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Endocrine, Metabolic & Immune Disorders - Drug Targets

Endocrine, Metabolic & Immune Disorders - Drug Targets

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ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

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Mini-Review Article

Comprehending the Role of Endocrine Disruptors in Inducing Epigenetic Toxicity

Author(s): Arikath Kirtana and Barathi Seetharaman*

Volume 22, Issue 11, 2022

Published on: 06 July, 2022

Page: [1059 - 1072] Pages: 14

DOI: 10.2174/1871530322666220411082656

Price: $65

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Abstract

Endocrine disruptors are natural or man-made chemicals that interfere with the body’s endocrine system leading to hormone synthesis and production defects. These chemicals are categorized as plasticizers and cosmetic chemicals, heavy metals, phytoestrogens, pesticides, detergents, surfactants, and flame retardants. Some of the most common endocrine disruptors are dioxins, bisphenol A, phthalates, perchlorate, perfluoroalkyl, and poly-fluoroalkyl substances (PFAs), phytoestrogens, polybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCB), triclosan, atrazine, lead, arsenic, mercury, organophosphate pesticides, and glycol ethers. Epigenetic alterations such as DNA methylation, histone modification, and miRNA regulation have been observed to play a major role in many diseases such as cancer, neurodegenerative diseases, PCOS, cardiovascular diseases, and various other disorders. In recent times, there has been a focus on endocrine-disrupting chemicals in epigenetic alterations. This review concentrates on estrogen and androgen disrupting effects, placental, and fetal effects, thyroid disrupting effects, and transgenerational effects of endocrine disruptors.

Keywords: Endocrine disruptors, epigenetics, DNA methylation, histone modification, mRNA disruption, placental toxicity, fetal toxicity, estrogen and androgen toxicity, thyroid disruption, transgenerational toxicity.

Graphical Abstract

Graphical abstract illustrating key findings of the study

[1]
Kabir, E.R.; Rahman, M.S.; Rahman, I. A review on endocrine disruptors and their possible impacts on human health. Environ. Toxicol. Pharmacol., 2015, 40(1), 241-258.
[http://dx.doi.org/10.1016/j.etap.2015.06.009] [PMID: 26164742]
[2]
Monneret, C. What is an endocrine disruptor? C. R. Biol., 2017, 340(9-10), 403-405.
[http://dx.doi.org/10.1016/j.crvi.2017.07.004] [PMID: 29126512]
[3]
Singh, S.; Li, S.S. Epigenetic effects of environmental chemicals bisphenol A and phthalates. Int. J. Mol. Sci., 2012, 13(8), 10143-10153.
[http://dx.doi.org/10.3390/ijms130810143] [PMID: 22949852]
[4]
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]
[5]
Fenichel, P.; Chevalier, N.; Brucker-Davis, F.; Bisphenol, A. An endocrine and metabolic disruptor. Ann. Endocrinol. (Paris), 2013, 74(3), 211-220.
[http://dx.doi.org/10.1016/j.ando.2013.04.002] [PMID: 23796010]
[6]
Schecter, A.; Birnbaum, L.; Ryan, J.J.; Constable, J.D. Dioxins: An overview. Environ. Res., 2006, 101(3), 419-428.
[http://dx.doi.org/10.1016/j.envres.2005.12.003] [PMID: 16445906]
[7]
Marinković, N.; Pašalić, D.; Ferenčak, G.; Gršković, B.; Stavljenić Rukavina, A. Dioxins and human toxicity. Arh. Hig. Rada Toksikol., 2010, 61(4), 445-453.
[http://dx.doi.org/10.2478/10004-1254-61-2010-2024] [PMID: 21183436]
[8]
Domingo, J.L.; Nadal, M. Human exposure to per- and polyfluoroalkyl substances (PFAS) through drinking water: A review of the recent scientific literature. Environ. Res., 2019, 177, 108648.
[http://dx.doi.org/10.1016/j.envres.2019.108648] [PMID: 31421451]
[9]
Kumarathilaka, P.; Oze, C.; Indraratne, S.P.; Vithanage, M. Perchlorate as an emerging contaminant in soil, water and food. Chemosphere, 2016, 150, 667-677.
[http://dx.doi.org/10.1016/j.chemosphere.2016.01.109] [PMID: 26868023]
[10]
Maffini, M.V.; Trasande, L.; Neltner, T.G. Perchlorate and diet: Human exposures, risks, and mitigation strategies. Curr. Environ. Health Rep., 2016, 3(2), 107-117.
[http://dx.doi.org/10.1007/s40572-016-0090-3] [PMID: 27029550]
[11]
Seltenrich, N. Glycol ethers and neurodevelopment: Investigating the impact of prenatal exposures. Environ. Health Perspect., 2017, 125(6), 064001.
[http://dx.doi.org/10.1289/EHP2094] [PMID: 28650840]
[12]
Ajao, C.; Andersson, M.A.; Teplova, V.V.; Nagy, S.; Gahmberg, C.G.; Andersson, L.C.; Hautaniemi, M.; Kakasi, B.; Roivainen, M.; Salkinoja-Salonen, M. Mitochondrial toxicity of triclosan on mammalian cells. Toxicol. Rep., 2015, 2, 624-637.
[http://dx.doi.org/10.1016/j.toxrep.2015.03.012] [PMID: 28962398]
[13]
Casati, L.; Sendra, R.; Poletti, A.; Negri-Cesi, P.; Celotti, F. Androgen receptor activation by polychlorinated biphenyls: Epigenetic effects mediated by the histone demethylase Jarid1b. Epigenetics, 2013, 8(10), 1061-1068.
[http://dx.doi.org/10.4161/epi.25811] [PMID: 23907094]
[14]
Maddela, N.R.; Venkateswarlu, K.; Kakarla, D.; Megharaj, M. Inevitable human exposure to emissions of polybrominated diphenyl ethers: A perspective on potential health risks. Environ. Pollut., 2020, 266(Pt 1), 115240.
[http://dx.doi.org/10.1016/j.envpol.2020.115240] [PMID: 32698055]
[15]
Siddiqi, M.A.; Laessig, R.H.; Reed, K.D. Polybrominated diphenyl ethers (PBDEs): New pollutants-old diseases. Clin. Med. Res., 2003, 1(4), 281-290.
[http://dx.doi.org/10.3121/cmr.1.4.281] [PMID: 15931321]
[16]
Zani, C.; Ceretti, E.; Covolo, L.; Donato, F. Do polychlorinated biphenyls cause cancer? A systematic review and meta-analysis of epidemiological studies on risk of cutaneous melanoma and non-Hodgkin lymphoma. Chemosphere, 2017, 183, 97-106.
[http://dx.doi.org/10.1016/j.chemosphere.2017.05.053] [PMID: 28535466]
[17]
Zani, C.; Toninelli, G.; Filisetti, B.; Donato, F. Polychlorinated biphenyls and cancer: An epidemiological assessment. J. Environ. Sci. Health Part C Environ. Carcinog. Ecotoxicol. Rev., 2013, 31(2), 99-144.
[http://dx.doi.org/10.1080/10590501.2013.782174] [PMID: 23672403]
[18]
Suratman, S.; Edwards, J.W.; Babina, K. Organophosphate pesticides exposure among farmworkers: Pathways and risk of adverse health effects. Rev. Environ. Health, 2015, 30(1), 65-79.
[http://dx.doi.org/10.1515/reveh-2014-0072] [PMID: 25741936]
[19]
Wirbisky-Hershberger, S.E.; Sanchez, O.F.; Horzmann, K.A.; Thanki, D.; Yuan, C.; Freeman, J.L. Atrazine exposure decreases the activity of DNMTs, global DNA methylation levels, and dnmt expression. Food Chem. Toxicol., 2017, 109(Pt 1), 727-734.
[http://dx.doi.org/10.1016/j.fct.2017.08.041] [PMID: 28859886]
[20]
Desmawati, D.; Sulastri, D. Phytoestrogens and their health effect. Open Access Maced. J. Med. Sci., 2019, 7(3), 495-499.
[http://dx.doi.org/10.3889/oamjms.2019.086] [PMID: 30834024]
[21]
Kamensky, O.L.; Horton, D.; Kingsley, D.P.; Bridges, C.C. A case of accidental mercury intoxication. J. Emerg. Med., 2019, 56(3), 275-278.
[http://dx.doi.org/10.1016/j.jemermed.2018.12.039] [PMID: 30718027]
[22]
Rice, K.M.; Walker, E.M., Jr; Wu, M.; Gillette, C.; Blough, E.R. Environmental mercury and its toxic effects. J. Prev. Med. Public Health, 2014, 47(2), 74-83.
[http://dx.doi.org/10.3961/jpmph.2014.47.2.74] [PMID: 24744824]
[23]
Tan, S.W.; Meiller, J.C.; Mahaffey, K.R. The endocrine effects of mercury in humans and wildlife. Crit. Rev. Toxicol., 2009, 39(3), 228-269.
[http://dx.doi.org/10.1080/10408440802233259] [PMID: 19280433]
[24]
Hall, A.H. Chronic arsenic poisoning. Toxicol. Lett., 2002, 128(1-3), 69-72.
[http://dx.doi.org/10.1016/S0378-4274(01)00534-3] [PMID: 11869818]
[25]
Li, L.; Bi, Z.; Wadgaonkar, P.; Lu, Y.; Zhang, Q.; Fu, Y.; Thakur, C.; Wang, L.; Chen, F. Metabolic and epigenetic reprogramming in the arsenic-induced cancer stem cells. Semin. Cancer Biol., 2019, 57, 10-18.
[http://dx.doi.org/10.1016/j.semcancer.2019.04.003] [PMID: 31009762]
[26]
Park, S.S.; Skaar, D.A.; Jirtle, R.L.; Hoyo, C. Epigenetics, obesity and early-life cadmium or lead exposure. Epigenomics, 2017, 9(1), 57-75.
[http://dx.doi.org/10.2217/epi-2016-0047] [PMID: 27981852]
[27]
Klotz, K.; Göen, T. Human biomonitoring of lead exposure. Met. Ions Life Sci., 2017, 17, 17.
[PMID: 28731299]
[28]
Zama, A.M.; Uzumcu, M. Epigenetic effects of endocrine-disrupting chemicals on female reproduction: An ovarian perspective. Front. Neuroendocrinol., 2010, 31(4), 420-439.
[http://dx.doi.org/10.1016/j.yfrne.2010.06.003] [PMID: 20609371]
[29]
Rosenfeld, C.S.; Cooke, P.S. Endocrine disruption through membrane es-trogen receptors and novel pathways leading to rapid toxicological and epigenetic effects. J. Steroid Biochem. Mol. Biol., 2019, 187, 106-117.
[30]
Welshons, W.V.; Thayer, K.A.; Judy, B.M.; Taylor, J.A.; Curran, E.M.; vom Saal, F.S. Large effects from small exposures. I. Mechanisms for endocrine-disrupting chemicals with estrogenic activity. Environ. Health Perspect., 2003, 111(8), 994-1006.
[http://dx.doi.org/10.1289/ehp.5494] [PMID: 12826473]
[31]
Anway, M.D.; Cupp, A.S.; Uzumcu, M.; Skinner, M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science, 2005, 308(5727), 1466-1469.
[http://dx.doi.org/10.1126/science.1108190] [PMID: 15933200]
[32]
Calaf, G.M.; Ponce-Cusi, R.; Aguayo, F.; Muñoz, J.P.; Bleak, T.C. Endocrine disruptors from the environment affecting breast cancer. Oncol. Lett., 2020, 20(1), 19-32.
[http://dx.doi.org/10.3892/ol.2020.11566] [PMID: 32565930]
[33]
Dhimolea, E.; Wadia, P.R.; Murray, T.J.; Settles, M.L.; Treitman, J.D.; Sonnenschein, C.; Shioda, T.; Soto, A.M. Prenatal exposure to BPA alters the epigenome of the rat mammary gland and increases the propensity to neoplastic development. PLoS One, 2014, 9(7), e99800.
[http://dx.doi.org/10.1371/journal.pone.0099800] [PMID: 24988533]
[34]
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]
[35]
Weng, Y.I.; Hsu, P.Y.; Liyanarachchi, S.; Liu, J.; Deatherage, D.E.; Huang, Y.W.; Zuo, T.; Rodriguez, B.; Lin, C.H.; Cheng, A.L.; Huang, T.H. Epigenetic influences of low-dose bisphenol A in primary human breast epithelial cells. Toxicol. Appl. Pharmacol., 2010, 248(2), 111-121.
[http://dx.doi.org/10.1016/j.taap.2010.07.014] [PMID: 20678512]
[36]
Eldridge, J.C.; Stevens, J.T.; Breckenridge, C.B. Atrazine interaction with estrogen expression systems. Rev. Environ. Contam. Toxicol., 2008, 196, 147-160.
[PMID: 19025096]
[37]
McBirney, M.; King, S.E.; Pappalardo, M.; Houser, E.; Unkefer, M.; Nilsson, E.; Sadler-Riggleman, I.; Beck, D.; Winchester, P.; Skinner, M.K. Atrazine induced epigenetic transgenerational inheritance of disease, lean phenotype and sperm epimutation pathology biomarkers. PLoS One, 2017, 12(9), e0184306.
[http://dx.doi.org/10.1371/journal.pone.0184306] [PMID: 28931070]
[38]
Ohtake, F.; Takeyama, K.; Matsumoto, T.; Kitagawa, H.; Yamamoto, Y.; Nohara, K.; Tohyama, C.; Krust, A.; Mimura, J.; Chambon, P.; Yanagisawa, J.; Fujii-Kuriyama, Y.; Kato, S. Modulation of oestrogen receptor signalling by association with the activated dioxin receptor. Nature, 2003, 423(6939), 545-550.
[http://dx.doi.org/10.1038/nature01606] [PMID: 12774124]
[39]
Matthews, J.; Gustafsson, J.A. Estrogen receptor and aryl hydrocarbon receptor signaling pathways. Nucl. Recept. Signal., 2006, 4(1), e016.
[http://dx.doi.org/10.1621/nrs.04016] [PMID: 16862222]
[40]
Giampaolino, P.; Della Corte, L.; Foreste, V.; Barra, F.; Ferrero, S.; Bifulco, G. Dioxin and endometriosis: A new possible relation based on epigenetic theory. Gynecol. Endocrinol., 2020, 36(4), 279-284.
[http://dx.doi.org/10.1080/09513590.2019.1698024] [PMID: 31805795]
[41]
Khan, Z.; Zheng, Y.; Jones, T.L.; Delaney, A.A.; Correa, L.F.; Shenoy, C.C.; Khazaie, K.; Daftary, G.S. Epigenetic therapy: Novel translational implications for arrest of environmental dioxin-induced disease in females. Endocrinology, 2018, 159(1), 477-489.
[http://dx.doi.org/10.1210/en.2017-00860] [PMID: 29165700]
[42]
Tirado, O.M.; Martinez, E.D.; Rodriguez, O.C.; Danielsen, M.; Selva, D.M.; Reventós, J.; Munell, F.; Suárez-Quian, C.A. Methoxyacetic acid disregulation of androgen receptor and androgen-binding protein expression in adult rat testis. Biol. Reprod., 2003, 68(4), 1437-1446.
[http://dx.doi.org/10.1095/biolreprod.102.004937] [PMID: 12606434]
[43]
Maradonna, F.; Carnevali, O. Lipid metabolism alteration by endocrine disruptors in animal models: An overview. Front. Endocrinol. (Lausanne), 2018, 9, 654.
[http://dx.doi.org/10.3389/fendo.2018.00654] [PMID: 30467492]
[44]
Mustieles, V.; D’Cruz, S.C.; Couderq, S.; Rodríguez-Carrillo, A.; Fini, J.B.; Hofer, T.; Steffensen, I.L.; Dirven, H.; Barouki, R.; Olea, N.; Fernández, M.F.; David, A. Bisphenol A and its analogues: A comprehensive review to identify and prioritize effect biomarkers for human biomonitoring. Environ. Int., 2020, 144, 105811.
[http://dx.doi.org/10.1016/j.envint.2020.105811] [PMID: 32866736]
[45]
Kishi, R.; Araki, A.; Minatoya, M.; Hanaoka, T.; Miyashita, C.; Itoh, S.; Kobayashi, S.; Ait Bamai, Y.; Yamazaki, K.; Miura, R.; Tamura, N.; Ito, K.; Goudarzi, H. members of The Hokkaido Study on Environment and Children’s Health. The Hokkaido Birth cohort study on environment and children’s health: Cohort profile-updated 2017. Environ. Health Prev. Med., 2017, 22(1), 46.
[http://dx.doi.org/10.1186/s12199-017-0654-3] [PMID: 29165157]
[46]
Kim, S.; Stroski, K.M.; Killeen, G.; Smitherman, C.; Simcik, M.F.; Brooks, B.W. 8:8 Perfluoroalkyl phosphinic acid affects neurobehavioral development, thyroid disruption, and DNA methylation in developing zebrafish. Sci. Total Environ., 2020, 736, 139600.
[http://dx.doi.org/10.1016/j.scitotenv.2020.139600] [PMID: 32474277]
[47]
Kim, S.; Cho, Y.H.; Won, S.; Ku, J.L.; Moon, H.B.; Park, J.; Choi, G.; Kim, S.; Choi, K. Maternal exposures to persistent organic pollutants are associated with DNA methylation of thyroid hormone-related genes in placenta differently by infant sex. Environ. Int., 2019, 130, 104956.
[http://dx.doi.org/10.1016/j.envint.2019.104956] [PMID: 31272017]
[48]
Pitto, L.; Gorini, F.; Bianchi, F.; Guzzolino, E. New insights into mechanisms of endocrine-disrupting chemicals in thyroid diseases: The epigenetic way. Int. J. Environ. Res. Public Health, 2020, 17(21), 7787.
[http://dx.doi.org/10.3390/ijerph17217787] [PMID: 33114343]
[49]
Faulk, C.; Kim, J.H.; Jones, T.R.; McEachin, R.C.; Nahar, M.S.; Dolinoy, D.C.; Sartor, M.A. Bisphenol A-associated alterations in genome-wide DNA methylation and gene expression patterns reveal sequence-dependent and non-monotonic effects in human fetal liver. Environ. Epigenet., 2015, 1(1), dvv006.
[http://dx.doi.org/10.1093/eep/dvv006] [PMID: 27358748]
[50]
Faulk, C.; Kim, J.H.; Anderson, O.S.; Nahar, M.S.; Jones, T.R.; Sartor, M.A.; Dolinoy, D.C. Detection of differential DNA methylation in repetitive DNA of mice and humans perinatally exposed to bisphenol A. Epigenetics, 2016, 11(7), 489-500.
[http://dx.doi.org/10.1080/15592294.2016.1183856] [PMID: 27267941]
[51]
Bromer, J.G.; Zhou, Y.; Taylor, M.B.; Doherty, L.; Taylor, H.S. Bisphenol-A exposure in utero leads to epigenetic alterations in the developmental programming of uterine estrogen response. FASEB J., 2010, 24(7), 2273-2280.
[http://dx.doi.org/10.1096/fj.09-140533] [PMID: 20181937]
[52]
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]
[53]
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]
[54]
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]
[55]
Ye, Y.; Tang, Y.; Xiong, Y.; Feng, L.; Li, X. Bisphenol A exposure alters placentation and causes preeclampsia-like features in pregnant mice involved in reprogramming of DNA methylation of WNT2. FASEB J., 2019, 33(2), 2732-2742.
[http://dx.doi.org/10.1096/fj.201800934RRR] [PMID: 30303745]
[56]
Poston, R.G.; Saha, R.N. Epigenetic effects of polybrominated diphenyl ethers on human health. Int. J. Environ. Res. Public Health, 2019, 16(15), 2703.
[http://dx.doi.org/10.3390/ijerph16152703] [PMID: 31362383]
[57]
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]
[58]
Ho, S.M.; Cheong, A.; Lam, H.M.; Hu, W.Y.; Shi, G.B.; Zhu, X.; Chen, J.; Zhang, X.; Medvedovic, M.; Leung, Y.K.; Prins, G.S. Exposure of human prostaspheres to bisphenol A epigenetically regulates snord family noncoding RNAs via histone modification. Endocrinology, 2015, 156(11), 3984-3995.
[http://dx.doi.org/10.1210/en.2015-1067] [PMID: 26248216]
[59]
Dutta, S.; Haggerty, D.K.; Rappolee, D.A.; Ruden, D.M. Phthalate exposure and long-term epigenomic consequences: A review. Front. Genet., 2020, 11, 405.
[http://dx.doi.org/10.3389/fgene.2020.00405] [PMID: 32435260]
[60]
Grindler, N.M.; Vanderlinden, L.; Karthikraj, R.; Kannan, K.; Teal, S.; Polotsky, A.J.; Powell, T.L.; Yang, I.V.; Jansson, T. Exposure to phthalate, an endocrine disrupting chemical, alters the first trimester placental methylome and transcriptome in women. Sci. Rep., 2018, 8(1), 6086.
[http://dx.doi.org/10.1038/s41598-018-24505-w] [PMID: 29666409]
[61]
Wocławek-Potocka, I.; Mannelli, C.; Boruszewska, D.; Kowalczyk-Zieba, I.; Waśniewski, T.; Skarżyński, D.J. Diverse effects of phytoestrogens on the reproductive performance: Cow as a model. Int. J. Endocrinol., 2013, 2013, 650984.
[http://dx.doi.org/10.1155/2013/650984] [PMID: 23710176]
[62]
Jefferson, W.N.; Patisaul, H.B.; Williams, C.J. Reproductive consequences of developmental phytoestrogen exposure. Reproduction, 2012, 143(3), 247-260.
[http://dx.doi.org/10.1530/REP-11-0369] [PMID: 22223686]
[63]
Plunk, E.C.; Richards, S.M. Epigenetic modifications due to environment, ageing, nutrition, and endocrine disrupting chemicals and their effects on the endocrine system. Int. J. Endocrinol., 2020, 2020, 9251980.
[http://dx.doi.org/10.1155/2020/9251980] [PMID: 32774366]
[64]
Reichard, J.F.; Puga, A. Effects of arsenic exposure on DNA methylation and epigenetic gene regulation. Epigenomics, 2010, 2(1), 87-104.
[http://dx.doi.org/10.2217/epi.09.45] [PMID: 20514360]
[65]
Bommarito, P.A.; Martin, E.; Fry, R.C. Effects of prenatal exposure to endocrine disruptors and toxic metals on the fetal epigenome. Epigenomics, 2017, 9(3), 333-350.
[http://dx.doi.org/10.2217/epi-2016-0112] [PMID: 28234024]
[66]
Rager, J.E.; Bailey, K.A.; Smeester, L.; Miller, S.K.; Parker, J.S.; Laine, J.E.; Drobná, Z.; Currier, J.; Douillet, C.; Olshan, A.F.; Rubio-Andrade, M.; Stýblo, M.; García-Vargas, G.; Fry, R.C. Prenatal arsenic exposure and the epigenome: Altered microRNAs associated with innate and adaptive immune signaling in newborn cord blood. Environ. Mol. Mutagen., 2014, 55(3), 196-208.
[http://dx.doi.org/10.1002/em.21842] [PMID: 24327377]
[67]
Maccani, J.Z.; Koestler, D.C.; Lester, B.; Houseman, E.A.; Armstrong, D.A.; Kelsey, K.T.; Marsit, C.J. Placental DNA methylation related to both infant toenail mercury and adverse neurobehavioral outcomes. Environ. Health Perspect., 2015, 123(7), 723-729.
[http://dx.doi.org/10.1289/ehp.1408561] [PMID: 25748564]
[68]
Anzalone, D.A.; Sampino, S.; Czernik, M.; Iuso, D.; Ptak, G.E. Polychlorinated biphenyls (PCBs) alter DNA methylation and genomic integrity of sheep fetal cells in a simplified in vitro model of pregnancy exposure. Toxicol. In Vitro, 2018, 46, 39-46.
[http://dx.doi.org/10.1016/j.tiv.2017.09.017] [PMID: 28964899]
[69]
Li, Q.; Kappil, M.A.; Li, A.; Dassanayake, P.S.; Darrah, T.H.; Friedman, A.E.; Friedman, M.; Lambertini, L.; Landrigan, P.; Stodgell, C.J.; Xia, Y.; Nanes, J.A.; Aagaard, K.M.; Schadt, E.E.; Murray, J.C.; Clark, E.B.; Dole, N.; Culhane, J.; Swanson, J.; Varner, M.; Moye, J.; Kasten, C.; Miller, R.K.; Chen, J. Exploring the associations between microRNA expression profiles and environmental pollutants in human placenta from the National Children’s Study (NCS). Epigenetics, 2015, 10(9), 793-802.
[http://dx.doi.org/10.1080/15592294.2015.1066960] [PMID: 26252056]
[70]
Patrizi, B.; Siciliani de Cumis, M. TCDD toxicity mediated by epigenetic mechanisms. Int. J. Mol. Sci., 2018, 19(12), 4101.
[http://dx.doi.org/10.3390/ijms19124101] [PMID: 30567322]
[71]
Pivonello, C.; Muscogiuri, G.; Nardone, A.; Garifalos, F.; Provvisiero, D.P.; Verde, N.; de Angelis, C.; Conforti, A.; Piscopo, M.; Auriemma, R.S.; Colao, A.; Pivonello, R.; Bisphenol, A. An emerging threat to female fertility. Reprod. Biol. Endocrinol., 2020, 18(1), 22.
[http://dx.doi.org/10.1186/s12958-019-0558-8] [PMID: 32171313]
[72]
Berger, A.; Ziv-Gal, A.; Cudiamat, J.; Wang, W.; Zhou, C.; Flaws, J.A. The effects of in utero bisphenol A exposure on the ovaries in multiple generations of mice. Reprod. Toxicol., 2016, 60, 39-52.
[http://dx.doi.org/10.1016/j.reprotox.2015.12.004] [PMID: 26746108]
[73]
Brehm, E.; Flaws, J.A. Transgenerational effects of endocrine-disrupting chemicals on male and female reproduction. Endocrinology, 2019, 160(6), 1421-1435.
[http://dx.doi.org/10.1210/en.2019-00034] [PMID: 30998239]
[74]
Baker, T.R.; Peterson, R.E.; Heideman, W. Using zebrafish as a model system for studying the transgenerational effects of dioxin. Toxicol. Sci., 2014, 138(2), 403-411.
[http://dx.doi.org/10.1093/toxsci/kfu006] [PMID: 24470537]
[75]
Zhou, C.; Gao, L.; Flaws, J.A. Exposure to an environmentally relevant phthalate mixture causes transgenerational effects on female reproduction in mice. Endocrinology, 2017, 158(6), 1739-1754.
[http://dx.doi.org/10.1210/en.2017-00100] [PMID: 28368545]
[76]
Leroux, S.; Gourichon, D.; Leterrier, C.; Labrune, Y.; Coustham, V.; Rivière, S.; Zerjal, T.; Coville, J.L.; Morisson, M.; Minvielle, F.; Pitel, F. Embryonic environment and transgenerational effects in quail. Genet. Sel. Evol., 2017, 49(1), 14.
[http://dx.doi.org/10.1186/s12711-017-0292-7] [PMID: 28125975]
[77]
Zhong, J.; Chen, L.; Zhang, L. High-throughput determination of high-quality interdiffusion coefficients in metallic solids: A review. J. Mater. Sci., 2020, 55(24), 1-36.
[http://dx.doi.org/10.1007/s10853-020-04805-1] [PMID: 32836381]
[78]
Alfonso, S.; Blanc, M.; Joassard, L.; Keiter, S.H.; Munschy, C.; Loizeau, V.; Bégout, M.L.; Cousin, X. Examining multi- and transgenerational behavioral and molecular alterations resulting from parental exposure to an environmental PCB and PBDE mixture. Aquat. Toxicol., 2019, 208, 29-38.
[http://dx.doi.org/10.1016/j.aquatox.2018.12.021] [PMID: 30605867]
[79]
Stenzel, A.; Wirt, H.; Patten, A.; Theodore, B.; King-Heiden, T. Larval exposure to environmentally relevant concentrations of triclosan impairs metamorphosis and reproductive fitness in zebrafish. Reprod. Toxicol., 2019, 87, 79-86.
[http://dx.doi.org/10.1016/j.reprotox.2019.05.055] [PMID: 31102721]
[80]
Köktürk, M.; Alak, G.; Atamanalp, M. The effects of n-butanol on oxidative stress and apoptosis in zebra fish (Danio rerio) larvae. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 2020, 227, 108636.
[http://dx.doi.org/10.1016/j.cbpc.2019.108636] [PMID: 31669665]
[81]
Meyer, D.N.; Crofts, E.J.; Akemann, C.; Gurdziel, K.; Farr, R.; Baker, B.B.; Weber, D.; Baker, T.R. Developmental exposure to Pb2+ induces transgenerational changes to zebrafish brain transcriptome. Chemosphere, 2020, 244, 125527.
[http://dx.doi.org/10.1016/j.chemosphere.2019.125527] [PMID: 31816550]
[82]
Zhang, X.; Zhong, H.Q.; Chu, Z.W.; Zuo, X.; Wang, L.; Ren, X.L.; Ma, H.; Du, R.Y.; Ju, J.J.; Ye, X.L.; Huang, C.P.; Zhu, J.H.; Wu, H.M. Arsenic induces transgenerational behavior disorders in Caenorhabditis elegans and its underlying mechanisms. Chemosphere, 2020, 252, 126510.
[http://dx.doi.org/10.1016/j.chemosphere.2020.126510] [PMID: 32203783]
[83]
Carvan, M.J., III; Kalluvila, T.A.; Klingler, R.H.; Larson, J.K.; Pickens, M.; Mora-Zamorano, F.X.; Connaughton, V.P.; Sadler-Riggleman, I.; Beck, D.; Skinner, M.K. Mercury-induced epigenetic transgenerational inheritance of abnormal neurobehavior is correlated with sperm epimutations in zebrafish. PLoS One, 2017, 12(5), e0176155.
[http://dx.doi.org/10.1371/journal.pone.0176155] [PMID: 28464002]
[84]
Schmitt, C.; Peterson, E.; Willis, A.; Kumar, N.; McManus, M.; Subbiah, S.; Crago, J. Transgenerational effects of developmental exposure to chlorpyrifos-oxon in zebrafish (Danio rerio). Toxicol. Appl. Pharmacol., 2020, 408, 115275.
[http://dx.doi.org/10.1016/j.taap.2020.115275] [PMID: 33049267]
[85]
Patel, N.J.; Hogan, K.J.; Rizk, E.; Stewart, K.; Madrid, A.; Meethal, S.V.; Alisch, R.; Borth, L.; Papale, L.A.; Ondoma, S.; Gorges, L.R.; Weber, K.; Lake, W.; Bauer, A.; Hariharan, N.; Kuehn, T.; Cook, T.; Keles, S.; Newton, M.A.; Iskandar, B.J. Correction to: Ancestral folate promotes neuronal regeneration in serial generations of progeny. Mol. Neurobiol., 2020, 57(4), 2048-2071.
[http://dx.doi.org/10.1007/s12035-019-01812-5] [PMID: 31919777]
[86]
Bertoldo, E.; Adami, G.; Rossini, M.; Giollo, A.; Orsolini, G.; Viapiana, O.; Gatti, D.; Fassio, A. The emerging roles of endocrine hormones in different arthritic disorders. Front. Endocrinol. (Lausanne), 2021, 12, 620920.
[http://dx.doi.org/10.3389/fendo.2021.620920] [PMID: 34093428]
[87]
Lee, H.W.; Ha, S.K.; Kim, Y. Bisphenol A disrupts inflammatory responses via Nod-like receptor protein 3 pathway in macrophages., Appl Biol Chem, 2020, 63.
[88]
Kuo, CH; Yang, SN; Kuo, PL; Hung, CH Immunomodulatory effects of environmental endocrine disrupting chemicals. Kaohsiung J. Med. Sci., 2012, 28(7)(Suppl.), S37-42.
[http://dx.doi.org/10.1016/j.kjms.2012.05.008]
[89]
Straub, R.H. Interaction of the endocrine system with inflammation: A function of energy and volume regulation. Arthritis Res. Ther., 2014, 16(1), 203.
[http://dx.doi.org/10.1186/ar4484] [PMID: 24524669]
[90]
Alpízar-Rodríguez, D.; Finckh, A. Environmental factors and hormones in the development of rheumatoid arthritis. Semin. Immunopathol., 2017, 39(4), 461-468.
[http://dx.doi.org/10.1007/s00281-017-0624-2] [PMID: 28451785]
[91]
Parks, CG; Hoppin, JA; De Roos, AJ; Costenbader, KH; Alavanja, MC; Sandler, DP Rheumatoid arthritis in agricultural health study spouses: Associations with pesticides and other farm exposures. Environ. Health Perspect., 2016, 124(11), 1728-1734.
[92]
Choi, S.W.; Friso, S. Epigenetics: A new bridge between nutrition and health. Adv. Nutr., 2010, 1(1), 8-16.
[http://dx.doi.org/10.3945/an.110.1004] [PMID: 22043447]
[93]
Anway, M.D.; Skinner, M.K. Epigenetic transgenerational actions of endocrine disruptors. Endocrinology, 2006, 147(6)(Suppl.), S43-S49.
[http://dx.doi.org/10.1210/en.2005-1058] [PMID: 16690803]
[94]
Liu, C.; Marioni, R.E.; Hedman, Å.K.; Pfeiffer, L.; Tsai, P.C.; Reynolds, L.M.; Just, A.C.; Duan, Q.; Boer, C.G.; Tanaka, T.; Elks, C.E.; Aslibekyan, S.; Brody, J.A.; Kühnel, B.; Herder, C.; Almli, L.M.; Zhi, D.; Wang, Y.; Huan, T.; Yao, C.; Mendelson, M.M.; Joehanes, R.; Liang, L.; Love, S.A.; Guan, W.; Shah, S.; McRae, A.F.; Kretschmer, A.; Prokisch, H.; Strauch, K.; Peters, A.; Visscher, P.M.; Wray, N.R.; Guo, X.; Wiggins, K.L.; Smith, A.K.; Binder, E.B.; Ressler, K.J.; Irvin, M.R.; Absher, D.M.; Hernandez, D.; Ferrucci, L.; Bandinelli, S.; Lohman, K.; Ding, J.; Trevisi, L.; Gustafsson, S.; Sandling, J.H.; Stolk, L.; Uitterlinden, A.G.; Yet, I.; Castillo-Fernandez, J.E.; Spector, T.D.; Schwartz, J.D.; Vokonas, P.; Lind, L.; Li, Y.; Fornage, M.; Arnett, D.K.; Wareham, N.J.; Sotoodehnia, N.; Ong, K.K.; van Meurs, J.B.J.; Conneely, K.N.; Baccarelli, A.A.; Deary, I.J.; Bell, J.T.; North, K.E.; Liu, Y.; Waldenberger, M.; London, S.J.; Ingelsson, E.; Levy, D. A DNA methylation biomarker of alcohol consumption. Mol. Psychiatry, 2018, 23(2), 422-433.
[http://dx.doi.org/10.1038/mp.2016.192] [PMID: 27843151]
[95]
Nebbioso, A.; Tambaro, F.P.; Dell’Aversana, C.; Altucci, L. Cancer epigenetics: Moving forward. PLoS Genet., 2018, 14(6), e1007362.
[http://dx.doi.org/10.1371/journal.pgen.1007362] [PMID: 29879107]
[96]
Mohammad, HP; Barbash, O.; Creasy, CL Targeting epigenetic modifications in cancer therapy: Erasing the roadmap to cancer. Nat. Med., 2019, 25(3), 403-418.
[http://dx.doi.org/10.1038/s41591-019-0376-8]
[97]
Aggarwal, R.; Jha, M.; Shrivastava, A.; Jha, A.K. Natural compounds: Role in reversal of epigenetic changes. Biochemistry, 2015, 80(8), 972-989.

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