DNA methylation in early mice embryogenesis under the influence of bisphenol A
- Authors: Noniashvili E.M.1, Grudinina N.A.1, Kustova M.E.1, Tran V.2,3, Suchkova I.O.1, Pavlinova L.I.1, Sasina L.K.1, Dergacheva N.I.1, Sofronov H.A.1, Patkin E.L.1
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Affiliations:
- Institute of Experimental Medicine RAS
- Voronezh State University
- Russia-Vietnam research and technological centre
- Issue: Vol 15, No 3 (2017)
- Pages: 42-53
- Section: Genetic toxicology
- URL: https://journals.rcsi.science/ecolgenet/article/view/6408
- DOI: https://doi.org/10.17816/ecogen15342-53
- ID: 6408
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Abstract
Background. Nonsteroid estrogen – bisphenol A (BPA) can have a detrimental effect on human health, and therefore poses a potential threat to humans. The critical window for the effect of BPA is the time of early development of the embryo, especially during the activation of the embryonic genome during development to the stage of blastocyst. Therefore, it is especially important to understand how DNA methylation is modified in embryos of the earliest developmental period under the influence of BPA.
Materials and methods. Mice hybrids F1 (CBAXC57BL) were once administered 0, 8 mg of BPA per mouse and the level of DNA methylation was estimated by detection the fluorescence of antibodies against 5-MeC in nuclei of GD3 and GD9 embryos. In other series, the level of DNA methylation and the rate of blastocyst development were estimated following cultivation of one- and two cells embryos in the presence of BPA (50 or 100 µM) during 72-96 hours in vitro.
Results. BPA exposure induced the decrease of the level of DNA methylation in GD3embryos received toxicant in utero, the amount of blastomeres in these embryos was decreased too. The level of DNA methylation in GD9 embryos was slightly higher than in control group. Upon cultivation of one-two cells embryos, BPA decreased the level of DNA methylation and the rate of embryos development to blastocyst stage.
Conclusion. We have determined that early embryogenesis is highly sensitive period to the BPA effects. Such effect is most likely due to active reprogramming processes in this period, primarily related to DNA demethylation/methylation de novo of both the whole genome and individual genes.
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##article.viewOnOriginalSite##About the authors
Ekaterina M. Noniashvili
Institute of Experimental Medicine RAS
Author for correspondence.
Email: katinka.04@list.ru
Cand. of Biol. Sci., senior researcher, Lab. Molecular Cytogenetics of Mammalian Development
Russian Federation, 12, Academic Pavlov street, Saint-Petersburg, 197376Natalia A. Grudinina
Institute of Experimental Medicine RAS
Email: strangecatnap@gmail.com
Cand. of Biol. Sci., senior researcher, Department of Molecular Genetics
Russian Federation, 12, Academic Pavlov street, Saint-Petersburg, 197376Marija E. Kustova
Institute of Experimental Medicine RAS
Email: kusmasha@yandex.ru
Cand. of Biol. Sci., senior researcher, Department of Molecular Genetics
Russian Federation, 12, Academic Pavlov street, Saint-Petersburg, 197376Van Truong Tran
Voronezh State University; Russia-Vietnam research and technological centre
Email: truongleky@gmail.com
PhD student, Department of Biochemistry and Cell Physiology, Voronezh State University, Voronezh, Russia; researcher, Russian-Vietnam research and technological centre
Russian Federation, 1, University square, Voronezh, 394063; HanoiIrina O. Suchkova
Institute of Experimental Medicine RAS
Email: irsuchkova@mail.ru
Cand. of Biol. Sci., head researcher, Lab. Molecular Cytogenetics of Mammalian Development
Russian Federation, 12, Academic Pavlov street, Saint-Petersburg, 197376Larisa I. Pavlinova
Institute of Experimental Medicine RAS
Email: lorhen45@gmail.com
Cand. of Biol. Sci., senior researcher, Lab. Molecular Cytogenetics of Mammalian Development
Russian Federation, 12, Academic Pavlov street, Saint-Petersburg, 197376Ludmila K. Sasina
Institute of Experimental Medicine RAS
Email: sassinal@gmail.com
Cand. of Biol. Sci., senior researcher, Lab. Molecular Cytogenetics of Mammalian Development
Russian Federation, 12, Academic Pavlov street, Saint-Petersburg, 197376Natalia I. Dergacheva
Institute of Experimental Medicine RAS
Email: natalia-9999@mail.ru
researcher, Lab. Molecular Cytogenetics of Mammalian Development
Russian Federation, 12, Academic Pavlov street, Saint-Petersburg, 197376Henrikh A. Sofronov
Institute of Experimental Medicine RAS
Email: gasofronov@mail.ru
academician of RAS, scientific director
Russian Federation, 12, Academic Pavlov street, Saint-Petersburg, 197376Eugene L. Patkin
Institute of Experimental Medicine RAS
Email: elp44@mail.ru
PhD, Professor. Head, Lab. Molecular Cytogenetics of Mammalian Development
Russian Federation, 12, Academic Pavlov street, Saint-Petersburg, 197376References
- Brotons JA, Olea-Serrano MF, Villalobos M, et al. Xenoestrogens released from lacquer coatings in food cans. Environ Health Perspect. 1995;103:608-612. PMID: 7556016. PMCID: PMC1519121.
- Mountfort KA, Kelly J, Jickells SM, Castle L. Investigations into the potential degradation of polycarbonate baby bottles during sterilization with consequent release of bisphenol A. Food Addit Contam. 1997;14:737-740. doi: 10.1080/02652039709374584.
- Serrano F, Rivas A, Novillo-Fertrell A, Pedraza V, et al. Estrogenicity of resin-based composites and sealants used in dentistry. Environ Health Perspect. 1996;104:298-305. PMID: 8919768.PMCID: PMC1469315.
- North EJ, Halden RU. Plastics and environmental health: the road ahead. Rev Environ Health. 2013;28:1-8. doi: 10.1515/reveh-2012-0030.
- Calafat AM, Kuklenyik Z, Reidy JA, et al. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ Health Perspect. 2005;113:391-395. PMID: 15811827. PMCID: PMC1278476.
- Vandenberg LN, Hauser R, Marcus M, et al. Human exposure to bisphenol A (BPA). Reprod Toxicol. 2007;24:139-177. doi: 10.1016/j.reprotox.2007.07.010.
- Ikezuki Y, Tsutsumi O, Takai Y, et al. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum Reprod. 2002;17(11):2839-2841. PMID: 12407035.
- Schonfelder G, Wittfoht W, Hopp H, et al. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect. 2002;110: A703-A707. PMID: 12417499. PMCID: PMC1241091.
- Golub MS, Wu KL, Kaufman FL, et al. Bisphenol A: developmental toxicity from early prenatal exposure. Birth Defects Res. (Part B). 2010;89:441-466. doi: 10.1002/bdrb.20275.
- 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;49C:145-54. doi: 10.1016/j.reprotox.2014.08.005.
- Peretz J, Vrooman L, Ricke WA, et al. Bisphenol a and reproductive health: update of experimental and human evidence, 2007-2013. Environ Health Perspect. 2014;122:775-786. doi: 10.1289/ehp.1307728.
- Caserta D, Di Segni N, Mallozzi M, et al. Bisphenol a and the female reproductive tract: an overview of recent laboratory evidence and epidemiological studies. Reprod Biol Endocrinol. 2014. doi: 10.1186/1477-7827-12-37.
- Takai Y, Tsutsumi O, Ikezuki Y, et al. Estrogen receptor-mediated effects of a xenoestrogen, bisphenol A, on preimplantation mouse embryos. Biochem Biophys Res Commun. 2000;270: 918-921. doi: 10.1006/bbrc.2000.2548.
- Takai Y, Tsutsumia O, Ikezukic Y, et al. Preimplantation exposure to bisphenol A advances postnatal development. Reprod Toxicol. 2001;15:71-74. PMID: 11137380.
- Lenie S, Cortvrindt R, Eichenlaub-Ritter U, Smitz J. Continuous exposure to bisphenol A during in vitro follicular development induces meiotic abnormalities. Mutat Res. 2008;65:71-81. doi: 10.1016/j.mrgentox.2007.10.017.
- Rodríguez HA, Santambrosio N, Santamaría CG, et al. Neonatal exposure to bisphenol A reduces the pool of primordial follicles in the rat ovary. Reprod Toxicol. 2010;30:550-557. doi: 10.1016/j.reprotox.2010.07.008.
- Rivera OE, Varayoud J, Rodríguez HA, et al. Neonatal exposure to bisphenol A or diethylstilbestrol alters the ovarian follicular dynamics in the lamb. Reprod Toxicol. 2011;32:304-312. doi: 10.1016/j.reprotox.2011.06.118.
- Abdel-Maksoud FM, Leasor KR, Butzen K, et al. Prenatal exposures of male rats to the environmental chemicals bisphenol A and di(2-Ethylhexyl) phthalate impact the sexual differentiation process. Endocrinology. 2015;156(12):4672-4683. doi: 10.1210/en.2015-1077.
- Rubin BS, Paranjpe M, DaFonte T, et al. Perinatal BPA exposure alters body weight and composition in a dose specific and sex specific manner: The addition of peripubertal exposure exacerbates adverse effects in female mice. Reprod Toxicol. 2017;68:130-144. doi: 10.1016/j.reprotox.2016.07.020.
- Manikkam M, Guerrero-Bosagna C, Tracey R, et al. Transgenerational actions of environmental compounds on reproductive disease and identification of epigenetic biomarkers of ancestral exposures. PLoS ONE. 2012;7: e31901. doi: 10.1371/journal.pone.0031901.
- Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner MK. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. PLoS One. 2013;8:e55387. doi: 10.1371/journal.pone.0055387.
- Melzer D, Gates P, Osborne NJ, et al. Urinary bisphenol a concentration and angiography-defined coronary artery stenosis. PLoS ONE. 2012;7: e43378. doi: 10.1371/journal.pone.0043378.
- Provvisiero DP, Pivonello C, Muscogiuri G, et al. Influence of Bisphenol A on Type 2 Diabetes Mellitus. Int J Environ Res Public Health. 2016;13(10): pii: E989. doi: 10.3390/ijerph13100989.
- Trasande L, Attina TM, Blustein J. Association between urinary bisphenol A concentration and obesity prevalence in children and adolescents. JAMA. 2012;308:1113-1121. doi: 10.1001/2012.jama.11461.
- Vafeiadi M, Roumeliotaki T, Myridakis A, et al. Association of early life exposure to bisphenol A with obesity and cardiometabolic traits in childhood. Environ Res. 2016;146:379-387. doi: 10.1016/j.envres.2016.01.017.
- Sugiura-Ogasawara M, Ozaki Y, Sonta S, et al. Exposure to bisphenol A is associated with recurrent miscarriage. Hum Reprod. 2005;20:2325-2329. doi: 10.1093/humrep/deh888.
- Spagnoletti A, Paulesu L, Mannelli C, et al. Low concentrations of Bisphenol A and para-Nonylphenol affect extravillous pathway of human trophoblast cells. Mol Cell Endocrinol. 2015;412:56-64. doi: 10.1016/j.mce.2015.05.023.
- Preciados M, Yoo C, Roy D. Estrogenic endocrine disrupting chemicals influencing NRF1 regulated gene networks in the development of complex human brain diseases. Int J Mol Sci. 2016;17(12): pii: E2086. doi: 10.3390/ijms17122086.
- Varshney M, Nalvarte I. Genes, gender, environment, and novel functions of estrogen receptor beta in the susceptibility to neurodevelopmental disorders. Brain Sci. 2017;7(3): pii: E24. doi: 10.3390/brainsci7030024.
- Kundakovic M, Gudsnuk K, Franks B, et al. Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure. Proc Natl Acad Sci USA. 2013;110:9956-9961. doi: 10.1073/pnas.1214056110.
- Паткин Е.Л., Сафронов Г.А. Эпигенетика популяций, экотоксикогенетика и болезни человека // Экологическая генетика. – 2012. – Т. 10. – Вып. 4. – С. 14–28. [Patkin EL, Sofronov GA. Epigenetics of populations, ecotoxicogenetics and human diseases. Ecologicheskaia genetica. 2012;10(4):14-28. (In Russ.)]
- Паткин Е.Л. Эпигенетические механизмы распространенных заболеваний человека. – СПб.: Нестор-История, 2008. – 200 с. [Patkin EL. Epigenetic mechanisms of human common diseases. Saint Petersburg: Nestor-History; 2008. 200 p. (In Russ.)]
- Millar D, Holliday R, Grigg G. Five not four: History and significance of the fifth base. In: Beck S, Olek A, editors. The Epigenome, molecular hide and seek. Wiley-VCH Verlag GmbH Co. KGaA; 2003. P. 3-20.
- Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science. 2001;293:1089-93. doi: 10.1126/science.1063443.
- Guerrero-Bosagna C, Savenkova M, Haque MM, et al. Environmentally induced epigenetic transgenerational inheritance of altered Sertoli cell transcriptome and epigenome: Molecular etiology of male infertility. PLoS ONE. 2013;8:e59922. doi: 10.1371/journal.pone.0059922.
- Hajkova P, Erhardt S, Lane N, et al. Epigenetic reprogramming in mouse primordial germ cells. Mech Dev. 2002;117(1-2):15-23. PMID: 12204247.
- Weaver IC, Champagne FA, Brown SE, et al. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J Neurosci. 2005;25:11045-54. doi: 10.1523/JNEUROSCI.3652-05.2005.
- Day KC, McCabe MT, Zhao X, et al. Rescue of embryonic epithelium reveals that the homozygous deletion of the retinoblastoma gene confers growth factor independence and immortality but does not influence epithelial differentiation or tissue morphogenesis. J Biol Chem.2002;277(46):44475-44484. doi: 10.1074/jbc.M205361200.
- Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science. 2001;(5532):1089-93. doi: 10.1126/science.1063443.
- Surani MA. Reprogramming of genome function through epigenetic inheritance. Nature. 2001;414(6859):122-8. doi: 10.1038/35102186.
- Wu Q, Ohsako S, Ishimura R, et al. Exposure of mouse preimplantation embryos to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) alters the methylation status of imprinted genes H19 and Igf2. Biol Reprod. 2004;70(6):1790-1797. doi: 10.1095/biolreprod.103.025387.
- Kundakovic M, Champagne FA. Epigenetic perspective on the developmental effects of bisphenol A. Brain Behav Immun. 2011;25:1084-1093. doi: 10.1016/j.bbi.2011.02.005.
- Santangeli S, Maradonna F, Olivotto I, et al. Effects of BPA on female reproductive function: The involvement of epigenetic mechanism. Gen Comp Endocrinol. 2017;245:122-126. doi: 10.1016/j.ygcen.2016.08.010.
- Грудинина Н.А., Сасина Л.К., Нониашвили Е.М., и др. Влияние условий предобработки препаратов на выявление 5-метилцитозина в метафазных хромосомах и интерфазных ядрах in situ // Цитология. – 2015. – Т. 57. – Вып. 8. – С. 592–601. [Grudinina NA, Sasina LK, Noniashvili EM, et al. The influence of sample preprocessing on in situ identification of 5-methylcytosine in metaphase chromosomes and interphase nuclei. Tsitologiya. 2015;57(8):592-601. (In Russ.)]. doi: 10.1134/S1990519X15060036.
- Pendina AA, Efimova OA, Fedorova ID, et al. DNA methylation patterns of metaphase chromosomes in human preimplantation embryos. Cytogenet Genome Res. 2011;132(1-2):1-7. doi: 10.1159/000318673.
- Santos F, Dean W. Using immunofluorescence to observe methylation changes in mammalian preimplantation embryos. Methods Mol Biol. 2006;325:129-37. doi: 10.1385/1-59745-005-7:129.
- Сучкова И.О., Баранова Т.В., Кустова М.Е., и др. Сателлитная ДНК индуцирует гетерохроматинизацию хромосомной ДНК реципиента в клетках транссателлитной мышиной эмбриональной тератокарциномы // Цитология. – 2004. – Т. 46. – Вып. 1. – С. 53–61. [Suchkova IO, Baranova TV, Kustova ME, et al. Bovine satellite DNA induces heterochromatinization of host chromosomal DNA in cells of trassatellite mouse embryonal carcinoma. Tsitologiia. 2004;46(1):53-61. PMID: 15112432. (In Russ.)]
- Sasina LK, Fedorova EM, Grudinina NA, et al. Modulation of reporter EGFP gene expression by a disease-associated human intra-intronic minisatellite upon transient and stable transfection. Int J Biol Engineering. 2013;3(1):1-10. doi: 10.5923/j.ijbe.20130301.01.
- Pan X, Wang X, Sun Y, et al. Inhibitory effects of preimplantation exposure to bisphenol-A on blastocyst development and implantation. Int J Clin Exp Med. 2015;15;8(6):8720-8729. PMID: 26309523. PMCID: PMC4538079.
- Xiao S, Diao H, Smith MA, et al. Preimplantation exposure to bisphenol A (BPA) affects embryo transport, preimplantation embryo development, and uterine receptivity in mice. Reprod Toxicol. 2011;32(4):434-441. doi: 10.1016/j.reprotox.2011.08.010.
- Berger RG, Foster WG, deCatanzaro D. Bisphenol-A exposure during the period of blastocyst implantation alters uterine morphology and perturbs measures of estrogen and progesterone receptor expression in mice. Reprod Toxicol. 2010;30:393-400. doi: 10.1016/j.reprotox.2010.06.006.
- Berger RG, Hancock T, deCatanzaro D. Influence of oral and subcutaneous bisphenol-A on intrauterine implantation of fertilized ova in inseminated female mice. Reprod Toxicol. 2007;23:138-44. doi: 10.1016/j.reprotox.2006.09.005.
- Berger RG, Shaw J, de Catanzaro D. Impact of acute bisphenol-A exposure upon intrauterine implantation of fertilized ova and urinary levels of progesterone and 17-estradiol. Reprod Toxicol. 2008;26:94-99. doi: 10.1016/j.reprotox.2008.06.007.
- Crawford BR, Decatanzaro D. Disruption of blastocyst implantation by triclosan in mice: impacts of repeated and acute doses and combination with bisphenol-A. Reprod Toxicol. 2012;34:607-613. doi: 10.1016/j.reprotox.2012.09.008.
- Zalko D, Soto AM, Dolo L, et al. Biotransformations of bisphenol A in a mammalian model: answers and new questions raised by low-dose metabolic fate studies in pregnant CD1 mice. Environ Health Perspect. 2003;111:309-319. PMID: 12611660. PMCID: PMC1241388.
- Jang YJ, Park HR, Kim TH, et al. High dose bisphenol A impairs hippocampal neurogenesis in female mice across generations. Toxicology. 2012;296(1-3):73-82. doi: 10.1016/j.tox.2012.03.007.
- Soto AM, Sonnenschein C. Environmental causes of cancer: endocrine disruptors as carcinogens. Nat Rev Endocrinol. 2010;6:363-70. doi: 10.1038/nrendo.2010.87.
- Caserta D, Di Segni N, Mallozzi M, et al. Bisphenol a and the female reproductive tract: an overview of recent laboratory evidence and epidemiological studies. Reprod Biol Endocrinol. 2014;12:37. doi: 10.1186/1477-7827-12-37.
- Hochberg Z, Feil R, Constancia M, et al. Child health, developmental plasticity, and epigenetic programming. Endocrinol Rev. 2011;32(2):159-224. doi: 10.1210/er.2009-0039.
- Mao Z, Xia W, Huo W, et al. Pancreatic impairment and Igf2 hypermethylation induced by developmental exposure to bisphenol A can be counteracted by maternal folate supplementation. J Appl Toxicol. 2017Feb6. doi: 10.1002/jat.3430.
- Anderson OS, Nahar MS, Faulk C, et al. Epigenetic responses following maternal dietary exposure to physiologically relevant levels of bisphenol A. Environ Mol Mutagen. 2012;53:334-342. doi: 10.1002/em.21692.
- Dolinoy DC, Huang D, Jirtle RL. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Natl Acad Sci USA. 2007;104(32):13056-61. doi: 10.1073/pnas.0703739104.
- Bromer JG1, Zhou Y, Taylor MB, et al. Bisphenol-A exposure in utero leads to epigenetic alterations in the developmental programming of uterine estrogen response. FASEB J. 2010;24(7):2273-2280. doi: 10.1096/fj.09-140533.
- Lee MS, Lee YS, Lee HH and Song HY. Human endometrial cell coculture reduces the endocrine disruptor toxicity on mouse embryo development. J Occup Med Toxicol. 2012;7(1):7. doi: 10.1186/1745-6673-7-7.
- Tang WY, Morey LM, Cheung YY, et al. Neonatal exposure to estradiol/bisphenol A alters promoter methylation and expression of Nsbp1 and Hpcal1 genes and transcriptional programs of Dnmt3a/b and Mbd2/4 in the rat prostate gland throughout life. Endocrinology. 2012;153:42-55. doi: 10.1210/en.2011-1308.
- Jorgensen EM, Alderman MH, Taylor HS. Preferential epigenetic programming of estrogen response after in utero xenoestrogen (bisphenol-A) exposure. FASEB J. 2016;30(9):3194-3201. doi: 10.1096/fj.201500089R.
- Rajakumar C, Guan H, Langlois D, et al. Bisphenol A disrupts gene expression in human placental trophoblast cells. Reprod Toxicol. 2015;53:39-44. doi: 10.1016/j.reprotox.2015.03.001.
- Varayoud J, Ramos JG, Bosquiazzo VL, et al. Neonatal exposure to bisphenol A alters rat uterine implantation-associated gene expression and reduces the number of implantation sites. Endocrinology. 2011;152(3):1101-11. doi: 10.1210/en.2009-1037.
- Susiarjo M, Sasson I, Mesaros C, et al. Bisphenol A exposure disrupts genomic imprinting in the mouse. PLoS Genet. 2013;9(4):e1003401. doi: 10.1371/journal.pgen.1003401.
- Mahfoudhi E, Talhaoui I, Cabagnols X, et al. TET2-mediated 5-hydroxymethylcytosine induces genetic instabilityand mutagenesis. DNA Repair. 2016;43:78-88. doi: 10.1016/j.dnarep.2016.05.031.
- Dion V, Lin Y, Price BA, et al., Genome-wide demethylation promotes triplet repeat instability independently of homologous recombination. DNA Repair (Amst). 2008;7(2):313-320. doi: 10.1016/j.dnarep.2007.11.002.
- Schuermann D, Weber AR, Schär P. Active DNA demethylation by DNA repair: Facts and uncertainties. DNA Repair (Amst). 2016;44:92-102. doi: 10.1016/j.dnarep.2016.05.013.
- Manfo FP, Jubendradass R, Nantia EA, et al. Adverse effects of bisphenol A on male reproductive function. Rev Environ Contam Toxicol. 2014;228:57-82. doi: 10.1007/978-3-319-01619-1_3.