Gestational Exposure to Bisphenol A Produces Transgenerational Changes in Behaviors and Gene Expression

Wolstenholme, Jennifer T.; Edwards, Michelle; Shetty, Savera R. J.; Gatewood, Jessica D.; Taylor, Julia A.; Rissman, Emilie F.; Connelly, Jessica J.

doi:10.1210/en.2012-1195

Cited by 319Effects and risks of endocrine disrupting chemicalsNeuroendocrine regulation and behaviorSexual Differentiation and Disorders

Gestational Exposure to Bisphenol A Produces Transgenerational Changes in Behaviors and Gene Expression

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Wolstenholme, Jennifer T., Edwards, Michelle, Shetty, Savera R. J., Gatewood, Jessica D., Taylor, Julia A., Rissman, Emilie F., Connelly, Jessica J.·2012·Endocrinology

DOI 10.1210/en.2012-1195PMC PMC3404345

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Abstract

Bisphenol A (BPA) is a plasticizer and an endocrine-disrupting chemical. It is present in a variety of products used daily including food containers, paper, and dental sealants and is now widely detected in human urine and blood. Exposure to BPA during development may affect brain organization and behavior, perhaps as a consequence of its actions as a steroid hormone agonist/antagonist and/or an epigenetic modifier. Here we show that BPA produces transgenerational alterations in genes and behavior. Female mice received phytoestrogen-free chow with or without BPA before mating and throughout gestation. Plasma levels of BPA in supplemented dams were in a range similar to those measured in humans. Juveniles in the first generation exposed to BPA in utero displayed fewer social interactions as compared with control mice, whereas in later generations (F2 and F4), the effect of BPA was to increase these social interactions. Brains from embryos (embryonic d 18.5) exposed to BPA had lower gene transcript levels for several estrogen receptors, oxytocin, and vasopressin as compared with controls; decreased vasopressin mRNA persisted into the F4 generation, at which time oxytocin was also reduced but only in males. Thus, exposure to a low dose of BPA, only during gestation, has immediate and long-lasting, transgenerational effects on mRNA in brain and social behaviors. Heritable effects of an endocrine-disrupting chemical have implications for complex neurological diseases and highlight the importance of considering gene-environment interactions in the etiology of complex disease.

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BPA alters AVP and OT neuron numbers and innervation of sexually dimorphic regions associated with social and aggressive behaviors in multiple species, and is anxiogenic in multiple species.
“Altered AVP and OT neuron numbers and innervation of sexually dimorphic regions associated with social and aggressive behaviors in multiple species; anxiogenic in multiple species”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [65]
The gene-expression results report altered Avp and Oxt mRNA in mouse brains, but the Discussion says the authors were still assessing which neuron subpopulations BPA affects; it does not establish changes in neuron numbers or innervation. The background mentions anxiety findings in mice and children, but the paper’s own elevated-plus-maze results state that gestational BPA did not alter anxiety-like behavior in any generation. (LLM, conf=0.88)
Experimental — accuracy not yet measured
AVP levels were decreased in F4 embryos of both sexes, albeit to a lesser degree, following BPA exposure.
“AVP levels were also decreased in the F4 embryos of both sexes albeit to a lesser degree (64, 65).”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [65]
The section on transgenerational effects reports significantly decreased Avp expression in F4 embryonic brains from the BPA lineage, with no sex difference. It does not establish that the decrease was smaller than in F1 embryos. The measurement was Avp gene expression, not AVP protein levels. (LLM, conf=0.84)
Experimental — accuracy not yet measured
In C57BL/6J mice, gestational BPA exposure (dams on approximately 170 μg/kg bw diet) produced social deficits, particularly in females, coinciding with decreased AVP mRNA in whole embryonic brains of ED18.5 siblings of both sexes.
“Mice reared on a diet delivering approximately 170 µg/kg bw BPA (to the dams) during gestation displayed social deficits, particularly in females, that coincided with a decrease in AVP mRNA expression levels in whole embryonic brains obtained from their ED18.5 siblings (both sexes).”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [65]
The Animals section (page unavailable) identifies C57BL/6J mice given 5 mg BPA/kg diet, and the qPCR results report lower Avp mRNA in E18.5 embryonic brains without a sex effect. The paper does not give the claimed approximately 170 µg/kg body-weight dose. Its juvenile social-interaction results find no sex-by-diet interaction, while its social-preference results show reduced preference in BPA-exposed males rather than females; thus “particularly in females” is not supported. (LLM, conf=0.90)
Experimental — accuracy not yet measured
Reduced OT mRNA expression was observed in F4 male mice following BPA exposure.
“Reduced OT mRNA expression was observed in the F4 males.”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [65]
Reduced expression of estrogen receptor, oxytocin, and vasopressin in the brain were observed in mice in the BPA lineages.
“Reduced expression of estrogen receptor, oxytocin, and vasopressin in the brain were observed and postulated to underlie the deficits in behavior of mice in the BPA lineages [ 148 ].”
From DNA methylation: a mechanism linking environmental chemical exposures to risk of autism spectrum disorders? (2016) · cites this paper as [148]

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Bonthuis, P. J., Cox, K. H., Searcy, B. T., Kumar, P., Tobet, S. A., & Rissman, E. F. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.05.001 · Cited by 90 · see citing works
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Intensity of multigenerational carcinogenesis from diethylstilbestrol in mice
Walker, B. (1997) · Carcinogenesis · doi:10.1093/carcin/18.4.791 · Cited by 90 · see citing works
Influence of endocrine active compounds on the developing rodent brain
Patisaul, H. B., & Polston, E. K. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.06.008 · Cited by 81 · see citing works
Epigenetic and gene expression changes related to transgenerational carcinogenesis
Cheng, R. Y. S., Hockman, T. M., Crawford, E. B., Anderson, L. M., & Shiao, Y. (2004) · Molecular Carcinogenesis · doi:10.1002/mc.20022 · Cited by 79 · see citing works
Roles of Oestrogen Receptors α and β in Behavioural Neuroendocrinology: Beyond Yin/Yang
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Differential Effects of Estrogen Receptor Alpha and Beta Specific Agonists on Social Learning of Food Preferences in Female Mice
Clipperton‐Allen, A. E., Spinato, J. M., Chernets, C., Pfaff, D. W., & Choleris, E. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301625 · Cited by 77 · see citing works
Alterations in male infant behaviors towards its mother by prenatal exposure to bisphenol A in cynomolgus monkeys (Macaca fascicularis) during early suckling period
Nakagami, A., Negishi, T., Kawasaki, K., Imai, N., Nishida, Y., Ihara, T., Kuroda, Y., Yoshikawa, Y., & Koyama, T. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.03.005 · Cited by 63 · see citing works
Developmental and metabolic brain alterations in rats exposed to bisphenol A during gestation and lactation
Kunz, N., Camm, E. J., Somm, E., Lodygensky, G. A., Darbre, S., Aubert, M. L., Hüppi, P. S., Sizonenko, S. V., & Rolf Gruetter, A. (2010) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2010.09.009 · Cited by 59 · see citing works
Oxytocin, vasopressin and estrogen receptor gene expression in relation to social recognition in female mice
Clipperton‐Allen, A. E., Lee, A. W., Reyes, A., Devidze, N., Phan, A., Pfaff, D. W., & Choleris, E. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.10.025 · Cited by 58 · see citing works
Genetic, epigenetic and environmental impact on sex differences in social behavior
Shepard, K. N., Michopoulos, V., Toufexis, D. J., & Wilson, M. E. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.02.016 · Cited by 57 · see citing works
An expression microarray approach for the identification of metastable epialleles in the mouse genome
Weinhouse, C., Anderson, O. S., Jones, T. R., Kim, J. H., Liberman, S. A., Nahar, M. S., Rozek, L. S., Jirtle, R. L., & Dolinoy, D. C. (2011) · Epigenetics · doi:10.4161/epi.6.9.17103 · Cited by 40 · see citing works

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EDC-2: the endocrine society's second scientific statement on endocrine-disrupting chemicals
Gore, A. C., Chappell, V. A., Fenton, S. E., Flaws, J. A., Nadal, A., Prins, G. S., Toppari, J., & Zoeller, R. T. (2015) · Endocrine Reviews · doi:10.1210/er.2015-1010 · Cited by 2,407 · see citing works
Scientific Opinion on the risks to public health related to the presence of bisphenol A (BPA) in foodstuffs
EFSA Panel on Food Contact Materials, E. (2015) · EFSA Journal · doi:10.2903/j.efsa.2015.3978 · Cited by 1,026 · see citing works
Consensus on the key characteristics of endocrine-disrupting chemicals as a basis for hazard identification
La Merrill, M. A., Vandenberg, L. N., Smith, M. T., Goodson, W., Browne, P., Patisaul, H. B., Guyton, K. Z., Kortenkamp, A., Cogliano, V. J., Woodruff, T. J., et al. (2020) · Nature Reviews Endocrinology · doi:10.1038/s41574-019-0273-8 · Cited by 1,005 · see citing works
Molecular mechanisms of transgenerational epigenetic inheritance
Fitz-James, M. H., & Cavalli, G. (2022) · Nature Reviews Genetics · doi:10.1038/s41576-021-00438-5 · Cited by 589 · see citing works
A review of solar and visible light active TiO2 photocatalysis for treating bacteria, cyanotoxins and contaminants of emerging concern
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Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure
Kundakovic, M., Gudsnuk, K., Franks, B., Madrid, J., Miller, R. L., Perera, F. P., & Champagne, F. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214056110 · Cited by 490 · see citing works
Developmental origins of health and disease: a paradigm for understanding disease cause and prevention
Heindel, J. J., & Vandenberg, L. N. (2015) · Current Opinion in Pediatrics · doi:10.1097/mop.0000000000000191 · Cited by 439 · see citing works
Endocrine disruptors and obesity
Heindel, J. J., Newbold, R. R., & Schug, T. T. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.163 · Cited by 429 · see citing works
Environmentally induced epigenetic transgenerational inheritance of disease
Nilsson, E. E., Sadler‐Riggleman, I., & Skinner, M. K. (2018) · Current Zoology · doi:10.1093/eep/dvy016 · Cited by 412 · see citing works
Transgenerational Inheritance of Increased Fat Depot Size, Stem Cell Reprogramming, and Hepatic Steatosis Elicited by Prenatal Exposure to the Obesogen Tributyltin in Mice
Chamorro-García, R., Sahu, M. B., Abbey, R. J., Laude, J., Pham, N., & Blumberg, B. (2013) · Environmental Health Perspectives · doi:10.1289/ehp.1205701 · Cited by 330 · see citing works
Gestational exposure to endocrine-disrupting chemicals and reciprocal social, repetitive, and stereotypic behaviors in 4- and 5-year-old children: the HOME Study
Braun, J. M., Kalkbrenner, A. E., Just, A. C., Yolton, K., Calafat, A. M., Sjödin, A., Hauser, R., Webster, G. M., Chen, A., & Lanphear, B. P. (2014) · Environmental Health Perspectives · doi:10.1289/ehp.1307261 · Cited by 328 · see citing works
Effects of the environmental estrogenic contaminants bisphenol A and 17α-ethinyl estradiol on sexual development and adult behaviors in aquatic wildlife species
Bhandari, R. K., Deem, S. L., Holliday, D. K., Jandegian, C. M., Kassotis, C. D., Nagel, S. C., Tillitt, D. E., Saal, F. S. V., & Rosenfeld, C. S. (2014) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2014.09.014 · Cited by 298 · see citing works
Current Knowledge on Endocrine Disrupting Chemicals (EDCs) from Animal Biology to Humans, from Pregnancy to Adulthood: Highlights from a National Italian Meeting
Street, M. E., Angelini, S., Bernasconi, S., Burgio, E., Cassio, A., Catellani, C., Cirillo, F., Deodati, A., Fabbrizi, E., Fanos, V., et al. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19061647 · Cited by 261 · see citing works
Endocrine disruptor induction of epigenetic transgenerational inheritance of disease
Skinner, M. K. (2014) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2014.07.019 · Cited by 239 · see citing works
Alterations in sperm DNA methylation, non-coding RNA and histone retention associate with DDT-induced epigenetic transgenerational inheritance of disease
Skinner, M. K., Maamar, M. B., Sadler‐Riggleman, I., Beck, D., Nilsson, E. E., McBirney, M., Klukovich, R., Xie, Y., Tang, C., & Yan, W. (2018) · Epigenetics & Chromatin · doi:10.1186/s13072-018-0178-0 · Cited by 221 · see citing works
Environmental stress and epigenetic transgenerational inheritance
Skinner, M. K. (2014) · BMC Medicine · doi:10.1186/s12916-014-0153-y · Cited by 225 · see citing works
Evolution of DOHaD: the impact of environmental health sciences
Haugen, A. C., Schug, T. T., Collman, G. W., & Heindel, J. J. (2014) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174414000580 · Cited by 212 · see citing works
Elucidating the links between endocrine disruptors and neurodevelopment
Schug, T. T., Blawas, A. M., Gray, K., Heindel, J. J., & Lawler, C. P. (2015) · Endocrinology · doi:10.1210/en.2014-1734 · Cited by 204 · see citing works
Bisphenol-A and diethylstilbestrol exposure induces the expression of breast cancer associated long noncoding RNA HOTAIR in vitro and in vivo
Bhan, A., Hussain, I., Ansari, K. I., Bobzean, S. A. M., Perrotti, L. I., & Mandal, S. S. (2014) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2014.02.002 · Cited by 182 · see citing works
Transgenerational effects from early developmental exposures to bisphenol A or 17α-ethinylestradiol in medaka, Oryzias latipes
Bhandari, R. K., Saal, F. S. V., & Tillitt, D. E. (2015) · Scientific Reports · doi:10.1038/srep09303 · Cited by 176 · see citing works
Developmental origins of epigenetic transgenerational inheritance
Hanson, M. A., & Skinner, M. K. (2016) · Current Zoology · doi:10.1093/eep/dvw002 · Cited by 171 · see citing works
DNA methylation: a mechanism linking environmental chemical exposures to risk of autism spectrum disorders?
Keil, K. P., & Lein, P. J. (2016) · Environmental Epigenetics · doi:10.1093/eep/dvv012 · Cited by 167 · see citing works
Epigenetic Transgenerational Inheritance of Obesity Susceptibility
King, S. E., & Skinner, M. K. (2020) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2020.02.009 · Cited by 164 · see citing works
Implications of Prenatal Steroid Perturbations for Neurodevelopment, Behavior, and Autism
Gore, A. C., Martien, K. M., Gagnidze, K., & Pfaff, D. W. (2014) · Endocrine Reviews · doi:10.1210/er.2013-1122 · Cited by 159 · see citing works
Bisphenol-A: Epigenetic Reprogramming and Effects on Reproduction and Behavior
Mileva, G. R., Baker, S., Konkle, A. T. M., & Bielajew, C. H. (2014) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph110707537 · Cited by 160 · see citing works
Transgenerational effects of prenatal bisphenol A on social recognition
Wolstenholme, J. T., Goldsby, J. A., & Rissman, E. F. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.09.007 · Cited by 157 · see citing works
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The role of non-genetic inheritance in evolutionary rescue: epigenetic buffering, heritable bet hedging and epigenetic traps
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
Endocrine-disrupting chemicals: Effects on neuroendocrine systems and the neurobiology of social behavior
Gore, A. C., Krishnan, K., & Reilly, M. P. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.11.006 · Cited by 152 · see citing works
Why Endocrine Disrupting Chemicals (EDCs) Challenge Traditional Risk Assessment and How to Respond
Futran Fuhrman, V., Tal, A., & Arnon, S. (2015) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2014.12.012 · Cited by 152 · see citing works
Bisphenol A Exposure in Children With Autism Spectrum Disorders
Stein, T. P., Schluter, M. D., Steer, R. A., Guo, L., & Ming, X. (2015) · Autism Research · doi:10.1002/aur.1444 · Cited by 151 · see citing works
Neuropsychopathology of Autism Spectrum Disorder: Complex Interplay of Genetic, Epigenetic, and Environmental Factors
Bhandari, R., Paliwal, J. K., & Kuhad, A. (2020) · Advances in neurobiology · doi:10.1007/978-3-030-30402-7_4 · Cited by 156 · see citing works
Current concepts in neuroendocrine disruption
León‐Olea, M., Martyniuk, C. J., Orlando, E. F., Ottinger, M. A., Rosenfeld, C. S., Wolstenholme, J. T., & Trudeau, V. L. (2014) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2014.02.005 · Cited by 144 · see citing works
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Prenatal bisphenol A exposure alters sex-specific estrogen receptor expression in the neonatal rat hypothalamus and amygdala
Cao, J., Rebuli, M. E., Rogers, J., Todd, K. L., Leyrer, S. M., Ferguson, S. A., & Patisaul, H. B. (2013) · Toxicological Sciences · doi:10.1093/toxsci/kft035 · Cited by 141 · see citing works
Environmentally Induced Epigenetic Transgenerational Inheritance of Altered Sertoli Cell Transcriptome and Epigenome: Molecular Etiology of Male Infertility
Guerrero‐Bosagna, C., Savenkova, M. I., Haque, M. M., Nilsson, E. E., & Skinner, M. K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059922 · Cited by 137 · see citing works
Transgenerational Epigenetic Effects on Brain Functions
Bohacek, J., Gapp, K., Saab, B. J., & Mansuy, I. M. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.08.019 · Cited by 137 · see citing works
Early life epigenetic programming and transmission of stress‐induced traits in mammals: How and when can environmental factors influence traits and their transgenerational inheritance?
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
Conjugated bisphenol A in maternal serum in relation to miscarriage risk
Lathi, R. B., Liebert, C. A., Brookfield, K., Taylor, J. A., Saal, F. S. V., Fujimoto, V. Y., & Baker, V. L. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.03.024 · Cited by 130 · see citing works
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Epigenetic and Neurological Impairments Associated with Early Life Exposure to Persistent Organic Pollutants
Grova, N., Schroeder, H., Olivier, J. L., & Turner, J. D. (2019) · International Journal of Genomics · doi:10.1155/2019/2085496 · Cited by 132 · see citing works
Bisphenol A and phthalate endocrine disruption of parental and social behaviors
Rosenfeld, C. S. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00057 · Cited by 119 · see citing works
Role of epigenetic transgenerational inheritance in generational toxicology
Nilsson, E. E., Maamar, M. B., & Skinner, M. K. (2022) · Current Zoology · doi:10.1093/eep/dvac001 · Cited by 118 · see citing works
Lifelong Exposure to Bisphenol A Alters Cardiac Structure/Function, Protein Expression, and DNA Methylation in Adult Mice
Patel, B. B., Raad, M., Sebag, I. A., & Chalifour, L. E. (2013) · Toxicological Sciences · doi:10.1093/toxsci/kft026 · Cited by 114 · see citing works
Pathological brain plasticity and cognition in the offspring of males subjected to postnatal traumatic stress
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
Nature, nurture and epigenetics
Crews, D. P., Gillette, R., Miller-Crews, I., Gore, A. C., & Skinner, M. K. (2014) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2014.07.013 · Cited by 117 · see citing works
Autism genes are selectively targeted by environmental pollutants including pesticides, heavy metals, bisphenol A, phthalates and many others in food, cosmetics or household products
Carter, C. J., & Blizard, R. (2016) · Neurochemistry International · doi:10.1016/j.neuint.2016.10.011 · Cited by 114 · see citing works
Minireview: transgenerational epigenetic inheritance: focus on endocrine disrupting compounds
Rissman, E. F., & Adli, M. (2014) · Endocrinology · doi:10.1210/en.2014-1123 · Cited by 113 · see citing works
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F0 maternal BPA exposure induced glucose intolerance of F2 generation through DNA methylation change in Gck
Li, G., Chang, H., Xia, W., Mao, Z., Li, Y., & Xu, S. (2014) · Toxicology Letters · doi:10.1016/j.toxlet.2014.04.012 · Cited by 111 · see citing works
Cellular and molecular features of EDC exposure: consequences for the GnRH network
Rodríguez, D. L., Franssen, D., Bakker, J., Lomniczi, A., & Parent, A. (2020) · Nature Reviews Endocrinology · doi:10.1038/s41574-020-00436-3 · Cited by 109 · see citing works
CLARITY‐BPA academic laboratory studies identify consistent low‐dose Bisphenol A effects on multiple organ systems
Prins, G. S., Patisaul, H. B., Belcher, S. M., & Vandenberg, L. N. (2018) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/bcpt.13125 · Cited by 107 · see citing works
Anxiogenic effects of developmental bisphenol A exposure are associated with gene expression changes in the juvenile rat amygdala and mitigated by soy
Patisaul, H. B., Sullivan, A. W., Radford, M. E., Walker, D. M., Adewale, H. B., Winnik, B., Coughlin, J. L., Buckley, B., & Gore, A. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043890 · Cited by 106 · see citing works
Assessment of sex specific endocrine disrupting effects in the prenatal and pre-pubertal rodent brain
Rebuli, M. E., & Patisaul, H. B. (2015) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2015.08.021 · Cited by 104 · see citing works
Epigenetic and transgenerational mechanisms in infection-mediated neurodevelopmental disorders
Weber‐Stadlbauer, U. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.78 · Cited by 98 · see citing works
Cultural Epigenetics
Jablonka, E. (2016) · The Sociological Review · doi:10.1111/2059-7932.12012 · Cited by 98 · see citing works
Transgenerational Effects of Bisphenol A on Gene Expression and DNA Methylation of Imprinted Genes in Brain
Drobná, Z., Henriksen, A. D. P., Wolstenholme, J. T., Montiel, C., Lambeth, P. S., Shang, S., Harris, E. P., Zhou, C., Flaws, J. A., Adli, M., et al. (2017) · Endocrinology · doi:10.1210/en.2017-00730 · Cited by 97 · see citing works
Self-citation
Perinatal exposure to endocrine disruptors: sex, timing and behavioral endpoints
Palanza, P., Nagel, S. C., Parmigiani, S., & Saal, F. S. V. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.11.017 · Cited by 96 · see citing works
Epigenomic strategies at the interface of genetic and environmental risk factors for autism
LaSalle, J. M. (2013) · Journal of Human Genetics · doi:10.1038/jhg.2013.49 · Cited by 95 · see citing works
Environmentally Induced Epigenetic Transgenerational Inheritance of Reproductive Disease1
Nilsson, E. E., & Skinner, M. K. (2015) · Biology of Reproduction · doi:10.1095/biolreprod.115.134817 · Cited by 91 · see citing works
Epigenetic impacts of endocrine disruptors in the brain
Walker, D. M., & Gore, A. C. (2017) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.09.002 · Cited by 94 · see citing works
Parental co-exposure to bisphenol A and nano-TiO2 causes thyroid endocrine disruption and developmental neurotoxicity in zebrafish offspring
Guo, Y., Chen, L., Wu, J., Hua, J., Yang, L., Wang, Q., Zhang, W., Lee, J., & Zhou, B. (2018) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2018.09.007 · Cited by 93 · see citing works
Transgenerational Inheritance of Environmentally Induced Epigenetic Alterations during Mammalian Development
Legoff, L., D’Cruz, S. C., Tevosian, S. G., Primig, M., & Smagulova, F. O. (2019) · Cells · doi:10.3390/cells8121559 · Cited by 91 · see citing works
Opening the black box of endocrine disruption of brain development: Lessons from the characterization of Bisphenol A
Nesan, D., Sewell, L., & Kurrasch, D. M. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.12.001 · Cited by 92 · see citing works
Atrazine induced transgenerational reproductive effects in medaka (Oryzias latipes)
Cleary, J. A., Tillitt, D. E., Saal, F. S. V., Nicks, D. K., Claunch, R. A., & Bhandari, R. K. (2019) · Environmental Pollution · doi:10.1016/j.envpol.2019.05.013 · Cited by 92 · see citing works
The plastic health map: A systematic evidence map of human health studies on plastic-associated chemicals
Seewoo, B. J., Goodes, L. M., Mofflin, L., Mulders, Y. R., Wong, E. V. S., Toshniwal, P., Brunner, M., Alex, J., Johnston, B., Elagali, A. E. M., et al. (2023) · Environment International · doi:10.1016/j.envint.2023.108225 · Cited by 98 · see citing works
Epigenetics and phenotypic variability: some interesting insights from birds
Frésard, L., Morisson, M., Brun, J. M. J. M., Collin, A., Pain, B., Minvielle, F., & Frédérique Pitel, A. (2013) · Genetics Selection Evolution · doi:10.1186/1297-9686-45-16 · Cited by 91 · see citing works
Prenatal Polycyclic Aromatic Hydrocarbon, Adiposity, Peroxisome Proliferator-Activated Receptor (PPAR) γ Methylation in Offspring, Grand-Offspring Mice
Yan, Z., Zhang, H., Maher, C., Arteaga‐Solis, E., Champagne, F. A., Wu, L., McDonald, J. D., Yan, B., Schwartz, G. J., & Miller, R. L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110706 · Cited by 89 · see citing works
Bisphenol AF compromises blood-testis barrier integrity and sperm quality in mice
Wu, D., Huang, C., Jiao, X., Ding, Z., Zhang, S.-X., Miao, Y., & Huo, L. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.124410 · Cited by 89 · see citing works
Multi- and Transgenerational Outcomes of an Exposure to a Mixture of Endocrine-Disrupting Chemicals (EDCs) on Puberty and Maternal Behavior in the Female Rat
Rodríguez, D. L., Aylwin, C. F., Delli, V., Sevrin, E., Campanile, M., Martin, M. J., Franssen, D., Gérard, A., Blacher, S., Tirelli, E., et al. (2021) · Environmental Health Perspectives · doi:10.1289/ehp8795 · Cited by 90 · see citing works
Are endocrine disrupting compounds environmental risk factors for autism spectrum disorder?
Moosa, A., Shu, H. T., Sarachana, T., & Hu, V. W. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.10.003 · Cited by 86 · see citing works
Impact of low dose oral exposure to bisphenol A (BPA) on the neonatal rat hypothalamic and hippocampal transcriptome: a clarity-BPA consortium study
Arambula, S. E., Belcher, S. M., Planchart, A., Turner, S. D., & Patisaul, H. B. (2016) · Endocrinology · doi:10.1210/en.2016-1339 · Cited by 87 · see citing works
Epigenetic Findings in Autism: New Perspectives for Therapy
Siniscalco, D., Cirillo, A., Bradstreet, J. J., & Antonucci, N. (2013) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph10094261 · Cited by 87 · see citing works
Direct and transgenerational effects of low doses of perinatal di-(2-ethylhexyl) phthalate (DEHP) on social behaviors in mice
Quinnies, K. M., Harris, E. P., Snyder, R. W., Sumner, S. S., & Rissman, E. F. (2017) · PLOS ONE · doi:10.1371/journal.pone.0171977 · Cited by 84 · see citing works
Self-citation
Elusive inheritance: Transgenerational effects and epigenetic inheritance in human environmental disease
Martos, S. N., Tang, W., & Wang, Z. (2015) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2015.02.011 · Cited by 83 · see citing works
Investigation of the effects of subchronic low dose oral exposure to bisphenol A (BPA) and ethinyl estradiol (EE) on estrogen receptor expression in the juvenile and adult female rat hypothalamus
Rebuli, M. E., Cao, J., Sluzas, E., Delclos, K. B., Camacho, L., Lewis, S. M., Vanlandingham, M. M., & Patisaul, H. B. (2014) · Toxicological Sciences · doi:10.1093/toxsci/kfu074 · Cited by 83 · see citing works
Marked for Life: Epigenetic Effects of Endocrine Disrupting Chemicals
Jacobs, M. N., Marczylo, E. L., Guerrero‐Bosagna, C., & Rüegg, J. (2017) · Annual Review of Environment and Resources · doi:10.1146/annurev-environ-102016-061111 · Cited by 81 · see citing works
A novel model for neuroendocrine toxicology: neurobehavioral effects of BPA exposure in a prosocial species, the prairie vole (Microtus ochrogaster)
Sullivan, A. W., Beach, E. C., Stetzik, L. A., Perry, A., D'Addezio, A. S., Cushing, B. S., & Patisaul, H. B. (2014) · Endocrinology · doi:10.1210/en.2014-1379 · Cited by 79 · see citing works
Association of Exposure to Diethylstilbestrol During Pregnancy With Multigenerational Neurodevelopmental Deficits
Kioumourtzoglou, M., Coull, B. A., O’Reilly, É. J., Ascherio, A., & Weisskopf, M. G. (2018) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2018.0727 · Cited by 79 · see citing works
Roll Over Weismann: Extracellular Vesicles in the Transgenerational Transmission of Environmental Effects
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Authors: Wolstenholme, J. T., Edwards, M., Shetty, S. R. J., Gatewood, J. D., Taylor, J. A., Rissman, E. F., & Connelly, J. J.
Affiliations: Departments of Biochemistry and Molecular Genetics (J.T.W., M.E., S.R.J.S., J.D.G., E.F.R.)
University of Missouri (US)
University of Virginia (US)
Corresponding author: Rissman, Emilie F.
ORCID: Wolstenholme, Jennifer T.
Taylor, Julia A.
Rissman, Emilie F.
Connelly, Jessica J.
Venue: Endocrinology
Publisher: The Endocrine Society
Published: 2012-06-15
Volume: 153
Issue: 8
Pages: 3828-3838
ISSN: 0013-7227 (ISSN-L)
1945-7170
DOI: 10.1210/en.2012-1195
PMC: PMC3404345
OpenAlex: W2124958203
Cited by: 319
References: 79
Citations by year: 2026: 4 · 2025: 12 · 2024: 13 · 2023: 16 · 2022: 15 · 2021: 22 · 2020: 24 · 2019: 24 · 2018: 29 · 2017: 31 · 2016: 29 · 2015: 29 · 2014: 38 · 2013: 25 · 2012: 8
FWCI: 22.14
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Endocrinology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Autism Speaks (AS4802)
National Institutes of Health
National Institute of Mental Health (R01MH086711)
National Institute of Environmental Health Sciences (F32ES019404)
Topics: Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
Keywords: bisphenol A, endocrine disruptors, transgenerational effects, prenatal exposure, social behavior, estrogen receptor, oxytocin, vasopressin, brain gene expression, epigenetic modifications, gene-environment interaction, developmental neurotoxicity
MeSH terms: Bisphenol A Compounds, Animals, Benzhydryl Compounds, Female, Male, Mice, Inbred C57BL, Phenols, Pregnancy, Prenatal Exposure Delayed Effects, Social Behavior, Gene Expression, Oligonucleotide Array Sequence Analysis, Mice, Endocrine Disruptors, Real-Time Polymerase Chain Reaction

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Gestational Exposure to Bisphenol A Produces Transgenerational Changes in Behaviors and Gene Expression

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