ncomms6466 · Cited by 170 · see citing works
Self-citationWeber-Stadlbauer, U., Richetto, J., Labouesse, M. A., Bohacek, J., Mansuy, I. M., & Meyer, U. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.41 · Cited by 170 · see citing works
Self-citationInheritable Effect of Unpredictable Maternal Separation on Behavioral Responses in Mice
Weiss, I. C., Franklin, T. B., Vizi, S., & Mansuy, I. M. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00003 · Cited by 169 · see citing works
Self-citationSchmahl, C., Herpertz, S. C., Bertsch, K., Ende, G., Flor, H., Kirsch, P., Lis, S., Meyer-Lindenberg, A., Rietschel, M., Schneider, M., et al. (2014) · Borderline Personality Disorder and Emotion Dysregulation · doi:10.1186/2051-6673-1-12 · Cited by 168 · see citing works
Environmentally induced epigenetic transgenerational inheritance of disease susceptibility
Nilsson, E. E., & Skinner, M. K. (2014) · Translational research · doi:10.1016/j.trsl.2014.02.003 · Cited by 149 · see citing works
Ancestral perinatal obesogen exposure results in a transgenerational thrifty phenotype in mice
Chamorro-García, R., Díaz-Castillo, C., Shoucri, B. M., Kaech, H., Leavitt, R., Shioda, T., & Blumberg, B. (2017) · Nature Communications · doi:10.1038/s41467-017-01944-z · Cited by 148 · see citing works
Transgenerational Inheritance of Glucose Intolerance in a Mouse Model of Neonatal Overnutrition
Pentinat, T., Ramon‐Krauel, M., Cebrià, J., Díaz, R., & Jiménez‐Chillarón, J. C. (2010) · Endocrinology · doi:10.1210/en.2010-0684 · Cited by 141 · see citing works
McBirney, M., King, S. E., Pappalardo, M., Houser, E., Unkefer, M. K., Nilsson, E. E., Sadler‐Riggleman, I., Beck, D., Winchester, P., & Skinner, M. K. (2017) · PLoS ONE · doi:10.1371/journal.pone.0184306 · Cited by 140 · see citing works
The Children of Mentally Ill Parents
Mattejat, F., & Remschmidt, H. (2008) · Deutsches Ärzteblatt international · doi:10.3238/arztebl.2008.0413 · Cited by 134 · see citing works
Choi, C. S., Gonzales, E. L., Kim, K. C., Yang, S. M., Kim, J., Mabunga, D. F. N., Cheong, J. H., Han, S., Bahn, G. H., & Shin, C. Y. (2016) · Scientific Reports · doi:10.1038/srep36250 · Cited by 130 · see citing works
Epigenetic Transgenerational Inheritance of Altered Sperm Histone Retention Sites
Maamar, M. B., Sadler‐Riggleman, I., Beck, D., & Skinner, M. K. (2018) · Scientific Reports · doi:10.1038/s41598-018-23612-y · Cited by 129 · see citing works
Moisiadis, V. G., Constantinof, A., Kostaki, A., Szyf, M., & Matthews, S. G. (2017) · Scientific Reports · doi:10.1038/s41598-017-11635-w · Cited by 122 · see citing works
Bohacek, J., Farinelli, M., Mirante, O., Steiner, G., Gapp, K., Coiret, G., Ebeling, M., Durán-Pacheco, G., Iniguez, A. L., Manuella, F., et al. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.80 · Cited by 111 · see citing works
Self-citationSocial Interaction in Borderline Personality Disorder
Lis, S., & Bohus, M. (2013) · Current Psychiatry Reports · doi:10.1007/s11920-012-0338-z · Cited by 108 · see citing works
Farr, O. M., Sloan, D. M., Keane, T. M., & Mantzoros, C. S. (2014) · Metabolism · doi:10.1016/j.metabol.2014.08.009 · Cited by 80 · see citing works
Chen, J., Wu, S., Wen, S., Shen, L., Peng, J., Yan, C., Cao, X., Zhou, Y., Long, C., Lin, T., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0126403 · Cited by 78 · see citing works
Hao, C., Gély-Pernot, A., Kervarrec, C., Boudjema, M., Becker, E., Khil, P. P., Tevosian, S. G., Jégou, B., & Smagulova, F. O. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw840 · Cited by 71 · see citing works
Association of Posttraumatic Stress Disorder With Increased Prevalence of Metabolic Syndrome
Jin, H., Lanouette, N. M., Mudaliar, S. R. D., Henry, R. R., Folsom, D. P., Khandrika, S., Glorioso, D., & Jeste, D. V. (2009) · Journal of Clinical Psychopharmacology · doi:10.1097/jcp.0b013e3181a45ed0 · Cited by 67 · see citing works
Kahl, K. G., Greggersen, W., Schweiger, U., Cordes, J., Correll, C. U., Frieling, H., Balijepalli, C., Lösch, C., & Moebus, S. (2012) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-012-0339-2 · Cited by 66 · see citing works
Beck, D., Sadler‐Riggleman, I., & Skinner, M. K. (2017) · Current Zoology · doi:10.1093/eep/dvx016 · Cited by 64 · see citing works
Stress transgenerationally programs metabolic pathways linked to altered mental health
Kiss, D., Ambeskovic, M., Montina, T., & Metz, G. A. S. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2272-4 · Cited by 52 · see citing works
Transgenerational effects of obesity and malnourishment on diabetes risk in F2 generation
Hanafi, M. Y., Saleh, M. M., Saad, M. I., Abdelkhalek, T. M., & Kamel, M. A. E.-N. (2015) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-015-2633-6 · Cited by 50 · see citing works
Brain metabolic alterations in mice subjected to postnatal traumatic stress and in their offspring
Gapp, K., Corcoba, A., van Steenwyk, G., Mansuy, I. M., & Duarte, J. M. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16667525 · Cited by 48 · see citing works
Self-citationKinder psychisch kranker Eltern
Gehrmann, J., & Sumargo, S. (2009) · Monatsschrift Kinderheilkunde · doi:10.1007/s00112-009-1971-4 · Cited by 35 · see citing works
Transgenerational inheritance of susceptibility to diabetes-induced male subfertility
Pavlínková, G., Margaryan, H., Žatecká, E., Valášková, E., Elzeinová, F., Kubátová, A., Bohuslavová, R., & Pěknicová, J. (2017) · Scientific Reports · doi:10.1038/s41598-017-05286-0 · Cited by 35 · see citing works
Borderline personality and the pain paradox.
Sansone, R. A., & Sansone, L. A. (2007) · PubMed · Cited by 27 · see citing works
Odacı, H., & Çelik, Ç. B. (2017) · Journal of Interpersonal Violence · doi:10.1177/0886260517696862 · Cited by 23 · see citing works
Eaton, S. A., Aiken, A., Young, P. E., Ho, J. W. K., Cropley, J. E., & Suter, C. M. (2017) · International Journal of Obesity · doi:10.1038/ijo.2017.247 · Cited by 7 · see citing works
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- [23]Skinner MK, Manikkam M, Tracey R, Nilsson E, Haque MM, Guerrero-Bosagna C. Ancestral DDT exposures promote epigenetic transgenerational inheritance of obesity. BMC Med 2013; 11: 228. 24228800 PMC3853586
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Epigenetic Transgenerational Inheritance of Obesity Susceptibility
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Health inequities and the inappropriate use of race in nephrology
Eneanya, N. D., Boulware, L. E., Tsai, J., Bruce, M. A., Ford, C. L., Harris, C., Morales, L. S., Ryan, M. J., Reese, P. P., Thorpe, R. J., et al. (2022) · Nature Reviews Nephrology · doi:10.1038/s41581-021-00501-8 · Cited by 140 · see citing works
Epigenetic-sensitive pathways in personalized therapy of major cardiovascular diseases
Schiano, C., Benincasa, G., Franzese, M., Mura, N. D., Pane, K., Salvatore, M., & Claudio Napoli, A. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107514 · Cited by 136 · see citing works
Silva, L. B. A. R., Castro, N., Novaes, G. M., Pascoal, G. D. F. L., & Ong, T. P. (2019) · Food Research International · doi:10.1016/j.foodres.2019.108646 · Cited by 116 · see citing works
Impact of Parental Exposure on Offspring Health in Humans
Jawaid, A., Jehle, K.-L., & Mansuy, I. M. (2020) · Trends in Genetics · doi:10.1016/j.tig.2020.10.006 · Cited by 103 · see citing works
Self-citationMatheson, K., Seymour, A. M., Landry, J., Ventura, K., Arsenault, E., & Anisman, H. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19116455 · Cited by 88 · see citing works
Citric acid and itaconic acid accumulation: variations of the same story?
Karaffa, L., & Kubicek, C. (2019) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-018-09607-9 · Cited by 62 · see citing works
Brewerton, T. D. (2022) · Journal of Eating Disorders · doi:10.1186/s40337-022-00696-6 · Cited by 71 · see citing works
Zhou, A., & Ryan, J. (2023) · Genes · doi:10.3390/genes14081639 · Cited by 57 · see citing works
Braz, C. U., Taylor, T., Namous, H., Townsend, J. A., Crenshaw, T. D., & Khatib, H. (2022) · PNAS Nexus · doi:10.1093/pnasnexus/pgac040 · Cited by 49 · see citing works
Involvement of circulating factors in the transmission of paternal experiences through the germline
van Steenwyk, G., Gapp, K., Jawaid, A., Germain, P., Manuella, F., Tanwar, D. K., Zamboni, N., Gaur, N., Efimova, A., Thumfart, K. M., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2020104579 · Cited by 48 · see citing works
Self-citationTransgenerational epigenetic inheritance of traumatic experience in mammals
Švorcová, J. (2023) · Genes · doi:10.3390/genes14010120 · Cited by 47 · see citing works
Paternal transgenerational epigenetic mechanisms mediating stress phenotypes of offspring
Cunningham, A. M., Walker, D. M., & Nestler, E. J. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14582 · Cited by 48 · see citing works
Racial disparities in pregnancy outcomes: genetics, epigenetics, and allostatic load
Leimert, K. B., & Olson, D. M. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2019.12.003 · Cited by 41 · see citing works
Mapping the past, present and future research landscape of paternal effects
Rutkowska, J., Lagisz, M., Russell Bonduriansky, A., & Nakagawa, S. (2020) · BMC Biology · doi:10.1186/s12915-020-00892-3 · Cited by 38 · see citing works
Epigenetic effects of paternal environmental exposures and experiences on offspring phenotypes
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Steele, E., Gorczynski, R. M., Lindley, R., Liu, Y.-S., Temple, R., Tokoro, G., Wickramasinghe, D. T., & Wickramasinghe, N. (2019) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2019.08.010 · Cited by 35 · see citing works
Dı́az, F., Kuijper, B., Hoyle, R. B., Talamantes, N., Coleman, J. M., & Matzkin, L. M. (2020) · Functional Ecology · doi:10.1111/1365-2435.13704 · Cited by 33 · see citing works
On the role of epigenetic modifications of HPA axis in posttraumatic stress disorder and resilience
Khan, Z., Messiri, N. E., Iqbal, E., Hassan, H., Tanweer, M. S., Sadia, S. R., Taj, M., Zaidi, U., Yusuf, K., Syed, N. I., et al. (2025) · Journal of Neurophysiology · doi:10.1152/jn.00345.2024 · Cited by 32 · see citing works
Natural cryptic variation in epigenetic modulation of an embryonic gene regulatory network
Ewe, C. K., Cleuren, Y. N. T., Flowers, S. E., Alok, G., Snell, R. G., & Rothman, J. H. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1920343117 · Cited by 27 · see citing works
Boscardin, C., Manuella, F., & Mansuy, I. M. (2022) · Current Zoology · doi:10.1093/eep/dvac024 · Cited by 29 · see citing works
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The active role of spermatozoa in transgenerational inheritance
Sciamanna, I., Serafino, A., Shapiro, J. A., & Spadafora, C. (2019) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2019.1263 · Cited by 27 · see citing works
Thorson, J. L. M., Beck, D., Maamar, M. B., Nilsson, E. E., McBirney, M., & Skinner, M. K. (2020) · PLoS ONE · doi:10.1371/journal.pone.0239380 · Cited by 26 · see citing works
The Ancestral Environment Shapes Antiviral CD8+ T cell Responses across Generations
Post, C. M., Boulé, L. A., Burke, C. G., O’Dell, C., Winans, B., & Lawrence, B. P. (2019) · iScience · doi:10.1016/j.isci.2019.09.014 · Cited by 22 · see citing works
Hoffmann, L. B., Li, B., Zhao, Q., Wei, W., Leighton, L. J., Bredy, T. W., Pang, T. Y., & Hannan, A. J. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02350-2 · Cited by 21 · see citing works
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Brass, K. E., Herndon, N., Gardner, S. A., Grindstaff, J. L., & Polly Campbell, A. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104806 · Cited by 19 · see citing works
Transgenerational Effects of Prenatal Ethanol Exposure in Prepubescent Mice
Bottom, R. T., Kozanian, O. O., Rohac, D. J., Erickson, M. A., & Huffman, K. J. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.812429 · Cited by 19 · see citing works
Intergenerational Perioperative Neurocognitive Disorder
Ju, L.-S., Morey, T. E., Seubert, C. N., & Martynyuk, A. E. (2023) · Biology · doi:10.3390/biology12040567 · Cited by 18 · see citing works
Schafte, K., & Bruna, S. P. (2023) · Epigenetics · doi:10.1080/15592294.2023.2260218 · Cited by 16 · see citing works
Zaidan, H., Galiani, D., & Gaisler‐Salomon, I. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01220-1 · Cited by 18 · see citing works
González, C. R., & González, B. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.630948 · Cited by 16 · see citing works
What does immunology have to do with brain development and neuropsychiatric disorders?
Leckman, J. F., de Alvarenga, P. G., Salto, A. B. R., & Johnson, I. N. S. (2019) · Revista de Medicina · doi:10.11606/issn.1679-9836.v98i4p241-253 · Cited by 15 · see citing works
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 15 · see citing works
Menezes, E. D. C., Geiger, H. M., Abreu, F. F., Rachmany, L., Wilson, D. A., Alldred, M. J., Castellanos, F. X., Fu, R., Sargin, D., Corvelo, A., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02499-4 · Cited by 16 · see citing works
Hime, G. R., Stonehouse, S. L., & Pang, T. Y. (2021) · World Journal of Psychiatry · doi:10.5498/wjp.v11.i10.711 · Cited by 13 · see citing works
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 · see citing works
Self-citationZaidan, H., Wnuk, A., Aderka, I. M., Kajta, M., & Gaisler‐Salomon, I. (2023) · Stress · doi:10.1080/10253890.2023.2201325 · Cited by 15 · see citing works
Tan, J., Zhang, Z., Yan, L. L., & Xu, X. (2024) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174424000035 · Cited by 13 · see citing works
Harman, J. C., Guidry, J. J., & Gidday, J. M. (2020) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.61.11.15 · Cited by 13 · see citing works
Eyolfson, E., Bhatt, D., Wang, M., Lohman, A. W., & Mychasiuk, R. (2021) · Genes Brain & Behavior · doi:10.1111/gbb.12736 · Cited by 13 · see citing works
Teltumbade, M. R., Bhalla, A., & Sharma, A. (2019) · Genomics · doi:10.1016/j.ygeno.2019.04.008 · Cited by 13 · see citing works
Transgenerational inheritance of fetal alcohol exposure adverse effects on immune gene interferon-ϒ
Gangisetty, O., Palagani, A., & Sarkar, D. K. (2020) · Clinical Epigenetics · doi:10.1186/s13148-020-00859-9 · Cited by 13 · see citing works
The paternal contribution to shaping the health of future generations
Casciaro, C., Hamada, H., Bloise, E., & Matthews, S. G. (2024) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2024.10.007 · Cited by 13 · see citing works
Impact of mothers’ experience and early‐life stress on aggression and cognition in adult male mice
Reshetnikov, V. V., Ryabushkina, Y. A., & Bondar, N. P. (2019) · Developmental Psychobiology · doi:10.1002/dev.21887 · Cited by 12 · see citing works
Hoffmann, L. B., McVicar, E. A., Harris, R. V., Collar-Fernández, C., Clark, M. B., Hannan, A. J., & Pang, T. Y. (2023) · BMC Biology · doi:10.1186/s12915-023-01678-z · Cited by 12 · see citing works
Rimawi, I., Ornoy, A., & Yanai, J. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.05.026 · Cited by 11 · see citing works
Rice, R. C., Gil, D. V., Baratta, A. M., Frawley, R. R., Hill, S. Y., Farris, S. P., & Homanics, G. E. (2023) · Neurobiology of Stress · doi:10.1016/j.ynstr.2023.100603 · Cited by 13 · see citing works
Thivisol, U., Ho, P., Li, B., Trompke, M., Hoffmann, L. B., Hannan, A. J., & Pang, T. Y. (2023) · Neuronal Signaling · doi:10.1042/ns20220097 · Cited by 10 · see citing works
Association of Parental Famine Exposure With Offspring Depression and Cognition Function
Liu, Y., Liu, Y., Lu, Y., Li, J., & He, S. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.812805 · Cited by 10 · see citing works
Heynen, J. P., Paxman, E., Sanghavi, P., McCreary, J. K., Montina, T., & Metz, G. A. S. (2022) · Metabolites · doi:10.3390/metabo12070572 · Cited by 10 · see citing works
Epigenetic mechanisms in maternal-fetal crosstalk: inter- and trans-generational inheritance
Tisato, V., D’Aversa, E., Salvatori, F., Sbracia, M., Peluso, G., Scarpellini, F., & Gemmati, D. (2025) · Epigenomics · doi:10.1080/17501911.2025.2568369 · Cited by 11 · see citing works
Challenging dogmas: How transgenerational epigenetics reshapes our views on life
Wang, H. D., & Allard, P. (2021) · Journal of Experimental Zoology Part A Ecological and Integrative Physiology · doi:10.1002/jez.2465 · Cited by 9 · see citing works
Addressing Structural Racism in Pediatric Clinical Practice
Laster, M. L., Kozman, D., & Norris, K. C. (2023) · Pediatric Clinics of North America · doi:10.1016/j.pcl.2023.03.010 · Cited by 9 · see citing works
Jawaid, A., Gomolka, M., Tomaszewska, W., Kunzi, M., Mansoor, M., Przybys, J., Gbadamosi, I., Maloburska, A., Khan, Z. Y., Hidayat, T., et al. (2020) · medRxiv · doi:10.1101/2020.08.11.20168393 · Cited by 8 · see citing works
Self-citationHuitzil, S., Huepe, C., Aldana, M., & Frank, A. (2023) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2023.1279938 · Cited by 11 · see citing works
Cardiometabolic disease management: influences from epigenetics
Atzemian, N., Mohammed, S. A., Venanzio, L. D., Gorica, E., Costantino, S., Ruschitzka, F. T., & Paneni, F. (2025) · Epigenomics · doi:10.1080/17501911.2025.2489921 · Cited by 8 · see citing works
Transgenerational Epigenetic DNA Methylation Editing and Human Disease
Tompkins, J. D. (2023) · Biomolecules · doi:10.3390/biom13121684 · Cited by 10 · see citing works
Mew, E. J., Nyhan, K., Bonumwezi, J., Blas, V., Gorman, H., Hennein, R., Quach, K., Shabanova, V., Hawley, N. L., & Lowe, S. R. (2022) · PLoS ONE · doi:10.1371/journal.pone.0276753 · Cited by 8 · see citing works
Eaton, S. A., Aiken, A., Young, P. E., Ho, J. W. K., Cropley, J. E., & Suter, C. M. (2017) · International Journal of Obesity · doi:10.1038/ijo.2017.247 · Cited by 7 · see citing works
Stress and its effects across generations
Engmann, O., & Mansuy, I. M. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813983-7.00018-5 · Cited by 7 · see citing works
Self-citationThe relevance of a rodent cohort in the Consortium on Individual Development
van der Veen, R., Bonapersona, V., & Joëls, M. (2020) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2020.100846 · Cited by 6 · see citing works
Belmonte, K. C. D., Holmgren, E. B., Wills, T. A., & Gidday, J. M. (2022) · Alzheimer s & Dementia · doi:10.1002/alz.12616 · Cited by 6 · see citing works
Freire, T., Pulpitel, T., Clark, X., Mackay, F., Raubenheimer, D., Simpson, S. J., Solon‐Biet, S. M., & Crean, A. J. (2024) · Physiology & Behavior · doi:10.1016/j.physbeh.2024.114533 · Cited by 6 · see citing works
Early life stress shifts critical periods and causes precocious visual cortex development
Poplawski, J., Montina, T., & Metz, G. A. S. (2024) · PLoS ONE · doi:10.1371/journal.pone.0316384 · Cited by 7 · see citing works
Effects of noninherited ancestral genotypes on offspring phenotypes†
Cullen, S. M., Hassan, N. A., & Smith-Raska, M. (2021) · Biology of Reproduction · doi:10.1093/biolre/ioab120 · Cited by 6 · see citing works
Epigenetic modifications and transgenerational inheritance in women victims of violence (EWVV)
Gemmati, D., Villanova, M., Scarpellini, F., Milani, D., Cecchi, R., Singh, A. V., Gaudio, R. M., & Tisato, V. (2025) · Current Zoology · doi:10.1093/eep/dvaf025 · Cited by 8 · see citing works
Post-genomics, Evo-Devo and the recurrence of teleologic thought†
Layer, P. G. (2022) · BioCosmos · doi:10.2478/biocosmos-2022-0002 · Cited by 5 · see citing works
Benoit, S., Henry, M. S., Fneich, S., Mathou, A., Xia, L., Foury, A., Jouin, M., Junien, C., Capuron, L., Jouneau, L., et al. (2023) · Frontiers in Nutrition · doi:10.3389/fnut.2023.1190392 · Cited by 5 · see citing works
Epigenetic inheritance of metabolic signals
van Steenwyk, G., Jawaid, A., & Mansuy, I. M. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-816843-1.00011-4 · Cited by 4 · see citing works
Self-citationEpigenetics and the Impact of Early-Life Stress Across Generations
van Steenwyk, G., & Mansuy, I. M. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-813156-5.00029-7 · Cited by 4 · see citing works
Self-citationEpigenetic inheritance of phenotypes associated with parental exposure to cocaine
Rich, M. T., Swinford-Jackson, S. E., & Pierce, R. C. (2023) · Advances in pharmacology · doi:10.1016/bs.apha.2023.10.004 · Cited by 3 · see citing works
Paternal adverse childhood experiences are associated with a low risk of atopy in the offspring
Puosi, E., Karlsson, H., Lukkarinen, H., Karlsson, L., & Lukkarinen, M. M. (2024) · Acta Paediatrica · doi:10.1111/apa.17345 · Cited by 3 · see citing works
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 · see citing works
Campbell, T. S., & Roth, T. L. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-821785-6.00013-x · Cited by 3 · see citing works
Hannan, A. J. (2020) · The EMBO Journal · doi:10.15252/embj.2020107014 · Cited by 3 · see citing works
Therapeutic Potential of Dietary Polyphenols
Stockert, A., & Hall, S. (2021) · IntechOpen eBooks · doi:10.5772/intechopen.99177 · Cited by 3 · see citing works
Karaburun, M. (2025) · Psikiyatride Guncel Yaklasimlar - Current Approaches in Psychiatry · doi:10.18863/pgy.1694859 · Cited by 2 · see citing works
Snyder, S. W., Meyer, W. C., Jorgenson, S. L., Contreras, E. B., Bland, T., & Cresko, W. A. (2026) · Journal of Evolutionary Biology · doi:10.1093/jeb/voag024 · Cited by 2 · see citing works
Iribarne, J., Brachetta, V., Kittlein, M. J., Schleich, C. E., & Zenuto, R. R. (2023) · Animal Cognition · doi:10.1007/s10071-023-01822-w · Cited by 3 · see citing works
Vázquez-Sánchez, A., Rodríguez‐Ríos, D., Colín‐Castelán, D., Molina‐Torres, J., Ramı́rez-Chávez, E., Romo-Morales, G. D. C., Zaina, S., & Lund, G. (2024) · PLoS ONE · doi:10.1371/journal.pone.0300141 · Cited by 2 · see citing works
Natural cryptic variation in epigenetic modulation of an embryonic gene regulatory networkPreprint
Ewe, C. K., Cleuren, Y. N. T., Flowers, S. E., Alok, G., Snell, R. G., & Rothman, J. H. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/831099 · Cited by 2 · see citing works
Džaferović, N., & Ašić, A. (2026) · Mammalian Genome · doi:10.1007/s00335-025-10192-2 · Cited by 1 · see citing works
Mendes, R. S. (2024) · Cosmological and Astrobiological Review Journal for the Study of the Universe Life and the Natural Sciences · doi:10.65932/car-2024-1-5 · Cited by 1 · see citing works
Jawaid, A., & Mansuy, I. M. (2021) · Nomos Verlagsgesellschaft mbH & Co. KG eBooks · doi:10.5771/9783748927242-277 · Cited by 1 · see citing works
Self-citationBroyles, E., Corell, D. H., & Gidday, J. M. (2023) · Behavioral Neuroscience · doi:10.1037/bne0000554 · Cited by 1 · see citing works
Epigenetic Inheritance and the Environment
Jablonka, E. (2024) · Springer eBooks · doi:10.1007/978-3-031-61187-2_5 · Cited by 1 · see citing works
Early Life Stress Accelerates Critical Periods and Causes Precocious Visual Cortex DevelopmentPreprint
Poplawski, J., Montina, T., & Metz, G. A. S. (2023) · Research Square · doi:10.21203/rs.3.rs-2715680/v1 · Cited by 1 · see citing works
The Influence of Maternal and Social Factors During Intrauterine Life
Santurtún, A., Riancho, J., & Riancho, J. A. (2019) · Springer eBooks · doi:10.1007/978-981-13-7256-8_8 · Cited by 1 · see citing works
Race in the social-epigenomic regulation of pre- and perinatal development
Lane, R. H., Majnik, A. V., & Segar, J. L. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-816843-1.00009-6
Brass, K. E. (2019) · SHAREOK (University of Oklahoma; Oklahoma State University; Central Oklahoma University)
Evo-Devo – das Beste aus zwei Welten
Lange, A. (2020) · Springer eBooks · doi:10.1007/978-3-662-60915-6_3
吴春旺, 韩阳, 邓志姣, 李虹轶, 陈平形, & 李承祖 (2011) · 理论物理通讯:英文版
Hoffmann, L. B., McVicar, E. A., Harris, R. V., Collar-Fernández, C., Clark, M. B., Hannan, A. J., & Pang, T. Y. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.09.495572
Healing Inherited Wounds: Transgenerational Trauma Therapy
Drexler, K. (2023) · Springer eBooks · doi:10.1007/978-3-031-43748-9_9
Evo-Devo – das Beste aus zwei Welten
Lange, A. (2024) · Springer eBooks · doi:10.1007/978-3-662-68962-2_3
Correa-Navarro, V. A., Romo-Morales, G. D. C., Sánchez-Palafox, J. E., Rodríguez‐Ríos, D., Molina‐Torres, J., Ramı́rez-Chávez, E., Zaina, S., & Lund, G. (2024) · Journal of Lipids · doi:10.1155/jl/3351340
When Women Lead in Global Health: Alternative Mobilizations
Alonso, C., Torres, I., & Profeta, B. (2024) · Sustainable development goals series · doi:10.1007/978-3-031-53793-6_21
- Authors
- van Steenwyk, G., Roszkowski, M., Manuella, F., Franklin, T. B., & Mansuy, I. M.
- Affiliations
- Laboratory of Neuroepigenetics, Brain Research Institute, Faculty of Medicine, University of Zurich & Institute for Neuroscience, Department of Health Science and Technology, ETH Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland
- University of Zurich (CH)
- Dalhousie University (CA)
- Corresponding author
- Mansuy, Isabelle M
- ORCID
- Venue
- Environmental Epigenetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2018-04-01
- Volume
- 4
- Issue
- 2
- Pages
- dvy023-dvy023
- ISSN
- 1674-5507 (ISSN-L)
- 2058-5888
- PMC
- PMC6190267
- OpenAlex
- W2897521748
- Cited by
- 116
- References
- 62
- Citations by year
- 2026: 9 · 2025: 11 · 2024: 14 · 2023: 20 · 2022: 12 · 2021: 12 · 2020: 17 · 2019: 19 · 2017: 1
- FWCI
- 13.25
- Type
- journal article
- Language
- en
- Open access
- diamond
- doi.org
- Licence
- Locations
- Current Zoology (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, cc-by-nc)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by-nc)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by-nc)
- ETH Zürich Research Collection
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- National Science Foundation
- Novartis Foundation
- Branco Weiss Fellowship – Society in Science
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Fondation pour la Recherche Médicale
- Novartis Stiftung für Medizinisch-Biologische Forschung
- Universität Zürich
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- transgenerational epigenetic inheritance, postpartum stress, depression-like behavior, risk-taking, glucose dysregulation, metabolic phenotypes, behavioral phenotypes, intergenerational transmission
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