Early Prenatal Stress Epigenetically Programs Dysmasculinization in Second-Generation Offspring via the Paternal Lineage
Open accessAbstract
Studies have linked sex-biased neurodevelopmental disorders, including autism and schizophrenia, with fetal antecedents such as prenatal stress. Further, these outcomes can persist into subsequent generations, raising the possibility that aspects of heritability in these diseases involve epigenetic mechanisms. Utilizing a mouse model in which we previously identified a period in early gestation when stress results in dysmasculinized and stress-sensitive male offspring, we have examined programming effects in second-generation offspring of prenatally stressed (F2-S) or control (F2-C) sires. Examination of gene expression patterns during the perinatal sensitive period, when organizational gonadal hormones establish the sexually dimorphic brain, confirmed dysmasculinization in F2-S males, where genes important in neurodevelopment showed a female-like pattern. Analyses of the epigenomic miRNA environment detected significant reductions in miR-322, miR-574, and miR-873 in the F2-S male brain, levels that were again more similar to those of control females. Increased expression of a common gene target for these three miRNAs, β-glycan, was confirmed in these males. These developmental effects were associated with the transmission of a stress-sensitive phenotype and shortened anogenital distance in adult F2-S males. As confirmation that the miRNA environment is responsive to organizational testosterone, neonatal males administered the aromatase inhibitor formestane exhibited dramatic changes in brain miRNA patterns, suggesting that miRNAs may serve a previously unappreciated role in organizing the sexually dimorphic brain. Overall, these data support the existence of a sensitive period of early gestation when epigenetic programming of the male germline can occur, permitting transmission of specific phenotypes into subsequent generations.
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In animal models of prenatal stress, exposure to chronic stress in utero increased male, but not female, HPA stress reactivity.
“exposure to chronic stress in utero increased male, but not female, HPA stress reactivity (e.g., behavioral response to the tail suspension test) 159,162”
From Intergenerational transmission of trauma effects: putative role of epigenetic mechanisms (2018) · cites this paper as [162]
The Results (Analysis of adult F2 behavior and physiology; page not supplied) report increased tail-suspension immobility in males, but not females, after paternal prenatal stress exposure. They report no significant effect on HPA-axis corticosterone responses in either sex. The claim conflates the behavioral result with increased HPA reactivity and does not distinguish the F2 offspring from the directly exposed F1 generation. (LLM, conf=0.90)
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Cites
MicroRNAs: Target Recognition and Regulatory Functions
Bartel, D. P. (2009) · Cell · doi:10.1016/j.cell.2009.01.002 · Cited by 20,068 · see citing works
The tail suspension test: A new method for screening antidepressants in mice
Steru, L., Chermat, R., Thierry, B., & Simon, P. (1985) · Psychopharmacology · doi:10.1007/bf00428203 · Cited by 3,534 · see citing works
PHOENIX, C. H., GOY, R. W., GERALL, A. A., & YOUNG, W. C. (1959) · Endocrinology · doi:10.1210/endo-65-3-369 · Cited by 1,934 · see citing works
Personal genomes: The case of the missing heritability
Maher, B. (2008) · Nature · doi:10.1038/456018a · Cited by 1,737 · see citing works
Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. M. (2008) · Epigenetics · doi:10.4161/epi.3.2.6034 · Cited by 1,432 · see citing works
Gonadal Steroid Induction of Structural Sex Differences in the Central Nervous System
Arnold, A. P., & Gorski, R. A. (1984) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.07.030184.002213 · Cited by 1,198 · see citing works
Epigenetic 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 · cited 3× · 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).”
BackgroundInfluentialSex-Specific Programming of Offspring Emotionality after Stress Early in Pregnancy
Mueller, B. R., & Bale, T. L. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1424-08.2008 · Cited by 988 · see citing works
Self-citationEarly Life Programming and Neurodevelopmental Disorders
Bale, T. L., Baram, T. Z., Brown, A. S., Goldstein, J. M., Insel, T. R., McCarthy, M. M., Nemeroff, C. B., Reyes, T. M., Simerly, R. B., Susser, E. S., et al. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.05.028 · Cited by 961 · see citing works
Self-citationmiRDB: A microRNA target prediction and functional annotation database with a wiki interface
Wang, X. (2008) · RNA · doi:10.1261/rna.965408 · Cited by 712 · see citing works
Prenatal stress, glucocorticoids and the programming of adult disease
Cottrell, E. C. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.019.2009 · Cited by 640 · see citing works
Betaglycan binds inhibin and can mediate functional antagonism of activin signalling
Lewis, K. A., Gray, P. C., Blount, A. L., MacConell, L., Wiater, E., Bilezikjian, L. M., & Vale, W. (2000) · Nature · doi:10.1038/35006129 · Cited by 585 · see citing works
Khashan, A. S., Abel, K. M., McNamee, R., Pedersen, M. G., Webb, R. T., Baker, P. N., Kenny, L. C., & Mortensen, P. B. (2008) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2007.20 · Cited by 576 · see citing works
Transgenerational Epigenetic Effects
Youngson, N. A., & Whitelaw, E. (2008) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.9.081307.164445 · Cited by 575 · see citing works
Prenatal Stress Feminizes and Demasculinizes the Behavior of Males
Ward, I. L. (1972) · Science · doi:10.1126/science.175.4017.82 · Cited by 545 · see citing works
Hypothalamic Abnormalities in Schizophrenia: Sex Effects and Genetic Vulnerability
Goldstein, J. M., Seidman, L. J., Makris, N., Ahern, T., O’Brien, L. M., Caviness, V. S., Kennedy, D. N., Faraone, S. V., & Tsuang, M. T. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.06.027 · Cited by 542 · see citing works
Prediction of both conserved and nonconserved microRNA targets in animals
Wang, X., & Naqa, I. E. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm595 · Cited by 529 · see citing works
Prenatal exposure to maternal stress and subsequent schizophrenia
van Os, J., & Selten, J. (1998) · The British Journal of Psychiatry · doi:10.1192/bjp.172.4.324 · Cited by 481 · see citing works
The Epigenetics of Sex Differences in the Brain: Figure 1.
McCarthy, M. M., Auger, A. P., Bale, T. L., Vries, G. J. D., Dunn, G. A., Forger, N. G., Murray, E. K., Nugent, B. M., Schwarz, J. M., & Wilson, M. E. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3331-09.2009 · Cited by 478 · see citing works
Self-citationEpigenetic Transgenerational Actions of Vinclozolin on Promoter Regions of the Sperm Epigenome
Guerrero‐Bosagna, C., Settles, M. L., Lucker, B. F., & Skinner, M. K. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013100 · Cited by 427 · see citing works
Ghosh, G., Subramanian, I. V., Adhikari, N., Zhang, X., Joshi, H. P., Basi, D. L., Chandrashekhar, Y., Hall, J. L., Roy, S., Zeng, Y., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci42980 · Cited by 417 · see citing works
Ivy, A. S., Rex, C. S., Chen, Y., Dubé, C., Maras, P. M., Grigoriadis, D. E., Gall, C. M., Lynch, G., & Baram, T. Z. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1784-10.2010 · Cited by 402 · see citing works
Champagne, F. A., & Meaney, M. J. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.6.1353 · Cited by 381 · see citing works
Prenatal Loss of Father and Psychiatric Disorders
HUTTUNEN, M. O. (1978) · Archives of General Psychiatry · doi:10.1001/archpsyc.1978.01770280039004 · Cited by 372 · see citing works
Maternal Stress Alters Plasma Testosterone in Fetal Males
Ward, I. L., & Weisz, J. (1980) · Science · doi:10.1126/science.7188648 · Cited by 370 · see citing works
Gender Differences in the Effects of Prenatal Stress on Brain Development and Behaviour
Weinstock, M. (2007) · Neurochemical Research · doi:10.1007/s11064-007-9339-4 · Cited by 349 · see citing works
Epigenetic Inheritance and the Missing Heritability Problem
Slatkin, M. (2009) · Genetics · doi:10.1534/genetics.109.102798 · Cited by 337 · cited 1× · see citing works
“These phenomena raise the interesting possibility that the heritability observed in neurodevelopmental diseases could be the product of both classic genetic and non-Mendelian, or epigenetic, mechanisms (Maher, 2008; Slatkin, 2009).”
BackgroundCaruso, P. L., MacLean, M. R., Khanin, R., McClure, J., Soon, E., Southgate, M. T., MacDonald, R. A., Greig, J. A., Robertson, K. E., Masson, R., et al. (2010) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.109.202028 · Cited by 329 · see citing works
Dunn, G. A., & Bale, T. L. (2009) · Endocrinology · doi:10.1210/en.2009-0500 · Cited by 317 · see citing works
Self-citationAutism Prevalence Following Prenatal Exposure to Hurricanes and Tropical Storms in Louisiana
Kinney, D. K., Miller, A. M., Crowley, D. J., Huang, E., & Gerber, E. (2008) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-007-0414-0 · Cited by 295 · see citing works
Amateau, S. K., Alt, J., Stamps, C. L., & McCarthy, M. M. (2004) · Endocrinology · doi:10.1210/en.2003-1363 · Cited by 242 · see citing works
Role of epigenetics in developmental biology and transgenerational inheritance
Skinner, M. K. (2011) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.20199 · Cited by 218 · see citing works
Early prenatal stress impact on coping strategies and learning performance is sex dependent
Mueller, B. R., & Bale, T. L. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.01.017 · Cited by 216 · see citing works
Self-citationQin, L., Chen, Y., Niu, Y., Chen, W., Wang, Q., Xiao, S., Li, A., Xie, Y., Li, J., Zhao, X. L., et al. (2010) · BMC Genomics · doi:10.1186/1471-2164-11-320 · Cited by 207 · see citing works
Kapoor, A., & Matthews, S. G. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.090191 · Cited by 206 · see citing works
Kőrösi, A., Shanabrough, M., McClelland, S., Liu, Z.-W., Borók, E., Gao, X., Horváth, T. L., & Baram, T. Z. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4214-09.2010 · Cited by 168 · see citing works
Impact of prenatal stress on long term body weight is dependent on timing and maternal sensitivity
MUELLER, B., & Bale, T. L. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.05.019 · Cited by 162 · see citing works
Self-citationMcCarthy, M. M., Wright, C. L., & Schwarz, J. M. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.02.012 · Cited by 156 · see citing works
Eiland, L. R., & McEwen, B. S. (2010) · Hippocampus · doi:10.1002/hipo.20862 · Cited by 148 · see citing works
Scott, H. M., Hutchison, G. R., Jobling, M. S., McKinnell, C., Drake, A. J., & Sharpe, R. M. (2008) · Endocrinology · doi:10.1210/en.2008-0413 · Cited by 145 · see citing works
Estrogen Regulation of MicroRNA Expression
Klinge, C. (2009) · Current Genomics · doi:10.2174/138920209788185289 · Cited by 138 · see citing works
Auger, C. J., Coss, D., Auger, A. P., & Forbes‐Lorman, R. M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100314108 · Cited by 119 · see citing works
Seale, J. V., Wood, S. A., Atkinson, H. C., Lightman, S. L., & Harbuz, M. S. (2004) · Endocrinology · doi:10.1210/en.2004-1201 · Cited by 109 · see citing works
A sexually dimorphic ratio of orbitofrontal to amygdala volume is altered in schizophrenia
Gur, R. E., Kohler, C. G., Turetsky, B. I., Siegel, S. J., Kanes, S., Bilker, W. B., Brennan, A. R., & Gur, R. C. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.10.009 · Cited by 103 · see citing works
Kapoor, A., & Matthews, S. G. (2008) · Endocrinology · doi:10.1210/en.2008-0347 · Cited by 97 · see citing works
Influence of maternal stress on the development of the fetal genital system
Dahlöf, L., Hȧrd, E., & Larsson, K. (1978) · Physiology & Behavior · doi:10.1016/0031-9384(78)90072-0 · Cited by 88 · see citing works
MacConell, L., Leal, A. M. O., & Vale, W. (2002) · Endocrinology · doi:10.1210/endo.143.3.8707 · Cited by 78 · see citing works
Meisel, R. L., Dohanich, G. P., & Ward, I. L. (1979) · Physiology & Behavior · doi:10.1016/0031-9384(79)90020-9 · Cited by 72 · see citing works
Biala, Y. N., Bogoch, Y., Bejar, C., Michal Linial, B., & Weinstock, M. (2010) · Hippocampus · doi:10.1002/hipo.20825 · Cited by 65 · see citing works
Testosterone-induced upregulation of miRNAs in the female mouse liver
Delić, D., Großer, C., Dkhil, M. A., Al‐Quraishy, S., & Wunderlich, F. T. (2010) · Steroids · doi:10.1016/j.steroids.2010.06.010 · Cited by 63 · see citing works
Резніков, А. Г., Nosenko, N. D., & Тарасенко, Л. В. (1999) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(98)00151-4 · Cited by 62 · see citing works
MicroRNAs Are Mediators of Androgen Action in Prostate and Muscle
Narayanan, R., Jiang, J., Gusev, Y., Jones, A. J., Kearbey, J. D., Miller, D. D., Schmittgen, T. D., & Dalton, J. T. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013637 · Cited by 62 · see citing works
Chapman, S. C., & Woodruff, T. K. (2003) · Endocrinology · doi:10.1210/en.2003-0670 · Cited by 50 · see citing works
van Rijn, S., Aleman, A., de Sonneville, L. M. J., Sprong, M., Ziermans, T. B., Schothorst, P. F., van Engeland, H., & Swaab, H. (2011) · Psychological Medicine · doi:10.1017/s0033291710002576 · Cited by 47 · see citing works
Endogenous Betaglycan Is Essential for High-Potency Inhibin Antagonism in Gonadotropes
Wiater, E., Lewis, K. A., Donaldson, C. J., et al. (2009) · Molecular Endocrinology · doi:10.1210/me.2009-0021 · Cited by 45 · see citing works
Bingham, B., & Viau, V. (2008) · Endocrinology · doi:10.1210/en.2007-1796 · Cited by 44 · see citing works
Epigenetic Turn Ons and Turn Offs: Chromatin Reorganization and Brain Differentiation
Auger, A. P., & Auger, C. J. (2010) · Endocrinology · doi:10.1210/en.2010-0793 · Cited by 39 · see citing works
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Dias, B. G., & Ressler, K. J. (2014) · Nature Neuroscience · doi:10.1038/nn.3594 · Cited by 1,338 · see citing works
Rodgers, 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
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Rodgers, A. B., Morgan, C. P., Leu, N. A., & Bale, T. L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1508347112 · Cited by 751 · see citing works
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Reh, R. K., Dias, B. G., Nelson, C. A., Kaufer, D., Werker, J. F., Kolb, B., Levine, J. D., & Hensch, T. K. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820836117 · Cited by 492 · see citing works
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Bale, T. L. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3818 · Cited by 505 · see citing works
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Bohacek, J., & Mansuy, I. M. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3964 · Cited by 318 · see citing works
Bronson, S. L., & Bale, T. L. (2014) · Endocrinology · doi:10.1210/en.2014-1040 · Cited by 299 · see citing works
Self-citationEarly-life experience, epigenetics, and the developing brain
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Epigenetic 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
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Provençal, N., & Binder, E. B. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2014.09.001 · Cited by 255 · see citing works
Parental 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
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Szyf, M. (2015) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.12.004 · Cited by 238 · see citing works
The placenta and neurodevelopment: sex differences in prenatal vulnerability
Bale, T. L. (2016) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2016.18.4/tbale · Cited by 236 · see citing works
Self-citationAn epigenetic framework for neurodevelopmental disorders: From pathogenesis to potential therapy
Millan, M. J. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.11.015 · Cited by 229 · 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
Zucchi, F. C. R., Yao, Y., Ward, I. D., Ilnytskyy, Y., Olson, D. M., Benzies, K., Kovalchuk, I., Kovalchuk, O., & Metz, G. A. S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056967 · Cited by 193 · see citing works
Epigenetic Signaling in Psychiatric Disorders
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Crudo, A., Petropoulos, S., Moisiadis, V. G., Iqbal, M., Kostaki, A., Machnes, Z., Szyf, M., & Matthews, S. G. (2012) · Endocrinology · doi:10.1210/en.2011-2160 · Cited by 156 · see citing works
Paternal Influences on Offspring Development: Behavioural and Epigenetic Pathways
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Gapp, K., von Ziegler, L., Tweedie‐Cullen, R. Y., & Mansuy, I. M. (2014) · BioEssays · doi:10.1002/bies.201300116 · Cited by 136 · see citing works
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Self-citationYeshurun, S., & Hannan, A. J. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0039-z · Cited by 121 · see citing works
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Self-citationBartlett, A. A., Singh, R., & Hunter, R. G. (2017) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-319-53889-1_8 · Cited by 91 · see citing works
A guide to designing germline-dependent epigenetic inheritance experiments in mammals
Bohacek, J., & Mansuy, I. M. (2017) · Nature Methods · doi:10.1038/nmeth.4181 · Cited by 80 · see citing works
Crudo, A., Petropoulos, S., Suderman, M., Moisiadis, V. G., Kostaki, A., Hallett, M., Szyf, M., & Matthews, S. G. (2013) · Endocrinology · doi:10.1210/en.2013-1484 · Cited by 73 · see citing works
The neurobiological effects of stress as contributors to psychiatric disorders: focus on epigenetics
Provencal, N., & Binder, E. B. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.08.007 · Cited by 64 · see citing works
Guerrero-Bosagna, C., Weeks, S., & Skinner, M. K. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100194 · Cited by 45 · see citing works
DNA methylation from germline cells in veterans with PTSD
Mehta, D., Pelzer, E. S., Bruenig, D., Lawford, B., McLeay, S., Morris, C. P., Gibson, J. N., Young, R. M., Voisey, J., McLeay, S., et al. (2019) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2019.06.001 · Cited by 37 · see citing works
- Authors
- Morgan, C. P., & Bale, T. L.
- Affiliations
- University of Pennsylvania (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-08-17
- Volume
- 31
- Issue
- 33
- Pages
- 11748-11755
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3164823
- OpenAlex
- W2070187535
- Cited by
- 346
- References
- 57
- Citations by year
- 2026: 1 · 2025: 11 · 2024: 6 · 2023: 23 · 2022: 36 · 2021: 15 · 2020: 21 · 2019: 15 · 2018: 24 · 2017: 23 · 2016: 26 · 2015: 29 · 2014: 56 · 2013: 33 · 2012: 25
- FWCI
- 15.05
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01mh091258-05)
- National Institute of Mental Health (MH087597, MH 091258, R01 MH-091258, R01MH087597)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- 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
- Keywords
- prenatal stress, epigenetic programming, transgenerational transmission, microRNA, male germline, anogenital distance, aromatase inhibition, formestane, testosterone, autism spectrum disorder, schizophrenia, neurodevelopmental disorders
- MeSH terms
- Age Factors, Animals, Female, Foxes, Male, Mice, Inbred C57BL, Pregnancy, Prenatal Exposure Delayed Effects, Random Allocation, Sex Characteristics, Stress, Psychological, Paternal Exposure, MicroRNAs, Mice, Mice, 129 Strain, Epigenomics
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