Effects of prenatal bisphenol S and bisphenol F exposure on behavior of offspring mice

References

• Ahn JS, Won J-H, Kim D-Y, Jung S-E, Kim B-J, Kim J-M, Ryu B-Y. 2022. Transcriptome alterations in spermatogonial stem cells exposed to bisphenol A. Anim Cells Syst. 26(2):70–83. doi:10.1080/19768354.2022.2061592.
   PubMed Web of Science ®Google Scholar
• Allard P, Colaiácovo MP. 2011. Chapter 50 – bisphenol A. In: Gupta RC, editor. Reproductive and developmental toxicology. San Diego: Academic Press; p. 673–686.
   Google Scholar
• Baek D-J, Lee C-B, Baek S-S. 2014. Effect of treadmill exercise on social interaction and tyrosine hydroxylase expression in the attention-deficit/hyperactivity disorder rats. J Exerc Rehabil. 10(5):252–257. doi:10.12965/jer.140162.
   PubMedGoogle Scholar
• Barak B, Feng G. 2016. Neurobiology of social behavior abnormalities in autism and Williams syndrome. Nat Neurosci. 19(5):647–655. doi:10.1038/nn.4276.
   PubMed Web of Science ®Google Scholar
• Bicks LK, Koike H, Akbarian S, Morishita H. 2015. Prefrontal cortex and social cognition in mouse and man. Front Psychol. 6:1805. doi:10.3389/fpsyg.2015.01805.
   PubMed Web of Science ®Google Scholar
• Birla H, Keswani C, Rai SN, Singh SS, Zahra W, Dilnashin H, Rathore AS, Singh SP. 2019. Neuroprotective effects of Withania somnifera in BPA induced-cognitive dysfunction and oxidative stress in mice. Behav Brain Funct. 15(1):9. doi:10.1186/s12993-019-0160-4.
   PubMed Web of Science ®Google Scholar
• Bornehag C-G, Engdahl E, Unenge Hallerbäck M, Wikström S, Lindh C, Rüegg J, Tanner E, Gennings C. 2021. Prenatal exposure to bisphenols and cognitive function in children at 7 years of age in the Swedish SELMA study. Environ Int. 150:106433. doi:10.1016/j.envint.2021.106433.
   PubMed Web of Science ®Google Scholar
• Castro B, Sánchez P, Torres JM, Ortega E. 2015. Bisphenol A, bisphenol F and bisphenol S affect differently 5α-reductase expression and dopamine–serotonin systems in the prefrontal cortex of juvenile female rats. Environ Res. 142:281–287. doi:10.1016/j.envres.2015.07.001.
   PubMed Web of Science ®Google Scholar
• Cevasco A, Urbatzka R, Bottero S, Massari A, Pedemonte F, Kloas W, Mandich A. 2008. Endocrine disrupting chemicals (EDC) with (anti)estrogenic and (anti)androgenic modes of action affecting reproductive biology of Xenopus laevis: II. Effects on gonad histomorphology. Comp Biochem Physiol C Toxicol Pharmacol. 147(2):241–251. doi:10.1016/j.cbpc.2007.10.001.
   PubMed Web of Science ®Google Scholar
• Chen D, Kannan K, Tan H, Zheng Z, Feng Y-L, Wu Y, Widelka M. 2016. Bisphenol analogues other than BPA: environmental occurrence, human exposure, and toxicity – A review. Environ Sci Technol. 50(11):5438–5453. doi:10.1021/acs.est.5b05387.
   PubMed Web of Science ®Google Scholar
• Da Silva BS, Pietrobon CB, Bertasso IM, Lopes BP, Carvalho JC, Peixoto-Silva N, Santos TR, Claudio-Neto S, Manhães AC, Oliveira E, et al. 2019. Short and long-term effects of bisphenol S (BPS) exposure during pregnancy and lactation on plasma lipids, hormones, and behavior in rats. Environ Pollut. 250:312–322. doi:10.1016/j.envpol.2019.03.100.
   PubMed Web of Science ®Google Scholar
• De Coster S, Van Larebeke N. 2012. Endocrine-Disrupting chemicals: associated disorders and mechanisms of action. J Environ Public Health. 2012:1–52. doi:10.1155/2012/713696.
   Google Scholar
• Diamanti-Kandarakis E, Bourguignon J-P, Giudice LC, Hauser R, Prins GS, Soto AM, Zoeller RT, Gore AC. 2009. Endocrine-disrupting chemicals: an endocrine society scientific statement. Endocr Rev. 30(4):293–342. doi:10.1210/er.2009-0002.
   PubMed Web of Science ®Google Scholar
• Di Benedetto B, Kallnik M, Weisenhorn DMV, Falls WA, Wurst W, Hölter SM. 2009. Activation of ERK/MAPK in the lateral amygdala of the mouse is required for acquisition of a fear-potentiated startle response. Neuropsychopharmacology. 34(2):356–366. doi:10.1038/npp.2008.57.
   PubMed Web of Science ®Google Scholar
• Eladak S, Grisin T, Moison D, Guerquin M-J, N'Tumba-Byn T, Pozzi-Gaudin S, Benachi A, Livera G, Rouiller-Fabre V, Habert R. 2015. A new chapter in the bisphenol A story: bisphenol S and bisphenol F are not safe alternatives to this compound. Fertil Steril. 103(1):11–21. doi:10.1016/j.fertnstert.2014.11.005.
   PubMed Web of Science ®Google Scholar
• Fitzgerald R, Loveren HV, Civitella C, Castoldi AF, Bernasconi G. 2020. Assessment of new information on Bisphenol S (BPS) submitted in response to the Decision 1 under REACH Regulation (EC) No 1907/2006. EFSA Supporting Publications. 17(4).
   Google Scholar
• Garí M, Moos R, Bury D, Kasper-Sonnenberg M, Jankowska A, Andysz A, Hanke W, Nowak D, Bose-O’Reilly S, Koch HM, et al. 2021. Human-biomonitoring derived exposure and daily intakes of bisphenol A and their associations with neurodevelopmental outcomes among children of the Polish mother and child cohort study. Environ Health. 20(1):95. doi:10.1186/s12940-021-00777-0.
   PubMed Web of Science ®Google Scholar
• Gill S, Kumara VMR. 2021. Comparative neurodevelopment effects of bisphenol A and bisphenol F on rat fetal neural stem cell models. Cells. 10(4):793–825. doi:10.3390/cells10040793.
   PubMed Web of Science ®Google Scholar
• Guo Y, Lv Z, Tang Z, Huang S, Peng C, Wang F, Zhou Z, Ding W, Liu W, Liu P, et al. 2021. Long-term exposure to low doses of bisphenol S has hypoglycaemic effect in adult male mice by promoting insulin sensitivity and repressing gluconeogenesis. Environ Pollut. 277:116630. doi:10.1016/j.envpol.2021.116630.
   PubMed Web of Science ®Google Scholar
• Hyun M, Rathor L, Kim H-J, McElroy T, Hwang KH, Wohlgemuth S, Curry S, Xiao R, Leeuwenburgh C, Heo J-D, et al. 2021. Comparative toxicities of BPA, BPS, BPF, and TMBPF in the nematode caenorhabditis elegans and mammalian fibroblast cells. Toxicology. 461:152924. doi:10.1016/j.tox.2021.152924.
   PubMed Web of Science ®Google Scholar
• Inadera H. 2015. Neurological effects of bisphenol A and its analogues. Int J Med Sci. 12(12):926–936. doi:10.7150/ijms.13267.
   PubMed Web of Science ®Google Scholar
• Jung E-M, Moffat JJ, Liu J, Dravid SM, Gurumurthy CB, Kim W-Y. 2017. Arid1b haploinsufficiency disrupts cortical interneuron development and mouse behavior. Nat Neurosci. 20(12):1694–1707. doi:10.1038/s41593-017-0013-0.
   PubMed Web of Science ®Google Scholar
• Kim B, Colon E, Chawla S, Vandenberg LN, Suvorov A. 2015. Endocrine disruptors alter social behaviors and indirectly influence social hierarchies via changes in body weight. Environ Health. 14:64. doi:10.1186/s12940-015-0051-6.
   PubMed Web of Science ®Google Scholar
• Kim ME, Park HR, Gong EJ, Choi SY, Kim HS, Lee J. 2011. Exposure to bisphenol A appears to impair hippocampal neurogenesis and spatial learning and memory. Food Chem Toxicol. 49(12):3383–3389. doi:10.1016/j.fct.2011.09.017.
   PubMed Web of Science ®Google Scholar
• Kimura E, Matsuyoshi C, Miyazaki W, Benner S, Hosokawa M, Yokoyama K, Kakeyama M, Tohyama C. 2016. Prenatal exposure to bisphenol A impacts neuronal morphology in the hippocampal CA1 region in developing and aged mice. Arch Toxicol. 90(3):691–700. doi:10.1007/s00204-015-1485-x.
   PubMed Web of Science ®Google Scholar
• Komada M, Nagao T, Kagawa N. 2020. Prenatal and postnatal bisphenol A exposure inhibits postnatal neurogenesis in the hippocampal dentate gyrus. J Toxicol Sci. 45(10):639–650. doi:10.2131/jts.45.639.
   PubMed Web of Science ®Google Scholar
• Komarowska MD, Grubczak K, Czerniecki J, Hermanowicz A, Hermanowicz JM, Debek W, Matuszczak E. 2021. Identification of the bisphenol A (BPA) and the two analogues BPS and BPF in cryptorchidism. Front Endocrinol. 12:694669. (English). doi:10.3389/fendo.2021.694669.
   PubMed Web of Science ®Google Scholar
• Lambré C, Barat Baviera JM, Bolognesi C, Chesson A, Cocconcelli PS, Crebelli R, Gott DM, Grob K, Lampi E, Mengelers M, et al. 2023. Re-evaluation of the risks to public health related to the presence of bisphenol A (BPA) in foodstuffs. EFSA J. 21(4):e06857. doi:10.2903/j.efsa.2023.6857.
   PubMedGoogle Scholar
• Li Y-Z, Wu Z-Y, Zhu B-Q, Wang Y-X, Kan Y-Q, Zeng H-C. 2022. The BDNF–TrkB–CREB signalling pathway Is involved in bisphenol S-induced neurotoxicity in male mice by regulating methylation. Toxics. 10(8):413–427. doi:10.3390/toxics10080413.
   PubMed Web of Science ®Google Scholar
• Mu X, Liu J, Wang H, Yuan L, Wang C, Li Y, Qiu J. 2022. Bisphenol F impaired zebrafish cognitive ability through inducing neural cell heterogeneous responses. Environ Sci Technol. 56(12):8528–8540. doi:10.1021/acs.est.2c01531.
   PubMed Web of Science ®Google Scholar
• Müller JE, Meyer N, Santamaria CG, Schumacher A, Luque EH, Zenclussen ML, Rodriguez HA, Zenclussen AC. 2018. Bisphenol A exposure during early pregnancy impairs uterine spiral artery remodeling and provokes intrauterine growth restriction in mice. Sci Rep. 8(1):9196–9206. doi:10.1038/s41598-018-27575-y.
   PubMedGoogle Scholar
• Naderi M, Puar P, JavadiEsfahani R, Kwong RW. 2022. Early developmental exposure to bisphenol A and bisphenol S disrupts socio-cognitive function, isotocin equilibrium, and excitation-inhibition balance in developing zebrafish. Neurotoxicology. 88:144–154. doi:10.1016/j.neuro.2021.11.009.
   PubMed Web of Science ®Google Scholar
• Naderi M, Salahinejad A, Attaran A, Chivers DP, Niyogi S. 2020. Chronic exposure to environmentally relevant concentrations of bisphenol S differentially affects cognitive behaviors in adult female zebrafish. Environ Pollut. 261:114060. doi:10.1016/j.envpol.2020.114060.
   PubMed Web of Science ®Google Scholar
• Nourian A, Soleimanzadeh A, Shalizar Jalali A, Najafi G. 2020. Bisphenol-A analogue (bisphenol-S) exposure alters female reproductive tract and apoptosis/oxidative gene expression in blastocyst-derived cells. Iran J Basic Med Sci. 23(5):576–585.
   PubMed Web of Science ®Google Scholar
• Ohtani N, Iwano H, Suda K, Tsuji E, Tanemura K, Inoue H, Yokota H. 2017. Adverse effects of maternal exposure to bisphenol F on the anxiety- and depression-like behavior of offspring. J Vet Med Sci. 79(2):432–439. doi:10.1292/jvms.16-0502.
   PubMed Web of Science ®Google Scholar
• Olsson A, Rutkowska A, Rachoń D. 2015. Health risk of exposure to bisphenol A (BPA). Rocz Panstw Zakl Hig. 66:5–11.
   PubMedGoogle Scholar
• Pang Q, Li Y, Meng L, Li G, Luo Z, Fan R. 2019. Neurotoxicity of BPA, BPS, and BPB for the hippocampal cell line (HT-22): An implication for the replacement of BPA in plastics. Chemosphere. 226:545–552. doi:10.1016/j.chemosphere.2019.03.177.
   PubMed Web of Science ®Google Scholar
• Park MJ, Yoo SW, Choe BS, Dantzer R, Freund GG. 2012. Acute hypoglycemia causes depressive-like behaviors in mice. Metabolism. 61(2):229–236. doi:10.1016/j.metabol.2011.06.013.
   PubMed Web of Science ®Google Scholar
• Rebolledo-Solleiro D. 2021. Impact of BPA on behavior, neurodevelopment and neurodegeneration Daniela. Front Biosci. 26(2):363–400. doi:10.2741/4898.
   Web of Science ®Google Scholar
• Rubin BS. 2011. Bisphenol A: An endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol. 127(1):27–34. doi:10.1016/j.jsbmb.2011.05.002.
   PubMed Web of Science ®Google Scholar
• Salahinejad A, Attaran A, Meuthen D, Rachamalla M, Chivers DP, Niyogi S. 2022. Maternal exposure to bisphenol S induces neuropeptide signaling dysfunction and oxidative stress in the brain, and abnormal social behaviors in zebrafish (Danio rerio) offspring. Sci Total Environ. 830:154794. doi:10.1016/j.scitotenv.2022.154794.
   PubMed Web of Science ®Google Scholar
• Salahinejad A, Attaran A, Naderi M, Meuthen D, Niyogi S, Chivers DP. 2021. Chronic exposure to bisphenol S induces oxidative stress, abnormal anxiety, and fear responses in adult zebrafish (Danio rerio). Sci Total Environ. 750:141633. doi:10.1016/j.scitotenv.2020.141633.
   PubMed Web of Science ®Google Scholar
• Salahinejad A, Naderi M, Attaran A, Meuthen D, Niyogi S, Chivers DP. 2020. Effects of chronic exposure to bisphenol-S on social behaviors in adult zebrafish: disruption of the neuropeptide signaling pathways in the brain. Environ Pollut. 262:113992. doi:10.1016/j.envpol.2020.113992.
   PubMed Web of Science ®Google Scholar
• Saleh AC, Sabry R, Mastromonaco GF, Favetta LA. 2021. BPA and BPS affect the expression of anti-Mullerian hormone (AMH) and its receptor during bovine oocyte maturation and early embryo development. Reprod Biol Endocrinol. 19(1):119. doi:10.1186/s12958-021-00773-6.
   PubMed Web of Science ®Google Scholar
• Santoro A, Chianese R, Troisi J, Richards S, Nori SL, Fasano S, Guida M, Plunk E, Viggiano A, Pierantoni R, et al. 2019. Neuro-toxic and reproductive effects of BPA. Curr Neuropharmacol. 17(12):1109–1132. doi:10.2174/1570159X17666190726112101.
   PubMed Web of Science ®Google Scholar
• Schug TT, Janesick A, Blumberg B, Heindel JJ. 2011. Endocrine disrupting chemicals and disease susceptibility. J Steroid Biochem Mol Biol. 127(3–5):204–215. doi:10.1016/j.jsbmb.2011.08.007.
   PubMed Web of Science ®Google Scholar
• Silverman JL, Yang M, Lord C, Crawley JN. 2010. Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci. 11(7):490–502. doi:10.1038/nrn2851.
   PubMed Web of Science ®Google Scholar
• Sur B, Lee B. 2022. Luteolin reduces fear, anxiety, and depression in rats with post-traumatic stress disorder. Anim Cells Syst. 26(4):174–182. doi:10.1080/19768354.2022.2104925.
   PubMed Web of Science ®Google Scholar
• Thoene M, Dzika E, Gonkowski S, Wojtkiewicz J. 2020. Bisphenol S in food causes hormonal and obesogenic effects comparable to or worse than bisphenol A: a literature review. Nutrients. 12(2):532–546. doi:10.3390/nu12020532.
   PubMed Web of Science ®Google Scholar
• Tong WH, Abdulai-Saiku S, Vyas A. 2019. Testosterone reduces fear and causes drastic hypomethylation of arginine vasopressin promoter in medial extended amygdala of male mice. Front Behav Neurosci. 13:33. doi:10.3389/fnbeh.2019.00033.
   PubMed Web of Science ®Google Scholar
• Ullah A, Pirzada M, Afsar T, Razak S, Almajwal A, Jahan S. 2019. Effect of bisphenol F, an analog of bisphenol A, on the reproductive functions of male rats. Environ Health Prev Med. 24(1):41. doi:10.1186/s12199-019-0797-5.
   PubMed Web of Science ®Google Scholar
• Ullah H, Ullah F, Rehman O, Jahan S, Afsar T, Al-Disi D, Almajwal A, Razak S. 2021. Chronic exposure of bisphenol S (BPS) affect hypothalamic-pituitary-testicular activities in adult male rats: possible in estrogenic mode of action. Environ Health Prev Med. 26(1):31. doi:10.1186/s12199-021-00954-0.
   PubMed Web of Science ®Google Scholar
• Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. 2007. Human exposure to bisphenol A (BPA). Reprod Toxicol. 24(2):139–177. doi:10.1016/j.reprotox.2007.07.010.
   PubMed Web of Science ®Google Scholar
• Viñas R, Watson CS. 2013. Bisphenol S disrupts estradiol-induced nongenomic signaling in a Rat pituitary cell line: effects on cell functions. Environ Health Perspect. 121(3):352–358. doi:10.1289/ehp.1205826.
   PubMed Web of Science ®Google Scholar
• Wang R, Fei Q, Liu S, Weng X, Liang H, Wu Y, Wen L, Hao G, Cao G, Jing C. 2022. The bisphenol F and bisphenol S and cardiovascular disease: results from NHANES 2013–2016. Environ Sci Eur. 34(1):4. doi:10.1186/s12302-021-00586-9.
   Web of Science ®Google Scholar
• Wang Y, Du X, Wang D, Wang J, Du J. 2020. Effects of bisphenol A exposure during pregnancy and lactation on hippocampal function in newborn rats. Int J Med Sci. 17(12):1751–1762. doi:10.7150/ijms.47300.
   PubMed Web of Science ®Google Scholar
• Wang Z, Alderman MH, Asgari C, Taylor HS. 2020. Fetal bisphenol-A induced changes in murine behavior and brain gene expression persisted in adult-aged offspring. Endocrinology. 161(12):1–15. doi:10.1210/endocr/bqaa164.
   Web of Science ®Google Scholar
• Wei P, Zhao F, Zhang X, Ru S. 2020. Long-term exposure of zebrafish to bisphenol S impairs stress function of hypothalamic-pituitary-interrenal axis and causes anxiety-like behavioral responses to novelty. Sci Total Environ. 716:137092. doi:10.1016/j.scitotenv.2020.137092.
   PubMed Web of Science ®Google Scholar
• Welch C, Mulligan K. 2022. Does bisphenol A confer risk of neurodevelopmental disorders? what we have learned from developmental neurotoxicity studies in animal models. Int J Mol Sci. 23(5):2894. doi:10.3390/ijms23052894.
   PubMed Web of Science ®Google Scholar
• Wilson CA, Koenig JI. 2014. Social interaction and social withdrawal in rodents as readouts for investigating the negative symptoms of schizophrenia. Eur Neuropsychopharmacol. 24(5):759–773. doi:10.1016/j.euroneuro.2013.11.008.
   PubMed Web of Science ®Google Scholar
• Wolstenholme JT, Edwards M, Shetty SRJ, Gatewood JD, Taylor JA, Rissman EF, Connelly JJ. 2012. Gestational exposure to bisphenol A produces transgenerational changes in behaviors and gene expression. Endocrinology. 153(8):3828–3838. doi:10.1210/en.2012-1195.
   PubMed Web of Science ®Google Scholar
• Xu X-h, Zhang J, Wang Y-m, Ye Y-p, Luo Q-q. 2010. 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(2):326–333. doi:10.1016/j.yhbeh.2010.02.012.
   PubMed Web of Science ®Google Scholar
• Yang Q, Yang X, Liu J, Ren W, Chen Y, Shen S. 2017. Effects of BPF on steroid hormone homeostasis and gene expression in the hypothalamic–pituitary–gonadal axis of zebrafish. Environ Sci Pollut Res. 24(26):21311–21322. doi:10.1007/s11356-017-9773-z.
   PubMed Web of Science ®Google Scholar
• Zhang Y-F, Ren X-M, Li Y-Y, Yao X-F, Li C-H, Qin Z-F, Guo L-H. 2018. Bisphenol A alternatives bisphenol S and bisphenol F interfere with thyroid hormone signaling pathway in vitro and in vivo. Environ Pollut. 237:1072–1079. doi:10.1016/j.envpol.2017.11.027.
   PubMed Web of Science ®Google Scholar
• Zhao Z, Zeng F, Wang H, Wu R, Chen L, Wu Y, Li S, Shao J, Wang Y, Wu J, et al. 2022. Encoding of social novelty by sparse GABAergic neural ensembles in the prelimbic cortex. Sci Adv. 8(35):eabo4884. doi:10.1126/sciadv.abo4884.
   PubMed Web of Science ®Google Scholar