Neuro-toxic and Reproductive Effects of BPA

Author(s): Antonietta Santoro, Rosanna Chianese, Jacopo Troisi, Sean Richards, Stefania Lucia Nori, Silvia Fasano, Maurizio Guida, Elizabeth Plunk, Andrea Viggiano, Riccardo Pierantoni, Rosaria Meccariello*.

Journal Name: Current Neuropharmacology

Volume 17 , Issue 12 , 2019

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Graphical Abstract:


Abstract:

Background: Bisphenol A (BPA) is one of the highest volume chemicals produced worldwide. It has recognized activity as an endocrine-disrupting chemical and has suspected roles as a neurological and reproductive toxicant. It interferes in steroid signaling, induces oxidative stress, and affects gene expression epigenetically. Gestational, perinatal and neonatal exposures to BPA affect developmental processes, including brain development and gametogenesis, with consequences on brain functions, behavior, and fertility.

Methods: This review critically analyzes recent findings on the neuro-toxic and reproductive effects of BPA (and its analogues), with focus on neuronal differentiation, synaptic plasticity, glia and microglia activity, cognitive functions, and the central and local control of reproduction.

Results: BPA has potential human health hazard associated with gestational, peri- and neonatal exposure. Beginning with BPA’s disposition, this review summarizes recent findings on the neurotoxicity of BPA and its analogues, on neuronal differentiation, synaptic plasticity, neuroinflammation, neuro-degeneration, and impairment of cognitive abilities. Furthermore, it reports the recent findings on the activity of BPA along the HPG axis, effects on the hypothalamic Gonadotropin Releasing Hormone (GnRH), and the associated effects on reproduction in both sexes and successful pregnancy.

Conclusion: BPA and its analogues impair neuronal activity, HPG axis function, reproduction, and fertility. Contrasting results have emerged in animal models and human. Thus, further studies are needed to better define their safety levels. This review offers new insights on these issues with the aim to find the “fil rouge”, if any, that characterize BPA’s mechanism of action with outcomes on neuronal function and reproduction.

Keywords: BPA, neuronal differentiation, synaptic plasticity, neuroinflammation, epigenetics, hypothalamus, HPG axis, GnRH, Kiss1, reproduction.

[1]
Rubin, B.S. Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J. Steroid Biochem. Mol. Biol., 2011, 127(1-2), 27-34.
[http://dx.doi.org/10.1016/j.jsbmb.2011.05.002] [PMID: 21605673]
[2]
Frye, C.A.; Bo, E.; Calamandrei, G.; Calzà, L.; Dessì-Fulgheri, F.; Fernández, M.; Fusani, L.; Kah, O.; Kajta, M.; Le Page, Y.; Patisaul, H.B.; Venerosi, A.; Wojtowicz, A.K.; Panzica, G.C. Endocrine disrupters: a review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems. J. Neuroendocrinol., 2012, 24(1), 144-159.
[http://dx.doi.org/10.1111/j.1365-2826.2011.02229.x] [PMID: 21951193]
[3]
Richter, C.A.; Birnbaum, L.S.; Farabollini, F.; Newbold, R.R.; Rubin, B.S.; Talsness, C.E.; Vandenbergh, J.G.; Walser-Kuntz, D.R.; vom Saal, F.S. In vivo effects of bisphenol A in laboratory rodent studies. Reprod. Toxicol., 2007, 24(2), 199-224.
[http://dx.doi.org/10.1016/j.reprotox.2007.06.004] [PMID: 17683900]
[4]
Tavares, R.S.; Escada-Rebelo, S.; Correia, M.; Mota, P.C.; Ramalho-Santos, J. The non-genomic effects of endocrine-disrupting chemicals on mammalian sperm. Reproduction, 2016, 151(1), R1-R13.
[http://dx.doi.org/10.1530/REP-15-0355] [PMID: 26585413]
[5]
Peretz, J.; Vrooman, L.; Ricke, W.A.; Hunt, P.A.; Ehrlich, S.
Hauser, R.; Padmanabhan, V.; Taylor, H.S.; Swan, S.H.; Vande, V.C.A.; Flaws, J.A. Bisphenol a and reproductive health: Update of experimental and human evidence, 2007-2013. Environ. Health Perspect., 2014, 122(8), 775-786.
[http://dx.doi.org/10.1289/ehp.1307728] [PMID: 24896072]
[6]
Corrales, J.; Kristofco, L.A.; Steele, W.B.; Yates, B.S.; Breed, C.S.; Williams, E.S.; Brooks, B.W. Global assessment of bisphenol a in the environment: Review and analysis of its occurrence and bioaccumulation. Dose-Response. An. Int. J., 2015, 13, 1-29.
[http://dx.doi.org/10.1177/1559325815598308]
[7]
Vandenberg, L.N.; Ehrlich, S.; Belcher, S.M.; Ben-Jonathan, N.; Dolinoy, D.C.; Hugo, E.R.; Hunt, P.A.; Newbold, R.R.; Rubin, B.S.; Saili, K.S.; Soto, A.M.; Wang, H.S.; vom Saal, F.S. Low dose effects of Bisphenol A: An integrated review of in vitro, laboratory animal and epidemiology studies. Endocr. Disrupt., 2013, 1 e25078
[http://dx.doi.org/10.4161/endo.26490]
[8]
Le Magueresse-Battistoni, B.; Multigner, L.; Beausoleil, C.; Rousselle, C. Effects of bisphenol A on metabolism and evidences of a mode of action mediated through endocrine disruption. Mol. Cell. Endocrinol., 2018, 475, 74-91.
[http://dx.doi.org/10.1016/j.mce.2018.02.009] [PMID: 29481862]
[9]
Chianese, R.; Troisi, J.; Richards, S.; Scafuro, M.; Fasano, S.; Guida, M.; Pierantoni, R.; Meccariello, R. Bisphenol A in reproduction: epigenetic effects. Curr. Med. Chem., 2018, 25(6), 748-770.
[PMID: 28990514]
[10]
Nunez, A.A.; Kannan, K.; Giesy, J.P.; Fang, J.; Clemens, L.G. Effects of bisphenol A on energy balance and accumulation in brown adipose tissue in rats. Chemosphere, 2001, 42(8), 917-922.
[http://dx.doi.org/10.1016/S0045-6535(00)00196-X] [PMID: 11272914]
[11]
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., 2008, 116(1), 39-44.
[http://dx.doi.org/10.1289/ehp.10753] [PMID: 18197297]
[12]
Mercogliano, R.; Santonicola, S. Investigation on bisphenol A levels in human milk and dairy supply chain: A review. Food Chem. Toxicol., 2018, 114, 98-107.
[http://dx.doi.org/10.1016/j.fct.2018.02.021] [PMID: 29448092]
[13]
Dualde, P.; Pardo, O.; Corpas-Burgos, F.; Kuligowski, J.; Gormaz, M.; Vento, M.; Pastor, A.; Yusà, V. Biomonitoring of bisphenols A, F, S in human milk and probabilistic risk assessment for breastfed infants. Sci. Total Environ., 2019, 668, 797-805.
[http://dx.doi.org/10.1016/j.scitotenv.2019.03.024] [PMID: 30870748]
[14]
Mørck, T.J.; Sorda, G.; Bechi, N.; Rasmussen, B.S.; Nielsen, J.B.; Ietta, F.; Rytting, E.; Mathiesen, L.; Paulesu, L.; Knudsen, L.E. Placental transport and in vitro effects of Bisphenol A. Reprod. Toxicol., 2010, 30(1), 131-137.
[http://dx.doi.org/10.1016/j.reprotox.2010.02.007] [PMID: 20214975]
[15]
Corbel, T.; Gayrard, V.; Puel, S.; Lacroix, M.Z.; Berrebi, A.; Gil, S.; Viguié, C.; Toutain, P.L.; Picard-Hagen, N. Bidirectional placental transfer of Bisphenol A and its main metabolite, Bisphenol A-Glucuronide, in the isolated perfused human placenta. Reprod. Toxicol., 2014, 47, 51-58.
[http://dx.doi.org/10.1016/j.reprotox.2014.06.001] [PMID: 24933518]
[16]
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., 2015, 13(1), 3978.
[http://dx.doi.org/10.2903/j.efsa.2015.3978]
[17]
EFSA A statement on the developmental immunotoxicity of bisphenol A (BPA): answer to the question from the Dutch Ministry of Health, Welfare and Sport. EFSA J., 2016, 14(10), 4580.
[18]
Rosenfeld, C.S. Neuroendocrine disruption in animal models due to exposure to bisphenol A analogues. Front. Neuroendocrinol., 2017, 47, 123-133.
[http://dx.doi.org/10.1016/j.yfrne.2017.08.001] [PMID: 28801100]
[19]
Andra, S.S.; Charisiadis, P.; Arora, M.; van Vliet-Ostaptchouk, J.V.; Makris, K.C. Biomonitoring of human exposures to chlorinated derivatives and structural analogs of bisphenol A. Environ. Int., 2015, 85, 352-379.
[http://dx.doi.org/10.1016/j.envint.2015.09.011] [PMID: 26521216]
[20]
Ullah, A.; Pirzada, M.; Jahan, S.; Ullah, H.; Shaheen, G.; Rehman, H.; Siddiqui, M.F.; Butt, M.A. Bisphenol A and its analogs bisphenol B, bisphenol F, and bisphenol S: Comparative in vitro and in vivo studies on the sperms and testicular tissues of rats. Chemosphere, 2018, 209, 508-516.
[http://dx.doi.org/10.1016/j.chemosphere.2018.06.089] [PMID: 29940534]
[21]
Rochester, J.R.; Bolden, A.L. Bisphenol S and F: A Systematic Review and Comparison of the Hormonal Activity of Bisphenol A Substitutes. Environ. Health Perspect., 2015, 123(7), 643-650.
[http://dx.doi.org/10.1289/ehp.1408989] [PMID: 25775505]
[22]
Chianese, R.; Coccurello, R.; Viggiano, A.; Scafuro, M.; Fiore, M.; Coppola, G.; Operto, F.F.; Fasano, S.; Layé, S.; Pierantoni, R.; Meccariello, R. Impact of dietary fats on brain functions. Curr. Neuropharmacol., 2018, 16(7), 1059-1085.
[http://dx.doi.org/10.2174/1570159X15666171017102547] [PMID: 29046155]
[23]
Motti, M.L.; D. Angelo, S.; Meccariello, R. MicroRNAs, cancer and diet: Facts and new exciting perspectives. Curr. Mol. Pharmacol., 2018, 11(2), 90-96.
[http://dx.doi.org/10.2174/1874467210666171013123733] [PMID: 29034844]
[24]
D’Angelo, S.; Scafuro, M.; Meccariello, R. BPA and nutraceuticals, simultaneous effects on endocrine functions. Endocr. Metab. Immune Disord. Drug Targets, 2019, 19(5), 594-604. Epub ahead of print
[http://dx.doi.org/10.2174/1871530319666190101120119] [PMID: 30621569]
[25]
Rebuli, M.E.; Patisaul, H.B. Assessment of sex specific endocrine disrupting effects in the prenatal and pre-pubertal rodent brain. J. Steroid Biochem. Mol. Biol., 2016, 160, 148-159.
[http://dx.doi.org/10.1016/j.jsbmb.2015.08.021] [PMID: 26307491]
[26]
Mhaouty-Kodja, S.; Belzunces, L.P.; Canivenc, M.C.; Schroeder, H.; Chevrier, C.; Pasquier, E. Impairment of learning and memory performances induced by BPA: Evidences from the literature of a MoA mediated through an ED. Mol. Cell. Endocrinol., 2018, 475, 54-73.
[http://dx.doi.org/10.1016/j.mce.2018.03.017] [PMID: 29605460]
[27]
Murata, M.; Kang, J.H.; Bisphenol, A.; Bisphenol, A. BPA) and cell signaling pathways. Biotechnol. Adv., 2018, 36(1), 311-327.
[http://dx.doi.org/10.1016/j.biotechadv.2017.12.002] [PMID: 29229539]
[28]
Barouki, R.; Melén, E.; Herceg, Z.; Beckers, J.; Chen, J.; Karagas, M.; Puga, A.; Xia, Y.; Chadwick, L.; Yan, W.; Audouze, K.; Slama, R.; Heindel, J.; Grandjean, P.; Kawamoto, T.; Nohara, K. Epigenetics as a mechanism linking developmental exposures to long-term toxicity. Environ. Int., 2018, 114, 77-86.
[http://dx.doi.org/10.1016/j.envint.2018.02.014] [PMID: 29499450]
[29]
Doshi, T.; Mehta, S.S.; Dighe, V.; Balasinor, N.; Vanage, G. Hypermethylation of estrogen receptor promoter region in adult testis of rats exposed neonatally to bisphenol A. Toxicology, 2011, 289(2-3), 74-82.
[http://dx.doi.org/10.1016/j.tox.2011.07.011] [PMID: 21827818]
[30]
Dolinoy, D.C. The agouti mouse model: An epigenetic biosensor for nutritional and environmental alterations on the fetal epigenome. Nutr. Rev., 2008, 66(Suppl. 1), S7-S11.
[http://dx.doi.org/10.1111/j.1753-4887.2008.00056.x] [PMID: 18673496]
[31]
Dolinoy, D.C.; Huang, D.; Jirtle, R.L. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc. Natl. Acad. Sci. USA, 2007, 104(32), 13056-13061.
[http://dx.doi.org/10.1073/pnas.0703739104] [PMID: 17670942]
[32]
Yaoi, T.; Itoh, K.; Nakamura, K.; Ogi, H.; Fujiwara, Y.; Fushiki, S. Genome-wide analysis of epigenomic alterations in fetal mouse forebrain after exposure to low doses of bisphenol A. Biochem. Biophys. Res. Commun., 2008, 376(3), 563-567.
[http://dx.doi.org/10.1016/j.bbrc.2008.09.028] [PMID: 18804091]
[33]
Wolstenholme, J.T.; Rissman, E.F.; Connelly, J.J. The role of Bisphenol A in shaping the brain, epigenome and behavior. Horm. Behav., 2011, 59(3), 296-305.
[http://dx.doi.org/10.1016/j.yhbeh.2010.10.001] [PMID: 21029734]
[34]
Kim, J.H.; Sartor, M.A.; Rozek, L.S.; Faulk, C.; Anderson, O.S.; Jones, T.R.; Nahar, M.S.; Dolinoy, D.C. Perinatal bisphenol A exposure promotes dose-dependent alterations of the mouse methylome. BMC Genomics, 2014, 15, 30.
[http://dx.doi.org/10.1186/1471-2164-15-30] [PMID: 24433282]
[35]
Tse, L.A.; Lee, P.M.Y.; Ho, W.M.; Lam, A.T.; Lee, M.K.; Ng, S.S.M.; He, Y.; Leung, K.S.; Hartle, J.C.; Hu, H.; Kan, H.; Wang, F.; Ng, C.F. Bisphenol A and other environmental risk factors for prostate cancer in Hong Kong. Environ. Int., 2017, 107, 1-7.
[http://dx.doi.org/10.1016/j.envint.2017.06.012] [PMID: 28644961]
[36]
Yin, L.; Dai, Y.; Jiang, X.; Liu, Y.; Chen, H.; Han, F.; Cao, J.; Liu, J. Role of DNA methylation in bisphenol A exposed mouse spermatocyte. Environ. Toxicol. Pharmacol., 2016, 48, 265-271.
[http://dx.doi.org/10.1016/j.etap.2016.11.003] [PMID: 27855348]
[37]
Zheng, H.; Zhou, X.; Li, D.K.; Yang, F.; Pan, H.; Li, T.; Miao, M.; Li, R.; Yuan, W. Genome-wide alteration in DNA hydroxymethylation in the sperm from bisphenol A-exposed men. PLoS One, 2017, 12(6)e0178535
[http://dx.doi.org/10.1371/journal.pone.0178535] [PMID: 28582417]
[38]
Ferguson-Smith, A.C. Genomic imprinting: the emergence of an epigenetic paradigm. Nat. Rev. Genet., 2011, 12(8), 565-575.
[http://dx.doi.org/10.1038/nrg3032] [PMID: 21765458]
[39]
Susiarjo, M.; Sasson, I.; Mesaros, C.; Bartolomei, M.S. Bisphenol a exposure disrupts genomic imprinting in the mouse. PLoS Genet., 2013, 9(4) e1003401
[http://dx.doi.org/10.1371/journal.pgen.1003401] [PMID: 23593014]
[40]
Drobná, Z.; Henriksen, A.D.; Wolstenholme, J.T.; Montiel, C.; Lambeth, P.S.; Shang, S.; Harris, E.P.; Zhou, C.; Flaws, J.A.; Adli, M.; Rissman, E.F. Transgenerational effects of bisphenol a on gene expression and DNA methylation of imprinted genes in brain. Endocrinology, 2018, 159(1), 132-144.
[http://dx.doi.org/10.1210/en.2017-00730] [PMID: 29165653]
[41]
Eichenlaub-Ritter, U.; Pacchierotti, F.; Bisphenol, A. Bisphenol a effects on mammalian oogenesis and epigenetic integrity of oocytes: A case study exploring risks of endocrine disrupting chemicals. BioMed Res. Int., 2015. 2015698795
[http://dx.doi.org/10.1155/2015/698795] [PMID: 26339634]
[42]
Doherty, L.F.; Bromer, J.G.; Zhou, Y.; Aldad, T.S.; Taylor, H.S. In utero exposure to diethylstilbestrol (DES) or bisphenol-A (BPA) increases EZH2 expression in the mammary gland: an epigenetic mechanism linking endocrine disruptors to breast cancer. Horm. Cancer, 2010, 1(3), 146-155.
[http://dx.doi.org/10.1007/s12672-010-0015-9] [PMID: 21761357]
[43]
Viré, E.; Brenner, C.; Deplus, R.; Blanchon, L.; Fraga, M.; Didelot, C.; Morey, L.; Van Eynde, A.; Bernard, D.; Vanderwinden, J.M.; Bollen, M.; Esteller, M.; Di Croce, L.; de Launoit, Y.; Fuks, F. The Polycomb group protein EZH2 directly controls DNA methylation. Nature, 2006, 439(7078), 871-874.
[http://dx.doi.org/10.1038/nature04431] [PMID: 16357870]
[44]
Chen, Z.; Zuo, X.; He, D.; Ding, S.; Xu, F.; Yang, H.; Jin, X.; Fan, Y.; Ying, L.; Tian, C.; Ying, C. Long-term exposure to a 'safe' dose of bisphenol A reduced protein acetylation in adult rat testes Sci. Rep, 2017, 9, 7. 40337
[45]
Godlewski, J.; Lenart, J.; Salinska, E. MicroRNA in brain pathology: Neurodegeneration the other side of the brain cancer. Noncoding RNA, 2019, 5(1)E20
[http://dx.doi.org/10.3390/ncrna5010020] [PMID: 30813461]
[46]
Shi, C.; Zhang, L.; Qin, C. Long non-coding RNAs in brain development, synaptic biology, and Alzheimer’s disease. Brain Res. Bull., 2017, 132, 160-169.
[http://dx.doi.org/10.1016/j.brainresbull.2017.03.010] [PMID: 28347717]
[47]
Sekar, S.; Liang, W.S. Circular RNA expression and function in the brain. Noncoding RNA Res., 2019, 4(1), 23-29.
[http://dx.doi.org/10.1016/j.ncrna.2019.01.001] [PMID: 30891534]
[48]
Leighton, L.J.; Bredy, T.W. Functional interplay between small non-coding RNAs and RNA modification in the brain. Noncoding RNA, 2018, 4(2) E15
[http://dx.doi.org/10.3390/ncrna4020015] [PMID: 29880782]
[49]
Noack, F.; Calegari, F. Epitranscriptomics: A New Regulatory Mechanism of Brain Development and Function. Front. Neurosci., 2018, 12, 85.
[http://dx.doi.org/10.3389/fnins.2018.00085] [PMID: 29515357]
[50]
Avissar-Whiting, M.; Veiga, K.R.; Uhl, K.M.; Maccani, M.A.; Gagne, L.A.; Moen, E.L.; Marsit, C.J. Bisphenol A exposure leads to specific microRNA alterations in placental cells. Reprod. Toxicol., 2010, 29(4), 401-406.
[http://dx.doi.org/10.1016/j.reprotox.2010.04.004] [PMID: 20417706]
[51]
Derghal, A.; Djelloul, M.; Trouslard, J.; Mounien, L. An emerging role of micro-RNA in the effect of the endocrine disruptors. Front. Neurosci., 2016, 10, 318.
[http://dx.doi.org/10.3389/fnins.2016.00318] [PMID: 27445682]
[52]
Gao, G.Z.; Zhao, Y.; Li, H.X.; Li, W. Bisphenol A-elicited miR-146a-5p impairs murine testicular steroidogenesis through negative regulation of Mta3 signaling. Biochem. Biophys. Res. Commun., 2018, 501(2), 478-485.
[http://dx.doi.org/10.1016/j.bbrc.2018.05.017] [PMID: 29746863]
[53]
Cho, H.; Kim, S.J.; Park, H.W.; Oh, M.J.; Yu, S.Y.; Lee, S.Y.; Park, C.; Han, G.R.; Oh, J.H.; Hwang, S.Y.; Yoon, S.J. A relationship between miRNA and gene expression in the mouse Sertoli cell line after exposure to bisphenol A. Biochip J., 2010, 4, 75-81.
[http://dx.doi.org/10.1007/s13206-010-4112-1]
[54]
Kuruto-Niwa, R.; Tateoka, Y.; Usuki, Y.; Nozawa, R. Measurement of bisphenol A concentrations in human colostrum. Chemosphere, 2007, 66(6), 1160-1164.
[http://dx.doi.org/10.1016/j.chemosphere.2006.06.073] [PMID: 16904728]
[55]
Guerrero-Bosagna, C.; Savenkova, M.; Haque, M.M.; Nilsson, E.; Skinner, M.K. Environmentally induced epigenetic transgenerational inheritance of altered Sertoli cell transcriptome and epigenome: molecular etiology of male infertility. PLoS One, 2013, 8(3) e59922
[http://dx.doi.org/10.1371/journal.pone.0059922] [PMID: 23555832]
[56]
Mendonca, K.; Hauser, R.; Calafat, A.M.; Arbuckle, T.E.; Duty, S.M. Bisphenol A concentrations in maternal breast milk and infant urine. Int. Arch. Occup. Environ. Health, 2014, 87(1), 13-20.
[http://dx.doi.org/10.1007/s00420-012-0834-9] [PMID: 23212895]
[57]
Dobrzyńska, M.M.; Gajowik, A.; Radzikowska, J.; Tyrkiel, E.J.; Jankowska-Steifer, E.A. Male-mediated F1 effects in mice exposed to bisphenol A, either alone or in combination with X-irradiation. Mutat. Res. Genet. Toxicol. Environ. Mutagen., 2015, 789-790, 36-45.
[http://dx.doi.org/10.1016/j.mrgentox.2015.06.015] [PMID: 26232256]
[58]
Marczylo, E.L.; Amoako, A.A.; Konje, J.C.; Gant, T.W.; Marczylo, T.H. Smoking induces differential miRNA expression in human spermatozoa: a potential transgenerational epigenetic concern? Epigenetics, 2012, 7(5), 432-439.
[http://dx.doi.org/10.4161/epi.19794] [PMID: 22441141]
[59]
Mielke, H.; Partosch, F.; Gundert-Remy, U. The contribution of dermal exposure to the internal exposure of bisphenol A in man. Toxicol. Lett., 2011, 204(2-3), 190-198.
[http://dx.doi.org/10.1016/j.toxlet.2011.04.032] [PMID: 21571050]
[60]
Marquet, F.; Payan, J.P.; Beydon, D.; Wathier, L.; Grandclaude, M.C.; Ferrari, E. In vivo and ex vivo percutaneous absorption of [14C]-bisphenol A in rats: a possible extrapolation to human absorption? Arch. Toxicol., 2011, 85(9), 1035-1043.
[http://dx.doi.org/10.1007/s00204-011-0651-z] [PMID: 21287149]
[61]
Nishikawa, M.; Iwano, H.; Yanagisawa, R.; Koike, N.; Inoue, H.; Yokota, H. Placental transfer of conjugated bisphenol A and subsequent reactivation in the rat fetus. Environ. Health Perspect., 2010, 118(9), 1196-1203.
[http://dx.doi.org/10.1289/ehp.0901575] [PMID: 20382578]
[62]
Schönfelder, G.; Wittfoht, W.; Hopp, H.; Talsness, C.E.; Paul, M.; Chahoud, I. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ. Health Perspect., 2002, 110(11), A703-A707.
[http://dx.doi.org/10.1289/ehp.021100703] [PMID: 12417499]
[63]
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., 2000, 108(10), 931-935.
[http://dx.doi.org/10.1289/ehp.00108931] [PMID: 11049811]
[64]
Teeguarden, J.G.; Twaddle, N.C.; Churchwell, M.I.; Doerge, D.R. Urine and serum biomonitoring of exposure to environmental estrogens I: Bisphenol A in pregnant women. Food Chem. Toxicol., 2016, 92, 129-142.
[http://dx.doi.org/10.1016/j.fct.2016.03.023] [PMID: 27038865]
[65]
Grandin, F.C.; Lacroix, M.Z.; Gayrard, V.; Viguié, C.; Mila, H.; de Place, A.; Vayssière, C.; Morin, M.; Corbett, J.; Gayrard, C.; Gely, C.A.; Toutain, P.L.; Picard-Hagen, N. Is bisphenol S a safer alternative to bisphenol A in terms of potential fetal exposure? Placental transfer across the perfused human placenta. Chemosphere, 2019, 221, 471-478.
[http://dx.doi.org/10.1016/j.chemosphere.2019.01.065] [PMID: 30654261]
[66]
Roen, E.L.; Wang, Y.; Calafat, A.M.; Wang, S.; Margolis, A.; Herbstman, J.; Hoepner, L.A.; Rauh, V.; Perera, F.P. Bisphenol A exposure and behavioral problems among inner city children at 7-9 years of age. Environ. Res., 2015, 142, 739-745.
[http://dx.doi.org/10.1016/j.envres.2015.01.014] [PMID: 25724466]
[67]
Kundakovic, M.; Gudsnuk, K.; Franks, B.; Madrid, J.; Miller, R.L.; Perera, F.P.; Champagne, F.A. Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure. Proc. Natl. Acad. Sci. USA, 2013, 110(24), 9956-9961.
[http://dx.doi.org/10.1073/pnas.1214056110] [PMID: 23716699]
[68]
McCaffrey, K.A.; Jones, B.; Mabrey, N.; Weiss, B.; Swan, S.H.; Patisaul, H.B. Sex specific impact of perinatal bisphenol A (BPA) exposure over a range of orally administered doses on rat hypothalamic sexual differentiation. Neurotoxicology, 2013, 36(36), 55-62.
[http://dx.doi.org/10.1016/j.neuro.2013.03.001] [PMID: 23500335]
[69]
Kohwi, M.; Doe, C.Q. Temporal fate specification and neural progenitor competence during development. Nat. Rev. Neurosci., 2013, 14(12), 823-838.
[http://dx.doi.org/10.1038/nrn3618] [PMID: 24400340]
[70]
Ohtsuka, T.; Kageyama, R. Regulation of temporal properties of neural stem cells and transition timing of neurogenesis and gliogenesis during mammalian neocortical development. Semin. Cell Dev. Biol, 2019, pii: S1084-9521. (18), 30062-4.
[http://dx.doi.org/10.1016/j.semcdb.2019.01.007]
[71]
Kempermann, G.; Jessberger, S.; Steiner, B.; Kronenberg, G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci., 2004, 27(8), 447-452.
[http://dx.doi.org/10.1016/j.tins.2004.05.013] [PMID: 15271491]
[72]
Kee, N.; Teixeira, C.M.; Wang, A.H.; Frankland, P.W. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci., 2007, 10(3), 355-362.
[http://dx.doi.org/10.1038/nn1847] [PMID: 17277773]
[73]
Zhao, C.; Deng, W.; Gage, F.H. Mechanisms and functional implications of adult neurogenesis. Cell, 2008, 132(4), 645-660.
[http://dx.doi.org/10.1016/j.cell.2008.01.033] [PMID: 18295581]
[74]
Stuchlik, A. Dynamic learning and memory, synaptic plasticity and neurogenesis: an update. Front. Behav. Neurosci., 2014, 8, 106.
[http://dx.doi.org/10.3389/fnbeh.2014.00106] [PMID: 24744707]
[75]
Cassé, F.; Richetin, K.; Toni, N. Astrocytes' contribution to adult neurogenesis in physiology and alzheimer's disease. Front. Cell. Neurosci, 2018, 12(432) eCollection 2018
[76]
Negri-Cesi, P.; Bisphenol, A. Bisphenol a interaction with brain development and functions. Dose Response, 2015, 13(2)1559325815590394
[http://dx.doi.org/10.1177/1559325815590394] [PMID: 26672480]
[77]
Tiwari, S.K.; Agarwal, S.; Seth, B.; Yadav, A.; Ray, R.S.; Mishra, V.N.; Chaturvedi, R.K. Inhibitory effects of bisphenol-a on neural stem cells proliferation and differentiation in the rat brain are dependent on Wnt/β-Catenin pathway. Mol. Neurobiol., 2015, 52(3), 1735-1757.
[http://dx.doi.org/10.1007/s12035-014-8940-1] [PMID: 25381574]
[78]
Kim, K.; Son, T.G.; Kim, S.J.; Kim, H.S.; Kim, T.S.; Han, S.Y.; Lee, J. Suppressive effects of bisphenol A on the proliferation of neural progenitor cells. J. Toxicol. Environ. Health A, 2007, 70(15-16), 1288-1295.
[http://dx.doi.org/10.1080/15287390701434216] [PMID: 17654246]
[79]
Kim, K.; Son, T.G.; Park, H.R.; Kim, S.J.; Kim, H.S.; Kim, H.S.; Kim, T.S.; Jung, K.K.; Han, S.Y.; Lee, J. Potencies of bisphenol A on the neuronal differentiation and hippocampal neurogenesis. J. Toxicol. Environ. Health A, 2009, 72(21-22), 1343-1351.
[http://dx.doi.org/10.1080/15287390903212501] [PMID: 20077206]
[80]
Agarwal, S.; Tiwari, S.K.; Seth, B.; Yadav, A.; Singh, A.; Mudawal, A.; Chauhan, L.K.; Gupta, S.K.; Choubey, V.; Tripathi, A.; Kumar, A.; Ray, R.S.; Shukla, S.; Parmar, D.; Chaturvedi, R.K. Activation of autophagic flux against xenoestrogen Bisphenol-A-induced hippocampal neurodegeneration via AMP kinase (AMPK)/mammalian target of Rapamycin (mTOR) pathways. J. Biol. Chem., 2015, 290(34), 21163-21184.
[http://dx.doi.org/10.1074/jbc.M115.648998] [PMID: 26139607]
[81]
Zhao, Y.G.; Zhang, H. The incredible ULKs: Autophagy and beyond. Mol. Cell, 2016, 62(4), 475-476.
[http://dx.doi.org/10.1016/j.molcel.2016.05.005] [PMID: 27203174]
[82]
Li, Z.; Zhao, K.; Lv, X.; Lan, Y.; Hu, S.; Shi, J.; Guan, J.; Yang, Y.; Lu, H.; He, H.; Gao, F.; He, W. Ulk1 governs nerve growth factor/trka signaling by mediating Rab5 GTPase activation in porcine hemagglutinating encephalomyelitis virus-induced neurodegenerative disorders. J. Virol., 2018, 92(16), e00325-e18.
[http://dx.doi.org/10.1128/JVI.00325-18] [PMID: 29875237]
[83]
Agarwal, S.; Yadav, A.; Tiwari, S.K.; Seth, B.; Chauhan, L.K.; Khare, P.; Ray, R.S.; Chaturvedi, R.K. Dynamin-related Protein 1 inhibition mitigates Bisphenol A-mediated alterations in mitochondrial dynamics and neural stem cell proliferation and differentiation. J. Biol. Chem., 2016, 291(31), 15923-15939.
[http://dx.doi.org/10.1074/jbc.M115.709493] [PMID: 27252377]
[84]
Jang, Y.J.; Park, H.R.; Kim, T.H.; Yang, W.J.; Lee, J.J.; Choi, S.Y.; Oh, S.B.; Lee, E.; Park, J.H.; Kim, H.P.; Kim, H.S.; Lee, J. High dose bisphenol A impairs hippocampal neurogenesis in female mice across generations. Toxicology, 2012, 296(1-3), 73-82.
[http://dx.doi.org/10.1016/j.tox.2012.03.007] [PMID: 22484357]
[85]
Kumar, D.; Thakur, M.K. Effect of perinatal exposure to Bisphenol-A on DNA methylation and histone acetylation in cerebral cortex and hippocampus of postnatal male mice. J. Toxicol. Sci., 2017, 42(3), 281-289.
[http://dx.doi.org/10.2131/jts.42.281] [PMID: 28496034]
[86]
Feng, J.; Zhou, Y.; Campbell, S.L.; Le, T.; Li, E.; Sweatt, J.D.; Silva, A.J.; Fan, G. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat. Neurosci., 2010, 13(4), 423-430.
[http://dx.doi.org/10.1038/nn.2514] [PMID: 20228804]
[87]
Campbell, R.R.; Wood, M.A. How the epigenome integrates information and reshapes the synapse. Nat. Rev. Neurosci., 2019, 20(3), 133-147.
[http://dx.doi.org/10.1038/s41583-019-0121-9] [PMID: 30696992]
[88]
Keverne, E.B. Significance of epigenetics for understanding brain development, brain evolution and behaviour. Neuroscience, 2014, 264, 207-217.
[http://dx.doi.org/10.1016/j.neuroscience.2012.11.030] [PMID: 23201253]
[89]
Bale, T.L. Epigenetic and transgenerational reprogramming of brain development. Nat. Rev. Neurosci., 2015, 16(6), 332-344.
[http://dx.doi.org/10.1038/nrn3818] [PMID: 25921815]
[90]
Cheong, A.; Johnson, S.A.; Howald, E.C.; Ellersieck, M.R.; Camacho, L.; Lewis, S.M.; Vanlandingham, M.M.; Ying, J.; Ho, S.M.; Rosenfeld, C.S. Gene expression and DNA methylation changes in the hypothalamus and hippocampus of adult rats developmentally exposed to bisphenol A or ethinyl estradiol: a CLARITY-BPA consortium study. Epigenetics, 2018, 13(7), 704-720.
[http://dx.doi.org/10.1080/15592294.2018.1497388] [PMID: 30001178]
[91]
Kitraki, E.; Nalvarte, I.; Alavian-Ghavanini, A.; Rüegg, J. Developmental exposure to bisphenol A alters expression and DNA methylation of Fkbp5, an important regulator of the stress response. Mol. Cell. Endocrinol., 2015, 417, 191-199.
[http://dx.doi.org/10.1016/j.mce.2015.09.028] [PMID: 26427651]
[92]
Alavian-Ghavanini, A.; Lin, P.I.; Lind, P.M.; Risén Rimfors, S.; Halin Lejonklou, M.; Dunder, L.; Tang, M.; Lindh, C.; Bornehag, C.G.; Rüegg, J. Prenatal bisphenol a exposure is linked to epigenetic changes in glutamate receptor subunit gene Grin2b in female rats and humans. Sci. Rep., 2018, 8(1), 11315.
[http://dx.doi.org/10.1038/s41598-018-29732-9] [PMID: 30054528]
[93]
Paoletti, P.; Bellone, C.; Zhou, Q. NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat. Rev. Neurosci., 2013, 14(6), 383-400.
[http://dx.doi.org/10.1038/nrn3504] [PMID: 23686171]
[94]
Aiba, T.; Saito, T.; Hayashi, A.; Sato, S.; Yunokawa, H.; Maruyama, T.; Fujibuchi, W.; Ohsako, S. Does the prenatal bisphenol A exposure alter DNA methylation levels in the mouse hippocampus? An analysis using a high-sensitivity methylome technique. Genes Environ., 2018, 40, 12.
[http://dx.doi.org/10.1186/s41021-018-0099-y] [PMID: 29881475]
[95]
Hajszan, T.; Leranth, C. Bisphenol A interferes with synaptic remodeling. Front. Neuroendocrinol., 2010, 31(4), 519-530.
[http://dx.doi.org/10.1016/j.yfrne.2010.06.004] [PMID: 20609373]
[96]
MacLusky, N.J.; Hajszan, T.; Leranth, C. The environmental estrogen bisphenol a inhibits estradiol-induced hippocampal synaptogenesis. Environ. Health Perspect., 2005, 113(6), 675-679.
[http://dx.doi.org/10.1289/ehp.7633] [PMID: 15929888]
[97]
Leranth, C.; Petnehazy, O.; MacLusky, N.J. Gonadal hormones affect spine synaptic density in the CA1 hippocampal subfield of male rats. J. Neurosci., 2003, 23(5), 1588-1592.
[http://dx.doi.org/10.1523/JNEUROSCI.23-05-01588.2003] [PMID: 12629162]
[98]
Leranth, C.; Hajszan, T.; Szigeti-Buck, K.; Bober, J.; MacLusky, N.J. Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates. Proc. Natl. Acad. Sci. USA, 2008, 105(37), 14187-14191.
[http://dx.doi.org/10.1073/pnas.0806139105] [PMID: 18768812]
[99]
Santoro, A.; Spinelli, C.C.; Martucciello, S.; Nori, S.L.; Capunzo, M.; Puca, A.A.; Ciaglia, E. Innate immunity and cellular senescence: The good and the bad in the developmental and aged brain. J. Leukoc. Biol., 2018, 103(3), 509-524.
[http://dx.doi.org/10.1002/JLB.3MR0118-003R] [PMID: 29389023]
[100]
Allen, N.J.; Lyons, D.A. Glia as architects of central nervous system formation and function. Science, 2018, 362(6411), 181-185.
[http://dx.doi.org/10.1126/science.aat0473] [PMID: 30309945]
[101]
Ramon-Cañellas, P.; Peterson, H.P.; Morante, J. From early to late neurogenesis: neural progenitors and the glial niche from a fly’s point of view. Neuroscience, 2019, 399, 39-52.
[http://dx.doi.org/10.1016/j.neuroscience.2018.12.014] [PMID: 30578972]
[102]
Schwarz, J.M.; Sholar, P.W.; Bilbo, S.D. Sex differences in microglial colonization of the developing rat brain. J. Neurochem., 2012, 120(6), 948-963.
[http://dx.doi.org/10.1111/j.1471-4159.2011.07630.x] [PMID: 22182318]
[103]
Williamson, L.L.; Sholar, P.W.; Mistry, R.S.; Smith, S.H.; Bilbo, S.D. Microglia and memory: modulation by early-life infection. J. Neurosci., 2011, 31(43), 15511-15521.
[http://dx.doi.org/10.1523/JNEUROSCI.3688-11.2011] [PMID: 22031897]
[104]
Rosin, J.M.; Kurrasch, D.M. Bisphenol A and microglia: could microglia be responsive to this environmental contaminant during neural development? Am. J. Physiol. Endocrinol. Metab., 2018, 315(2), E279-E285.
[http://dx.doi.org/10.1152/ajpendo.00443.2017] [PMID: 29812986]
[105]
Sadowski, R.N.; Wise, L.M.; Park, P.Y.; Schantz, S.L.; Juraska, J.M. Early exposure to bisphenol A alters neuron and glia number in the rat prefrontal cortex of adult males, but not females. Neuroscience, 2014, 279, 122-131.
[http://dx.doi.org/10.1016/j.neuroscience.2014.08.038] [PMID: 25193849]
[106]
Wise, L.M.; Sadowski, R.N.; Kim, T.; Willing, J.; Juraska, J.M. Long-term effects of adolescent exposure to bisphenol A on neuron and glia number in the rat prefrontal cortex: Differences between the sexes and cell type. Neurotoxicology, 2016, 53, 186-192.
[http://dx.doi.org/10.1016/j.neuro.2016.01.011] [PMID: 26828634]
[107]
Takahashi, M.; Komada, M.; Miyazawa, K.; Goto, S.; Ikeda, Y. Bisphenol A exposure induces increased microglia and microglial related factors in the murine embryonic dorsal telencephalon and hypothalamus. Toxicol. Lett., 2018, 284, 113-119.
[http://dx.doi.org/10.1016/j.toxlet.2017.12.010] [PMID: 29248573]
[108]
Luo, G.; Wang, S.; Li, Z.; Wei, R.; Zhang, L.; Liu, H.; Wang, C.; Niu, R.; Wang, J. Maternal bisphenol a diet induces anxiety-like behavior in female juvenile with neuroimmune activation. Toxicol. Sci., 2014, 140(2), 364-373.
[http://dx.doi.org/10.1093/toxsci/kfu085] [PMID: 24824810]
[109]
Zhu, J.; Jiang, L.; Liu, Y.; Qian, W.; Liu, J.; Zhou, J.; Gao, R.; Xiao, H.; Wang, J. MAPK and NF-κB pathways are involved in bisphenol A-induced TNF-α and IL-6 production in BV2 microglial cells. Inflammation, 2015, 38(2), 637-648.
[http://dx.doi.org/10.1007/s10753-014-9971-5] [PMID: 25047101]
[110]
Bilbo, S.D.; Frank, A.; Frank, A. Beach award: programming of neuroendocrine function by early-life experience: a critical role for the immune system. Horm. Behav., 2013, 63(5), 684-691.
[http://dx.doi.org/10.1016/j.yhbeh.2013.02.017] [PMID: 23474365]
[111]
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. Anxiogenic effects of developmental bisphenol A exposure are associated with gene expression changes in the juvenile rat amygdala and mitigated by soy. PLoS One, 2012, 7(9) e43890
[http://dx.doi.org/10.1371/journal.pone.0043890] [PMID: 22957036]
[112]
Rebuli, M.E.; Gibson, P.; Rhodes, C.L.; Cushing, B.S.; Patisaul, H.B. Sex differences in microglial colonization and vulnerabilities to endocrine disruption in the social brain. Gen. Comp. Endocrinol., 2016, 238, 39-46.
[http://dx.doi.org/10.1016/j.ygcen.2016.04.018] [PMID: 27102938]
[113]
Xu, X.B.; Fan, S.J.; He, Y.; Ke, X.; Song, C.; Xiao, Y.; Zhang, W.H.; Zhang, J.Y.; Yin, X.P.; Kato, N.; Pan, B.X. Loss of hippocampal oligodendrocytes contributes to the deficit of contextual fear learning in adult rats experiencing early bisphenol A exposure. Mol. Neurobiol., 2017, 54(6), 4524-4536.
[http://dx.doi.org/10.1007/s12035-016-0003-3] [PMID: 27364615]
[114]
Hu, F.; Li, T.; Gong, H.; Chen, Z.; Jin, Y.; Xu, G.; Wang, M. Bisphenol A impairs synaptic plasticity by both pre- and postsynaptic mechanisms. Adv. Sci. (Weinh.), 2017, 4(8) 1600493
[http://dx.doi.org/10.1002/advs.201600493] [PMID: 28852612]
[115]
Ishido, M.; Yonemoto, J.; Morita, M. Mesencephalic neurodegeneration in the orally administered bisphenol A-caused hyperactive rats. Toxicol. Lett., 2007, 173(1), 66-72.
[http://dx.doi.org/10.1016/j.toxlet.2007.06.014] [PMID: 17689037]
[116]
Chen, Z.; Li, T.; Zhang, L.; Wang, H.; Hu, F. Bisphenol A exposure remodels cognition of male rats attributable to excitatory alterations in the hippocampus and visual cortex. Toxicology, 2018, 410, 132-141.
[http://dx.doi.org/10.1016/j.tox.2018.10.002] [PMID: 30312744]
[117]
Zhou, Y.; Wang, Z.; Xia, M.; Zhuang, S.; Gong, X.; Pan, J.; Li, C.; Fan, R.; Pang, Q.; Lu, S. Neurotoxicity of low bisphenol A (BPA) exposure for young male mice: Implications for children exposed to environmental levels of BPA. Environ. Pollut., 2017, 229, 40-48.
[http://dx.doi.org/10.1016/j.envpol.2017.05.043] [PMID: 28577381]
[118]
Eilam-Stock, T.; Serrano, P.; Frankfurt, M.; Luine, V. Bisphenol-A impairs memory and reduces dendritic spine density in adult male rats. Behav. Neurosci., 2012, 126(1), 175-185.
[http://dx.doi.org/10.1037/a0025959] [PMID: 22004261]
[119]
Kuwahara, R.; Kawaguchi, S.; Kohara, Y.; Cui, H.; Yamashita, K. Perinatal exposure to low-dose bisphenol A impairs spatial learning and memory in male rats. J. Pharmacol. Sci., 2013, 123(2), 132-139.
[http://dx.doi.org/10.1254/jphs.13093FP] [PMID: 24077108]
[120]
Diaz Weinstein, S.; Villafane, J.J.; Juliano, N.; Bowman, R.E. Adolescent exposure to Bisphenol-A increases anxiety and sucrose preference but impairs spatial memory in rats independent of sex. Brain Res., 2013, 1529, 56-65.
[http://dx.doi.org/10.1016/j.brainres.2013.07.018] [PMID: 23872220]
[121]
Xu, X.H.; Wang, Y.M.; Zhang, J.; Luo, Q.Q.; Ye, Y.P.; Ruan, Q. Perinatal exposure to bisphenol-A changes N-methyl-D-aspartate receptor expression in the hippocampus of male rat offspring. Environ. Toxicol. Chem., 2010, 29(1), 176-181.
[http://dx.doi.org/10.1002/etc.18] [PMID: 20821433]
[122]
Kubo, K.; Arai, O.; Ogata, R.; Omura, M.; Hori, T.; Aou, S. Exposure to bisphenol A during the fetal and suckling periods disrupts sexual differentiation of the locus coeruleus and of behavior in the rat. Neurosci. Lett., 2001, 304(1-2), 73-76.
[http://dx.doi.org/10.1016/S0304-3940(01)01760-8] [PMID: 11335058]
[123]
Kubo, K.; Arai, O.; Omura, M.; Watanabe, R.; Ogata, R.; Aou, S. Low dose effects of bisphenol A on sexual differentiation of the brain and behavior in rats. Neurosci. Res., 2003, 45(3), 345-356.
[http://dx.doi.org/10.1016/S0168-0102(02)00251-1] [PMID: 12631470]
[124]
Elsworth, J.D.; Jentsch, J.D.; Groman, S.M.; Roth, R.H.; Redmond, E.D., Jr; Leranth, C. Low circulating levels of bisphenol-A induce cognitive deficits and loss of asymmetric spine synapses in dorsolateral prefrontal cortex and hippocampus of adult male monkeys. J. Comp. Neurol., 2015, 523(8), 1248-1257.
[http://dx.doi.org/10.1002/cne.23735] [PMID: 25557059]
[125]
Braun, J.M.; Yolton, K.; Dietrich, K.N.; Hornung, R.; Ye, X.; Calafat, A.M.; Lanphear, B.P. Prenatal bisphenol A exposure and early childhood behavior. Environ. Health Perspect., 2009, 117(12), 1945-1952.
[http://dx.doi.org/10.1289/ehp.0900979] [PMID: 20049216]
[126]
Braun, J.M.; Kalkbrenner, A.E.; Calafat, A.M.; Yolton, K.; Ye, X.; Dietrich, K.N.; Lanphear, B.P. Impact of early-life bisphenol A exposure on behavior and executive function in children. Pediatrics, 2011, 128(5), 873-882.
[http://dx.doi.org/10.1542/peds.2011-1335] [PMID: 22025598]
[127]
Perera, F.; Vishnevetsky, J.; Herbstman, J.B.; Calafat, A.M.; Xiong, W.; Rauh, V.; Wang, S. Prenatal bisphenol a exposure and child behavior in an inner-city cohort. Environ. Health Perspect., 2012, 120(8), 1190-1194.
[http://dx.doi.org/10.1289/ehp.1104492] [PMID: 22543054]
[128]
Lim, Y.H.; Bae, S.; Kim, B.N.; Shin, C.H.; Lee, Y.A.; Kim, J.I.; Hong, Y.C. Prenatal and postnatal bisphenol A exposure and social impairment in 4-year-old children. Environ. Health, 2017, 16(1), 79.
[http://dx.doi.org/10.1186/s12940-017-0289-2] [PMID: 28747197]
[129]
Miodovnik, A.; Engel, S.M.; Zhu, C.; Ye, X.; Soorya, L.V.; Silva, M.J.; Calafat, A.M.; Wolff, M.S. Endocrine disruptors and childhood social impairment. Neurotoxicology, 2011, 32(2), 261-267.
[http://dx.doi.org/10.1016/j.neuro.2010.12.009] [PMID: 21182865]
[130]
Carter, C.J.; Blizard, R.A. 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., 2016, 101, 83-109.
[http://dx.doi.org/10.1016/j.neuint.2016.10.011] [PMID: 27984170]
[131]
Thongkorn, S.; Kanlayaprasit, S.; Jindatip, D.; Tencomnao, T.; Hu, V.W.; Sarachana, T. Sex differences in the effects of prenatal bisphenol A exposure on genes associated with autism spectrum disorder in the hippocampus. Sci. Rep., 2019, 9(1), 3038.
[http://dx.doi.org/10.1038/s41598-019-39386-w] [PMID: 30816183]
[132]
Harley, K.G.; Gunier, R.B.; Kogut, K.; Johnson, C.; Bradman, A.; Calafat, A.M.; Eskenazi, B. Prenatal and early childhood bisphenol A concentrations and behavior in school-aged children. Environ. Res., 2013, 126, 43-50.
[http://dx.doi.org/10.1016/j.envres.2013.06.004] [PMID: 23870093]
[133]
Ghassabian, A.; Bell, E.M.; Ma, W.L.; Sundaram, R.; Kannan, K.; Buck Louis, G.M.; Yeung, E. Concentrations of perfluoroalkyl substances and bisphenol A in newborn dried blood spots and the association with child behavior. Environ. Pollut, 2018, 243(Pt B), 1629-1636.
[http://dx.doi.org/10.1016/j.envpol.2018.09.107]
[134]
Matsushima, A.; Liu, X.; Okada, H.; Shimohigashi, M.; Shimohigashi, Y. Bisphenol AF is a full agonist for the estrogen receptor ERalpha but a highly specific antagonist for ERbeta. Environ. Health Perspect., 2010, 118(9), 1267-1272.
[http://dx.doi.org/10.1289/ehp.0901819] [PMID: 20427257]
[135]
Li, Y.; Burns, K.A.; Arao, Y.; Luh, C.J.; Korach, K.S. Differential estrogenic actions of endocrine-disrupting chemicals bisphenol A, bisphenol AF, and zearalenone through estrogen receptor α and β in vitro. Environ. Health Perspect., 2012, 120(7), 1029-1035.
[http://dx.doi.org/10.1289/ehp.1104689] [PMID: 22494775]
[136]
Molina-Molina, J.M.; Amaya, E.; Grimaldi, M.; Sáenz, J.M.; Real, M.; Fernández, M.F.; Balaguer, P.; Olea, N. In vitro study on the agonistic and antagonistic activities of bisphenol-S and other bisphenol-A congeners and derivatives via nuclear receptors. Toxicol. Appl. Pharmacol., 2013, 272(1), 127-136.
[http://dx.doi.org/10.1016/j.taap.2013.05.015] [PMID: 23714657]
[137]
Danzl, E.; Sei, K.; Soda, S.; Ike, M.; Fujita, M. Biodegradation of bisphenol A, bisphenol F and bisphenol S in seawater. Int. J. Environ. Res. Public Health, 2009, 6(4), 1472-1484.
[http://dx.doi.org/10.3390/ijerph6041472] [PMID: 19440529]
[138]
Liao, C.; Liu, F.; Kannan, K. Bisphenol s, a new bisphenol analogue, in paper products and currency bills and its association with bisphenol a residues. Environ. Sci. Technol., 2012, 46(12), 6515-6522.
[http://dx.doi.org/10.1021/es300876n] [PMID: 22591511]
[139]
Inadera, H. Neurological Effects of Bisphenol A and its Analogues. Int. J. Med. Sci., 2015, 12(12), 926-936.
[http://dx.doi.org/10.7150/ijms.13267] [PMID: 26664253]
[140]
Kim, B.; Colon, E.; Chawla, S.; Vandenberg, L.N.; Suvorov, A. Endocrine disruptors alter social behaviors and indirectly influence social hierarchies via changes in body weight. Environ. Health, 2015, 14, 64.
[http://dx.doi.org/10.1186/s12940-015-0051-6] [PMID: 26242739]
[141]
Ohtani, N.; Iwano, H.; Suda, K.; Tsuji, E.; Tanemura, K.; Inoue, H.; Yokota, H. Adverse effects of maternal exposure to bisphenol F on the anxiety- and depression-like behavior of offspring. J. Vet. Med. Sci., 2017, 79(2), 432-439.
[http://dx.doi.org/10.1292/jvms.16-0502] [PMID: 28025458]
[142]
Catanese, M.C.; Vandenberg, L.N.; Bisphenol, S. BPS) alters maternal behavior and brain in mice exposed during pregnancy/lactation and their daughters. Endocrinology, 2017, 158(3), 516-530.
[PMID: 28005399]
[143]
Castro, B.; Sánchez, P.; Torres, J.M.; Ortega, E. 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., 2015, 142, 281-287.
[http://dx.doi.org/10.1016/j.envres.2015.07.001] [PMID: 26186136]
[144]
Lee, S.; Kim, Y.K.; Shin, T.Y.; Kim, S.H. Neurotoxic effects of bisphenol AF on calcium-induced ROS and MAPKs. Neurotox. Res., 2013, 23(3), 249-259.
[http://dx.doi.org/10.1007/s12640-012-9353-4] [PMID: 22996013]
[145]
Pierantoni, R.; Cobellis, G.; Meccariello, R.; Fasano, S. Evolutionary aspects of cellular communication in the vertebrate hypothalamo-hypophysio-gonadal axis. Int. Rev. Cytol., 2002, 218, 69-141.
[http://dx.doi.org/10.1016/S0074-7696(02)18012-0] [PMID: 12199520]
[146]
Pierantoni, R.; Cobellis, G.; Meccariello, R.; Cacciola, G.; Chianese, R.; Chioccarelli, T.; Fasano, S. CB1 activity in male reproduction: mammalian and nonmammalian animal models. Vitam. Horm., 2009, 81, 367-387.
[http://dx.doi.org/10.1016/S0083-6729(09)81014-5] [PMID: 19647119]
[147]
Pierantoni, R.; Cobellis, G.; Meccariello, R.; Cacciola, G.; Chianese, R.; Chioccarelli, T.; Fasano, S. Testicular gonadotropin-releasing hormone activity, progression of spermatogenesis, and sperm transport in vertebrates. Ann. N. Y. Acad. Sci., 2009, 1163, 279-291.
[http://dx.doi.org/10.1111/j.1749-6632.2008.03617.x] [PMID: 19456349]
[148]
Cacciola, G.; Chianese, R.; Chioccarelli, T.; Ciaramella, V.; Fasano, S.; Pierantoni, R.; Meccariello, R.; Cobellis, G. Cannabinoids and reproduction: A lasting and intriguing history. Pharmac., 2010, 3, 3275-3323.
[http://dx.doi.org/10.3390/ph3103275]
[149]
Chianese, R.; Chioccarelli, T.; Cacciola, G.; Ciaramella, V.; Fasano, S.; Pierantoni, R.; Meccariello, R.; Cobellis, G. The contribution of lower vertebrate animal models in human reproduction research. Gen. Comp. Endocrinol., 2011, 171(1), 17-27.
[http://dx.doi.org/10.1016/j.ygcen.2010.12.011] [PMID: 21192939]
[150]
Meccariello, R.; Chianese, R.; Chioccarelli, T.; Ciaramella, V.; Fasano, S.; Pierantoni, R.; Cobellis, G. Intra-testicular signals regulate germ cell progression and production of qualitatively mature spermatozoa in vertebrates. Front. Endocrinol. (Lausanne), 2014, 5, 69.
[http://dx.doi.org/10.3389/fendo.2014.00069] [PMID: 24847312]
[151]
Chianese, R.; Cobellis, G.; Chioccarelli, T.; Ciaramella, V.; Migliaccio, M.; Fasano, S.; Pierantoni, R.; Meccariello, R. Kisspeptins, estrogens and male fertility. Curr. Med. Chem., 2016, 23(36), 4070-4091.
[http://dx.doi.org/10.2174/0929867323666160902155434] [PMID: 27593959]
[152]
Cobellis, G.; Meccariello, R.; Chianese, R.; Chioccarelli, T.; Fasano, S.; Pierantoni, R. Effects of neuroendocrine CB1 activity on adult Leydig cells. Front. Endocrinol. (Lausanne), 2016, 7, 47.
[http://dx.doi.org/10.3389/fendo.2016.00047] [PMID: 27375550]
[153]
Chianese, R.; Colledge, W.H.; Fasano, S.; Meccariello, R. Editorial: The Multiple Facets of Kisspeptin Activity in Biological Systems. Front. Endocrinol. (Lausanne), 2018, 9, 727.
[http://dx.doi.org/10.3389/fendo.2018.00727] [PMID: 30559719]
[154]
Meccariello, R.; Fasano, S.; Pierantoni, R.; Cobellis, G. Modulators of hypothalamic-pituitary-gonadal axis for the control of spermatogenesis and sperm quality in vertebrates. Front. Endocrinol. (Lausanne), 2014, 5, 135.
[http://dx.doi.org/10.3389/fendo.2014.00135] [PMID: 25183961]
[155]
Ciaramella, V.; Chianese, R.; Pariante, P.; Fasano, S.; Pierantoni, R.; Meccariello, R. Expression analysis of gnrh1 and gnrhr1 in spermatogenic cells of rat. Int. J. Endocrinol., 2015, 2015 982726
[http://dx.doi.org/10.1155/2015/982726] [PMID: 25861269]
[156]
Cobellis, G.; Meccariello, R.; Pierantoni, R.; Fasano, S. Intratesticular signals for progression of germ cell stages in vertebrates. Gen. Comp. Endocrinol., 2003, 134(3), 220-228.
[http://dx.doi.org/10.1016/S0016-6480(03)00281-8] [PMID: 14636628]
[157]
Chianese, R.; Ciaramella, V.; Fasano, S.; Pierantoni, R.; Meccariello, R. Kisspeptin regulates steroidogenesis and spermiation in anuran amphibian. Reproduction, 2017, 154(4), 403-414.
[http://dx.doi.org/10.1530/REP-17-0030] [PMID: 28878091]
[158]
Chianese, R.; Ciaramella, V.; Fasano, S.; Pierantoni, R.; Meccariello, R. Kisspeptin drives germ cell progression in the anuran amphibian Pelophylax esculentus: a study carried out in ex vivo testes. Gen. Comp. Endocrinol., 2015, 211, 81-91.
[http://dx.doi.org/10.1016/j.ygcen.2014.11.008] [PMID: 25452028]
[159]
Huo, X.; Chen, D.; He, Y.; Zhu, W.; Zhou, W.; Zhang, J. Bisphenol-A and Female Infertility: A Possible Role of Gene-Environment Interactions. Int. J. Environ. Res. Public Health, 2015, 12(9), 11101-11116.
[http://dx.doi.org/10.3390/ijerph120911101] [PMID: 26371021]
[160]
Cariati, F.; D’Uonno, N.; Borrillo, F.; Iervolino, S.; Galdiero, G.; Tomaiuolo, R. Bisphenol a: an emerging threat to male fertility. Reprod. Biol. Endocrinol., 2019, 17(1), 6.
[http://dx.doi.org/10.1186/s12958-018-0447-6] [PMID: 30660193]
[161]
Franssen, D.; Gérard, A.; Hennuy, B.; Donneau, A.F.; Bourguignon, J.P.; Parent, A.S. Delayed neuroendocrine sexual maturation in female rats after a very low dose of bisphenol a through altered GABAergic neurotransmission and opposing effects of a high dose. Endocrinology, 2016, 157(5), 1740-1750.
[http://dx.doi.org/10.1210/en.2015-1937] [PMID: 26950200]
[162]
Oliveira, I.M.; Romano, R.M.; de Campos, P.; Cavallin, M.D.; Oliveira, C.A.; Romano, M.A. Delayed onset of puberty in male offspring from bisphenol A-treated dams is followed by the modulation of gene expression in the hypothalamic-pituitary-testis axis in adulthood. Reprod. Fertil. Dev., 2017, 29(12), 2496-2505.
[http://dx.doi.org/10.1071/RD17107] [PMID: 28641706]
[163]
de Roux, N.; Genin, E.; Carel, J.C.; Matsuda, F.; Chaussain, J.L.; Milgrom, E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc. Natl. Acad. Sci. USA, 2003, 100(19), 10972-10976, 10972, 10976..
[http://dx.doi.org/10.1073/pnas.1834399100] [PMID: 12944565]
[164]
Seminara, S.B.; Messager, S.; Chatzidaki, E.E.; Thresher, R.R.; Acierno, J.S., Jr; Shagoury, J.K.; Bo-Abbas, Y.; Kuohung, W.; Schwinof, K.M.; Hendrick, A.G.; Zahn, D.; Dixon, J.; Kaiser, U.B.; Slaugenhaupt, S.A.; Gusella, J.F.; O’Rahilly, S.; Carlton, M.B.; Crowley, W.F., Jr; Aparicio, S.A.; Colledge, W.H. The GPR54 gene as a regulator of puberty. N. Engl. J. Med., 2003, 349(17), 1614-1627.
[http://dx.doi.org/10.1056/NEJMoa035322] [PMID: 14573733]
[165]
Pinilla, L.; Aguilar, E.; Dieguez, C.; Millar, R.P.; Tena-Sempere, M. Kisspeptins and reproduction: Physiological roles and regulatory mechanisms. Physiol. Rev., 2012, 92(3), 1235-1316.
[http://dx.doi.org/10.1152/physrev.00037.2010] [PMID: 22811428]
[166]
Patisaul, H.B.; Todd, K.L.; Mickens, J.A.; Adewale, H.B. Impact of neonatal exposure to the ERalpha agonist PPT, bisphenol-A or phytoestrogens on hypothalamic kisspeptin fiber density in male and female rats. Neurotoxicology, 2009, 30(3), 350-357.
[http://dx.doi.org/10.1016/j.neuro.2009.02.010] [PMID: 19442818]
[167]
Cao, J.; Mickens, J.A.; McCaffrey, K.A.; Leyrer, S.M.; Patisaul, H.B. Neonatal bisphenol a exposure alters sexually dimorphic gene expression in the postnatal rat hypothalamus. Neurotoxicology, 2012, 33(1), 23-36.
[http://dx.doi.org/10.1016/j.neuro.2011.11.002] [PMID: 22101008]
[168]
Arambula, S.E.; Fuchs, J.; Cao, J.; Patisaul, H.B. Effects of perinatal bisphenol A exposure on the volume of sexually-dimorphic nuclei of juvenile rats: A CLARITY-BPA consortium study. Neurotoxicology, 2017, 63, 33-42.
[http://dx.doi.org/10.1016/j.neuro.2017.09.002] [PMID: 28890130]
[169]
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, 2016, 157(10), 3856-3872.
[http://dx.doi.org/10.1210/en.2016-1339] [PMID: 27571134]
[170]
Kurian, J.R.; Keen, K.L.; Kenealy, B.P.; Garcia, J.P.; Hedman, C.J.; Terasawa, E. Acute influences of bisphenol a exposure on hypothalamic release of gonadotropin-releasing hormone and kisspeptin in female rhesus monkeys. Endocrinology, 2015, 156(7), 2563-2570.
[http://dx.doi.org/10.1210/en.2014-1634] [PMID: 25853665]
[171]
Klenke, U.; Constantin, S.; Wray, S. BPA directly decreases GnRH neuronal activity via noncanonical pathway. Endocrinology, 2016, 157(5), 1980-1990.
[http://dx.doi.org/10.1210/en.2015-1924] [PMID: 26934298]
[172]
McIlwraith, E.K.; Loganathan, N.; Belsham, D.D. Phoenixin expression is regulated by the fatty acids palmitate, docosahexaenoic acid and oleate, and the endocrine disrupting chemical bisphenol a in immortalized hypothalamic neurons. Front. Neurosci., 2018, 12, 838.
[http://dx.doi.org/10.3389/fnins.2018.00838] [PMID: 30524225]
[173]
McIlwraith, E.K.; Loganathan, N.; Belsham, DD. Regulation of Gpr173 expression, a putative phoenixin receptor, by saturated fatty acid palmitate and endocrine-disrupting chemical bisphenol A through a p38-mediated mechanism in immortalized hypothalamic neurons. Mol. Cell. Endocrinol, 2019, pii: S0303-7207. (19), 30038-3.
[http://dx.doi.org/10.1016/j.mce.2019.01.026]
[174]
Legeay, S.; Faure, S. Is bisphenol A an environmental obesogen? Food Chem. Toxicol., 2018, 114, 98-107.
[175]
Errico, S.; Portaccio, M.; Nicolucci, C.; Meccariello, R.; Chianese, R.; Scafuro, M.; Lepore, M.; Diano, N. A novel experimental approach for liver analysis in rats exposed to Bisphenol A by means of LC-mass spectrometry and infrared spectroscopy. J. Pharm. Biomed. Anal., 2019, 165, 207-212.
[http://dx.doi.org/10.1016/j.jpba.2018.12.011] [PMID: 30553981]
[176]
Shu, L.; Meng, Q.; Diamante, G.; Tsai, B.; Chen, Y.W.; Mikhail, A.; Luk, H.; Ritz, B.; Allard, P.; Yang, X. Prenatal bisphenol a exposure in mice induces multitissue multiomics disruptions linking to cardiometabolic disorders. Endocrinology, 2019, 160(2), 409-429.
[http://dx.doi.org/10.1210/en.2018-00817] [PMID: 30566610]
[177]
Friedman, J.M.; Halaas, J.L. Leptin and the regulation of body weight in mammals. Nature, 1998, 395(6704), 763-770.
[http://dx.doi.org/10.1038/27376] [PMID: 9796811]
[178]
Smith, J.T.; Acohido, B.V.; Clifton, D.K.; Steiner, R.A. KiSS-1 neurones are direct targets for leptin in the ob/ob mouse. J. Neuroendocrinol., 2006, 18(4), 298-303.
[http://dx.doi.org/10.1111/j.1365-2826.2006.01417.x] [PMID: 16503925]
[179]
Castellano, J.M.; Navarro, V.M.; Fernández-Fernández, R.; Nogueiras, R.; Tovar, S.; Roa, J.; Vazquez, M.J.; Vigo, E.; Casanueva, F.F.; Aguilar, E.; Pinilla, L.; Dieguez, C.; Tena-Sempere, M. Changes in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition. Endocrinology, 2005, 146(9), 3917-3925.
[http://dx.doi.org/10.1210/en.2005-0337] [PMID: 15932928]
[180]
Castellano, J.M.; Navarro, V.M.; Roa, J.; Pineda, R.; Sánchez-Garrido, M.A.; García-Galiano, D.; Vigo, E.; Dieguez, C.; Aguilar, E.; Pinilla, L.; Tena-Sempere, M. Alterations in hypothalamic KiSS-1 system in experimental diabetes: early changes and functional consequences. Endocrinology, 2009, 150(2), 784-794.
[http://dx.doi.org/10.1210/en.2008-0849] [PMID: 18845637]
[181]
Dudek, M.; Kołodziejski, P.A.; Pruszyńska-Oszmałek, E.; Sassek, M.; Ziarniak, K.; Nowak, K.W.; Sliwowska, J.H. Effects of high-fat diet-induced obesity and diabetes on Kiss1 and GPR54 expression in the hypothalamic-pituitary-gonadal (HPG) axis and peripheral organs (fat, pancreas and liver) in male rats. Neuropeptides, 2016, 56, 41-49.
[http://dx.doi.org/10.1016/j.npep.2016.01.005] [PMID: 26853724]
[182]
Roepke, T.A.; Yang, J.A.; Yasrebi, A.; Mamounis, K.J.; Oruc, E.; Zama, A.M.; Uzumcu, M. Regulation of arcuate genes by developmental exposures to endocrine-disrupting compounds in female rats. Reprod. Toxicol., 2016, 62, 18-26.
[http://dx.doi.org/10.1016/j.reprotox.2016.04.014] [PMID: 27103539]
[183]
Desai, M.; Ferrini, M.G.; Han, G.; Jellyman, J.K.; Ross, M.G. In vivo maternal and in vitro BPA exposure effects on hypothalamic neurogenesis and appetite regulators. Environ. Res., 2018, 164, 45-52.
[http://dx.doi.org/10.1016/j.envres.2018.02.011] [PMID: 29476947]
[184]
Cornejo, M.P.; Hentges, S.T.; Maliqueo, M.; Coirini, H.; Becu-Villalobos, D.; Elias, C.F. Neuroendocrine Regulation of Metabolism. J. Neuroendocrinol., 2016, 28(7), 12395.
[http://dx.doi.org/10.1111/jne.12395] [PMID: 27114114]
[185]
Wilson, J.L.; Enriori, P.J. A talk between fat tissue, gut, pancreas and brain to control body weight. Mol. Cell. Endocrinol., 2015, 418(Pt 2), 108-119.
[http://dx.doi.org/10.1016/j.mce.2015.08.022] [PMID: 26316427]
[186]
Salehi, A.; Loganathan, N.; Belsham, D.D. Bisphenol A induces Pomc gene expression through neuroinflammatory and PPARγ nuclear receptor-mediated mechanisms in POMC-expressing hypothalamic neuronal models. Mol. Cell. Endocrinol., 2019, 479, 12-19.
[http://dx.doi.org/10.1016/j.mce.2018.08.009] [PMID: 30149043]
[187]
MacKay, H.; Patterson, Z.R.; Abizaid, A. Perinatal Exposure to low-dose bisphenol-a disrupts the structural and functional development of the hypothalamic feeding circuitry. Endocrinology, 2017, 158(4), 768-777.
[http://dx.doi.org/10.1210/en.2016-1718] [PMID: 28323920]
[188]
Rezg, R.; Abot, A.; Mornagui, B.; Aydi, S.; Knauf, C. Effects of Bisphenol S on hypothalamic neuropeptides regulating feeding behavior and apelin/APJ system in mice. Ecotoxicol. Environ. Saf., 2018, 161, 459-466.
[http://dx.doi.org/10.1016/j.ecoenv.2018.06.001] [PMID: 29909315]
[189]
Pagotto, U.; Marsicano, G.; Cota, D.; Lutz, B.; Pasquali, R. The emerging role of the endocannabinoid system in endocrine regulation and energy balance. Endocr. Rev., 2006, 27(1), 73-100.
[http://dx.doi.org/10.1210/er.2005-0009] [PMID: 16306385]
[190]
Battista, N.; Meccariello, R.; Cobellis, G.; Fasano, S.; Di Tommaso, M.; Pirazzi, V.; Konje, J.C.; Pierantoni, R.; Maccarrone, M. The role of endocannabinoids in gonadal function and fertility along the evolutionary axis. Mol. Cell. Endocrinol., 2012, 355(1), 1-14.
[http://dx.doi.org/10.1016/j.mce.2012.01.014] [PMID: 22305972]
[191]
Meccariello, R.; Battista, N.; Bradshaw, H.B.; Wang, H. Updates in reproduction coming from the endocannabinoid system. Int. J. Endocrinol., 2014, 2014412354
[http://dx.doi.org/10.1155/2014/412354] [PMID: 24550985]
[192]
Bovolin, P.; Cottone, E.; Pomatto, V.; Fasano, S.; Pierantoni, R.; Cobellis, G.; Meccariello, R. Endocannabinoids are involved in male vertebrate reproduction: regulatory mechanisms at central and gonadal level. Front. Endocrinol. (Lausanne), 2014, 5, 54.
[http://dx.doi.org/10.3389/fendo.2014.00054] [PMID: 24782832]
[193]
Meccariello, R.; Franzoni, M.F.; Chianese, R.; Cottone, E.; Scarpa, D.; Donna, D.; Cobellis, G.; Guastalla, A.; Pierantoni, R.; Fasano, S. Interplay between the endocannabinoid system and GnRH-I in the forebrain of the anuran amphibian Rana esculenta. Endocrinology, 2008, 149(5), 2149-2158.
[http://dx.doi.org/10.1210/en.2007-1357] [PMID: 18218699]
[194]
Chianese, R.; Cobellis, G.; Pierantoni, R.; Fasano, S.; Meccariello, R. Non-mammalian vertebrate models and the endocannabinoid system: relationships with gonadotropin-releasing hormone. Mol. Cell. Endocrinol., 2008, 286(1-2)(Suppl. 1), S46-S51.
[http://dx.doi.org/10.1016/j.mce.2008.01.009] [PMID: 18325658]
[195]
Ciaramella, V.; Meccariello, R.; Chioccarelli, T.; Sirleto, M.; Fasano, S.; Pierantoni, R.; Chianese, R. Anandamide acts via kisspeptin in the regulation of testicular activity of the frog, Pelophylax esculentus. Mol. Cell. Endocrinol., 2016, 420, 75-84.
[http://dx.doi.org/10.1016/j.mce.2015.11.011] [PMID: 26586207]
[196]
Osei-Hyiaman, D.; Depetrillo, M.; Harvey-White, J.; Bannon, A.W.; Cravatt, B.F.; Kuhar, M.J.; Mackie, K.; Palkovits, M.; Kunos, G. Cocaine- and amphetamine-related transcript is involved in the orexigenic effect of endogenous anandamide. Neuroendocrinology, 2005, 81(4), 273-282.
[http://dx.doi.org/10.1159/000087925] [PMID: 16131814]
[197]
Suglia, A.; Chianese, R.; Migliaccio, M.; Ambrosino, C.; Fasano, S.; Pierantoni, R.; Cobellis, G.; Chioccarelli, T. Bisphenol A induces hypothalamic down-regulation of the the cannabinoid receptor 1 and anorexigenic effects in male mice. Pharmacol. Res., 2016, 113(Pt A), 376-383.
[http://dx.doi.org/10.1016/j.phrs.2016.09.005]
[198]
Loganathan, N.; Salehi, A.; Chalmers, J.A.; Belsham, D.D.; Bisphenol, A. Bisphenol a alters bmal1, Per2, and Rev-Erba mRNA and requires bmal1 to increase neuropeptide Y expression in hypothalamic neurons. Endocrinology, 2019, 160(1), 181-192.
[http://dx.doi.org/10.1210/en.2018-00881] [PMID: 30500912]
[199]
Chen, W.; Lau, S.W.; Fan, Y.; Wu, R.S.S.; Ge, W. Juvenile exposure to bisphenol A promotes ovarian differentiation but suppresses its growth - Potential involvement of pituitary follicle-stimulating hormone. Aquat. Toxicol., 2017, 193, 111-121.
[http://dx.doi.org/10.1016/j.aquatox.2017.10.008] [PMID: 29055862]
[200]
Maffini, M.V.; Rubin, B.S.; Sonnenschein, C.; Soto, A.M. Endocrine disruptors and reproductive health: The case of bisphenol-A. Mol. Cell. Endocrinol., 2006, 254-255, 179-186.
[http://dx.doi.org/10.1016/j.mce.2006.04.033] [PMID: 16781053]
[201]
Zhang, H-Q.; Zhang, X-F.; Zhang, L-J.; Chao, H-H.; Pan, B.; Feng, Y-M.; Li, L.; Sun, X.F.; Shen, W. Fetal exposure to bisphenol A affects the primordial follicle formation by inhibiting the meiotic progression of oocytes. Mol. Biol. Rep., 2012, 39(5), 5651-5657.
[http://dx.doi.org/10.1007/s11033-011-1372-3] [PMID: 22187349]
[202]
Susiarjo, M.; Hassold, T.J.; Freeman, E.; Hunt, P.A. Bisphenol A exposure in utero disrupts early oogenesis in the mouse. PLoS Genet., 2007, 3(1)e5
[http://dx.doi.org/10.1371/journal.pgen.0030005] [PMID: 17222059]
[203]
Hunt, P.A.; Lawson, C.; Gieske, M.; Murdoch, B.; Smith, H.; Marre, A.; Hassold, T.; VandeVoort, C.A. Bisphenol A alters early oogenesis and follicle formation in the fetal ovary of the rhesus monkey. Proc. Natl. Acad. Sci. USA, 2012, 109(43), 17525-17530.
[http://dx.doi.org/10.1073/pnas.1207854109] [PMID: 23012422]
[204]
Karavan, J.R.; Pepling, M.E. Effects of estrogenic compounds on neonatal oocyte development. Reprod. Toxicol., 2012, 34(1), 51-56.
[http://dx.doi.org/10.1016/j.reprotox.2012.02.005] [PMID: 22406039]
[205]
Rodríguez, H.A.; Santambrosio, N.; Santamaría, C.G.; Muñoz-de-Toro, M.; Luque, E.H. Neonatal exposure to bisphenol A reduces the pool of primordial follicles in the rat ovary. Reprod. Toxicol., 2010, 30(4), 550-557.
[http://dx.doi.org/10.1016/j.reprotox.2010.07.008] [PMID: 20692330]
[206]
Chao, H-H.; Zhang, X-F.; Chen, B.; Pan, B.; Zhang, L-J.; Li, L.; Sun, X-F.; Shi, Q-H.; Shen, W. Bisphenol A exposure modifies methylation of imprinted genes in mouse oocytes via the estrogen receptor signaling pathway. Histochem. Cell Biol., 2012, 137(2), 249-259.
[http://dx.doi.org/10.1007/s00418-011-0894-z] [PMID: 22131059]
[207]
Laing, L.V.; Viana, J.; Dempster, E.L.; Trznadel, M.; Trunkfield, L.A.; Uren Webster, T.M.; van Aerle, R.; Paull, G.C.; Wilson, R.J.; Mill, J.; Santos, E.M. Bisphenol A causes reproductive toxicity, decreases dnmt1 transcription, and reduces global DNA methylation in breeding zebrafish (Danio rerio). Epigenetics, 2016, 11(7), 526-538.
[http://dx.doi.org/10.1080/15592294.2016.1182272] [PMID: 27120497]
[208]
Liu, Y.; Yuan, C.; Chen, S.; Zheng, Y.; Zhang, Y.; Gao, J.; Wang, Z. Global and cyp19a1a gene specific DNA methylation in gonads of adult rare minnow Gobiocypris rarus under bisphenol A exposure. Aquat. Toxicol., 2014, 156, 10-16.
[http://dx.doi.org/10.1016/j.aquatox.2014.07.017] [PMID: 25125231]
[209]
Santangeli, S.; Maradonna, F.; Gioacchini, G.; Cobellis, G.; Piccinetti, C.C.; Dalla Valle, L.; Carnevali, O. BPA-induced deregulation of epigenetic patterns: Effects on female zebrafish reproduction. Sci. Rep., 2016, 6, 21982.
[http://dx.doi.org/10.1038/srep21982] [PMID: 26911650]
[210]
Kandaraki, E.; Chatzigeorgiou, A.; Livadas, S.; Palioura, E.; Economou, F.; Koutsilieris, M.; Palimeri, S.; Panidis, D.; Diamanti-Kandarakis, E. Endocrine disruptors and polycystic ovary syndrome (PCOS): Elevated serum levels of bisphenol A in women with PCOS. J. Clin. Endocrinol. Metab., 2011, 96(3), E480-E484.
[http://dx.doi.org/10.1210/jc.2010-1658] [PMID: 21193545]
[211]
Rutkowska, A.; Rachoń, D.; Bisphenol, A.; Bisphenol, A. BPA) and its potential role in the pathogenesis of the polycystic ovary syndrome (PCOS). Gynecol. Endocrinol., 2014, 30(4), 260-265.
[http://dx.doi.org/10.3109/09513590.2013.871517] [PMID: 24397396]
[212]
Takeuchi, T.; Tsutsumi, O. Serum bisphenol a concentrations showed gender differences, possibly linked to androgen levels. Biochem. Biophys. Res. Commun., 2002, 291(1), 76-78.
[http://dx.doi.org/10.1006/bbrc.2002.6407] [PMID: 11829464]
[213]
Takeuchi, T.; Tsutsumi, O.; Ikezuki, Y.; Takai, Y.; Taketani, Y. Positive relationship between androgen and the endocrine disruptor, bisphenol A, in normal women and women with ovarian dysfunction. Endocr. J., 2004, 51(2), 165-169.
[http://dx.doi.org/10.1507/endocrj.51.165] [PMID: 15118266]
[214]
Zhou, W.; Liu, J.; Liao, L.; Han, S.; Liu, J. Effect of bisphenol A on steroid hormone production in rat ovarian theca-interstitial and granulosa cells. Mol. Cell. Endocrinol., 2008, 283(1-2), 12-18.
[http://dx.doi.org/10.1016/j.mce.2007.10.010] [PMID: 18191889]
[215]
Fernández, M.; Bourguignon, N.; Lux-Lantos, V.; Libertun, C. Neonatal exposure to bisphenol a and reproductive and endocrine alterations resembling the polycystic ovarian syndrome in adult rats. Environ. Health Perspect., 2010, 118(9), 1217-1222.
[http://dx.doi.org/10.1289/ehp.0901257] [PMID: 20413367]
[216]
Seachrist, D.D.; Bonk, K.W.; Ho, S-M.; Prins, G.S.; Soto, A.M.; Keri, R.A. A review of the carcinogenic potential of bisphenol A. Reprod. Toxicol., 2016, 59, 167-182.
[http://dx.doi.org/10.1016/j.reprotox.2015.09.006] [PMID: 26493093]
[217]
Mallozzi, M.; Leone, C.; Manurita, F.; Bellati, F.; Caserta, D. Endocrine disrupting chemicals and endometrial cancer: An overview of recent laboratory evidence and epidemiological studies. Int. J. Environ. Res. Public Health, 2017, 14(3), 14.
[http://dx.doi.org/10.3390/ijerph14030334] [PMID: 28327540]
[218]
Aghajanova, L.; Giudice, L.C. Effect of bisphenol A on human endometrial stromal fibroblasts in vitro. Reprod. Biomed. Online, 2011, 22(3), 249-256.
[http://dx.doi.org/10.1016/j.rbmo.2010.12.007] [PMID: 21273127]
[219]
Pollock, T.; deCatanzaro, D. Presence and bioavailability of bisphenol A in the uterus of rats and mice following single and repeated dietary administration at low doses. Reprod. Toxicol., 2014, 49, 145-154.
[http://dx.doi.org/10.1016/j.reprotox.2014.08.005] [PMID: 25181699]
[220]
Diamanti-Kandarakis, E.; Bourguignon, J-P.; Giudice, L.C.; Hauser, R.; Prins, G.S.; Soto, A.M.; Zoeller, R.T.; Gore, A.C. Endocrine-disrupting chemicals: An Endocrine Society scientific statement. Endocr. Rev., 2009, 30(4), 293-342.
[http://dx.doi.org/10.1210/er.2009-0002] [PMID: 19502515]
[221]
Aldad, T.S.; Rahmani, N.; Leranth, C.; Taylor, H.S. Bisphenol-A exposure alters endometrial progesterone receptor expression in the nonhuman primate. Fertil. Steril., 2011, 96(1), 175-179.
[http://dx.doi.org/10.1016/j.fertnstert.2011.04.010] [PMID: 21536273]
[222]
Hiroi, H.; Tsutsumi, O.; Takeuchi, T.; Momoeda, M.; Ikezuki, Y.; Okamura, A.; Yokota, H.; Taketani, Y. Differences in serum bisphenol a concentrations in premenopausal normal women and women with endometrial hyperplasia. Endocr. J., 2004, 51(6), 595-600.
[http://dx.doi.org/10.1507/endocrj.51.595] [PMID: 15644579]
[223]
Han, T.S.; Lean, M.E. A clinical perspective of obesity, metabolic syndrome and cardiovascular disease. JRSM Cardiovasc. Dis., 2016, 52048004016633371
[http://dx.doi.org/10.1177/2048004016633371] [PMID: 26998259]
[224]
Shafiee, M.N.; Seedhouse, C.; Mongan, N.; Chapman, C.; Deen, S.; Abu, J.; Atiomo, W. Up-regulation of genes involved in the insulin signalling pathway (IGF1, PTEN and IGFBP1) in the endometrium may link polycystic ovarian syndrome and endometrial cancer. Mol. Cell. Endocrinol., 2016, 424, 94-101.
[http://dx.doi.org/10.1016/j.mce.2016.01.019] [PMID: 26802879]
[225]
Dickerson, S.M.; Gore, A.C. Estrogenic environmental endocrine-disrupting chemical effects on reproductive neuroendocrine function and dysfunction across the life cycle. Rev. Endocr. Metab. Disord., 2007, 8(2), 143-159.
[http://dx.doi.org/10.1007/s11154-007-9048-y] [PMID: 17674209]
[226]
Rich, A.L.; Phipps, L.M.; Tiwari, S.; Rudraraju, H.; Dokpesi, P.O. The increasing prevalence in intersex variation from toxicological dysregulation in fetal reproductive tissue differentiation and development by endocrine-disrupting chemicals. Environ. Health Insights, 2016, 10, 163-171.
[http://dx.doi.org/10.4137/EHI.S39825] [PMID: 27660460]
[227]
Strakovsky, R.S.; Schantz, S.L. Impacts of bisphenol A (BPA) and phthalate exposures on epigenetic outcomes in the human placenta. Environ. Epigenet., 2018, 4(3)dvy022
[http://dx.doi.org/10.1093/eep/dvy022] [PMID: 30210810]
[228]
Newbold, R.R.; Jefferson, W.N.; Padilla-Banks, E. Prenatal exposure to bisphenol a at environmentally relevant doses adversely affects the murine female reproductive tract later in life. Environ. Health Perspect., 2009, 117(6), 879-885.
[http://dx.doi.org/10.1289/ehp.0800045] [PMID: 19590677]
[229]
Pinney, S.E.; Mesaros, C.A.; Snyder, N.W.; Busch, C.M.; Xiao, R.; Aijaz, S.; Ijaz, N.; Blair, I.A.; Manson, J.M. Second trimester amniotic fluid bisphenol A concentration is associated with decreased birth weight in term infants. Reprod. Toxicol., 2017, 67, 1-9.
[http://dx.doi.org/10.1016/j.reprotox.2016.11.007] [PMID: 27829162]
[230]
Snijder, C.A.; Heederik, D.; Pierik, F.H.; Hofman, A.; Jaddoe, V.W.; Koch, H.M.; Longnecker, M.P.; Burdorf, A. Fetal growth and prenatal exposure to bisphenol A: the generation R study. Environ. Health Perspect., 2013, 121(3), 393-398.
[http://dx.doi.org/10.1289/ehp.1205296] [PMID: 23459363]
[231]
Burstyn, I.; Martin, J.W.; Beesoon, S.; Bamforth, F.; Li, Q.; Yasui, Y.; Cherry, N.M. Maternal exposure to bisphenol-A and fetal growth restriction: a case-referent study. Int. J. Environ. Res. Public Health, 2013, 10(12), 7001-7014.
[http://dx.doi.org/10.3390/ijerph10127001] [PMID: 24336026]
[232]
Casas, M.; Valvi, D.; Ballesteros-Gomez, A.; Gascon, M.; Fernández, M.F.; Garcia-Esteban, R.; Iñiguez, C.; Martínez, D.; Murcia, M.; Monfort, N.; Luque, N.; Rubio, S.; Ventura, R.; Sunyer, J.; Vrijheid, M. Exposure to bisphenol a and phthalates during pregnancy and ultrasound measures of fetal growth in the INMA-sabadell cohort. Environ. Health Perspect., 2016, 124(4), 521-528.
[http://dx.doi.org/10.1289/ehp.1409190] [PMID: 26196298]
[233]
Xu, X.; Chiung, Y.M.; Lu, F.; Qiu, S.; Ji, M.; Huo, X. Associations of cadmium, bisphenol A and polychlorinated biphenyl co-exposure in utero with placental gene expression and neonatal outcomes. Reprod. Toxicol., 2015, 52, 62-70.
[http://dx.doi.org/10.1016/j.reprotox.2015.02.004] [PMID: 25687722]
[234]
Morrissey, R.E.; George, J.D.; Price, C.J.; Tyl, R.W.; Marr, M.C.; Kimmel, C.A. The developmental toxicity of bisphenol A in rats and mice. Fundam. Appl. Toxicol., 1987, 8(4), 571-582.
[http://dx.doi.org/10.1016/0272-0590(87)90142-4] [PMID: 3609543]
[235]
Miao, M.; Yuan, W.; He, Y.; Zhou, Z.; Wang, J.; Gao, E.; Li, G.; Li, D-K. In utero exposure to bisphenol-A and anogenital distance of male offspring. Birth Defects Res. A Clin. Mol. Teratol., 2011, 91(10), 867-872.
[http://dx.doi.org/10.1002/bdra.22845] [PMID: 21987463]
[236]
Huo, W.; Xia, W.; Wan, Y.; Zhang, B.; Zhou, A.; Zhang, Y.; Huang, K.; Zhu, Y.; Wu, C.; Peng, Y.; Jiang, M.; Hu, J.; Chang, H.; Xu, B.; Li, Y.; Xu, S. Maternal urinary bisphenol A levels and infant low birth weight: A nested case-control study of the Health Baby Cohort in China. Environ. Int., 2015, 85, 96-103.
[http://dx.doi.org/10.1016/j.envint.2015.09.005] [PMID: 26382648]
[237]
Troisi, J.; Mikelson, C.; Richards, S.; Symes, S.; Adair, D.; Zullo, F.; Guida, M. Placental concentrations of bisphenol A and birth weight from births in the Southeastern U.S. Placenta, 2014, 35(11), 947-952.
[http://dx.doi.org/10.1016/j.placenta.2014.08.091] [PMID: 25227326]
[238]
Behnia, F.; Peltier, M.; Getahun, D.; Watson, C.; Saade, G.; Menon, R. High bisphenol A (BPA) concentration in the maternal, but not fetal, compartment increases the risk of spontaneous preterm delivery. J. Matern. Fetal Neonatal Med., 2016, 29(22), 3583-3589.
[http://dx.doi.org/10.3109/14767058.2016.1139570] [PMID: 26911979]
[239]
Cantonwine, D.E.; Ferguson, K.K.; Mukherjee, B.; McElrath, T.F.; Meeker, J.D. Urinary Bisphenol A Levels during Pregnancy and Risk of Preterm Birth. Environ. Health Perspect., 2015, 123(9), 895-901.
[http://dx.doi.org/10.1289/ehp.1408126] [PMID: 25815860]
[240]
Weinberger, B.; Vetrano, A.M.; Archer, F.E.; Marcella, S.W.; Buckley, B.; Wartenberg, D.; Robson, M.G.; Klim, J.; Azhar, S.; Cavin, S.; Wang, L.; Rich, D.Q. Effects of maternal exposure to phthalates and bisphenol A during pregnancy on gestational age. J. Matern. Fetal Neonatal Med., 2014, 27(4), 323-327.
[http://dx.doi.org/10.3109/14767058.2013.815718] [PMID: 23795657]
[241]
Padmanabhan, V.; Siefert, K.; Ransom, S.; Johnson, T.; Pinkerton, J.; Anderson, L.; Tao, L.; Kannan, K. Maternal bisphenol-A levels at delivery: a looming problem? J. Perinatol., 2008, 28(4), 258-263.
[http://dx.doi.org/10.1038/sj.jp.7211913] [PMID: 18273031]
[242]
Smarr, M.M.; Grantz, K.L.; Sundaram, R.; Maisog, J.M.; Kannan, K.; Louis, G.M.B. Parental urinary biomarkers of preconception exposure to bisphenol A and phthalates in relation to birth outcomes. Environ. Health, 2015, 14, 73.
[http://dx.doi.org/10.1186/s12940-015-0060-5] [PMID: 26362861]
[243]
Guida, M.; Troisi, J.; Ciccone, C.; Granozio, G.; Cosimato, C.; Di Spiezio Sardo, A.; Ferrara, C.; Guida, M.; Nappi, C.; Zullo, F.; Di Carlo, C. Bisphenol A and congenital developmental defects in humans. Mutat. Res., 2015, 774, 33-39.
[http://dx.doi.org/10.1016/j.mrfmmm.2015.02.007] [PMID: 25796969]
[244]
Balakrishnan, B.; Henare, K.; Thorstensen, E.B.; Ponnampalam, A.P.; Mitchell, M.D. Transfer of bisphenol A across the human placenta. Am. J. Obstet. Gynecol., 2010, 202(4), 393.e1-393.e7.
[http://dx.doi.org/10.1016/j.ajog.2010.01.025] [PMID: 20350650]
[245]
Machtinger, R.; Combelles, C.M.H.; Missmer, S.A.; Correia, K.F.; Williams, P.; Hauser, R.; Racowsky, C. Bisphenol-A and human oocyte maturation in vitro. Hum. Reprod., 2013, 28(10), 2735-2745.
[http://dx.doi.org/10.1093/humrep/det312] [PMID: 23904465]
[246]
Christiansen, S.; Axelstad, M.; Boberg, J.; Vinggaard, A.M.; Pedersen, G.A.; Hass, U. Low-dose effects of bisphenol A on early sexual development in male and female rats. Reproduction, 2014, 147(4), 477-487.
[http://dx.doi.org/10.1530/REP-13-0377] [PMID: 24298045]
[247]
Timms, B.G.; Howdeshell, K.L.; Barton, L.; Bradley, S.; Richter, C.A.; vom Saal, F.S. Estrogenic chemicals in plastic and oral contraceptives disrupt development of the fetal mouse prostate and urethra. Proc. Natl. Acad. Sci. USA, 2005, 102(19), 7014-7019.
[http://dx.doi.org/10.1073/pnas.0502544102] [PMID: 15867144]
[248]
Ho, S-M.; Tang, W-Y.; Belmonte de Frausto, J.; Prins, G.S. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res., 2006, 66(11), 5624-5632.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-0516] [PMID: 16740699]
[249]
Chen, J.; Wu, S.; Wen, S.; Shen, L.; Peng, J.; Yan, C.; Cao, X.; Zhou, Y.; Long, C.; Lin, T.; He, D.; Hua, Y.; Wei, G. The mechanism of environmental endocrine disruptors (DEHP) induces epigenetic transgenerational inheritance of cryptorchidism. PLoS One, 2015, 10(6)e0126403
[http://dx.doi.org/10.1371/journal.pone.0126403] [PMID: 26035430]
[250]
Fernández, M.F.; Arrebola, J.P.; Jiménez-Díaz, I.; Sáenz, J.M.; Molina-Molina, J.M.; Ballesteros, O.; Kortenkamp, A.; Olea, N. Bisphenol A and other phenols in human placenta from children with cryptorchidism or hypospadias. Reprod. Toxicol., 2016, 59, 89-95.
[http://dx.doi.org/10.1016/j.reprotox.2015.11.002] [PMID: 26602963]
[251]
Fiorini, C.; Tilloy-Ellul, A.; Chevalier, S.; Charuel, C.; Pointis, G. Sertoli cell junctional proteins as early targets for different classes of reproductive toxicants. Reprod. Toxicol., 2004, 18(3), 413-421.
[http://dx.doi.org/10.1016/j.reprotox.2004.01.002] [PMID: 15082077]
[252]
Salian, S.; Doshi, T.; Vanage, G. Neonatal exposure of male rats to Bisphenol A impairs fertility and expression of sertoli cell junctional proteins in the testis. Toxicology, 2009, 265(1-2), 56-67.
[http://dx.doi.org/10.1016/j.tox.2009.09.012] [PMID: 19782717]
[253]
Chianese, R.; Viggiano, A.; Urbanek, K.; Cappetta, D.; Troisi, J.; Scafuro, M.; Guida, M.; Esposito, G.; Ciuffreda, L.P.; Rossi, F.; Berrino, L.; Fasano, S.; Pierantoni, R.; De Angelis, A.; Meccariello, R. Chronic exposure to low dose of bisphenol A impacts on the first round of spermatogenesis via SIRT1 modulation. Sci. Rep., 2018, 8(1), 2961.
[http://dx.doi.org/10.1038/s41598-018-21076-8] [PMID: 29440646]
[254]
Zhang, G.L.; Zhang, X.F.; Feng, Y.M.; Li, L.; Huynh, E.; Sun, X.F.; Sun, Z.Y.; Shen, W. Exposure to bisphenol A results in a decline in mouse spermatogenesis. Reprod. Fertil. Dev., 2013, 25(6), 847-859.
[http://dx.doi.org/10.1071/RD12159] [PMID: 22951085]
[255]
Xie, M.; Bu, P.; Li, F.; Lan, S.; Wu, H.; Yuan, L.; Wang, Y. Neonatal bisphenol A exposure induces meiotic arrest and apoptosis of spermatogenic cells. Oncotarget, 2016, 7(9), 10606-10615.
[http://dx.doi.org/10.18632/oncotarget.7218] [PMID: 26863571]
[256]
Liu, C.; Duan, W.; Li, R.; Xu, S.; Zhang, L.; Chen, C.; He, M.; Lu, Y.; Wu, H.; Pi, H.; Luo, X.; Zhang, Y.; Zhong, M.; Yu, Z.; Zhou, Z. Exposure to bisphenol A disrupts meiotic progression during spermatogenesis in adult rats through estrogen-like activity. Cell Death Dis., 2013, 4 e676
[http://dx.doi.org/10.1038/cddis.2013.203] [PMID: 23788033]
[257]
Allard, P.; Colaiácovo, M.P. Bisphenol A impairs the double-strand break repair machinery in the germline and causes chromosome abnormalities. Proc. Natl. Acad. Sci. USA, 2010, 107(47), 20405-20410.
[http://dx.doi.org/10.1073/pnas.1010386107] [PMID: 21059909]
[258]
Horan, T.S.; Pulcastro, H.; Lawson, C.; Gerona, R.; Martin, S.; Gieske, M.C.; Sartain, C.V.; Hunt, P.A. Replacement Bisphenols Adversely Affect Mouse Gametogenesis with Consequences for Subsequent Generations. Curr. Biol., 2018, 28(18), 2948-2954.e3.
[http://dx.doi.org/10.1016/j.cub.2018.06.070] [PMID: 30220498]
[259]
Sasaki, M.; Lange, J.; Keeney, S. Genome destabilization by homologous recombination in the germ line. Nat. Rev. Mol. Cell Biol., 2010, 11(3), 182-195.
[http://dx.doi.org/10.1038/nrm2849] [PMID: 20164840]
[260]
Mínguez-Alarcón, L.; Hauser, R.; Gaskins, A.J. Effects of bisphenol A on male and couple reproductive health: A review. Fertil. Steril., 2016, 106(4), 864-870.
[http://dx.doi.org/10.1016/j.fertnstert.2016.07.1118] [PMID: 27498136]
[261]
Meeker, J.D.; Ehrlich, S.; Toth, T.L.; Wright, D.L.; Calafat, A.M.; Trisini, A.T.; Ye, X.; Hauser, R. Semen quality and sperm DNA damage in relation to urinary bisphenol A among men from an infertility clinic. Reprod. Toxicol., 2010, 30(4), 532-539.
[http://dx.doi.org/10.1016/j.reprotox.2010.07.005] [PMID: 20656017]
[262]
Rahman, M.S.; Kwon, W.S.; Lee, J.S.; Yoon, S.J.; Ryu, B.Y.; Pang, M.G. Bisphenol-A affects male fertility via fertility-related proteins in spermatozoa. Sci. Rep., 2015, 5, 9169.
[http://dx.doi.org/10.1038/srep09169] [PMID: 25772901]
[263]
Li, J.; Mao, R.; Zhou, Q.; Ding, L.; Tao, J.; Ran, M.M.; Gao, E.S.; Yuan, W.; Wang, J.T.; Hou, L.F. Exposure to bisphenol A (BPA) in Wistar rats reduces sperm quality with disruption of ERK signal pathway. Toxicol. Mech. Methods, 2016, 26(3), 180-188.
[http://dx.doi.org/10.3109/15376516.2016.1139024] [PMID: 26862991]
[264]
Kotwicka, M.; Skibinska, I.; Piworun, N.; Jendraszak, M.; Chmielewska, M.; Jedrzejczak, P. Bisphenol A modifies human spermatozoa motility in vitro. J. Medical. Sci, 2016, 85, 39-45.
[http://dx.doi.org/10.20883/jms.2016.5]
[265]
Lan, H.C.; Wu, K.Y.; Lin, I.W.; Yang, Z.J.; Chang, A.A.; Hu, M.C. Bisphenol A disrupts steroidogenesis and induces a sex hormone imbalance through c-Jun phosphorylation in Leydig cells. Chemosphere, 2017, 185, 237-246.
[http://dx.doi.org/10.1016/j.chemosphere.2017.07.004] [PMID: 28697429]
[266]
Feng, Y.; Jiao, Z.; Shi, J.; Li, M.; Guo, Q.; Shao, B. Effects of bisphenol analogues on steroidogenic gene expression and hormone synthesis in H295R cells. Chemosphere, 2016, 147, 9-19.
[http://dx.doi.org/10.1016/j.chemosphere.2015.12.081] [PMID: 26751127]
[267]
Ullah, A.; Pirzada, M.; Jahan, S.; Ullah, H.; Turi, N.; Ullah, W.; Siddiqui, M.F.; Zakria, M.; Lodhi, K.Z.; Khan, M.M. Impact of low-dose chronic exposure to bisphenol A and its analogue bisphenol B, bisphenol F and bisphenol S on hypothalamo-pituitary-testicular activities in adult rats: A focus on the possible hormonal mode of action. Food Chem. Toxicol., 2018, 121, 24-36.
[http://dx.doi.org/10.1016/j.fct.2018.08.024] [PMID: 30120946]
[268]
Desdoits-Lethimonier, C.; Lesné, L.; Gaudriault, P.; Zalko, D.; Antignac, J.P.; Deceuninck, Y.; Platel, C.; Dejucq-Rainsford, N.; Mazaud-Guittot, S.; Jégou, B. Parallel assessment of the effects of bisphenol A and several of its analogs on the adult human testis. Hum. Reprod., 2017, 32(7), 1465-1473.
[http://dx.doi.org/10.1093/humrep/dex093] [PMID: 28482050]
[269]
Roelofs, M.J.; van den Berg, M.; Bovee, T.F.; Piersma, A.H.; van Duursen, M.B. Structural bisphenol analogues differentially target steroidogenesis in murine MA-10 Leydig cells as well as the glucocorticoid receptor. Toxicology, 2015, 329, 10-20.
[http://dx.doi.org/10.1016/j.tox.2015.01.003] [PMID: 25576683]
[270]
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. A new chapter in the bisphenol A story: bisphenol S and bisphenol F are not safe alternatives to this compound. Fertil. Steril., 2015, 103(1), 11-21.
[http://dx.doi.org/10.1016/j.fertnstert.2014.11.005] [PMID: 25475787]
[271]
Kokkinaki, M.; Lee, T.L.; He, Z.; Jiang, J.; Golestaneh, N.; Hofmann, M.C.; Chan, W.Y.; Dym, M. The molecular signature of spermatogonial stem/progenitor cells in the 6-day-old mouse testis. Biol. Reprod., 2009, 80(4), 707-717.
[http://dx.doi.org/10.1095/biolreprod.108.073809] [PMID: 19109221]
[272]
Liang, S.; Yin, L.; Shengyang Yu, K.; Hofmann, M.C.; Yu, X. High-Content Analysis Provides Mechanistic Insights into the Testicular Toxicity of Bisphenol A and Selected Analogues in Mouse Spermatogonial Cells. Toxicol. Sci., 2017, 155(1), 43-60.
[http://dx.doi.org/10.1093/toxsci/kfw178] [PMID: 27633978]
[273]
Sidorkiewicz, I.; Czerniecki, J.; Jarząbek, K.; Zbucka-Krętowska, M.; Wołczyński, S. Cellular, transcriptomic and methylome effects of individual and combined exposure to BPA, BPF, BPS on mouse spermatocyte GC-2 cell line. Toxicol. Appl. Pharmacol., 2018, 359, 1-11.
[http://dx.doi.org/10.1016/j.taap.2018.09.006] [PMID: 30196065]
[274]
Shi, M.; Sekulovskii, N.; MacLean, J.A. II; Hayashi, K. Effects of bisphenol A analogues on reproductive functions in mice. Reprod. Toxicol., 2017, 73, 280-291.
[http://dx.doi.org/10.1016/j.reprotox.2017.06.134] [PMID: 28676390]
[275]
Shi, M.; Sekulovski, N.; MacLean, J.A., II; Hayashi, K. Prenatal exposure to bisphenol a analogues on male reproductive functions in mice. Toxicol. Sci, 2018, 163(2), 620-31.
[http://dx.doi.org/10.1093/toxsci/kfy061] [PMID: 29741722]
[276]
Jégou, B. The Sertoli-germ cell communication network in mammals. Int. Rev. Cytol., 1993, 147, 25-96.
[http://dx.doi.org/10.1016/S0074-7696(08)60766-4] [PMID: 8225836]
[277]
Liu, C.; Wang, H.; Shang, Y.; Liu, W.; Song, Z.; Zhao, H.; Wang, L.; Jia, P.; Gao, F.; Xu, Z.; Yang, L.; Gao, F.; Li, W. Autophagy is required for ectoplasmic specialization assembly in sertoli cells. Autophagy, 2016, 12(5), 814-832.
[http://dx.doi.org/10.1080/15548627.2016.1159377] [PMID: 26986811]
[278]
Ullah, H.; Ambreen, A.; Ahsan, N.; Jahan, S. Bisphenol S induces oxidative stress and DNA damage in rat spermatozoa in vitro and disrupts daily sperm production in vivo. J. Toxicol. Environmental. Chem, 2017, 99, 953-965.


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