Effects of endocrine-disrupting chemicals on the ovary

Biology of Reproduction

Volumn 93, Issue 1, 2015, Pages

  Patel, Shreya ^a   Zhou, Changqing ^a   Rattan, Saniya ^a   Flaws, Jodi A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

2,3,7,8 tetrachloro p dibenzodioxin; Bisphenol a; Folliculogenesis; Genistein; Methoxychlor; Ovary; Phthalates; Steroidogenesis

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 4,4' ISOPROPYLIDENEDIPHENOL; ENDOCRINE DISRUPTOR; GENISTEIN; METHOXYCHLOR; PHTHALIC ACID DERIVATIVE; BENZHYDRYL DERIVATIVE; PHENOL DERIVATIVE; PHTHALIC ACID; POLLUTANT; POLYCHLORINATED DIBENZODIOXIN;

HUMAN; NONHUMAN; OVARY; OVARY FOLLICLE DEVELOPMENT; OVARY FUNCTION; PRIORITY JOURNAL; SHORT SURVEY; STEROIDOGENESIS; ANIMAL; DRUG EFFECTS; FEMALE; OVARY FOLLICLE; PHARMACOLOGY; POLLUTANT; REPRODUCTION;

ANIMALS; BENZHYDRYL COMPOUNDS; ENDOCRINE DISRUPTORS; ENVIRONMENTAL POLLUTANTS; FEMALE; GENISTEIN; HUMANS; METHOXYCHLOR; OVARIAN FOLLICLE; OVARY; PHENOLS; PHTHALIC ACIDS; POLYCHLORINATED DIBENZODIOXINS; REPRODUCTION;

EID: 84938917988     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.115.130336     Document Type: Short Survey

References (132)

1. Silbergeld EK, Flaws JA. Environmental exposures and women's health. Clin Obstet Gynecol 2002; 45:1119-1128.
2. Craig ZR, Wang W, Flaws JA. Endocrine-disrupting chemicals in ovarian function: effects on steroidogenesis, metabolism and nuclear receptor signaling. Reproduction 2011; 142:633-646.
3. Sowers MR, La Pietra MT. Menopause: its epidemiology and potential association with chronic diseases. Epidemiol Rev 1995; 17:287-302.
4. Bagur AC, Mautalen CA. Risk for developing osteoporosis in untreated premature menopause. Calcif Tissue Int 1992; 51:4-7.
5. Sharara FI, Seifer DB, Flaws JA. Environmental toxicants and female reproduction. Fertil Steril 1998; 70:613-622.
6. Zama AM, Uzumcu M. Epigenetic effects of endocrine-disrupting chemicals on female reproduction: an ovarian perspective. Front Neuroendocrinol 2010; 31:420-439.
7. Padmanabhan V, Sarma HN, Savabieasfahani M, Steckler TL, Veiga-Lopez A. Developmental reprogramming of reproductive and metabolic dysfunction in sheep: native steroids vs. environmental steroid receptor modulators. Int J Androl 2010; 33:394-404.
8. Jefferson WN, Padilla-Banks E, Newbold RR. Disruption of the developing female reproductive system by phytoestrogens: genistein as an example. Mol Nutr Food Res 2007; 51:832-844.
9. Uzumcu M, Zachow R. Developmental exposure to environmental endocrine disruptors: consequences within the ovary and on female reproductive function. Reprod Toxicol 2007; 23:337-352.
10. Peretz J, Vrooman L, Ricke WA, Hunt PA, Ehrlich S, Hauser R, Padmanabhan V, Taylor HS, Swan SH, VandeVoort CA, Flaws JA. Bisphenol a and reproductive health: update of experimental and human evidence, 2007-2013. Environ Health Perspect 2014; 122:775-786.
11. Badach H, Nazimek T, Kaminski R, Turski W. Organochlorine pesticides concentration in the drinking water from regions of extensive agriculture in Poland. Ann Agric Environ Med 2000; 7:25-28.
12. Badach H, Nazimek T, Kaminska IA. Pesticide content in drinking water samples collected from orchard areas in central Poland. Ann Agric Environ Med 2007; 14:109-114.
13. Krol WJ, Arsenault TL, Pylypiw HM Jr, Incorvia Mattina MJ. Reduction of pesticide residues on produce by rinsing. J Agric Food Chem 2000; 48:4666-4670.
14. Golovleva LA, Polyakova AB, Pertsova RN, Finkelshtein ZI. The fate of methoxychlor in soils and transformation by soil microorganisms. J Environ Sci Health B 1984; 19:523-538.
15. Shegunova P, Klanova J, Holoubek I. Residues of organochlorinated pesticides in soils from the Czech Republic. Environ Pollut 2007; 146:257-261.
16. Armenti AE, Zama AM, Passantino L, Uzumcu M. Developmental methoxychlor exposure affects multiple reproductive parameters and ovarian folliculogenesis and gene expression in adult rats. Toxicol Appl Pharmacol 2008; 233:286-296.
17. Hannon PR, Flaws JA. The effects of phthalates on the ovary. Front Endocrinol (Lausanne) 2015; 6:8.
18. Schecter A, Birnbaum L, Ryan JJ, Constable JD. Dioxins: an overview. Environ Res 2006; 101:419-428.
19. Polkowski K, Mazurek AP. Biological properties of genistein. A review of in vitro and in vivo data. Acta Pol Pharm 2000; 57:135-155.
20. Jefferson WN. Adult ovarian function can be affected by high levels of soy. J Nutr 2010; 140:2322s-2325s.
21. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reprod Toxicol 2007; 24:139-177.
22. Sajiki J, Takahashi K, Yonekubo J. Sensitive method for the determination of bisphenol-A in serum using two systems of highperformance liquid chromatography. J Chromatogr B Biomed Sci Appl 1999; 736:255-261.
23. Inoue K, Kato K, Yoshimura Y, Makino T, Nakazawa H. Determination of bisphenol A in human serum by high-performance liquid chromatography with multi-electrode electrochemical detection. J Chromatogr B Biomed Sci Appl 2000; 749:17-23.
24. Takeuchi T, Tsutsumi O. Serum bisphenol a concentrations showed gender differences, possibly linked to androgen levels. Biochem Biophys Res Commun 2002; 291:76-78.
25. Inoue K, Yamaguchi A, Wada M, Yoshimura Y, Makino T, Nakazaw H. Quantitative detection of bisphenol A and bisphenol A diglycidyl ether metabolites in human plasma by liquid chromatography-electrospray mass spectrometry. J Chromatogr B Biomed Sci Appl 2001; 765:121-126.
26. Volkel W, Bittner N, Dekant W. Quantitation of bisphenol A and bisphenol A glucuronide in biological samples by high performance liquid chromatography-tandem mass spectrometry. Drug Metab Dispos 2005; 33:1748-1757.
27. Genuis SJ, Beesoon S, Birkholz D, Lobo RA. Human excretion of bisphenol A: blood, urine, and sweat (BUS) study. J Environ Public Health 2012; 2012:185731.
28. Otaka H, Yasuhara A, Morita M. Determination of bisphenol A and 4-nonylphenol in human milk using alkaline digestion and cleanup by solid-phase extraction. Anal Sci 2003; 19:1663-1666.
29. Sun Y, Irie M, Kishikawa N, Wada M, Kuroda N, Nakashima K. Determination of bisphenol A in human breast milk by HPLC with column-switching and fluorescence detection. Biomed Chromatogr 2004; 18:501-507.
30. Ikezuki Y, Tsutsumi O, Takai Y, Kamei Y, Taketani Y. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum Reprod 2002; 17:2839-2841.
31. Yamada H, Furuta I, Kato EH, Kataoka S, Usuki Y, Kobashi G, Sata F, Kishi R, Fujimoto S. Maternal serum and amniotic fluid bisphenol A concentrations in the early second trimester. Reprod Toxicol 2002; 16:735-739.
32. Engel SM, Levy B, Liu Z, Kaplan D, WolffMS. Xenobiotic phenols in early pregnancy amniotic fluid. Reprod Toxicol 2006; 21:110-112.
33. Schonfelder G, Wittfoht W, Hopp H, Talsness CE, Paul M, Chahoud I. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect 2002; 110:A703-707.
34. Todaka E, Mori C. Necessity to establish new risk assessment and risk communication for human fetal exposure to multiple endocrine disruptors in Japan. Congenit Anom (Kyoto) 2002; 42:87-93.
35. Taylor JA, Vom Saal FS, Welshons WV, Drury B, Rottinghaus G, Hunt PA, Toutain PL, Laffont CM, VandeVoort CA. Similarity of bisphenol A pharmacokinetics in rhesus monkeys and mice: relevance for human exposure. Environ Health Perspect 2011; 119:422-430.
36. 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:E480-484.
37. Caserta D, Di Segni N, Mallozzi M, Giovanale V, Mantovani A, Marci R, Moscarini M. Bisphenol A and the female reproductive tract: an overview of recent laboratory evidence and epidemiological studies. Reprod Biol Endocrinol 2014; 12:37.
38. Souter I, Smith KW, Dimitriadis I, Ehrlich S, Williams PL, Calafat AM, Hauser R. The association of bisphenol-A urinary concentrations with antral follicle counts and other measures of ovarian reserve in women undergoing infertility treatments. Reprod Toxicol 2013; 42:224-231.
39. Mok-Lin E, Ehrlich S, Williams PL, Petrozza J, Wright DL, Calafat AM, Ye X, Hauser R. Urinary bisphenol A concentrations and ovarian response among women undergoing IVF. Int J Androl 2010; 33:385-393.
40. Wang W, Hafner KS, Flaws JA. In utero bisphenol A exposure disrupts germ cell nest breakdown and reduces fertility with age in the mouse. Toxicol Appl Pharmacol 2014; 276:157-164.
41. Peretz J, Gupta RK, Singh J, Hernandez-Ochoa I, Flaws JA. Bisphenol A impairs follicle growth, inhibits steroidogenesis, and downregulates ratelimiting enzymes in the estradiol biosynthesis pathway. Toxicol Sci 2011; 119:209-217.
42. Ziv-Gal A, Craig ZR, Wang W, Flaws JA. Bisphenol A inhibits cultured mouse ovarian follicle growth partially via the aryl hydrocarbon receptor signaling pathway. Reprod Toxicol 2013; 42:58-67.
43. Peretz J, Craig ZR, Flaws JA. Bisphenol A inhibits follicle growth and induces atresia in cultured mouse antral follicles independently of the genomic estrogenic pathway. Biol Reprod 2012; 87:63.
44. Xu J, Osuga Y, Yano T, Morita Y, Tang X, Fujiwara T, Takai Y, Matsumi H, Koga K, Taketani Y, Tsutsumi O. Bisphenol A induces apoptosis and G2-to-M arrest of ovarian granulosa cells. Biochem Biophys Res Commun 2002; 292:456-462.
45. Lee SG, Kim JY, Chung JY, Kim YJ, Park JE, Oh S, Yoon YD, Yoo KS, Yoo YH, Kim JM. Bisphenol A exposure during adulthood causes augmentation of follicular atresia and luteal regression by decreasing 17beta-estradiol synthesis via downregulation of aromatase in rat ovary. Environ Health Perspect 2013; 121:663-669.
46. Wetherill YB, Akingbemi BT, Kanno J, McLachlan JA, Nadal A, Sonnenschein C, Watson CS, Zoeller RT, Belcher SM. In vitro molecular mechanisms of bisphenol A action. Reprod Toxicol 2007; 24:178-198.
47. Susiarjo M, Hassold TJ, Freeman E, Hunt PA. Bisphenol A exposure in utero disrupts early oogenesis in the mouse. PLoS Genet 2007; 3:e5.
48. Bouskine A, Nebout M, Brucker-Davis F, Benahmed M, Fenichel P. Low doses of bisphenol A promote human seminoma cell proliferation by activating PKA and PKG via a membrane G-protein-coupled estrogen receptor. Environ Health Perspect 2009; 117:1053-1058.
49. Hunt PA, Koehler KE, Susiarjo M, Hodges CA, Ilagan A, Voigt RC, Thomas S, Thomas BF, Hassold TJ. Bisphenol a exposure causes meiotic aneuploidy in the female mouse. Curr Biol 2003; 13:546-553.
50. TrapphoffT, Heiligentag M, El Hajj N, Haaf T, Eichenlaub-Ritter U. Chronic exposure to a low concentration of bisphenol A during follicle culture affects the epigenetic status of germinal vesicles and metaphase II oocytes. Fertil Steril 2013; 100:1758-1767. e1751.
51. Mlynarcikova A, Nagyova E, Fickova M, Scsukova S. Effects of selected endocrine disruptors on meiotic maturation, cumulus expansion, synthesis of hyaluronan and progesterone by porcine oocyte-cumulus complexes. Toxicol in Vitro 2009; 23:371-377.
52. 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; 283:12-18.
53. Mlynarcikova A, Kolena J, Fickova M, Scsukova S. Alterations in steroid hormone production by porcine ovarian granulosa cells caused by bisphenol A and bisphenol A dimethacrylate. Mol Cell Endocrinol 2005; 244:57-62.
54. Grasselli F, Baratta L, Baioni L, Bussolati S, Ramoni R, Grolli S, Basini G. Bisphenol A disrupts granulosa cell function. Domest Anim Endocrinol 2010; 39:34-39.
55. Peretz J, Flaws JA. Bisphenol A down-regulates rate-limiting Cyp11a1 to acutely inhibit steroidogenesis in cultured mouse antral follicles. Toxicol Appl Pharmacol 2013; 271:249-256.
56. Kabuto H, Hasuike S, Minagawa N, Shishibori T. Effects of bisphenol A on the metabolisms of active oxygen species in mouse tissues. Environ Res 2003; 93:31-35.
57. El-Beshbishy HA, Aly HA, El-Shafey M. Lipoic acid mitigates bisphenol A-induced testicular mitochondrial toxicity in rats. Toxicol Ind Health 2013; 29:875-887.
58. D'Cruz SC, Jubendradass R, Jayakanthan M, Rani SJ, Mathur PP. Bisphenol A impairs insulin signaling and glucose homeostasis and decreases steroidogenesis in rat testis: an in vivo and in silico study. Food Chem Toxicol 2012; 50:1124-1133.
59. Chouhan S, Yadav SK, Prakash J, Westfall S, Ghosh A, Agarwal NK, Singh SP. Increase in the expression of inducible nitric oxide synthase on exposure to bisphenol A: a possible cause for decline in steroidogenesis in male mice. Environ Toxicol Pharmacol 2015; 39:405-416.
60. Avci B, Bahadir A, Tuncel OK, Bilgici B. Influence of alpha-tocopherol and alpha-lipoic acid on bisphenol-A-induced oxidative damage in liver and ovarian tissue of rat. Toxicol Ind Health 2014
61. Stresser DM, Kupfer D. Human cytochrome P450-catalyzed conversion of the proestrogenic pesticide methoxychlor into an estrogen. Role of CYP2C19 and CYP1A2 in O-demethylation. Drug Metab Dispos 1998; 26:868-874.
62. Uzumcu M, Kuhn PE, Marano JE, Armenti AE, Passantino L. Early postnatal methoxychlor exposure inhibits folliculogenesis and stimulates anti-Müllerian hormone production in the rat ovary. J Endocrinol 2006; 191:549-558.
63. Gupta RK, Meachum S, Hernandez-Ochoa I, Peretz J, Yao HH, Flaws JA. Methoxychlor inhibits growth of antral follicles by altering cell cycle regulators. Toxicol Appl Pharmacol 2009; 240:1-7.
64. Miller KP, Gupta RK, Greenfeld CR, Babus JK, Flaws JA. Methoxychlor directly affects ovarian antral follicle growth and atresia through Bcl-2-and Bax-mediated pathways. Toxicol Sci 2005; 88:213-221.
65. Gupta RK, Schuh RA, Fiskum G, Flaws JA. Methoxychlor causes mitochondrial dysfunction and oxidative damage in the mouse ovary. Toxicol Appl Pharmacol 2006; 216:436-445.
66. Symonds DA, Merchenthaler I, Flaws JA. Methoxychlor and estradiol induce oxidative stress DNA damage in the mouse ovarian surface epithelium. Toxicol Sci 2008; 105:182-187.
67. Basavarajappa MS, Craig ZR, Hernandez-Ochoa I, Paulose T, Leslie TC, Flaws JA. Methoxychlor reduces estradiol levels by altering steroidogenesis and metabolism in mouse antral follicles in vitro. Toxicol Appl Pharmacol 2011; 253:161-169.
68. Akgul Y, Derk RC, Meighan T, Rao KM, Murono EP. The methoxychlor metabolite, HPTE, inhibits rat luteal cell progesterone production. Reprod Toxicol 2011; 32:77-84.
69. Zachow R, Uzumcu M. The methoxychlor metabolite, 2,2-bis-(phydroxyphenyl)-1,1,1-trichloroethane, inhibits steroidogenesis in rat ovarian granulosa cells in vitro. Reprod Toxicol 2006; 22:659-665.
70. Craig ZR, Hannon PR, Flaws JA. Pregnenolone co-treatment partially restores steroidogenesis, but does not prevent growth inhibition and increased atresia in mouse ovarian antral follicles treated with monohydroxy methoxychlor. Toxicol Appl Pharmacol 2013; 272:780-786.
71. Craig ZR, Leslie TC, Hatfield KP, Gupta RK, Flaws JA. Mono-hydroxy methoxychlor alters levels of key sex steroids and steroidogenic enzymes in cultured mouse antral follicles. Toxicol Appl Pharmacol 2010; 249:107-113.
72. Gaido KW, Maness SC, McDonnell DP, Dehal SS, Kupfer D, Safe S. Interaction of methoxychlor and related compounds with estrogen receptor alpha and beta, and androgen receptor: structure-activity studies. Mol Pharmacol 2000; 58:852-858.
73. Waters KM, Safe S, Gaido KW. Differential gene expression in response to methoxychlor and estradiol through ERalpha, ERbeta, and AR in reproductive tissues of female mice. Toxicol Sci 2001; 63:47-56.
74. Zama AM, Uzumcu M. Fetal and neonatal exposure to the endocrine disruptor methoxychlor causes epigenetic alterations in adult ovarian genes. Endocrinology 2009; 150:4681-4691.
75. Paulose T, Hernandez-Ochoa I, Basavarajappa MS, Peretz J, Flaws JA. Increased sensitivity of estrogen receptor alpha overexpressing antral follicles to methoxychlor and its metabolites. Toxicol Sci 2011; 120:447-459.
76. Basavarajappa MS, Hernandez-Ochoa I, Wang W, Flaws JA. Methoxychlor inhibits growth and induces atresia through the aryl hydrocarbon receptor pathway in mouse ovarian antral follicles. Reprod Toxicol 2012; 34:16-21.
77. Hites RA. Dioxins: an overview and history. Environ Sci Technol 2011; 45:16-20.
78. Frakes RA, Zeeman CQ, Mower B. Bioaccumulation of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) by fish downstream of pulp and paper mills in Maine. Ecotoxicol Environ Saf 1993; 25:244-252.
79. Tuppurainen K, Asikainen A, Ruokojarvi P, Ruuskanen J. Perspectives on the formation of polychlorinated dibenzo-p-dioxins and dibenzofurans during municipal solid waste (MSW) incineration, and other combustion processes. Acc Chem Res 2003; 36:652-658.
80. Humblet O, Sergeyev O, Altshul L, Korrick SA, Williams PL, Emond C, Birnbaum LS, Burns JS, Lee MM, Revich B, Shelepchikov A, Feshin D, et al. Temporal trends in serum concentrations of polychlorinated dioxins, furans, and PCBs among adult women living in Chapaevsk, Russia: a longitudinal study from 2000 to 2009. Environ Health 2011; 10:62.
81. Ulaszewska MM, Zuccato E, Davoli E. PCDD/Fs and dioxin-like PCBs in human milk and estimation of infants' daily intake: a review. Chemosphere 2011; 83:774-782.
82. Tsutsumi O, Uechi H, Sone H, Yonemoto J, Takai Y, Momoeda M, Tohyama C, Hashimoto S, Morita M, Taketani Y. Presence of dioxins in human follicular fluid: their possible stage-specific action on the development of preimplantation mouse embryos. Biochem Biophys Res Commun 1998; 250:498-501.
83. Karman BN, Basavarajappa MS, Craig ZR, Flaws JA. 2,3,7,8-Tetrachlorodibenzo-p-dioxin activates the aryl hydrocarbon receptor and alters sex steroid hormone secretion without affecting growth of mouse antral follicles in vitro. Toxicol Appl Pharmacol 2012; 261:88-96.
84. Grochowalski A, Pieklo R, Gasinska A, Chrzaszcz R, Gregoraszczuk EL. Accumulation of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in porcine preovulatory follicles after in vitro exposure to TCDD: effects on steroid secretion and cell proliferation. Cytobios 2000; 102:21-31.
85. Heimler I, Trewin AL, Chaffin CL, Rawlins RG, Hutz RJ. Modulation of ovarian follicle maturation and effects on apoptotic cell death in Holtzman rats exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in utero and lactationally. Reprod Toxicol 1998; 12:69-73.
86. Valdez KE, Shi Z, Ting AY, PetroffBK. Effect of chronic exposure to the aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-pdioxin in female rats on ovarian gene expression. Reprod Toxicol 2009; 28:32-37.
87. Hernandez-Ochoa I, Karman BN, Flaws JA. The role of the aryl hydrocarbon receptor in the female reproductive system. Biochem Pharmacol 2009; 77:547-559.
88. Gao X, PetroffBK, Rozman KK, Terranova PF. Gonadotropin-releasing hormone (GnRH) partially reverses the inhibitory effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on ovulation in the immature gonadotropintreated rat. Toxicology 2000; 147:15-22.
89. PetroffBK, Gao X, Rozman KK, Terranova PF. Interaction of estradiol and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in an ovulation model:evidence for systemic potentiation and local ovarian effects. Reprod Toxicol 2000; 14:247-255.
90. Jung NK, Park JY, Park JH, Kim SY, Park JK, Chang WK, Lee HC, Kim SW, Chun SY. Attenuation of cell cycle progression by 2,3,7,8-tetrachlorodibenzo-p-dioxin eliciting ovulatory blockade in gonadotropin- primed immature rats. Endocr J 2010; 57:863-871.
91. Karman BN, Basavarajappa MS, Hannon P, Flaws JA. Dioxin exposure reduces the steroidogenic capacity of mouse antral follicles mainly at the level of HSD17B1 without altering atresia. Toxicol Appl Pharmacol 2012; 264:1-12.
92. Dasmahapatra AK, Wimpee BA, Trewin AL, Wimpee CF, Ghorai JK, Hutz RJ. Demonstration of 2,3,7,8-tetrachlorodibenzo-p-dioxin attenuation of P450 steroidogenic enzyme mRNAs in rat granulosa cell in vitro by competitive reverse transcriptase-polymerase chain reaction assay. Mol Cell Endocrinol 2000; 164:5-18.
93. Gregoraszczuk EL. Dioxin exposure and porcine reproductive hormonal activity. Cad Saude Publica 2002; 18:453-462.
94. Heimler I, Rawlins RG, Owen H, Hutz RJ. Dioxin perturbs, in a doseand time-dependent fashion, steroid secretion, and induces apoptosis of human luteinized granulosa cells. Endocrinology 1998; 139:4373-4379.
95. Huang L, Huang R, Ran XR, Liu HY, Zhang Y, Dai LJ, Li B. Threegeneration experiment showed female C57BL/6J mice drink drainage canal water containing low level of TCDD-like activity causing high pup mortality. J Toxicol Sci 2011; 36:713-724.
96. Chen X, Ma XM, Ma SW, Coenraads PJ, Zhang CM, Liu J, Zhao LJ, Sun M, Tang NJ. Proteomic analysis of the rat ovary following chronic lowdose exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). J Toxicol Environ Health A 2009; 72:717-726.
97. Maranghi F, Tassinari R, Moracci G, Altieri I, Rasinger JD, Carroll TS, Hogstrand C, Lundebye AK, Mantovani A. Dietary exposure of juvenile female mice to polyhalogenated seafood contaminants (HBCD, BDE-47, PCB-153, TCDD): comparative assessment of effects in potential target tissues. Food Chem Toxicol 2013; 56:443-449.
98. Sechman A, Antos P, Katarzynska D, Grzegorzewska A, Wojtysiak D, Hrabia A. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on secretion of steroids and STAR, HSD3B and CYP19A1 mRNA expression in chicken ovarian follicles. Toxicol Lett 2014; 225:264-274.
99. Grochowalski A, Chrzaszcz R, Pieklo R, Gregoraszczuk EL. Estrogenic and antiestrogenic effect of in vitro treatment of follicular cells with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Chemosphere 2001; 43:823-827.
100. Blount BC, Milgram KE, Silva MJ, Malek NA, Reidy JA, Needham LL, Brock JW. Quantitative detection of eight phthalate metabolites in human urine using HPLC-APCI-MS/MS. Anal Chem 2000; 72:4127-4134.
101. Berge A, Cladiere M, Gasperi J, Coursimault A, Tassin B, Moilleron R. Meta-analysis of environmental contamination by phthalates. Environ Sci Pollut Res Int 2013; 20:8057-8076.
102. Hongjun Y, Wenjun X, Qing L, Jingtao L, Hongwen Y, Zhaohua L. Distribution of phthalate esters in topsoil: a case study in the Yellow River Delta, China. Environ Monit Assess 2013; 185:8489-8500.
103. Martine B, Marie-Jeanne T, Cendrine D, Fabrice A, Marc C. Assessment of adult human exposure to phthalate esters in the urban centre of Paris (France). Bull Environ Contam Toxicol 2013; 90:91-96.
104. National Toxicology Program. Di(2-ethylhexyl) phthalate. Rep Carcinog 2011; 12:156-159.
105. Koch HM, Calafat AM. Human body burdens of chemicals used in plastic manufacture. Philos Trans R Soc Lond B Biol Sci 2009; 364:2063-2078.
106. Hannon PR, Peretz J, Flaws JA. Daily exposure to Di(2-ethylhexyl) phthalate alters estrous cyclicity and accelerates primordial follicle recruitment potentially via dysregulation of the phosphatidylinositol 3-kinase signaling pathway in adult mice. Biol Reprod 2014; 90:136.
107. Hannon PR, Brannick KE, Wang W, Flaws JA. Mono(2-ethylhexyl) phthalate accelerates early folliculogenesis and inhibits steroidogenesis in cultured mouse whole ovaries and antral follicle. Biol Reprod 2015;
108. Craig ZR, Hannon PR, Wang W, Ziv-Gal A, Flaws JA. Di-n-butyl phthalate disrupts the expression of genes involved in cell cycle and apoptotic pathways in mouse ovarian antral follicles. Biol Reprod 2013; 88:23.
109. Xu C, Chen JA, Qiu Z, Zhao Q, Luo J, Yang L, Zeng H, Huang Y, Zhang L, Cao J, Shu W. Ovotoxicity and PPAR-mediated aromatase downregulation in female Sprague-Dawley rats following combined oral exposure to benzo[a]pyrene and di-(2-ethylhexyl) phthalate. Toxicol Lett 2010; 199:323-332.
110. Wang W, Craig ZR, Basavarajappa MS, Hafner KS, Flaws JA. Mono-(2-ethylhexyl) phthalate induces oxidative stress and inhibits growth of mouse ovarian antral follicles. Biol Reprod 2012; 87:152.
111. Chen HS, Chiang PH, Wang YC, Kao MC, Shieh TH, Tsai CF, Tsai EM. Benzyl butyl phthalate induces necrosis by AhR mediation of CYP1B1 expression in human granulosa cells. Reprod Toxicol 2012; 33:67-75.
112. Gupta RK, Singh JM, Leslie TC, Meachum S, Flaws JA, Yao HH. Di-(2-ethylhexyl) phthalate and mono-(2-ethylhexyl) phthalate inhibit growth and reduce estradiol levels of antral follicles in vitro. Toxicol Appl Pharmacol 2010; 242:224-230.
113. Hannon PR, Brannick KE, Wang W, Gupta RK, Flaws JA. Di(2-ethylhexyl) phthalate inhibits antral follicle growth, induces atresia, and inhibits steroid hormone production in cultured mouse antral follicles. Toxicol Appl Pharmacol 2015; 284:42-53.
114. Reinsberg J, Wegener-Toper P, van der Ven K, van der Ven H, Klingmueller D. Effect of mono-(2-ethylhexyl) phthalate on steroid production of human granulosa cells. Toxicol Appl Pharmacol 2009; 239:116-123.
115. Inada H, Chihara K, Yamashita A, Miyawaki I, Fukuda C, Tateishi Y, Kunimatsu T, Kimura J, Funabashi H, Miyano T. Evaluation of ovarian toxicity of mono-(2-ethylhexyl) phthalate (MEHP) using cultured rat ovarian follicles. J Toxicol Sci 2012; 37:483-490.
116. Mazur W. Phytoestrogen content in foods. Baillieres Clin Endocrinol Metab 1998; 12:729-742.
117. Khan SI, Zhao J, Khan IA, Walker LA, Dasmahapatra AK. Potential utility of natural products as regulators of breast cancer-associated aromatase promoters. Reprod Biol Endocrinol 2011; 9:91.
118. Andres S, Abraham K, Appel KE, Lampen A. Risks and benefits of dietary isoflavones for cancer. Crit Rev Toxicol 2011; 41:463-506.
119. Reinli K, Block G. Phytoestrogen content of foods-a compendium of literature values. Nutr Cancer 1996; 26:123-148.
120. Yoon K, Kwack SJ, Kim HS, Lee BM. Estrogenic endocrine-disrupting chemicals: molecular mechanisms of actions on putative human diseases. J Toxicol Environ Health B Crit Rev 2014; 17:127-174.
121. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998; 139:4252-4263.
122. Bialesova L, Brtko J, Lenko V, Macejova D. Nuclear receptors-target molecules for isoflavones in cancer chemoprevention. Gen Physiol Biophys 2013; 32:467-478.
123. Medigovic I, Ristic N, Trifunovic S, Manojlovic-Stojanoski M, Milosevic V, Zikic D, Nestorovic N. Genistein affects ovarian folliculogenesis:a stereological study. Microsc Res Tech 2012; 75:1691-1699.
124. Zhuang XL, Fu YC, Xu JJ, Kong XX, Chen ZG, Luo LL. Effects of genistein on ovarian follicular development and ovarian life span in rats. Fitoterapia 2010; 81:998-1002.
125. Wang W, Sun Y, Liu J, Li Y, Li H, Xiao S, Weng S, Zhang W. Soy isoflavones administered to rats from weaning until sexual maturity affect ovarian follicle development by inducing apoptosis. Food Chem Toxicol 2014; 72:51-60.
126. Gregoraszczuk E, Slomczynska M, Stoklosowa S. Effect of genistein, tyrphostin and herbimycin on prolactin-stimulated progesterone production by porcine theca and luteal cells. J Physiol Pharmacol 1999; 50:477-484.
127. Whitehead SA, Cross JE, Burden C, Lacey M. Acute and chronic effects of genistein, tyrphostin and lavendustin A on steroid synthesis in luteinized human granulosa cells. Hum Reprod 2002; 17:589-594.
128. Lacey M, Bohday J, Fonseka SM, Ullah AI, Whitehead SA. Doseresponse effects of phytoestrogens on the activity and expression of 3beta-hydroxysteroid dehydrogenase and aromatase in human granulosaluteal cells. J Steroid Biochem Mol Biol 2005; 96:279-286.
129. Whitehead SA, Lacey M. Protein tyrosine kinase activity of lavendustin A and the phytoestrogen genistein on progesterone synthesis in cultured rat ovarian cells. Fertil Steril 2000; 73:613-619.
130. Haynes-Johnson D, Lai MT, Campen C, Palmer S. Diverse effects of tyrosine kinase inhibitors on follicle-stimulating hormone-stimulated estradiol and progesterone production from rat granulosa cells in serumcontaining medium and serum-free medium containing epidermal growth factor. Biol Reprod 1999; 61:147-153.
131. Rice S, Mason HD, Whitehead SA. Phytoestrogens and their low dose combinations inhibit mRNA expression and activity of aromatase in human granulosa-luteal cells. J Steroid Biochem Mol Biol 2006; 101:216-225.
132. Tiemann U, Schneider F, Vanselow J, Tomek W. In vitro exposure of porcine granulosa cells to the phytoestrogens genistein and daidzein:effects on the biosynthesis of reproductive steroid hormones. Reprod Toxicol 2007; 24:317-325.