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.
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
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?
Multigenerational early-life stress models demonstrate enduring regulatory and behavioral variation, including depressive-like behaviors and altered responses to environmental novelty.
“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]
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.
“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]
Enduring behavioral responses to stress and epigenetic alterations in adult offspring have been demonstrated to be mediated by changes in gametes, in utero effects, variations in early postnatal care, and/or other early life experiences influenced by parental exposure.
“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]
Epigenetic effects in maternal or paternal gametes are a potential explanation for epigenetic effects in offspring, but blood samples will not permit ascertainment of gamete-dependent transmission.
“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]
Early-life postnatal adversity in animal models can persistently affect behavior across generations and DNA methylation in the germline.
“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.
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 · see citing works
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 · see citing works
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 · see citing works
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 3,462 · see citing works
DNA methylation and human disease
Robertson, K. D. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1655 · Cited by 2,864 · 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
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 · see citing works
Environmental epigenomics and disease susceptibility
Jirtle, R. L., & Skinner, M. K. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2045 · Cited by 2,492 · see citing works
Weber, M., Hellmann, I., Stadler, M. B., Ramos, L., Pääbo, S., Rebhan, M., & Schübeler, D. (2007) · Nature Genetics · doi:10.1038/ng1990 · Cited by 2,267 · see citing works
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 · 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
Epigenetic regulation in psychiatric disorders
Tsankova, N., Renthal, W., Kumar, A., & Nestler, E. J. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2132 · Cited by 1,400 · see citing works
Lasting epigenetic influence of early-life adversity on the BDNF gene
Roth, T. L., Lubin, F. D., Funk, A. J., & Sweatt, J. D. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.11.028 · Cited by 1,273 · see citing works
Maternal care, hippocampal synaptogenesis and cognitive development in rats
Liu, D., Diorio, J., Day, J. C., Francis, D. D., & Meaney, M. J. (2000) · Nature Neuroscience · doi:10.1038/77702 · Cited by 1,195 · see citing works
Dynamic DNA methylation programs persistent adverse effects of early-life stress
Murgatroyd, C., Patchev, A. V., Wu, Y., Micale, V., Bockmühl, Y., Fischer, D., Holsboer, F., Wotjak, C. T., Almeida, O. F. X., & Spengler, D. (2009) · Nature Neuroscience · doi:10.1038/nn.2436 · Cited by 1,162 · see citing works
Sex-specific, male-line transgenerational responses in humans
The ALSPAC Study Team, Pembrey, M. E., Bygren, L. O., Kaati, G., Edvinsson, S., Northstone, K., Sjöström, M., & Golding, J. (2006) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5201538 · Cited by 1,150 · see citing works
The Dutch Famine and Its Long-Term Consequences for Adult Health
Roseboom, T., de Rooij, S., & Painter, R. (2006) · Early Human Development · doi:10.1016/j.earlhumdev.2006.07.001 · Cited by 1,137 · see citing works
SÁNCHEZ, M. M., LADD, C. O., & PLOTSKY, P. M. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003029 · Cited by 1,003 · see citing works
Cyclical DNA methylation of a transcriptionally active promoter
Métivier, R., Gallais, R., Tiffoche, C., Péron, C. L., Jurkowska, R., Carmouche, R. P., Ibberson, D., Baráth, P., Demay, F., Reid, G., et al. (2008) · Nature · doi:10.1038/nature06544 · Cited by 942 · see citing works
DNA hypomethylation and human diseases
Wilson, A. S., Power, B. E., & Molloy, P. L. (2007) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2006.08.007 · Cited by 804 · see citing works
Transgeneration memory of stress in plants
Molinier, J., Ries, G., Zipfel, C., & Höhn, B. (2006) · Nature · doi:10.1038/nature05022 · Cited by 675 · see citing works
DNA methylation analysis by pyrosequencing
Tost, J., & Gut, I. G. (2007) · Nature Protocols · doi:10.1038/nprot.2007.314 · Cited by 665 · see citing works
Research and treatment approaches to depression
Wong, M.-L., & Licinio, J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35072566 · Cited by 656 · see citing works
Rakyan, V. K., Chong, S., Blewitt, M. E., Cuthbert, P. C., Morgan, H. D., Luu, K. V. K., & Whitelaw, E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0436776100 · Cited by 642 · see citing works
Cryan, J. F., & Mombereau, C. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001457 · Cited by 616 · see citing works
Evidence That DNA (Cytosine-5) Methyltransferase Regulates Synaptic Plasticity in the Hippocampus
Levenson, J. M., Roth, T. L., Lubin, F. D., Miller, C. A., Huang, I.-C., Desai, P., Malone, L. M., & Sweatt, J. D. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m511767200 · Cited by 615 · see citing works
Epigenetic mechanisms in neurological diseases: genes, syndromes, and therapies
Urdinguio, R. G., Sanchez-Mut, J. V., & Esteller, M. (2009) · The Lancet Neurology · doi:10.1016/s1474-4422(09)70262-5 · Cited by 581 · see citing works
Variations in maternal care in infancy regulate the development of stress reactivity
Caldji, C., Diorio, J. C., & Meaney, M. J. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01084-2 · Cited by 574 · see citing works
5-HT1A receptor function in major depressive disorder
Savitz, J. B., Lucki, I., & Drevets, W. C. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.01.009 · Cited by 573 · see citing works
DNA Methylation Analysis by Pyrosequencing
Busato, F., & Tost, J. (2014) · Springer eBooks · doi:10.1007/978-1-4614-6418-1_799-1 · Cited by 500 · see citing works
Pryce, C. R., Rüedi‐Bettschen, D., Dettling, A. C., Weston, A. A., Russig, H. D., Ferger, B., & Feldon, J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.011 · Cited by 414 · see citing works
Self-citationMillstein, R. A., & Holmes, A. (2007) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.05.003 · Cited by 407 · see citing works
Stress, genes and the mechanism of programming the brain for later life
de Kloet, E. R., Sibug, R. M., Helmerhorst, F. M., & Schmidt, M. V. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.10.008 · Cited by 370 · see citing works
Epigenetic programming of stress responses through variations in maternal care
FISH, E. W., SHAHROKH, D., BAGOT, R., CALDJI, C., BREDY, T., SZYF, M., & MEANEY, M. J. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1330.011 · Cited by 361 · see citing works
Epigenomics: beyond CpG islands
Fazzari, M. J., & Greally, J. M. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1349 · Cited by 352 · see citing works
Sterba, S. K., Prinstein, M. J., & Cox, M. J. (2007) · Development and Psychopathology · doi:10.1017/s0954579407070174 · Cited by 316 · see citing works
Early life genetic, epigenetic and environmental factors shaping emotionality in rodents
Holmes, A., Guisquet, A. M. L., Vogel, E., Millstein, R. A., Leman, S., & Belzung, C. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.012 · Cited by 296 · see citing works
Understanding the potency of stressful early life experiences on brain and body function
McEwen, B. S. (2008) · Metabolism · doi:10.1016/j.metabol.2008.07.006 · Cited by 260 · see citing works
de Kloet, E. R. (2003) · PubMed · Cited by 255 · see citing works
Epigenetic inheritance in the mouse
Römer, I., Reik, W., Dean, W., & Klose, J. (1997) · Current Biology · doi:10.1016/s0960-9822(06)00124-2 · Cited by 248 · see citing works
Stress sensitivity and the development of affective disorders
Bale, T. L. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.033 · Cited by 245 · see citing works
Mammalian cytosine methylation at a glance
Ooi, S. K. T., O’Donnell‐Luria, A., & Bestor, T. H. (2009) · Journal of Cell Science · doi:10.1242/jcs.015123 · Cited by 241 · see citing works
Epigenetic germline inheritance
Chong, S., & Whitelaw, E. (2004) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2004.09.001 · Cited by 239 · see citing works
Griebel, G., Belzung, C., Misslin, R., & Vogel, E. (1993) · Behavioural Pharmacology · doi:10.1097/00008877-199312000-00009 · Cited by 239 · see citing works
Sex, trauma, stress hormones and depression
Young, E., & Korszun, A. (2010) · Molecular Psychiatry · doi:10.1038/mp.2009.94 · Cited by 235 · see citing works
McGill, B. E., Bundle, S. F., Yaylaoglu, M., Carson, J. P., Christina Thaller, B., & Zoghbi, H. Y. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608702103 · Cited by 229 · see citing works
Monoamine Oxidase Inhibitors:A Modern Guide to an Unrequited Class of Antidepressants
Stahl, S. M., & Felker, A. (2008) · CNS Spectrums · doi:10.1017/s1092852900016965 · Cited by 191 · see citing works
Bifulco, A. T., Moran, P. M., Ball, C., Jacobs, C., Baines, R., Bunn, A., & Cavagin, J. (2002) · Journal of Child Psychology and Psychiatry · doi:10.1111/1469-7610.00234 · Cited by 189 · see citing works
Nilsson, E. E., Anway, M. D., Stanfield, J., & Skinner, M. K. (2008) · Reproduction · doi:10.1530/rep-07-0542 · Cited by 184 · see citing works
Epigenetic Inheritance and the Intergenerational Transfer of Experience.
Harper, L. V. (2005) · Psychological Bulletin · doi:10.1037/0033-2909.131.3.340 · Cited by 171 · see citing works
Bale, T. L., & Vale, W. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-12-05295.2003 · Cited by 169 · see citing works
Cameron, N. M., Shahrokh, D. K., Corpo, A. D., Dhir, S. K., Moshe Szyf, A., Champagne, F. A., & Meaney, M. J. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01725.x · Cited by 167 · see citing works
Behavioural and Neurochemical Consequences of Early Weaning in Rodents
Kikusui, T., & Mori, Y. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01837.x · Cited by 158 · see citing works
Pelleymounter, M. A., Joppa, M. A., LING, N. C., & Foster, A. C. (2002) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.302.1.145 · Cited by 147 · see citing works
Epigenetics in spermatogenesis
Trasler, J. M. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.12.018 · Cited by 145 · see citing works
Kim, H. K., Capaldi, D. M., Pears, K. C., Kerr, D., & Owen, L. D. (2009) · Criminal Behaviour and Mental Health · doi:10.1002/cbm.708 · Cited by 126 · see citing works
Gamete imprinting: setting epigenetic patterns for the next generation
Trasler, J. M. (2005) · Reproduction Fertility and Development · doi:10.1071/rd05118 · Cited by 124 · see citing works
Pelleymounter, M. A., Joppa, M. A., Ling, N., & Foster, A. C. (2004) · Peptides · doi:10.1016/j.peptides.2004.01.008 · Cited by 110 · see citing works
Godmann, M., Lambrot, R., & Kimmins, S. (2009) · Microscopy Research and Technique · doi:10.1002/jemt.20715 · Cited by 109 · see citing works
Hinshaw, S. P. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1301.016 · Cited by 103 · see citing works
Marco, E. M., Adriani, W., Llorente, R., Giovanni Laviola, A., & Viveros, M. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.03.008 · Cited by 95 · see citing works
DNA Methylation: Its Role in Cancer Development and Therapy
Kurkjian, C. D., Kummar, S., & Murgo, A. J. (2008) · Current Problems in Cancer · doi:10.1016/j.currproblcancer.2008.08.002 · Cited by 79 · see citing works
Evidence for Transgenerational Transmission of Epigenetic Tumor Susceptibility in Drosophila
Xing, Y., Shi, S., Le, L. X., Lee, C. A., Silver-Morse, L., & Li, W. X. (2007) · PLoS Genetics · doi:10.1371/journal.pgen.0030151 · Cited by 78 · see citing works
Role of psychological trauma in the cause and treatment of anxiety and depressive disorders
Laugharne, J. D. E., Lillee, A., & Janča, A. (2009) · Current Opinion in Psychiatry · doi:10.1097/yco.0b013e3283345dc5 · Cited by 61 · see citing works
Sexual Dimorphism in Non-Mendelian Inheritance
Vigé, A., Gallou‐Kabani, C., & Junien, C. (2008) · Pediatric Research · doi:10.1203/pdr.0b013e318165b896 · Cited by 44 · see citing works
Mani, S. T., & Thakur, M. K. (2005) · Brain Research · doi:10.1016/j.brainres.2005.10.006 · Cited by 39 · see citing works
Risk factors for mental health: Translational models from behavioural neuroscience
Cirulli, F., Laviola, G., & Ricceri, L. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.01.006 · Cited by 24 · see citing works
Singh, K., & Prasad, S. (2008) · Biogerontology · doi:10.1007/s10522-008-9178-y · Cited by 17 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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-citationParental 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
Modabbernia, A., Velthorst, E., & Reichenberg, A. (2017) · Molecular Autism · doi:10.1186/s13229-017-0121-4 · Cited by 809 · see citing works
“Assisted reproductive technology and maternal stress (due to immigration) have also been linked to epigenetic alterations [65, 66], although the importance of such association with respect to ASD is unknown.”
BackgroundRodgers, A. B., Morgan, C. P., Bronson, S. L., Revello, S., & Bale, T. L. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.0914-13.2013 · Cited by 814 · see citing works
Holocaust Exposure Induced Intergenerational Effects on FKBP5 Methylation
Yehuda, R., Daskalakis, N. P., Bierer, L. M., Bader, H. N., Klengel, T., Holsboer, F., & Binder, E. B. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.08.005 · Cited by 782 · see citing works
Sex differences and stress across the lifespan
Bale, T. L., & Epperson, C. N. (2015) · Nature Neuroscience · doi:10.1038/nn.4112 · Cited by 751 · see citing works
Gene–Stress–Epigenetic regulation of FKBP5: clinical and translational implications
Zannas, A. S., Wiechmann, T., Gassen, N. C., & Binder, E. B. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.235 · Cited by 622 · see citing works
“Among these, DNA methylation is the most established lasting epigenetic modification induced by early life stressor exposure (Franklin et al, 2010; Weaver et al, 2004; Zannas and West, 2014b).”
BackgroundDaskalakis, N. P., Bagot, R. C., Parker, K. J., Vinkers, C. H., & de Kloet, E. R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.008 · Cited by 579 · see citing works
“Some recent findings suggest the intriguing possibility that the epigenetic signature of the environment induced early in life or in adulthood may be transferred through generations (Franklin et al., 2010; Dietz et al., 2011; Rodgers et al., 2013), although the mechanism by which this may occur is unclear.”
BackgroundIntergenerational Transmission of Stress in Humans
Bowers, M. E., & Yehuda, R. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.247 · Cited by 564 · see citing works
“…affect offspring via epigenetic modifications in sperm (similar to changes in DNA methylation or microRNA content observed in rodent models; Franklin et al, 2010; Dias and Ressler, 2014; Rodgers et al, 2013; Gapp et al, 2014) or early postnatal care; however, paternal stress may indirectly…”
BackgroundInfluentialBabenko, O., Kovalchuk, I., & Metz, G. A. S. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.013 · Cited by 513 · see citing works
Epigenetic and transgenerational reprogramming of brain development
Bale, T. L. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3818 · Cited by 505 · see citing works
Yehuda, R., Daskalakis, N. P., Lehrner, A., Desarnaud, F., Bader, H. N., Makotkine, I., Flory, J. D., Bierer, L. M., & Meaney, M. J. (2014) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2014.13121571 · Cited by 514 · see citing works
“However, studies with rodents demonstrate that preconception paternal stress can influence behavior and biology in progeny through epigenetic changes in sperm (37), such that germ-line transmission of epigenetic marks associated with PTSD risk is possible.”
BackgroundNeural Mechanisms of Stress Resilience and Vulnerability
Franklin, T. B., Saab, B. J., & Mansuy, I. M. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.016 · Cited by 500 · see citing works
“This progeny, but also the following, show multiple stress-related symptoms such as depressive-like behaviors, and social anxiety (Franklin et al., 2011; Franklin et al., 2010; Weiss et al., 2011).”
Self-citationEndocannabinoid signalling in reward and addiction
Parsons, L. H., & Hurd, Y. L. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn4004 · Cited by 474 · see citing works
The cognitive cell: bacterial behavior reconsidered
Lyon, P. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00264 · Cited by 411 · see citing works
Faulk, C., & Dolinoy, D. C. (2011) · Epigenetics · doi:10.4161/epi.6.7.16209 · Cited by 386 · see citing works
“Interestingly, these mice can transmit this phenotype and DNA methylation pattern transgenerationally through the male line with the shift of methylation in F1 sperm being mirrored by its pattern in F2 brain.(30) Early life stress in humans is also linked with gene expression changes for a polymorphic form of serotoni…”
BackgroundInfluentialEpigenetic regulation of gene expression in physiological and pathological brain processes
Gräff, J., Kim, D., Dobbin, M. M., & Tsai, L.-H. (2011) · Physiological Reviews · doi:10.1152/physrev.00012.2010 · Cited by 373 · see citing works
“And in the second, maternal stress-induced DNA methylation changes at the MeCP2, CB1 (cannabinoid receptor 1) and CRFR2 (corticotropin-releasing factor 2) genes were similar in the sperm of males subjected to maternal stress, and fascinatingly, also in the brain of their offspring, which themselves did not experience…”
BackgroundSelf-citationMaternal High-Fat Diet Effects on Third-Generation Female Body Size via the Paternal Lineage
Dunn, G. A., & Bale, T. L. (2011) · Endocrinology · doi:10.1210/en.2010-1461 · Cited by 372 · see citing works
“Similarly counterintuitive fluctuations in phenotypes across generations have been reported previously (41).”
BackgroundTransgenerational inheritance: Models and mechanisms of non–DNA sequence–based inheritance
Miska, E. A., & Ferguson-Smith, A. C. (2016) · Science · doi:10.1126/science.aaf4945 · Cited by 367 · see citing works
The recent progress in animal models of depression
Wang, Q., Timberlake, M. A., Prall, K., & Dwivedi, Y. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.04.008 · Cited by 370 · see citing works
“Epigenetic changes following neglect and abuse adversity have also been reported in other genes such as Crh (Elliott et al., 2010), Dlgap2 (Chertkow-Deutsher et al., 2010), Mecp2, Cnr1, and Crhr2 (Franklin et al., 2010), indicating that interaction of early life stress and DNA methylation can induce alterations in mul…”
Morgan, C. P., & Bale, T. L. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.1887-11.2011 · Cited by 346 · see citing works
“…Copyright © 2011 the authors 0270-6474/11/3111748-08$15.00/0 transgenerational phenotypic inheritance following exposure to environmental factors such as maternal stress, diet, and endocrine disruptors (Dunn and Bale, 2009; Franklin et al., 2010; Guerrero-Bosagna et al., 2010; Skinner, 2011).”
BackgroundInfluentialPaternal Transmission of Stress-Induced Pathologies
Dietz, D. M., LaPlant, Q., Watts, E. L., Hodes, G. E., Russo, S. J., Feng, J., Oosting, R. S., Vialou, V., & Nestler, E. J. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.005 · Cited by 346 · see citing works
Gabory, A., Roseboom, T. J., Moore, T., Moore, L. G., & Junien, C. (2013) · Biology of Sex Differences · doi:10.1186/2042-6410-4-5 · Cited by 344 · see citing works
“Comparable changes in DNA methylation are also present in the brain of the offspring and are associated with altered gene expression [94].”
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-citationPembrey, 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
Physical exercise as an epigenetic modulator of brain plasticity and cognition
Fernandes, J., Arida, R. M., & Gómez‐Pinilla, F. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.06.012 · Cited by 326 · see citing works
“The increased DNA methylation observed in the MeCP2 promoter of F1 sperm cells can be also found in F2 sperm and brain, suggesting that the changes in DNA methylation triggered by maternal separation survived epigenetic reprogramming during embryogenesis (Franklin et al., 2010).”
BackgroundCan environmental conditions experienced in early life influence future generations?
Burton, T., & Metcalfe, N. B. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.0311 · Cited by 307 · see citing works
“early life experiences of the parent and transmitted, by both parental lineages, to subsequent generations [10,15–17].”
BackgroundEarly-life experience, epigenetics, and the developing brain
Kundakovic, M., & Champagne, F. A. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.140 · Cited by 304 · see citing works
“In male mice, the experience of maternal separation during postnatal development is associated with impaired social behavior and altered anxiety-and depressive-like responses that persist across generations and coincide with altered serotonergic function (Franklin et al, 2010, 2011).”
BackgroundInfluentialThe Placenta as a Mediator of Stress Effects on Neurodevelopmental Reprogramming
Bronson, S. L., & Bale, T. L. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.231 · Cited by 285 · see citing works
Gene × Environment Interactions in Autism Spectrum Disorders: Role of Epigenetic Mechanisms
Tordjman, S., Somogyi, E., Coulon, N., Kermarrec, S., Cohen, D., Bronsard, G., Bonnot, O., Weismann-Arcache, C., Botbol, M., Lauth, B., et al. (2014) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2014.00053 · Cited by 283 · see citing works
“Thus, chronic and unpredictable early maternal separation from day 1 to 14 induces in mice depressive-like behaviors and DNA methylation changes in the separated male pups (this finding was not observed in female pups confirming previous findings that maternal separation and prenatal stress have a negative influence p…”
BackgroundEpigenetic Mechanisms of Depression and Antidepressant Action
Vialou, V., Feng, J., Robison, A. J., & Nestler, E. J. (2013) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010611-134540 · Cited by 277 · see citing works
“(173) showed that most of the behavioral alterations induced by early-life maternal separation are expressed by the F1 offspring of males subjected to maternal separation.”
BackgroundTractenberg, S. G., Levandowski, M. L., de Azeredo, L. A., Orso, R., Roithmann, L. G., Hoffmann, E. S., Brenhouse, H., & Grassi-Oliveira, R. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.06.021 · Cited by 267 · see citing works
Chronic Social Instability Induces Anxiety and Defective Social Interactions Across Generations
Saavedra-Rodríguez, L., & Feig, L. A. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.06.035 · Cited by 270 · see citing works
“A previous study on the effects of a different form of stress, early postnatal disruption of mothering, demonstrated different transgenerational effects (30).”
Gene–environment interactions at the FKBP5 locus: sensitive periods, mechanisms and pleiotropism
Zannas, A. S., & Binder, E. B. (2013) · Genes Brain & Behavior · doi:10.1111/gbb.12104 · Cited by 268 · see citing works
“On the other hand, stressor-induced DNA methylation has been suggested to be a stable and potentially heritable epigenetic modification (Franklin et al. 2010; Hoffmann & Spengler in press), rendering it a plausible mechanism mediating long-lasting molecular signatures of early trauma.”
BackgroundStigma and the perpetuation of obesity
Brewis, A. (2014) · Social Science & Medicine · doi:10.1016/j.socscimed.2014.08.003 · Cited by 269 · see citing works
“and this then shapes later depression-like behavior (Franklin et al., 2010).”
BackgroundNew insights into perinatal depression: pathogenesis and treatment during pregnancy and postpartum
Meltzer-Brody, S. E. (2011) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2011.13.1/smbrody · Cited by 266 · see citing works
“Franklin and colleagues demonstrated in rats that the stress of chronic and unpredictable early life maternal separation in offspring altered the profile of DNA methylation in the promoter of several candidate genes in the germline of the separated males.(59) Additionally, Weaver, Champagne, and colleagues discovered…”
Epigenetic Inheritance: Concepts, Mechanisms and Perspectives
Lacal, I., & Ventura, R. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00292 · Cited by 261 · see citing works
“Postnatal trauma elicits depressive-like behaviors that are evident for up to three generations, even after crossfostering (Franklin et al., 2010).”
BackgroundThe effects of early life stress on the epigenome: From the womb to adulthood and even before
Provençal, N., & Binder, E. B. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2014.09.001 · Cited by 255 · see citing works
Buss, C., Entringer, S., Moog, N. K., Toepfer, P., Fair, D. A., Simhan, H. N., Heim, C. M., & Wadhwa, P. D. (2017) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2017.03.001 · Cited by 250 · see citing works
Curley, J. P., & Champagne, F. A. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.11.001 · Cited by 257 · see citing works
“Variation in (Weaver et al., 2004) or deprivation of (Murgatroyd et al., 2009; Franklin et al., 2010) maternal care has been demonstrated to induce long-term epigenetic alterations, with implications for the development of neural circuits and the function of these circuits in adulthood.”
BackgroundXavier, M. J., Roman, S. D., Aitken, R. J., & Nixon, B. (2019) · Human Reproduction Update · doi:10.1093/humupd/dmz017 · Cited by 258 · see citing works
Naumova, O. Y., Lee, M., Koposov, R. A., Moshe Szyf, A., Dozier, M., & Grigorenko, E. L. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000605 · Cited by 251 · see citing works
“…under the influence of behavioral programming, epigenetic changes are detected in various cells and tissues, such as the central nervous system (Franklin et al., 2010; McGowan, Sasaki, D’Alessio, et al., 2009; McGowan, et al., 2008; Murgatroyd, et al., 2009), liver (Bateson et al., 2004;…”
BackgroundInfluentialParental Advisory: Maternal and Paternal Stress Can Impact Offspring Neurodevelopment
Chan, J. C., Nugent, B. M., & Bale, T. L. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.10.005 · Cited by 241 · see citing works
“In another study, male offspring exposed to maternal separation stress early in life sired offspring with depressivelike behaviors (94).”
BackgroundNongenetic inheritance and transgenerational epigenetics
Szyf, M. (2015) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.12.004 · Cited by 238 · see citing works
Sex differences in prenatal epigenetic programing of stress pathways
Bale, T. L. (2011) · Stress · doi:10.3109/10253890.2011.586447 · Cited by 237 · see citing works
“Recent studies examining the transgenerational effects of early life stress support an involvement of stress regulation on these genes in which similar changes were reported for MeCP2 expression and methylation in the brains of first and second generation stressed mice (Franklin et al. 2010).”
DNA methylation and childhood maltreatment: From animal models to human studies
Lutz, P.-E., & Turecki, G. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.07.069 · Cited by 236 · see citing works
“…et al, 2012b; [2] Kember et al, 2012; [3], LaBonte et al, 2012a; [4] Murgatroyd et al, 2009; [5], Champagne et al, 2006; [6] Roth et al, 2009; [7], Franklin et al, 2010; [8], Perroud et al, 2011, Radtke et al, 2011, Tyrka et al, 2012; [9], Smith et al, 2011, Naumova et al, 2012, Yang et al, 2013;…”
BackgroundMethodInfluentialGowland, R. L. (2015) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22820 · Cited by 232 · see citing works
“…rodents have challenged this, finding that aspects of health such as chronic social instability can cause enhanced anxiety and behavioral alterations in three generations of offspring, with DNA methylation being retained in the germ-line (Franklin et al., 2010; Saavedra-Rodriguez and Feig, 2013).”
BackgroundSex differences in antidepressant efficacy
LeGates, T. A., Kvarta, M. D., & Thompson, S. M. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0156-z · Cited by 225 · see citing works
Short, A. K., Fennell, K. A., Perreau, V. M., Fox, A., O’Bryan, M. K., Kim, J. H., Bredy, T. W., Pang, T. Y., & Hannan, A. J. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.109 · Cited by 230 · see citing works
Marczylo, E. L., Amoako, A. A., Konje, J. C., Gant, T. W., & Marczylo, T. H. (2012) · Epigenetics · doi:10.4161/epi.19794 · Cited by 227 · see citing works
Epigenetics of posttraumatic stress disorder: current evidence, challenges, and future directions
Zannas, A. S., Provençal, N., & Binder, E. B. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.04.003 · Cited by 218 · see citing works
Bridging the transgenerational gap with epigenetic memory
Lim, J. P., & Brunet, A. (2013) · Trends in Genetics · doi:10.1016/j.tig.2012.12.008 · Cited by 219 · see citing works
Chan, J. C., Morgan, C. P., Leu, N. A., Shetty, A. C., Cissé, Y. M., Nugent, B. M., Morrison, K. E., Jašarević, E., Huang, W., Kanyuch, N., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15305-w · Cited by 222 · see citing works
Epigenetic mechanisms of depression
Nestler, E. J. (2014) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.4291 · Cited by 217 · see citing works
Epigenetic inheritance and plasticity: The responsive germline
Jablonka, E. (2012) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2012.08.014 · Cited by 213 · see citing works
“…for an unpredictable few hours during each of the first 14 days after birth induced heritable, depressivelike adult behaviors, and altered their responses to novel and aversive environments; the early stress also altered the methylation profile of specific germline genes (Franklin et al., 2010).”
BackgroundInfluence of Early Stress on Social Abilities and Serotonergic Functions across Generations in Mice
Franklin, T. B., Linder, N., Russig, H. D., Thöny, B., & Mansuy, I. M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021842 · Cited by 212 · see citing works
“weaning (PND21), as previously described [9].”
BackgroundMethodInfluentialSelf-citationReduced levels of miRNAs 449 and 34 in sperm of mice and men exposed to early life stress
Dickson, D. A., Paulus, J. K., Mensah, V., Lem, J., Saavedra-Rodriguez, L., Gentry, A., Pagidas, K., & Feig, L. A. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0146-2 · Cited by 208 · see citing works
Animal models in cardiovascular research: hypertension and atherosclerosis
Leong, X.-F., Ng, C.-Y., & Jaarin, K. (2015) · BioMed Research International · doi:10.1155/2015/528757 · Cited by 203 · see citing works
“Hence, they make good models, as they can be studied over their whole life cycle or even across several generations [2, 3].”
BackgroundBraun, T., Challis, J. R., Newnham, J. P., & Sloboda, D. M. (2013) · Endocrine Reviews · doi:10.1210/er.2013-1012 · Cited by 196 · see citing works
McIntyre, L., Williams, J. V. A., Lavorato, D. H., & Patten, S. B. (2012) · Journal of Affective Disorders · doi:10.1016/j.jad.2012.11.029 · Cited by 197 · see citing works
The fetal programming of telomere biology hypothesis: an update
Entringer, S., de Punder, K., Buß, C., & Wadhwa, P. D. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2017.0151 · Cited by 189 · see citing works
Wang, Y., Liu, H., & Sun, Z. S. (2017) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12322 · Cited by 192 · see citing works
“Increasing evidence suggests that certain epigenetic changes, such as DNA methylation (Morgan et al., 1999; Rakyan et al., 2003; Carone et al., 2010; Franklin et al., 2010; Padmanabhan et al., 2013; Radford et al., 2014; Wei et al., 2014), histone modification (Katz et al.”
BackgroundMethodInfluentialBygren, L. O., Tinghög, P., Carstensen, J. M., Edvinsson, S., Kaati, G., Pembrey, M. E., & Sjöstróm, M. (2014) · BMC Genetics · doi:10.1186/1471-2156-15-12 · Cited by 188 · see citing works
“In epidemiology, and to some extent today in molecular biology, especially in the field of epigenetics, unpredictable environmental change is often considered to be an important agent in the etiology of diseases [25].”
BackgroundEpigenetic Influence of Stress and the Social Environment
Gudsnuk, K. M., & Champagne, F. A. (2012) · ILAR Journal · doi:10.1093/ilar.53.3-4.279 · Cited by 185 · see citing works
Neurodevelopmental Disorders and Environmental Toxicants: Epigenetics as an Underlying Mechanism
Tran, N. Q. V., & Miyake, K. (2017) · International Journal of Genomics · doi:10.1155/2017/7526592 · Cited by 183 · see citing works
“Furthermore, epigenomic alterations in brain and behavioral abnormalities were identified not only in children but also in grandchildren [195, 196].”
BackgroundEpigenetic mechanisms mediating vulnerability and resilience to psychiatric disorders
Dudley, K. J., Li, X., Kobor, M. S., Kippin, T. E., & Bredy, T. W. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.12.016 · Cited by 180 · see citing works
Epigenetic marking of sperm by post-translational modification of histones and protamines
Brunner, A. M., Nanni, P., & Mansuy, I. M. (2014) · Epigenetics & Chromatin · doi:10.1186/1756-8935-7-2 · Cited by 181 · see citing works
“Mature sperm was collected from the caudal epididymis of adult 3- to 12-month-old C57BL/6 males as previously described [38].”
Self-citationEpigenetic Inheritance of Disease and Disease Risk
Bohacek, J., & Mansuy, I. M. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.110 · Cited by 176 · see citing works
“…brain are the long-term epigenetic remodeling of the stress axis in response to stressful experiences early in life (Murgatroyd et al, 2009; Franklin et al, 2010), or the cascade of epigenetic events involved in the development of drug addiction (Kumar et al, 2005; Robison and Nestler,…”
BackgroundInfluentialSelf-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
“RT–PCR showing MR expression in the hippocampus in F1 MSUS males (controls n1⁄4 7, MSUS n1⁄4 8; t(13)1⁄4 2.”
MethodSelf-citationValor, L. M., Viosca, J., López‐Atalaya, J. P., & Barco, Á. (2013) · Current Pharmaceutical Design · doi:10.2174/13816128113199990382 · Cited by 168 · see citing works
“Extensive correlative evidence supports a role for histone acetylation in memory storage that seems highly conserved through evolution [8-13].”
BackgroundPotential 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-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-citationKundaković, M., Lim, S. C., Gudsnuk, K. M., & Champagne, F. A. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00078 · Cited by 172 · see citing works
“and may account for the transmission of behavioral and epigenetic effects of MS-rearing across generations (21, 71).”
BackgroundMethodInfluentialLiyanage, V. R. B., & Rastegar, M. (2014) · NeuroMolecular Medicine · doi:10.1007/s12017-014-8295-9 · Cited by 171 · see citing works
“results in altered expression of Mecp2 (Franklin et al. 2010).”
Backgroundde Haan, S. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108685214 · Cited by 178 · see citing works
Inheritable 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-citationThe neural mechanisms and consequences of paternal caregiving
Feldman, R., Braun, K., & Champagne, F. A. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0124-6 · Cited by 168 · see citing works
Breton, C. V., Landon, R., Kahn, L. G., Enlow, M. B., Peterson, A. K., Bastain, T. M., Braun, J. M., Comstock, S. S., Duarte, C. S., Hipwell, A. E., et al. (2021) · Communications Biology · doi:10.1038/s42003-021-02316-6 · Cited by 167 · see citing works
Gapp, K., van Steenwyk, G., Germain, P. L., Matsushima, W., Rudolph, K. L. M., Manuella, F., Roszkowski, M., Vernaz, G., Ghosh, T., Pelczar, P., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-018-0271-6 · Cited by 195 · see citing works
“First, using the MSUS paradigm, we produced a cohort of mice exposed to traumatic stress in early postnatal life and confirmed their behavioural phenotype in adulthood described previously [2, 10] (Supplementary Figure 1).”
MethodSelf-citationJawahar, M. C., Murgatroyd, C., Harrison, E. L., & Baune, B. T. (2015) · Clinical Epigenetics · doi:10.1186/s13148-015-0156-3 · Cited by 165 · see citing works
Maternal PTSD associates with greater glucocorticoid sensitivity in offspring of Holocaust survivors
Lehrner, A., Bierer, L. M., Passarelli, V., Pratchett, L. C., Flory, J. D., Bader, H. N., Harris, I. R., Bedi, A., Daskalakis, N. P., Makotkine, I., et al. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.11.019 · Cited by 160 · see citing works
“The effects of paternal stress exposure on offspring in animal models have been primarily attributed to preconception influences on gamete development (Franklin and Mansuy, 2010; Franklin et al., 2010; Rodgers et al., 2013).”
BackgroundInfluentialEpigenetic inheritance and reproductive mode in plants and animals
Anastasiadi, D., Venney, C. J., Bernatchez, L., & Wellenreuther, M. (2021) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2021.08.006 · Cited by 162 · see citing works
The social brain meets the reactive genome: neuroscience, epigenetics and the new social biology
Meloni, M. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00309 · Cited by 158 · see citing works
Sarker, G., Sun, W., Rosenkranz, D., Pelczar, P., Opitz, L., Efthymiou, V., Wolfrum, C., & Peleg‐Raibstein, D. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820810116 · Cited by 160 · see citing works
Schiele, M. A., Gottschalk, M. G., & Domschke, K. (2020) · Clinical Psychology Review · doi:10.1016/j.cpr.2020.101830 · Cited by 156 · see citing works
Heim, C. M., Entringer, S., & Buss, C. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.12.011 · Cited by 158 · see citing works
“Animal data support the possibility of inter-and trans-generational transmission of ELS-induced behavioral traits mediated by epigenetic modifications through the paternal germ line (Franklin et al., 2010; Gapp et al., 2014; Pang et al., 2017; Rodgers et al., 2015; Zhang et al., 2018).”
BackgroundNorouzitallab, P., Baruah, K., Vandegehuchte, M., Stappen, G. V., Catania, F., Bussche, J. V., Vanhaecke, L., Sorgeloos, P., & Bossier, P. (2014) · The FASEB Journal · doi:10.1096/fj.14-252049 · Cited by 158 · see citing works
Epigenetics for behavioral ecologists
Ledón‐Rettig, C. C., Richards, C. L., & Martin, L. B. (2012) · Behavioral Ecology · doi:10.1093/beheco/ars145 · Cited by 156 · see citing works
Kubota, T., Miyake, K., & Hirasawa, T. (2012) · Clinical Epigenetics · doi:10.1186/1868-7083-4-1 · Cited by 157 · see citing works
“Recent research on animals has shown that behavioral characteristics can be inherited [60].”
BackgroundPaternal Influences on Offspring Development: Behavioural and Epigenetic Pathways
Braun, K., & Champagne, F. A. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12174 · Cited by 157 · see citing works
Nätt, D., Rubin, C., Wright, D., Johnsson, M., Bélteky, J., Andersson, L., & Jensen, P. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-59 · Cited by 157 · see citing works
Peter, C. J., Fischer, L. K., Kundaković, M., Garg, P., Jakovcevski, M., Dincer, A., Amaral, A. C. S., Ginns, E. I., Galdzicka, M. M., Bryce, C. P., et al. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.03.2100 · Cited by 156 · see citing works
“N: 0006-3223 Biologica SEE COMMENTARY exist in the offspring of a parent exposed to malnutrition in infancy, similar to the multigenerational transmission of DNA methylation signatures after maternal separation stress in postnatal mice (8,9).”
BackgroundBekdash, R. A., Zhang, C., & Sarkar, D. K. (2013) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12082 · Cited by 155 · see citing works
Benito, E., Kerimoglu, C., Ramachandran, B., Pena‐Centeno, T., Jain, G., Stilling, R. M., Islam, R., Capece, V., Zhou, Q., Edbauer, D., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.03.059 · Cited by 155 · see citing works
Timescales of Human Adaptation: The Role of Epigenetic Processes
Kuzawa, C. W., & Thayer, Z. M. (2011) · Epigenomics · doi:10.2217/epi.11.11 · Cited by 149 · see citing works
O’Dea, R. E., Noble, D. W. A., Johnson, S. L., Hesselson, D., & Nakagawa, S. (2016) · Current Zoology · doi:10.1093/eep/dvv014 · Cited by 153 · see citing works
Northstone, K., Golding, J., Smith, G. D., Miller, L. L., & Pembrey, M. E. (2014) · European Journal of Human Genetics · doi:10.1038/ejhg.2014.31 · Cited by 152 · see citing works
Development and the epigenome: the ‘synapse’ of gene–environment interplay
Boyce, W. T., & Kobor, M. S. (2014) · Developmental Science · doi:10.1111/desc.12282 · Cited by 152 · see citing works
Karatekin, C., & Ahluwalia, R. (2016) · Journal of Interpersonal Violence · doi:10.1177/0886260516681880 · Cited by 150 · see citing works
“…& Hartwick, 2012; Bartlett & Easterbrooks, 2012; Kim, 2009; Marshall, Huang, & Ryan, 2011; Widom, Czaja, & DuMont, 2015) and biological level through epigenetic transmission of stressful experiences (Franklin et al., 2010; Neigh, Gillespie, & Nemeroff, 2009; Roth, Lubin, Funk, & Sweatt, 2009).”
BackgroundGABAergic Control of Depression-Related Brain States
Luscher, B., & Fuchs, T. (2015) · Advances in Pharmacology · doi:10.1016/bs.apha.2014.11.003 · Cited by 149 · see citing works
“Environmental risk factors implicated in affective disorders that have been shown to program heritable behavioral traits in mice include fearful experiences in adulthood (Dias & Ressler, 2014) as well as early life stress (Bohacek et al., 2014; Franklin et al., 2010).”
Background
- 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
