A Critical Analysis of the Association between Endocrine Disrupting Chemicals and Human Metabolic Disorders

Authors

  • Ali A. Rizvi Emory University School of Medicine, Atlanta, Georgia, USA

DOI:

https://doi.org/10.12970/2308-8044.2020.08.03

Keywords:

 Endocrine-disrupting chemicals, hormone, metabolism, diabetes, obesity.

Abstract

 Endocrine-disrupting chemicals (EDCs) are synthetic compounds predominantly of human design that are capable of causing interference in the hormonal functions of living organisms. They have the potential for causing adverse effects on the metabolic, cardiovascular, neurologic, immunologic, hematologic, and reproductive systems in the human body. Early exposure can impact growth and development and alter susceptibility to disease that may be pervasive and immutable. Reduction or augmentation of hormone action at the molecular, cellular, or systemic level can occur, leading to interference with signaling and feedback loops. EDCs can impact the production, secretion, transportation, action, or elimination of hormones. The endocrine system may be affected by EDCs from pesticides, plastic components, food additives, preservatives, soaps, detergents, pharmaceuticals, cosmetics, and even health supplements. These chemicals may gain entry into the human body through inhalation, ingestion, or absorption through the skin and mucous membranes. Metabolic disorders thought to be linked to EDC exposure include brain neurotransmitter dysfunction, appetite dysregulation, weight gain, obesity, glucose intolerance, metabolic syndrome, dyslipidemia, and cardiovascular diseases. Assessment and recommendations from the manufacturing industry, regulatory agencies, and the scientific community are ongoing in an effort to further understand and possibly mitigate the adverse consequences of EDC exposure. Further research is imperative to gain insight into the impact of EDCs on human health. A brief review of the metabolic and endocrine target systems thought to be affected by these chemicals as they have made their way into the everyday fabric of human society over the past century is given. 

References

Gore AC, Chappell VA, Fenton SE, et al. EDC-2: The Endocrine Society's Second Scientific Statement onEndocrine-Disrupting Chemicals. Endocr Rev 2015; 36(6): E1-E150. https://doi.org/10.1210/er.2015-1010

Zou E. Invisible endocrine disruption and its mechanisms: A current review. Gen Comp Endocrinol 2020; 293: 113470. https://doi.org/10.1016/j.ygcen.2020.113470

Taghvafard H, Medvedev A, Proskurnikov AV. Cao M. Impulsive model of endocrine regulation with a local continuous feedback. Math Biosci 2019; 310: 128-135. https://doi.org/10.1016/j.mbs.2019.02.006

Lauretta R, Sansone A, Sansone M, Romanelli F, Appetecchia M. Endocrine disrupting hemicals: effects on endocrine glands. Front Endocrinol (Lausanne) 2019; 10: 178. https://doi.org/10.3389/fendo.2019.00178

Karthikeyan BS, Ravichandran J, Mohanraj K, Vivek-Ananth RP, Samal A. A curated knowledgebase on endocrine disrupting chemicals and their biological systems-level perturbations. Sci Total Environ 2019; 692: 281-296. https://doi.org/10.1016/j.scitotenv.2019.07.225

Yilmaz B, Terekeci H, Sandal S, Kelestimur F. Endocrine disrupting chemicals: exposure, effects on human health, mechanism of action, models for testing and strategies for prevention. Rev Endocr Metab Disord 2020; 21(1): 127-147. https://doi.org/10.1007/s11154-019-09521-z

Hall JM, Greco CW. Perturbation of nuclear hormone receptors by endocrine disrupting chemicals: mechanisms and pathological consequences of exposure. Cells. 2019; 9(1). pii: E13. https://doi.org/10.3390/cells9010013

Martinez-Arguelles DB, Campioli E, Lienhart C, et al. In utero exposure to the endocrine disruptor di-(2-ethylhexyl) phthalate induces long-term changes in gene expression in the adult male adrenal gland. Endocrinology 2014; 155: 1667–1678. https://doi.org/10.1210/en.2013-1921

Prins GS, Patisaul HB, Belcher SM, Vandenberg LN. CLARITY-BPA academic laboratory studies identify consistent low-dose Bisphenol A effects on multiple organ systems. Basic Clin Pharmacol Toxicol 2019; 125 Suppl 3: 14-31. https://doi.org/10.1111/bcpt.13125

Uenoyama Y, Tomikawa J, Inoue N, et al. Molecular and epigenetic mechanism regulating hypothalamic Kiss1 gene expression in mammals. Neuroendocrinology 2016; 103(6): 640-9. https://doi.org/10.1159/000445207

Kopras E, Potluri V, Bermudez ML, Williams K, Belcher S, Kasper S. Actions of endocrine-disrupting chemicals on stem/progenitor cells during development and disease. Endocr Relat Cancer 2014; 21(2): T1-12. https://doi.org/10.1530/ERC-13-0360

Hunt JP, Schinn SM, Jones MD, Bundy BC. Rapid, portable detection of endocrine disrupting chemicals through ligandnuclear hormone receptor interactions. Analyst 2017; 142(24): 4595-4600. https://doi.org/10.1039/C7AN01540B

Barouki R, Gluckman PD, Grandjean P, Hanson M, Heindel JJ. Developmental origins of non-communicable disease: implications for research and public health. Environ Health 2012; 11: 42. https://doi.org/10.1186/1476-069X-11-42

Fall T, Ingelsson E. Genome-wide association studies of obesity and metabolic syndrome. Mol Cell Endocrinol 2014; 382: 740–757. https://doi.org/10.1016/j.mce.2012.08.018

Heindel JJ, Blumberg B, Cave M, et al. Metabolism disrupting chemicals and metabolic disorders. Reprod Toxicol 2017; 68: 3-33. https://doi.org/10.1016/j.reprotox.2016.10.001

Alavian-Ghavanini A, Rüegg J. Understanding epigenetic effects of endocrine disrupting chemicals: from mechanisms to novel test methods. Basic Clin Pharmacol Toxicol 2018; 122(1): 38-45. https://doi.org/10.1111/bcpt.12878

Rissman EF, Adli M. Minireview: transgenerational epigenetic inheritance: focus on endocrine disrupting compounds. Endocrinology 2014; 155: 2770–2780. https://doi.org/10.1210/en.2014-1123

McLachlan JA, Burow M, Chiang TC, Li SF. Gene imprinting in developmental toxicology: a possible interface between physiology and pathology. Toxicol Lett 2001; 120: 161–164. https://doi.org/10.1016/S0378-4274(01)00295-8

Ho SM, Johnson A, Tarapore P, Janakiram V, Zhang X, Leung YK. Environmental epigenetics and its implication on disease risk and health outcomes. Ilar J 2012; 53: 289–305. https://doi.org/10.1093/ilar.53.3-4.289

Gore AC, Martien KM, Gagnidze K, Pfaff D. Implications of prenatal steroid perturbations for neurodevelopment, behavior, and autism. Endocr Rev 2014; 35: 961–991. https://doi.org/10.1210/er.2013-1122

Skinner MK, Manikkam M, Guerrero-Bosagna C. Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab 2010; 21: 214–222. https://doi.org/10.1016/j.tem.2009.12.007

Vandenberg LN, Colborn T, Hayes TB, et al. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev 2012; 33(3): 378-455. https://doi.org/10.1210/er.2011-1050

Anwer F, Chaurasia S, Khan AA. Hormonally active agents in the environment: a state-of-the-art review. Rev Environ Health. 2016; 31(4): 415-433. https://doi.org/10.1515/reveh-2016-0014

Søeborg T, Frederiksen H, Andersson AM. Considerations for estimating daily intake values of nonpersistent environmental endocrine disruptors based on urinary biomonitoring data. Reproduction 2014; 147(4): 455-63. https://doi.org/10.1530/REP-13-0458

Nicolopoulou-Stamati P, Hens L, Sasco AJ. Cosmetics as endocrine disruptors: are they a health risk? Rev Endocr Metab Disord 2015; 16(4): 373-83. https://doi.org/10.1007/s11154-016-9329-4

Bucher JR. The National Toxicology Program rodent bioassay: designs, interpretations, and scientific contributions. Ann NY Acad Sci 2002; 982: 198–207. https://doi.org/10.1111/j.1749-6632.2002.tb04934.x

Ahrens A, Moilanen M, Martin S, et al. European Union regulators and industry agree on improving specific environmental release categories: Report from the exchange network for exposure scenarios specific environmental release category workshop on May 13, 2016. Integr Environ Assess Manag 2017; 13(5): 815-820. https://doi.org/10.1002/ieam.1897

Rudel RA, Attfield KR, Schifano JN, Brody JG. Chemicals causing mammary gland tumors in animals signal new directions for epidemiology, chemicals testing, and risk assessment for breast cancer prevention. Cancer. 2007; 109: 2635-2666. https://doi.org/10.1002/cncr.22653

Browne P, Noyes PD, Casey WM, Dix DJ. Application of Adverse Outcome Pathways to U.S. EPA's Endocrine Disruptor Screening Program. Environ Health Perspect 2017; 125(9): 096001. https://doi.org/10.1289/EHP1304

Tice RR, Austin CP, Kavlock RJ, Bucher JR. Improving the human hazard characterization of chemicals: a Tox21 update. Environ Health Perspect 2013; 121: 756–765. https://doi.org/10.1289/ehp.1205784

Kavlock R, Chandler K, Houck K, et al. Update on EPA's ToxCast program: providing high throughput decision support tools for chemical risk management. Chem Res Toxicol 2012; 25: 1287–1302. https://doi.org/10.1021/tx3000939

Heindel JJ. Endocrine disruptors and the obesity epidemic. Toxicol Sci 2003; 76: 247–249. https://doi.org/10.1093/toxsci/kfg255

Warner M, Mocarelli P, Samuels S, Needham L, Brambilla P, Eskenazi B. Dioxin exposure and cancer risk in the Seveso Women's Health Study. Environ Health Perspect 2011; 119: 1700–1705. https://doi.org/10.1289/ehp.1103720

Mocarelli P, Gerthoux PM, Needham LL, et al. Perinatal exposure to low doses of dioxin can permanently impair human semen quality. Environ Health Perspect 2011; 119: 713–718. https://doi.org/10.1289/ehp.1002134

Mocarelli P, Marocchi A, Brambilla P, Gerthoux P, Young DS, Mantel N. Clinical laboratory manifestations of exposure to dioxin in children. A six-year study of the effects of an environmental disaster near Seveso, Italy. JAMA 1986; 256: 2687–2695. https://doi.org/10.1001/jama.1986.03380190057025

Agency for Toxic Substances and Disease Registry. 2014. Camp Lejeune, NC. Available at: http://www.atsdr.cdc.gov/ sites/lejeune/index.html, accessed May 16, 2020.

Wu CF, Chang-Chien GP, Su SW, Chen BH, Wu MT. Findings of 2731 suspected phthalate-tainted foodstuffs during the 2011 phthalates incident in Taiwan. J Formos Med Assoc 2014; 113: 600–605. https://doi.org/10.1016/j.jfma.2014.02.010

U.S. Environmental Protection Agency. Phthalates: TEACH Chemical Summary. Document #905B07006. 2007.

Hines EP, Calafat AM, Silva MJ, Mendola P, Fenton SE. Concentrations of phthalate metabolites in milk, urine, saliva, and serum of lactating North Carolina women. Environ Health Perspect 2009; 117: 86–92. https://doi.org/10.1289/ehp.11610

Meeker JD, Ferguson KK. Relationship between urinary phthalate and bisphenol A concentrations and serum thyroid measures in U.S. adults and adolescents from the National Health and Nutrition Examination Survey (NHANES) 2007– 2008. Environ Health Perspect 2011; 119: 1396–1402. https://doi.org/10.1289/ehp.1103582

Patterson TA, Twaddle NC, Roegge CS, Callicott RJ, Fisher JW, Doerge DR. Concurrent determination of bisphenol A pharmacokinetics in maternal and fetal rhesus monkeys. Toxicol Appl Pharmacol 2013; 267: 41–48. https://doi.org/10.1016/j.taap.2012.12.006

Churchwell MI, Camacho L, Vanlandingham MM, et al. Comparison of life-stage-dependent internal dosimetry for bisphenol A, ethinyl estradiol, a reference estrogen, and endogenous estradiol to test an estrogenic mode of action in Sprague Dawley rats. Toxicol Sci 2014; 139: 4–20. https://doi.org/10.1093/toxsci/kfu021

Vandenberg LN, Gerona RR, Kannan K, et al. A round robin approach to the analysis of bisphenol A (BPA) in human blood samples. Environ Health 2014; 13: 25. https://doi.org/10.1186/1476-069X-13-25

United States Environmental Protection Agency. Assessing and managing chemicals under TSCA. Risk Management for Bisphenol A (BPA). Available at: https://www.epa.gov/ assessing-and-managing-chemicals-under-tsca/riskmanagement-bisphenol-bpa, accessed May 16, 2020.

Ho SM, Tang WY, Belmonte de Frausto J, Prins GS. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res 2006; 66: 5624–5632. https://doi.org/10.1158/0008-5472.CAN-06-0516

Tang WY, Morey LM, Cheung YY, Birch L, Prins GS, Ho SM. 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. https://doi.org/10.1210/en.2011-1308

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. https://doi.org/10.1002/em.21692

Gianessi LP. Benefits of triazine herbicides. In: Ballantine LG, McFarland JE, Hackett DS, eds. Triazine Herbicides: Risk Assessment. Vol 683. Washington, DC: American Chemical Society; 1998: 1–8. https://doi.org/10.1021/bk-1998-0683.ch001

Solomon KR, Giesy JP, LaPoint TW, Giddings JM, Richards RP. Ecological risk assessment of atrazine in North American surface waters. Environ Toxicol Chem 2013; 32: 10–11. https://doi.org/10.1002/etc.2050

Gillette R, Miller-Crews I, Nilsson EE, Skinner MK, Gore AC, Crews D. Sexually dimorphic effects of ancestral exposure to vinclozolin on stress reactivity in rats. Endocrinology 2014; 155: 3853–3866. https://doi.org/10.1210/en.2014-1253

Guerrero-Bosagna C, Covert TR, Haque MM, et al. Epigenetic transgenerational inheritance of vinclozolin induced mouse adult onset disease and associated sperm epigenome biomarkers. Reprod Toxicol 2012; 34: 694–707. https://doi.org/10.1016/j.reprotox.2012.09.005

Nilsson E, Larsen G, Manikkam M, Guerrero-Bosagna C, Savenkova MI, Skinner MK. Environmentally induced epigenetic transgenerational inheritance of ovarian disease. PLoS One 2012; 7: e36129. https://doi.org/10.1371/journal.pone.0036129

Skinner MK, Guerrero-Bosagna C, Haque M, Nilsson E, Bhandari R, McCarrey JR. Environmentally induced transgenerational epigenetic reprogramming of primordial germ cells and the subsequent germ line. PLoS One 2013; 8: e66318. https://doi.org/10.1371/journal.pone.0066318

Baillie-Hamilton PF. Chemical toxins: a hypothesis to explain the global obesity epidemic. J Altern Complement Med. 2002; 8: 185–192. https://doi.org/10.1089/107555302317371479

Newbold RR, Padilla-Banks E, Snyder RJ, Jefferson WN. Developmental exposure to estrogenic compounds and obesity. Birth Defects Res A Clin Mol Teratol. 2005;73:478– 480. https://doi.org/10.1002/bdra.20147

Grün F, Blumberg B. Environmental obesogens: organotins and endocrine disruption via nuclear receptor signaling. Endocrinology 2006; 147: S50–S55. https://doi.org/10.1210/en.2005-1129

Sargis RM, Simmons RA. Environmental neglect: endocrine disruptors as underappreciated but potentially modifiable diabetes risk factors. Diabetologia 2019; 62(10): 1811-1822. https://doi.org/10.1007/s00125-019-4940-z

Chevalier N, Fénichel P. Endocrine disruptors: new players in the pathophysiology of type 2 diabetes? Diabetes Metab 2015; 41(2): 107-15. https://doi.org/10.1016/j.diabet.2014.09.005

Song Y, Chou EL, Baecker A, You NC, Song Y, Sun Q, Liu S. Endocrine-disrupting chemicals, risk of type 2 diabetes, and diabetes-related metabolic traits: A systematic review and meta-analysis. J Diabetes 2016; 8(4): 516-32. https://doi.org/10.1111/1753-0407.12325

Papalou O, Kandaraki EA, Papadakis G, DiamantiKandarakis E. Endocrine Disrupting Chemicals: An occult mediator of metabolic disease. Front Endocrinol (Lausanne) 2019; 10: 112. https://doi.org/10.3389/fendo.2019.00112

Janesick AS, Blumberg B. Obesogens: an emerging threat to public health. Am J Obstet Gynecol 2016; 214(5): 559-65. https://doi.org/10.1016/j.ajog.2016.01.182

Casals-Casas C, Desvergne B. Endocrine disruptors: from endocrine to metabolic disruption. Annu Rev Physiol 2011; 73: 135-62. https://doi.org/10.1146/annurev-physiol-012110-142200

Foulds CE, Treviño LS, York B, Walker CL. Endocrinedisrupting chemicals and fatty liver disease. Nat Rev Endocrinol 2017; 13(8): 445-457. https://doi.org/10.1038/nrendo.2017.42

Enan E, Liu PC. Matsumura F. 2,3,7,8-Tetrachlorodibenzo-pdioxin causes reduction of glucose transporting activities in the plasma membranes of adipose tissue and pancreas from the guinea pig. J Biolo Chem 1992; 267: 19785-91. https://doi.org/10.1080/03601239209372797

Kim YH, Shim YJ, Shin YJ, Sul D, Lee E, Min BH. 2,3,7,8- tetrachlorodibenzo-p-dioxin (TCDD) induces calcium influx through T-type calcium channel and enhances lysosomal exocytosis and insulin secretion in INS-1 cells. Int J Toxicol 2009; 28: 151–61. https://doi.org/10.1177/1091581809336885

Alonso-Magdalena P, Garcia-Arevalo M, Quesada I, Nadal A. Bisphenol-A treatment during pregnancy in mice: a new window of susceptibility for the development of diabetes in mothers later in life. Endocrinology 2015; 156: 1659–70. https://doi.org/10.1210/en.2014-1952

Nadal, Alonso-Magdalena P, Soriano S, Quesada I, Ropero AB. The pancreatic beta-cell as a target of estrogens and xenoestrogens: implications for blood glucose homeostasis and diabetes. Mol Cell Endocrinol 2009; 304: 63–8. https://doi.org/10.1016/j.mce.2009.02.016

Mimoto MS, Nadal A, Sargis RM. Polluted pathways: mechanisms of metabolic disruption by endocrine disrupting chemicals. Curr Environ Health Rep 2017; 4: 208–222. https://doi.org/10.1007/s40572-017-0137-0

Bodin J, Bolling AK, Samuelsen M, Becher R, Lovik M, Nygaard UC. Long-term bisphenol A exposure accelerates insulitis development in diabetes-prone NOD mice. Immunopharmacol Immunotoxicol 2013; 35: 349–58. https://doi.org/10.3109/08923973.2013.772195

Watt MJ, Miotto PM, De Nardo W, Montgomery MK. The liver as an endocrine organ-linking NAFLD and insulin resistance. Endocr Rev. 2019; 40(5): 1367-1393. https://doi.org/10.1210/er.2019-00034

Mellor CL, Steinmetz FP, Cronin MT. The identification of nuclear receptors associated with hepatic steatosis to develop and extend adverse outcome pathways. Crit Rev Toxicol 2016; 46: 138–52. https://doi.org/10.3109/10408444.2015.1089471

Al-Eryani L, Wahlang B, Falkner KC, Guardiola JJ, Clair HB, Prough RA, et al. Identification of environmental chemicals associated with the development of toxicant-associated fatty liver disease in rodents. Toxicol Pathol 2015; 43: 482–97. https://doi.org/10.1177/0192623314549960

Moon MK, Jeong IK, Jung Oh T, Ahn HY, Kim HH, Park YJ, et al. Long-term oral exposure to bisphenol A induces glucose intolerance and insulin resistance. J Endocrinol 2015; 226: 35–42. https://doi.org/10.1530/JOE-14-0714

Marroqui L, Tudurí E, Alonso-Magdalena P, Quesada I, Nadal Á, Dos Santos RS. Mitochondria as target of endocrine-disrupting chemicals: implications for type 2 diabetes. J Endocrinol 2018; 239(2): R27-R45. https://doi.org/10.1530/JOE-18-0362

Batista TM, Alonso-Magdalena P, Vieira E, Amaral ME, Cederroth CR, Nef S, et al. Short-term treatment with bisphenol-A leads to metabolic abnormalities in adult male mice. PLoS ONE 2012; 7: e33814. https://doi.org/10.1371/journal.pone.0033814

Regnier SM, Sargis RM. Adipocytes under assault: environmental disruption of adipose physiology. Biochim et Biophys Acta 2014; 1842: 520–33. https://doi.org/10.1016/j.bbadis.2013.05.028

Bateman ME, Strong AL, McLachlan JA, Burow ME, Bunnell BA. The effects of endocrine disruptors on adipogenesis and osteogenesis in mesenchymal stem cells: a review. Front Endocrinol 2016; 7: 171. https://doi.org/10.3389/fendo.2016.00171

Zhang HY, Xue WY, Li YY, Ma Y, Zhu YS, Huo WQ, et al. Perinatal exposure to 4-nonylphenol affects adipogenesis in first and second generation rats offspring. Toxicol Lett 2014; 225: 325–32. https://doi.org/10.1016/j.toxlet.2013.12.011

Wang J, Sun B, Hou M, Pan X, Li X. The environmental obesogen bisphenol A promotes adipogenesis by increasing the amount of 11-beta-hydroxysteroid dehydrogenase type 1 in the adipose tissue of children. Int J Obes 2013; 37: 999– 1005. https://doi.org/10.1038/ijo.2012.173

Neel BA, Brady MJ, Sargis RM. The endocrine disrupting chemical tolylfluanid alters adipocyte metabolism via glucocorticoid receptor activation. Mol Endocrinol 2013; 27: 394–406. https://doi.org/10.1210/me.2012-1270

Sargis RM, Neel BA, Brock CO, Lin Y, Hickey AT, Carlton DA, et al. The novel endocrine disruptor tolylfluanid impairs insulin signaling in primary rodent and human adipocytes through a reduction in insulin receptor substrate-1 levels. Biochim et Biophys Acta 2012; 1822: 952–60. https://doi.org/10.1016/j.bbadis.2012.02.015

Angle BM, Do RP, Ponzi D, Stahlhut RW, Drury BE, Nagel SC, et al. Metabolic disruption in male mice due to fetal exposure to low but not high doses of bisphenol A (BPA): evidence for effects on body weight, food intake, adipocytes, leptin, adiponectin, insulin and glucose regulation. Reprod Toxicol 2013; 42: 256–68. https://doi.org/10.1016/j.reprotox.2013.07.017

Hugo ER, Brandebourg TD, Woo JG, Loftus J, Alexander JW, Ben-Jonathan N. Bisphenol A at environmentally relevant doses inhibits adiponectin release from human adipose tissue explants and adipocytes. Environ Health Perspect 2008; 116: 1642–7. https://doi.org/10.1289/ehp.11537

Valentino R, D'Esposito V, Passaretti F, Liotti A, Cabaro S, Longo M, et al. Bisphenol-A impairs insulin action and upregulates inflammatory pathways in human subcutaneous adipocytes and 3T3-L1 cells. PLoS ONE 2013; 8:e82099. https://doi.org/10.1371/journal.pone.0082099

Walley SN, Roepke TA. Perinatal exposure to endocrine disrupting compounds and the control of feeding behavior-an overview. Hormon Behav 2018; 101:22–28. https://doi.org/10.1016/j.yhbeh.2017.10.017

Mackay H, Patterson ZR, Khazall R, Patel S, Tsirlin D, Abizaid A. Organizational effects of perinatal exposure to bisphenol-A and diethylstilbestrol on arcuate nucleus circuitry controlling food intake and energy expenditure in male and female CD-1 mice. Endocrinology 2013; 154:1465–75. https://doi.org/10.1210/en.2012-2044

Monje L, Varayoud J, Munoz-de-Toro M, Luque EH, Ramos JG. Exposure of neonatal female rats to bisphenol A disrupts hypothalamic LHRH pre-mRNA processing and estrogen receptor alpha expression in nuclei controlling estrous cyclicity. Reproduct Toxicol 2010; 30: 625–34. https://doi.org/10.1016/j.reprotox.2010.08.004

Drobna Z, Henriksen AD, Wolstenholme JT, Montiel C, Lambeth PS, Shang S, et al. Transgenerational effects of Bisphenol A on gene expression and DNA methylation of imprinted genes in brain. Endocrinology 2018; 159: 132–44. https://doi.org/10.1210/en.2017-00730

Decherf S, Seugnet I, Fini JB, Clerget-Froidevaux MS, Demeneix BA. Disruption of thyroid hormone-dependent hypothalamic set-points by environmental contaminants. Mol Cell Endocrinol 2010; 323: 172–82. https://doi.org/10.1016/j.mce.2010.04.010

Bansal A, Henao-Mejia J, Simmons RA. Immune System: An emerging player in mediating effects of endocrine disruptors on metabolic health. Endocrinology 2018; 159(1): 32-45. https://doi.org/10.1210/en.2017-00882

O'Brien E, Dolinoy DC, Mancuso P. Perinatal bisphenol A exposures increase production of pro-inflammatory mediators in bone marrow-derived mast cells of adult mice. J Immunotoxicol 2014; 11: 205–12. https://doi.org/10.3109/1547691X.2013.822036

Miao S, Gao Z, Kou Z, Xu G, Su C, Liu N. Influence of Bisphenol A on developing rat estrogen receptors and some cytokines in rats: a two-generational study. J Toxicol Environ Health. Part A 2008; 71: 1000–8. https://doi.org/10.1080/15287390801907467

Pascale, Marchesi N, Marelli C, Coppola A, Luzi L, Govoni S, et al. Microbiota and metabolic diseases. Endocrine 2018; 61: 357–71. https://doi.org/10.1007/s12020-018-1605-5

Claus SP, Guillou H, Ellero-Simatos S. The gut microbiota: a major player in the toxicity of environmental pollutants? NPJ Biofilms Microbiomes 2016; 2: 16003. https://doi.org/10.1038/npjbiofilms.2016.3

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