Sex differences in the effects of prenatal bisphenol A exposure on autism-related genes and their relationships with the hippocampus functions.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
13 01 2021
13 01 2021
Historique:
received:
10
08
2020
accepted:
21
12
2020
entrez:
14
1
2021
pubmed:
15
1
2021
medline:
11
8
2021
Statut:
epublish
Résumé
Our recent study has shown that prenatal exposure to bisphenol A (BPA) altered the expression of genes associated with autism spectrum disorder (ASD). In this study, we further investigated the effects of prenatal BPA exposure on ASD-related genes known to regulate neuronal viability, neuritogenesis, and learning/memory, and assessed these functions in the offspring of exposed pregnant rats. We found that prenatal BPA exposure increased neurite length, the number of primary neurites, and the number of neurite branches, but reduced the size of the hippocampal cell body in both sexes of the offspring. However, in utero exposure to BPA decreased the neuronal viability and the neuronal density in the hippocampus and impaired learning/memory only in the male offspring while the females were not affected. Interestingly, the expression of several ASD-related genes (e.g. Mief2, Eif3h, Cux1, and Atp8a1) in the hippocampus were dysregulated and showed a sex-specific correlation with neuronal viability, neuritogenesis, and/or learning/memory. The findings from this study suggest that prenatal BPA exposure disrupts ASD-related genes involved in neuronal viability, neuritogenesis, and learning/memory in a sex-dependent manner, and these genes may play an important role in the risk and the higher prevalence of ASD in males subjected to prenatal BPA exposure.
Identifiants
pubmed: 33441873
doi: 10.1038/s41598-020-80390-2
pii: 10.1038/s41598-020-80390-2
pmc: PMC7806752
doi:
Substances chimiques
Benzhydryl Compounds
0
Phenols
0
bisphenol A
MLT3645I99
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1241Références
Goldinger, D. M. et al. Endocrine activity of alternatives to BPA found in thermal paper in Switzerland. Regul. Toxicol. Pharmacol. 71, 453–462 (2015).
pubmed: 25579646
doi: 10.1016/j.yrtph.2015.01.002
Dodson, R. E. et al. Endocrine disruptors and asthma-associated chemicals in consumer products. Environ. Health Perspect. 120, 935–943 (2012).
pubmed: 22398195
pmcid: 3404651
doi: 10.1289/ehp.1104052
Hirai, H. et al. Organic micropollutants in marine plastics debris from the open ocean and remote and urban beaches. Mar. Pollut. Bull. 62, 1683–1692 (2011).
pubmed: 21719036
doi: 10.1016/j.marpolbul.2011.06.004
Campanale, C., Massarelli, C., Savino, I., Locaputo, V. & Uricchio, V. F. A detailed review study on potential effects of microplastics and additives of concern on human health. Int. J. Environ. Res. Public Health 17, 1212 (2020).
pmcid: 7068600
doi: 10.3390/ijerph17041212
Park, S.-R., Park, S.-J., Jeong, M.-J., Choi, J. C. & Kim, M. Fast and simple determination and exposure assessment of bisphenol A, phenol, p-tert-butylphenol, and diphenylcarbonate transferred from polycarbonate food-contact materials to food simulants. Chemosphere 203, 300–306 (2018).
pubmed: 29625319
doi: 10.1016/j.chemosphere.2018.03.185
Brotons, J. A., Olea-Serrano, M. F., Villalobos, M., Pedraza, V. & Olea, N. Xenoestrogens released from lacquer coatings in food cans. Environ. Health Perspect. 103, 608–612. https://doi.org/10.1289/ehp.95103608 (1995).
doi: 10.1289/ehp.95103608
pubmed: 7556016
pmcid: 1519121
Habib, C. M. & Kugel, G. Estrogenicity of resin-based composites and sealants in dentistry. Environ. Health Perspect. 104, 808. https://doi.org/10.1289/ehp.104-1469430 (1996).
doi: 10.1289/ehp.104-1469430
pubmed: 8875145
pmcid: 1469430
Krishnan, A. V., Stathis, P., Permuth, S. F., Tokes, L. & Feldman, D. Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 132, 2279–2286. https://doi.org/10.1210/endo.132.6.8504731 (1993).
doi: 10.1210/endo.132.6.8504731
pubmed: 8504731
Calafat, A. M., Ye, X., Wong, L. Y., Reidy, J. A. & Needham, L. L. Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003–2004. Environ. Health Perspect. 116, 39–44. https://doi.org/10.1289/ehp.10753 (2008).
doi: 10.1289/ehp.10753
pubmed: 18197297
Vandenberg, L. N., Hauser, R., Marcus, M., Olea, N. & Welshons, W. V. Human exposure to bisphenol A (BPA). Reprod. Toxicol. 24, 139–177 (2007).
pubmed: 17825522
doi: 10.1016/j.reprotox.2007.07.010
Balakrishnan, B., Henare, K., Thorstensen, E. B., Ponnampalam, A. P. & Mitchell, M. D. Transfer of bisphenol A across the human placenta. Am. J. Obst. Gynecol. 202, 393 (2010).
doi: 10.1016/j.ajog.2010.01.025
Takahashi, O. & Oishi, S. Disposition of orally administered 2, 2-Bis (4-hydroxyphenyl) propane (Bisphenol A) in pregnant rats and the placental transfer to fetuses. Environ. Health Perspect. 108, 931–935 (2000).
pubmed: 11049811
pmcid: 1240124
doi: 10.1289/ehp.00108931
Schönfelder, G. et al. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ. Health Perspect. 110, A703–A707 (2002).
pubmed: 12417499
pmcid: 1241091
doi: 10.1289/ehp.021100703
Itoh, K., Yaoi, T. & Fushiki, S. Bisphenol A, an endocrine-disrupting chemical, and brain development. Neuropathology 32, 447–457 (2012).
pubmed: 22239237
doi: 10.1111/j.1440-1789.2011.01287.x
Sun, Y., Nakashima, M. N., Takahashi, M., Kuroda, N. & Nakashima, K. Determination of bisphenol A in rat brain by microdialysis and column switching high-performance liquid chromatography with fluorescence detection. Biomed. Chromatogr. 16, 319–326 (2002).
pubmed: 12210505
doi: 10.1002/bmc.161
Lee, J. et al. Bisphenol A distribution in serum, urine, placenta, breast milk, and umbilical cord serum in a birth panel of mother–neonate pairs. Sci. Total Environ. 626, 1494–1501 (2018).
pubmed: 29146078
doi: 10.1016/j.scitotenv.2017.10.042
Thongkorn, S. et al. Sex differences in the effects of prenatal bisphenol A exposure on genes associated with autism spectrum disorder in the hippocampus. Sci. Rep. 9, 3038 (2019).
pubmed: 30816183
pmcid: 6395584
doi: 10.1038/s41598-019-39386-w
Moosa, A., Shu, H., Sarachana, T. & Hu, V. W. Are endocrine disrupting compounds environmental risk factors for autism spectrum disorder?. Horm. Behav. 101, 13–21 (2018).
pubmed: 29042182
doi: 10.1016/j.yhbeh.2017.10.003
Kardas, F. et al. Increased serum phthalates (MEHP, DEHP) and bisphenol A concentrations in children with autism spectrum disorder: the role of endocrine disruptors in autism etiopathogenesis. J. Child Neurol. 31, 629–635. https://doi.org/10.1177/0883073815609150 (2016).
doi: 10.1177/0883073815609150
pubmed: 26450281
Kondolot, M. et al. Plasma phthalate and bisphenol a levels and oxidant–antioxidant status in autistic children. Environ. Toxicol. Pharmacol. 43, 149–158. https://doi.org/10.1016/j.etap.2016.03.006 (2016).
doi: 10.1016/j.etap.2016.03.006
pubmed: 26991849
Stein, T. P., Schluter, M. D., Steer, R. A., Guo, L. & Ming, X. Bisphenol A exposure in children with autism spectrum disorders. Autism Res. Off. J. Int. Soc. Autism Res. 8, 272–283. https://doi.org/10.1002/aur.1444 (2015).
doi: 10.1002/aur.1444
Sukjamnong, S. et al. Prenatal exposure to bisphenol A alters the transcriptome-interactome profiles of genes associated with Alzheimer’s disease in the offspring hippocampus. Sci. Rep. 10, 9487. https://doi.org/10.1038/s41598-020-65229-0 (2020).
doi: 10.1038/s41598-020-65229-0
pubmed: 32528016
pmcid: 7289845
Tian, Y. H., Baek, J. H., Lee, S. Y. & Jang, C. G. Prenatal and postnatal exposure to bisphenol a induces anxiolytic behaviors and cognitive deficits in mice. Synapse 64, 432–439 (2010).
pubmed: 20169576
doi: 10.1002/syn.20746
Braun, J. M. et al. Impact of early-life bisphenol A exposure on behavior and executive function in children. Pediatrics 128, 873–882 (2011).
pubmed: 22025598
pmcid: 3208956
doi: 10.1542/peds.2011-1335
Hu, V. W. & Steinberg, M. E. Novel clustering of items from the autism diagnostic interview-revised to define phenotypes within autism spectrum disorders. Autism Res. 2, 67–77 (2009).
pubmed: 19455643
pmcid: 2737479
doi: 10.1002/aur.72
Pichitpunpong, C. et al. Phenotypic subgrouping and multi-omics analyses reveal reduced diazepam-binding inhibitor (DBI) protein levels in autism spectrum disorder with severe language impairment. PLoS ONE 14, e0214198 (2019).
pubmed: 30921354
pmcid: 6438570
doi: 10.1371/journal.pone.0214198
Hu, V. W. et al. Gene expression profiling differentiates autism case–controls and phenotypic variants of autism spectrum disorders: evidence for circadian rhythm dysfunction in severe autism. Autism Res. 2, 78–97 (2009).
pubmed: 19418574
pmcid: 2737477
doi: 10.1002/aur.73
Miles, J. H. Autism spectrum disorders—a genetics review. Genet. Med. 13, 278–294 (2011).
pubmed: 21358411
doi: 10.1097/GIM.0b013e3181ff67ba
Hu, V. W. & Bi, C. Phenotypic subtyping and re-analyses of existing transcriptomic data from autistic probands in simplex families reveal differentially expressed and ASD trait-associated genes. Front. Neurol. 11, 1502 (2020).
doi: 10.3389/fneur.2020.578972
Lee, E. C. & Hu, V. W. Phenotypic subtyping and re-analysis of existing methylation data from autistic probands in simplex families reveal ASD subtype-associated differentially methylated genes and biological functions. Int. J. Mol. Sci. 21, 6877 (2020).
pmcid: 7555936
doi: 10.3390/ijms21186877
Maenner, M. J., Shaw, K. A. & Baio, J. Prevalence of autism spectrum disorder among children aged 8 years—autism and developmental disabilities monitoring network, 11 sites, United States, 2016. MMWR Surveill. Summ. 69, 1 (2020).
pubmed: 32214087
pmcid: 7119644
doi: 10.15585/mmwr.ss6904a1
Baron-Cohen, S. et al. Why are autism spectrum conditions more prevalent in males?. PLoS Biol. 9, e1001081 (2011).
pubmed: 21695109
pmcid: 3114757
doi: 10.1371/journal.pbio.1001081
Hu, V. W., Sarachana, T., Sherrard, R. M. & Kocher, K. M. Investigation of sex differences in the expression of RORA and its transcriptional targets in the brain as a potential contributor to the sex bias in autism. Mol. Autism 6, 7 (2015).
pubmed: 26056561
pmcid: 4459681
doi: 10.1186/2040-2392-6-7
Sarachana, T. & Hu, V. W. Differential recruitment of coregulators to the RORA promoter adds another layer of complexity to gene (dys) regulation by sex hormones in autism. Mol. Autism 4, 1–17 (2013).
doi: 10.1186/2040-2392-4-39
Sarachana, T. & Hu, V. W. Genome-wide identification of transcriptional targets of RORA reveals direct regulation of multiple genes associated with autism spectrum disorder. Mol. Autism 4, 1–19 (2013).
doi: 10.1186/2040-2392-4-14
Sarachana, T., Xu, M., Wu, R.-C. & Hu, V. W. Sex hormones in autism: androgens and estrogens differentially and reciprocally regulate RORA, a novel candidate gene for autism. PLoS ONE 6, e17116 (2011).
pubmed: 21359227
pmcid: 3040206
doi: 10.1371/journal.pone.0017116
Saeliw, T. et al. Integrated genome-wide Alu methylation and transcriptome profiling analyses reveal novel epigenetic regulatory networks associated with autism spectrum disorder. Mol. Autism 9, 27 (2018).
pubmed: 29686828
pmcid: 5902935
doi: 10.1186/s13229-018-0213-9
Tangsuwansri, C. et al. Investigation of epigenetic regulatory networks associated with autism spectrum disorder (ASD) by integrated global LINE-1 methylation and gene expression profiling analyses. PLoS ONE 13, e0201071 (2018).
pubmed: 30036398
pmcid: 6056057
doi: 10.1371/journal.pone.0201071
Lasalle, J. M. Autism genes keep turning up chromatin. OA autism 1, 14 (2013).
pubmed: 24404383
pmcid: 3882126
doi: 10.13172/2052-7810-1-2-610
Sun, W. et al. Histone acetylome-wide association study of autism spectrum disorder. Cell 167, 1385–1397 (2016).
pubmed: 27863250
doi: 10.1016/j.cell.2016.10.031
Sarachana, T., Zhou, R., Chen, G., Manji, H. K. & Hu, V. W. Investigation of post-transcriptional gene regulatory networks associated with autism spectrum disorders by microRNA expression profiling of lymphoblastoid cell lines. Genome Med. 2, 23 (2010).
pubmed: 20374639
pmcid: 2873801
doi: 10.1186/gm144
Roberts, E. M. et al. Maternal residence near agricultural pesticide applications and autism spectrum disorders among children in the California Central Valley. Environ. Health Perspect. 115, 1482–1489 (2007).
pubmed: 17938740
pmcid: 2022638
doi: 10.1289/ehp.10168
Oulhote, Y. et al. Gestational exposures to phthalates and folic acid, and autistic traits in canadian children. Environ. Health Perspect. 128, 027004 (2020).
pmcid: 7064316
doi: 10.1289/EHP5621
Carter, C. J. & Blizard, R. Autism genes are selectively targeted by environmental pollutants including pesticides, heavy metals, bisphenol A, phthalates and many others in food, cosmetics or household products. Neurochem. Int. 101, 83–109 (2016).
doi: 10.1016/j.neuint.2016.10.011
von Ehrenstein, O. S. et al. Prenatal and infant exposure to ambient pesticides and autism spectrum disorder in children: population based case-control study. BMJ 364, l962 (2019).
doi: 10.1136/bmj.l962
Kalkbrenner, A. E. et al. Maternal smoking during pregnancy and the prevalence of autism spectrum disorders, using data from the autism and developmental disabilities monitoring network. Environ. Health Perspect. 120, 1042–1048 (2012).
pubmed: 22534110
pmcid: 3404663
doi: 10.1289/ehp.1104556
Adams, J. B. et al. Toxicological status of children with autism vs. neurotypical children and the association with autism severity. Biol. Trace Elem. Res. 151, 171–180 (2013).
pubmed: 23192845
doi: 10.1007/s12011-012-9551-1
Geier, D. A., Audhya, T., Kern, J. K. & Geier, M. R. Blood mercury levels in autism spectrum disorder: Is there a threshold level?. Acta Neurobiol. Exp. 70, 177–186 (2010).
Arambula, S. E., Belcher, S. M., Planchart, A., Turner, S. D. & Patisaul, H. B. Impact of low dose oral exposure to bisphenol A (BPA) on the neonatal rat hypothalamic and hippocampal transcriptome: A CLARITY-BPA consortium study. Endocrinology 157, 3856–3872. https://doi.org/10.1210/en.2016-1339 (2016).
doi: 10.1210/en.2016-1339
pubmed: 27571134
pmcid: 5045502
Mathisen, G. H. et al. Prenatal exposure to bisphenol A interferes with the development of cerebellar granule neurons in mice and chicken. Int. J. Dev. Neurosci. Off. J. Int. Soc. Dev. Neurosci. 31, 762–769. https://doi.org/10.1016/j.ijdevneu.2013.09.009 (2013).
doi: 10.1016/j.ijdevneu.2013.09.009
Castro, B., Sanchez, P., Torres, J. M. & Ortega, E. Effects of adult exposure to bisphenol a on genes involved in the physiopathology of rat prefrontal cortex. PLoS ONE 8, e73584. https://doi.org/10.1371/journal.pone.0073584 (2013).
doi: 10.1371/journal.pone.0073584
pubmed: 24066056
pmcid: 3774751
Hovey, D. et al. Associations between oxytocin-related genes and autistic-like traits. Soc. Neurosci. 9, 378–386 (2014).
pubmed: 24635660
doi: 10.1080/17470919.2014.897995
Crider, A., Thakkar, R., Ahmed, A. O. & Pillai, A. Dysregulation of estrogen receptor beta (ERβ), aromatase (CYP19A1), and ER co-activators in the middle frontal gyrus of autism spectrum disorder subjects. Mol. Autism 5, 46 (2014).
pubmed: 25221668
pmcid: 4161836
doi: 10.1186/2040-2392-5-46
MacLusky, N. J., Hajszan, T. & Leranth, C. The environmental estrogen bisphenol A inhibits estradiol-induced hippocampal synaptogenesis. Environ. Health Perspect. 113, 675–679 (2005).
pubmed: 15929888
pmcid: 1257590
doi: 10.1289/ehp.7633
Kim, K. et al. Potencies of bisphenol A on the neuronal differentiation and hippocampal neurogenesis. J. Toxicol. Environ. Health Part A 72, 1343–1351 (2009).
doi: 10.1080/15287390903212501
Wolstenholme, J. T. et al. Gestational exposure to bisphenol a produces transgenerational changes in behaviors and gene expression. Endocrinology 153, 3828–3838. https://doi.org/10.1210/en.2012-1195 (2012).
doi: 10.1210/en.2012-1195
pubmed: 22707478
pmcid: 3404345
Perera, F. et al. Bisphenol A exposure and symptoms of anxiety and depression among inner city children at 10–12 years of age. Environ. Res. 151, 195–202. https://doi.org/10.1016/j.envres.2016.07.028 (2016).
doi: 10.1016/j.envres.2016.07.028
pubmed: 27497082
pmcid: 5071142
Mhaouty-Kodja, S. et al. Impairment of learning and memory performances induced by BPA: evidences from the literature of a MoA mediated through an ED. Mol. Cell. Endocrinol. 475, 54–73. https://doi.org/10.1016/j.mce.2018.03.017 (2018).
doi: 10.1016/j.mce.2018.03.017
pubmed: 29605460
Gonçalves, C. R., Cunha, R. W., Barros, D. M. & Martínez, P. E. Effects of prenatal and postnatal exposure to a low dose of bisphenol A on behavior and memory in rats. Environ. Toxicol. Pharmacol. 30, 195–201 (2010).
pubmed: 21787652
doi: 10.1016/j.etap.2010.06.003
Xu, X. H., Zhang, J., Wang, Y. M., Ye, Y. P. & Luo, Q. Q. Perinatal exposure to bisphenol-A impairs learning-memory by concomitant down-regulation of N-methyl-D-aspartate receptors of hippocampus in male offspring mice. Horm. Behav. 58, 326–333. https://doi.org/10.1016/j.yhbeh.2010.02.012 (2010).
doi: 10.1016/j.yhbeh.2010.02.012
pubmed: 20206181
Zhang, H. et al. Low-dose bisphenol A exposure impairs learning and memory ability with alterations of neuromorphology and neurotransmitters in rats. Sci. Total Environ. 697, 134036 (2019).
pubmed: 31476513
doi: 10.1016/j.scitotenv.2019.134036
Zhang, H. et al. Maternal exposure to environmental bisphenol A impairs the neurons in hippocampus across generations. Toxicology 432, 152393 (2020).
pubmed: 32027964
doi: 10.1016/j.tox.2020.152393
Zoghbi, H. Y. & Bear, M. F. Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities. Cold Spring Harbor Perspect. Biol. 4, a009886 (2012).
doi: 10.1101/cshperspect.a009886
Chiocchetti, A. et al. Transcriptomic signatures of neuronal differentiation and their association with risk genes for autism spectrum and related neuropsychiatric disorders. Transl. Psychiatry 6, e864–e864 (2016).
pubmed: 27483382
pmcid: 5022076
doi: 10.1038/tp.2016.119
Barak, B. & Feng, G. Neurobiology of social behavior abnormalities in autism and Williams syndrome. Nat. Neurosci. 19, 647–655 (2016).
pubmed: 29323671
pmcid: 4896837
doi: 10.1038/nn.4276
Stoner, R. et al. Patches of disorganization in the neocortex of children with autism. N. Engl. J. Med. 370, 1209–1219 (2014).
pubmed: 24670167
pmcid: 4499461
doi: 10.1056/NEJMoa1307491
Schafer, S. T. et al. Pathological priming causes developmental gene network heterochronicity in autistic subject-derived neurons. Nat. Neurosci. 22, 243–255 (2019).
pubmed: 30617258
pmcid: 6402576
doi: 10.1038/s41593-018-0295-x
Krämer, A., Green, J., Pollard, J. Jr. & Tugendreich, S. Causal analysis approaches in ingenuity pathway analysis. Bioinformatics 30, 523–530 (2014).
pubmed: 24336805
doi: 10.1093/bioinformatics/btt703
Zhou, L. et al. Foxo3a inhibits mitochondrial fission and protects against doxorubicin-induced cardiotoxicity by suppressing MIEF2. Free Radic. Biol. Med. 104, 360–370 (2017).
pubmed: 28137654
doi: 10.1016/j.freeradbiomed.2017.01.037
Xu, S. et al. Mitochondrial E3 ubiquitin ligase MARCH5 controls mitochondrial fission and cell sensitivity to stress-induced apoptosis through regulation of MiD49 protein. Mol. Biol. Cell 27, 349–359 (2016).
pubmed: 26564796
pmcid: 4713136
doi: 10.1091/mbc.e15-09-0678
Zhu, Q. et al. Elevated expression of eukaryotic translation initiation factor 3H is associated with proliferation, invasion and tumorigenicity in human hepatocellular carcinoma. Oncotarget 7, 49888 (2016).
pubmed: 27340783
pmcid: 5226555
doi: 10.18632/oncotarget.10222
Wei, G. et al. Patient mutations of the intellectual disability gene KDM5C downregulate netrin G2 and suppress neurite growth in neuro2a cells. J. Mol. Neurosci. 60, 33–45 (2016).
pubmed: 27421841
pmcid: 5412133
doi: 10.1007/s12031-016-0770-3
Cubelos, B. et al. Cux1 and Cux2 regulate dendritic branching, spine morphology, and synapses of the upper layer neurons of the cortex. Neuron 66, 523–535 (2010).
pubmed: 20510857
pmcid: 2894581
doi: 10.1016/j.neuron.2010.04.038
Szpara, M. L. et al. Analysis of gene expression during neurite outgrowth and regeneration. BMC Neurosci. 8, 100 (2007).
pubmed: 18036227
pmcid: 2245955
doi: 10.1186/1471-2202-8-100
Huang, G.-H., Sun, Z.-L., Li, H.-J. & Feng, D.-F. Rho GTPase-activating proteins: Regulators of Rho GTPase activity in neuronal development and CNS diseases. Mol. Cell. Neurosci. 80, 18–31 (2017).
pubmed: 28163190
doi: 10.1016/j.mcn.2017.01.007
Jarrard, L. E. On the role of the hippocampus in learning and memory in the rat. Behav. Neural Biol. 60, 9–26 (1993).
pubmed: 8216164
doi: 10.1016/0163-1047(93)90664-4
Levano, K. et al. Atp8a1 deficiency is associated with phosphatidylserine externalization in hippocampus and delayed hippocampus-dependent learning. J. Neurochem. 120, 302–313 (2012).
pubmed: 22007859
doi: 10.1111/j.1471-4159.2011.07543.x
Organization, W. H. Food and Agriculture Organization of Unated Nations: Bisphenol A (BPA) Current state of knowledge and future actions by WHO and FAO. International Food Safety Authorities Network (INFOSAN) (2009).
EFSA Panel on Food Contact Materials, Enzymes, Flavourings and Processing Aids (CEF). Scientific opinion on the risks to public health related to the presence of bisphenol A (BPA) in foodstuffs. EFSA J. 13, 3978 (2015).
doi: 10.2903/j.efsa.2015.3978
Ribeiro, E., Ladeira, C. & Viegas, S. Occupational exposure to bisphenol A (BPA): a reality that still needs to be unveiled. Toxics 5, 22 (2017).
pmcid: 5634705
doi: 10.3390/toxics5030022
Gerona, R., vom Saal, F. S. & Hunt, P. A. BPA: Have flawed analytical techniques compromised risk assessments?. Lancet Diabetes Endocrinol. 8, 11–13 (2020).
pubmed: 31813841
doi: 10.1016/S2213-8587(19)30381-X
Cao, J., Joyner, L., Mickens, J. A., Leyrer, S. M. & Patisaul, H. B. Sex-specific Esr2 mRNA expression in the rat hypothalamus and amygdala is altered by neonatal bisphenol A exposure. Reproduction (Cambridge, England) 147, 537–554. https://doi.org/10.1530/rep-13-0501 (2014).
doi: 10.1530/rep-13-0501
Xu, X., Tian, D., Hong, X., Chen, L. & Xie, L. Sex-specific influence of exposure to bisphenol-A between adolescence and young adulthood on mouse behaviors. Neuropharmacology 61, 565–573. https://doi.org/10.1016/j.neuropharm.2011.04.027 (2011).
doi: 10.1016/j.neuropharm.2011.04.027
pubmed: 21570416
Ponzi, D., Gioiosa, L., Parmigiani, S. & Palanza, P. Effects of prenatal exposure to a low-dose of bisphenol A on sex differences in emotional behavior and central alpha2-adrenergic receptor binding. Int. J. Mol. Sci. 21, 3269 (2020).
pmcid: 7246441
doi: 10.3390/ijms21093269
Xian, H. & Liou, Y.-C. Loss of MIEF1/MiD51 confers susceptibility to BAX-mediated cell death and PINK1-PRKN-dependent mitophagy. Autophagy 15, 2107–2125 (2019).
pubmed: 30894073
pmcid: 6844504
doi: 10.1080/15548627.2019.1596494
Otera, H., Miyata, N., Kuge, O. & Mihara, K. Drp1-dependent mitochondrial fission via MiD49/51 is essential for apoptotic cristae remodeling. J. Cell Biol. 212, 531–544 (2016).
pubmed: 26903540
pmcid: 4772499
doi: 10.1083/jcb.201508099
Lee, A. S., Kranzusch, P. J. & Cate, J. H. eIF3 targets cell-proliferation messenger RNAs for translational activation or repression. Nature 522, 111–114 (2015).
pubmed: 25849773
pmcid: 4603833
doi: 10.1038/nature14267
Choudhuri, A., Evans, T. & Maitra, U. Non-core subunit eIF3h of translation initiation factor eIF3 regulates zebrafish embryonic development. Dev. Dyn. 239, 1632–1644 (2010).
pubmed: 20503360
pmcid: 3089590
doi: 10.1002/dvdy.22289
Zhang, L., Smit-McBride, Z., Pan, X., Rheinhardt, J. & Hershey, J. W. An oncogenic role for the phosphorylated h-subunit of human translation initiation factor eIF3. J. Biol. Chem. 283, 24047–24060 (2008).
pubmed: 18544531
pmcid: 2527115
doi: 10.1074/jbc.M800956200
Guo, X. et al. EIF3H promotes aggressiveness of esophageal squamous cell carcinoma by modulating Snail stability. J. Exp. Clin. Cancer Res. 39, 1–15 (2020).
doi: 10.1186/s13046-020-01678-9
Ferreira, E., Shaw, D. & Oddo, S. Identification of learning-induced changes in protein networks in the hippocampi of a mouse model of Alzheimer’s disease. Transl. Psychiatry 6, e849–e849 (2016).
pubmed: 27378549
pmcid: 4969764
doi: 10.1038/tp.2016.114
Machado, C. O. F. et al. Collybistin binds and inhibits mTORC1 signaling: a potential novel mechanism contributing to intellectual disability and autism. Eur. J. Hum. Genet. 24, 59–65 (2016).
pubmed: 25898924
doi: 10.1038/ejhg.2015.69
Wang, Y., Du, X., Wang, D., Wang, J. & Du, J. Effects of bisphenol A exposure during pregnancy and lactation on hippocampal function in newborn rats. Int. J. Med. Sci. 17, 1751 (2020).
pubmed: 32714078
pmcid: 7378672
doi: 10.7150/ijms.47300
Wynder, C., Stalker, L. & Doughty, M. L. Role of H3K4 demethylases in complex neurodevelopmental diseases. Epigenomics 2, 407–418 (2010).
pubmed: 22121901
doi: 10.2217/epi.10.12
Hayashi, T. et al. PX-RICS, a novel splicing variant of RICS, is a main isoform expressed during neural development. Genes Cells 12, 929–939 (2007).
pubmed: 17663722
doi: 10.1111/j.1365-2443.2007.01101.x
Doan, R. N. et al. Mutations in human accelerated regions disrupt cognition and social behavior. Cell 167, 341–354 (2016).
pubmed: 27667684
pmcid: 5063026
doi: 10.1016/j.cell.2016.08.071
Choi, J., Ababon, M. R., Matteson, P. G. & Millonig, J. H. Cut-like homeobox 1 and nuclear factor I/B mediate ENGRAILED2 autism spectrum disorder-associated haplotype function. Hum. Mol. genetics 21, 1566–1580 (2012).
doi: 10.1093/hmg/ddr594
Vallianatos, C. N. et al. Altered gene-regulatory function of KDM5C by a novel mutation associated with autism and intellectual disability. Front. Mol. Neurosci. 11, 104 (2018).
pubmed: 29670509
pmcid: 5893713
doi: 10.3389/fnmol.2018.00104
Akshoomoff, N., Mattson, S. N. & Grossfeld, P. D. Evidence for autism spectrum disorder in Jacobsen syndrome: identification of a candidate gene in distal 11q. Genet. Med. 17, 143–148 (2015).
pubmed: 25058499
doi: 10.1038/gim.2014.86
Conroy, J. et al. Fine mapping and association studies in a candidate region for autism on chromosome 2q31–q32. Am. J. Med. Genet. Part B Neuropsychiatr. Genet. 150, 535–544 (2009).
doi: 10.1002/ajmg.b.30854
Seki, S. et al. Bisphenol-A suppresses neurite extension due to inhibition of phosphorylation of mitogen-activated protein kinase in PC12 cells. Chem. Biol. Interact. 194, 23–30 (2011).
pubmed: 21871873
doi: 10.1016/j.cbi.2011.08.001
Liang, X. et al. Bisphenol A and several derivatives exert neural toxicity in human neuron-like cells by decreasing neurite length. Food Chem. Toxicol. 135, 111015 (2020).
pubmed: 31812737
doi: 10.1016/j.fct.2019.111015
Wang, H., Chang, L., Aguilar, J. S., Dong, S. & Hong, Y. Bisphenol-A exposure induced neurotoxicity in glutamatergic neurons derived from human embryonic stem cells. Environ. Int. 127, 324–332 (2019).
pubmed: 30953815
doi: 10.1016/j.envint.2019.01.059
Liu, Z. H. et al. Early developmental bisphenol-A exposure sex-independently impairs spatial memory by remodeling hippocampal dendritic architecture and synaptic transmission in rats. Sci. Rep. 6, 32492. https://doi.org/10.1038/srep32492 (2016).
doi: 10.1038/srep32492
pubmed: 27578147
pmcid: 5006158
Raymond, G. V., Bauman, M. L. & Kemper, T. L. Hippocampus in autism: a Golgi analysis. Acta Neuropathol. 91, 117–119 (1995).
doi: 10.1007/s004010050401
Bauman, M. L. & Kemper, T. L. Neuroanatomic observations of the brain in autism: a review and future directions. Int. J. Dev. Neurosci. 23, 183–187 (2005).
pubmed: 15749244
doi: 10.1016/j.ijdevneu.2004.09.006
Kerr, D. J. et al. Aberrant hippocampal Atp8a1 levels are associated with altered synaptic strength, electrical activity, and autistic-like behavior. Biochim. Biophys. Acta (BBA) Mol. Basis Dis. 1862, 1755–1765 (2016).
doi: 10.1016/j.bbadis.2016.06.005
Kundakovic, M. et al. DNA methylation of BDNF as a biomarker of early-life adversity. Proc. Natl. Acad. Sci. U.S.A. 112, 6807–6813. https://doi.org/10.1073/pnas.1408355111 (2015).
doi: 10.1073/pnas.1408355111
pubmed: 25385582
Jardim, N. S., Sartori, G., Sari, M. H. M., Muller, S. G. & Nogueira, C. W. Bisphenol A impairs the memory function and glutamatergic homeostasis in a sex-dependent manner in mice: beneficial effects of diphenyl diselenide. Toxicol. Appl. Pharmacol. 329, 75–84. https://doi.org/10.1016/j.taap.2017.05.035 (2017).
doi: 10.1016/j.taap.2017.05.035
pubmed: 28572023
Kumar, D. & Thakur, M. K. Anxiety like behavior due to perinatal exposure to Bisphenol-A is associated with decrease in excitatory to inhibitory synaptic density of male mouse brain. Toxicology 378, 107–113. https://doi.org/10.1016/j.tox.2017.01.010 (2017).
doi: 10.1016/j.tox.2017.01.010
pubmed: 28089772
Beaudoin, G. M. 3rd. et al. Culturing pyramidal neurons from the early postnatal mouse hippocampus and cortex. Nat. Protoc. 7, 1741–1754. https://doi.org/10.1038/nprot.2012.099 (2012).
doi: 10.1038/nprot.2012.099
pubmed: 22936216
Falk, T. et al. U-Net: deep learning for cell counting, detection, and morphometry. Nat. Methods 16, 67–70 (2019).
pubmed: 30559429
doi: 10.1038/s41592-018-0261-2
Reger, M. L., Hovda, D. A. & Giza, C. C. Ontogeny of rat recognition memory measured by the novel object recognition task. Dev. Psychobiol. 51, 672–678. https://doi.org/10.1002/dev.20402 (2009).
doi: 10.1002/dev.20402
pubmed: 19739136
pmcid: 2956740
Saeed, A. et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374–378 (2003).
pubmed: 12613259
doi: 10.2144/03342mt01
Quackenbush, J. Microarray data normalization and transformation. Nat. Genet. 32, 496–501 (2002).
pubmed: 12454644
doi: 10.1038/ng1032
Pavlidis, P. & Noble, W. S. Analysis of strain and regional variation in gene expression in mouse brain. Genome Biol. 2, research0042.1 (2001).
doi: 10.1186/gb-2001-2-10-research0042