Reproductive Biology and Endocrinology | |
Bisphenol a and the female reproductive tract: an overview of recent laboratory evidence and epidemiological studies | |
Massimo Moscarini1  Roberto Marci3  Alberto Mantovani2  Valentina Giovanale1  Maddalena Mallozzi1  Noemi Di Segni1  Donatella Caserta1  | |
[1] Department of Gynecology-Obstetrics and Urological Sciences, “Sapienza”, University of Rome, S. Andrea Hospital, Rome, Italy;Food and Veterinary Toxicology Section, Istituto Superiore di Sanità, Roma, Italy;Department of Biomedical Sciences and Advanced Therapies, Section of Obstetrics and Gynaecology, University of Ferrara, Ferrara, Italy | |
关键词: Genital tract; Reproductive health; Fertility; Endocrine disruptors; Bisphenol A; | |
Others : 804260 DOI : 10.1186/1477-7827-12-37 |
|
received in 2014-01-31, accepted in 2014-05-01, 发布年份 2014 | |
【 摘 要 】
Bisphenol A (BPA) is a high production volume monomer used for making a wide variety of polycarbonate plastics and resins. A large body of evidence links BPA to endocrine disruption in laboratory animals, and a growing number of epidemiological studies support a link with health disorders in humans. The aim of this review is to summarize the recent experimental studies describing the effects and mechanisms of BPA on the female genital tract and to compare them to the current knowledge regarding the impact of BPA impact on female reproductive health. In particular, BPA has been correlated with alterations in hypothalamic-pituitary hormonal production, reduced oocyte quality due to perinatal and adulthood exposure, defective uterine receptivity and the pathogenesis of polycystic ovary syndrome. Researchers have reported conflicting results regarding the effect of BPA on premature puberty and endometriosis development. Experimental studies suggest that BPA’s mechanism of action is related to life stage and that its effect on the female reproductive system may involve agonism with estrogen nuclear receptors as well as other mechanisms (steroid biosynthesis inhibition). Notwithstanding uncertainties and knowledge gaps, the available evidence should be seen as a sufficient grounds to take precautionary actions against excess exposure to BPA.
【 授权许可】
2014 Caserta et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20140708055442894.pdf | 261KB | download |
【 参考文献 】
- [1]Gregoraszczuk EL, Ptak A: Endocrine-Disrupting Chemicals: Some Actions of POPs on Female Reproduction. Int J Endocrinol 2013, 2013:828532.
- [2]Richter CA, Birnbaum LS, Farabollini F, Newbold RR, Rubin BS, Talsness CE, Vandenbergh JG, Walser-Kuntz DR, Vom Saal FS: In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol 2007, 24:199-224.
- [3]Rubin BS: Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol 2011, 127:27-34.
- [4]Caserta D, Mantovani A, Marci R, Fazi A, Ciardo F, La Rocca C, Maranghi F, Moscarini M: Environment and women's reproductive health. Human Reprod Update 2011, 17:418-33.
- [5]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(2):178-98.
- [6]Alonso-Magdalena P, Laribi O, Ropero AB, Fuentes E, Ripoll C, Soria B, Nadal A: Low doses of bisphenol A and diethylstilbestrol impair Ca2+ signals in pancreatic alpha-cells through a nonclassical membrane estrogen receptor within intact islets of Langerhans. Environ Health Perspect 2005, 113:969-77.
- [7]Cabaton NJ, Wadia PR, Rubin BS, Zalko D, Schaeberle CM, Askenase MH, Gadbois JL, Tharp AP, Whitt GS, Sonnenschein C, Soto AM: Perinatal exposure to environmentally relevant levels of bisphenol A decreases fertility and fecundity in CD-1 mice. Environ Health Perspect 2011, 119(4):547-52.
- [8]Maffini MV, Rubin BS, Sonnenschein C, Soto AM: Endocrine disruptors and reproductive health: the case of bisphenol-A. Mol Cell Endocrinol. 2006, 254–255:179-86.
- [9]Nah WH, Park MJ, Gye MC: Effects of early prepubertal exposure to bisphenol A on the onset of puberty, ovarian weights, and estrous cycle in female mice. Clin Exp Reprod Med 2011, 38:75-81.
- [10]Ehrlich S, Williams PL, Missmer SA, Flaws JA, Ye X, Calafat AM, Petrozza JC, Wright D, Hauser R: Urinary bisphenol A concentrations and early reproductive health outcomes among women undergoing IVF. Hum Reprod 2012, 27:3583-92.
- [11]Caserta D, Ciardo F, Bordi G, Guerranti C, Fanello E, Perra G, Borghini F, La Rocca C, Tait S, Bergamasco B, Stecca L, Marci R, Lo Monte G, Soave I, Focardi S, Mantovani A, Moscarini M: Correlation of endocrine disrupting chemicals serum levels and white blood cells gene expression of nuclear receptors in a population of infertile women. Int J Endocrinol 2013, 2013:510703.
- [12]Rochester JR: Bisphenol A and human health: A review of the literature. Reprod Toxicol 2013, 42:132-55.
- [13]Cantonwine DE, Hauser R, Meeker JD: Bisphenol A and Human Reproductive Health. Expert Rev Obstet Gynecol 2013, 8(4):329-335.
- [14]Balabanič D, Rupnik M, Klemenčič AK: Negative impact of endocrine-disrupting compounds on human reproductive health. Reprod Fertil Dev. 2011, 23:403-16.
- [15]Talsness CE, Andrade AJ, Kuriyama SN, Taylor JA, Vom Saal FS: Components of plastic: experimental studies in animals and relevance for human health. Philos Trans R Soc Lond B Biol Sci 2009, 27:2079-96.
- [16]Monje L, Varayoud J, Munoz-de-toro M, Luque EH, Ramos JG: Exposure of neonatal female rats to bisphenol A disrupt hypothalamic LHRH pre-mRNA processing and estrogen receptor alpha expression in nuclei controlling estrous cyclicity. Reprod Toxicol 2010, 30:625-34.
- [17]Patisaul HB, Fortino AE, Polston EK: Neonatal ginestein or bisphenol-A exposure alters sexual differentiation of the AVPV. Neurotoxicol Teratol 2006, 28:111-118.
- [18]Rubin BS, Lenkowski JR, Schaeberle CM, Vandenberg LN, Ronsheim PM, Soto AM: Evidence of altered brain sexual differentiation in mice exposed perinatally to low environmentally relevant levels of bisphenol A. Endocrinology 2006, 147:3681-3691.
- [19]Wolstenholme JT, Rissman EF, Connelly JJ: The role of Bisphenol A in shaping the brain, epigenome and behavior. Horm Behav 2011, 59:296-305.
- [20]Kundakovic M, Gudsnuk K, Franks B, Madrid J, Miller RL, Perera FP, Champagne FA: Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure. Proc Natl Acad Sci U S A 2013, 110(24):9956-61.
- [21]Fernandez M, Bianchi M, Lux-Lantos V, Libertun C: Neonatal exposure to bisphenol A alters reproductive parameters and gonadotropin releasing hormone signalling in female rats. Environ Health perspect 2009, 117:757-762.
- [22]Maranghi F, Mantovani A: Targeted toxicological testing to investigate the role of endocrine disrupters in puberty disorders. Reproductive Toxicology 2012, 33:290-6.
- [23]Navarro VM, Sánchez-Garrido MA, Castellano JM, Roa J, García-Galiano D, Pineda R, Aguilar E, Pinilla L, Tena-Sempere M: Persistent impairment of hypothalamic KiSS-1 system after exposures to estrogenic compounds at critical periods of brain sex differentiation. Endocrinology 2009, 150:2359-67.
- [24]Bai Y, Chang F, Zhou R, Jin PP, Matsumoto H, Sokabe M, Chen L: Increase of anteroventral periventricular kisspeptin neurons and generation of E2-induced LH-surge system in male rats exposed perinatally to environmental dose of bisphenol-A. Endocrinology 2011, 152:1562-71.
- [25]Xi W, Lee CK, Yeung WS, Giesy JP, Wong MH, Zhang X, Hecker M, Wong CK: Effect of perinatal and postnatal bisphenol A exposure to the regulatory circuits at the hypothalamus-pituitary-gonadal axis of CD-1 mice. Reprod Toxicol 2011, 31:409-17.
- [26]Wolff MS, Britton JA, Boguski L, Hochman S, Maloney N, Serra N, Liu Z, Berkowitz G, Larson S, Forman J: Environmental exposures and puberty in inner-city girls. Environ Res 2008, 107:393-400.
- [27]Qiao L, Zheng L, Cai D: Study on the levels of bisphenol A, octylphenol, 4-nonylphenol in serum of precocious girls. Wei Sheng Yan Jiu 2010, 39:9-12.
- [28]Doerge DR, Twaddle NC, Vanlandingham M, Fisher JW: Pharmacokinetics of bisphenol in neonatal and adult CD-1 mice: inter-species comparisons with Sprague–Dawley rats and rhesus monkeys. Toxicol Lett 2011, 207:298-305.
- [29]Zhang HQ, Zhang XF, Zhang LJ, Chao HH, Pan B, Feng YM, Li L, Sun XF, Shen W: Fetal exposure to bisphenol A affects the primordial follicle formation by inhibiting the meiotic progression of oocytes. Mol Biol Rep 2012, 39:5651-7.
- [30]Hunt PA, Lawson C, Gieske M, Murdoch B, Smith H, Marre A, Hassold T, VandeVoort CA: Bisphenol A alters early oogenesis and follicle formation in the fetal ovary of the rhesus monkey. Proc Natl Acad Sci USA 2012, 109:17525-30.
- [31]Susiarjo M, Hassold TJ, Freeman E, Hunt PA: Bisphenol A exposure in utero disrupts early oogenesis in the mouse. PLos Genet 2007, 12:3.
- [32]Rivera OE, Varayoud J, Rodríguez HA, Muñoz-de-Toro M, Luque EH: Neonatal exposure to bisphenol A or diethylstilbestrol alters the ovarian follicular dynamics in the lamb. Reprod Toxicol 2011, 32:304-12.
- [33]Karavan JR, Pepling ME: Effects of estrogenic compounds on neonatal oocyte development. Reprod Toxicol 2012, 34:51-6.
- [34]Lawson C, Gieske M, Murdoch B, Ye P, Li Y, Hassold T, Hunt PA: Gene expression in the fetal mouse ovary is altered by exposure to low doses of bisphenol A. Biol Reprod 2011, 84:79-86.
- [35]Rodríguez HA, Santambrosio N, Santamaría CG, Muñoz-de-Toro M, Luque EH: Neonatal exposure to bisphenol A reduces the pool of primordial follicles in the rat ovary. Reprod Toxicol 2010, 30(4):550-7.
- [36]Chao HH, Zhang XF, Chen B, Pan B, Zhang LJ, Li L, Sun XF, Shi QH, Shen W: Bisphenol A exposure modifies methylation of imprinted genes in mouse oocytes via the estrogen receptor signaling pathway. Histochem Cell Biol 2012, 137:249-59.
- [37]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 17β-estradiol synthesis via downregulation of aromatase in rat ovary. Environ Health Perspect 2013, 121:663-9.
- [38]Peretz J, Gupta RK, Singh J, Hernandez-Ochoa I, Flaws JA: Bisphenol A impairs follicle growth, inhibits steroidogenesis, and downregulates rate-limiting enzymes in the estradiol biosynthesis pathway. Toxicol Sci 2011, 119:209-17.
- [39]Grasselli F, Baratta L, Baioni L, Bussolati S, Ramoni R, Grolli S, Basini G: Bisphenol A disrupts granulosa cell function. Domest Anim Endocrinol 2010, 39:34-9.
- [40]Romani F, Tropea A, Scarinci E, Dello Russo C, Lisi L, Catino S, Lanzone A, Apa R: Endocrine disruptors and human corpus luteum: in vitro effects of phenols on luteal cells function. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 2013, 31:170-80.
- [41]Dominguez MA, Petre MA, Neal MS, Foster WG: Bisphenol A concentration-dependently increases human granulosa-lutein cell matrix metalloproteinase-9 (MMP-9) enzyme output. Reprod Toxicol 2008, 25:420-5.
- [42]Brieño-Enríquez MA, Reig-Viader R, Cabero L, Toran N, Martínez F, Roig I, Garcia Caldés M: Gene expression is altered after bisphenol A exposure in human fetal oocytes in vitro. Mol Human Reprod 2012, 18:171-83.
- [43]Machtinger R, Combelles CM, Missmer SA, Correia KF, Williams P, Hauser R, Racowsky C: Bisphenol-A and human oocyte maturation in vitro. Human Reprod 2013, 28:2735-45.
- [44]Bloom MS, Kim D, Vom Saal FS, Taylor JA, Cheng G, Lamb JD, Fujimoto VY: Bisphenol A exposure reduces the estradiol response to gonadotropin stimulation during in vitro fertilization. Fertil Steril 2011, 96(3):672-677.
- [45]Caserta D, Bordi G, Ciardo F, Marci R, La Rocca C, Tait S, Bergamasco B, Stecca L, Mantovani A, Guerranti C, Fanello EL, Perra G, Borghini F, Focardi SE, Moscarini M: The influence of endocrine disruptors in a selected population of infertile women. Gynecol Endocrinol 2013, 29:444-7.
- [46]Sugiura-Ogasawara M, Ozaki Y, Sonta S, Makino T, Suzumori K: Exposure to bisphenol A is associated with recurrent miscarriage. Hum Reprod 2005, 20(8):2325-9.
- [47]Zheng YM, Wang Y, Zhao J, Dai YH, Luo XM, Shen ZJ, Chen X, Yuan W, Shen YP: Association between serum bisphenol-A and recurrent spontaneous abortion: a 1:2 case–control study, China [abstract]. Zhonghua Liu Xing Bing Xue Za Zhi 2012, 33(8):841-5.
- [48]Mendoza-Rodríguez CA, García-Guzmán M, Baranda-Avila N, Morimoto S, Perrot-Applanat M, Cerbón M: Administration of bisphenol A to dams during perinatal period modifies molecular and morphological reproductive parameters of the offspring. Reprod Toxicol 2011, 31:177-83.
- [49]Aghajanova L, Giudice LC: Effect of bisphenol A on human endometrial stromal fibroblasts in vitro. Reprod Biomed Online 2011, 22:249-56.
- [50]Bredhult C, Sahlin L, Olovsson M: Gene expression analysis of human endometrial endothelial cells exposed to Bisphenol A. Reprod Toxicol 2009, 28:18-25.
- [51]Newbold RR, Jefferson WN, Padilla-Banks E: Prenatal exposure to bisphenol a at environmentally relevant doses adversely affects the murine female reproductive tract later in life. Environ Health Perspect 2009, 117:879-85.
- [52]Hiroi H, Tsutsumi O, Takeuchi T, Momoeda M, Ikezuki Y, Okamura A, Yokota H, Taketani Y: Differences in serum bisphenol a concentrations in premenopausal normal women and women with endometrial hyperplasia. Endocr J 2004, 51:595-600.
- [53]Varayoud J, Ramos JG, Bosquiazzo VL, Lower M, Muñoz-de-Toro M, Luque EH: Neonatal exposure to bisphenol A alters rat uterine implantation-associated gene expression and reduces the number of implantation sites. Endocrinology 2011, 152:1101-11.
- [54]Bromer JG, Zhou Y, Taylor MB, Doherty L, Taylor HS: Bisphenol-A exposure in utero leads to epigenetic alterations in the developmental programming of uterine estrogen response. FASEB J 2010, 24:2273-80.
- [55]Xiao S, Diao H, Smith MA, Song X, Ye X: Preimplantation exposure to bisphenol A (BPA) affects embryo transport, preimplantation embryo development, and uterine receptivity in mice. Reprod Toxicol 2011, 32:434-41.
- [56]Ehrlich S, Williams PL, Missmer SA, Flaws JA, Berry KF, Calafat AM, Ye X, Petrozza JC, Wright D, Hauser R: Urinary bisphenol A concentrations and implantation failure among women undergoing in vitro fertilization. Environ Health Perspect 2012, 120:978-83.
- [57]Tarantino G, Valentino R, Di Somma C, D'Esposito V, Passaretti F, Pizza G, Brancato V, Orio F, Formisano P, Colao A, Savastano S: Bisphenol A in polycystic ovary syndrome and its association with liver-spleen axis. Clin Endocrinol 2013, 78:447-53.
- [58]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, 96:480-4.
- [59]Fernández M, Bourguignon N, Lux-Lantos V, Libertun C: Neonatal exposure to bisphenol a and reproductive and endocrine alterations resembling the polycystic ovarian syndrome in adult rats. Environ Health Perspect 2010, 118:1217-22.
- [60]Missmer SA, Hankinson SE, Spiegelman D, Barbieri RL, Michels KB, Hunter DJ: In utero exposure and the incidence of endometriosis. Fertil Steril 2004, 82:1501-1508.
- [61]Signorile PG, Spugnini EP, Mita L, Mellone P, D’Avino A, Bianco M, Diano N, Caputo L, Rea F, Viceconte R, Portaccio M, Viggiano E, Citro G, Pierantoni R, Sica V, Vincenzi B, Mita DG, Baldi F, Baldi A: Pre-natal exposure of mice to bisphenol A elicits an endometriosis-likephenotype in female offspring. Gen Comp Endocrinol 2010, 168:318-25.
- [62]Cobellis L, Colacurci N, Trabucco E, Carpentiero C, Grumetto L: Measurement of bisphenol A and bisphenol B levels in human blood sera from healthy and endometriotic women. Biomed Chromatogr 2009, 23:1186-90.
- [63]Buck Louis GM, Peterson CM, Chen Z, Croughan M, Sundaram R, Stanford J, Varner MW, Kennedy A, Giudice L, Fujimoto VY, Sun L, Wang L, Guo Y, Kannan K: Bisphenol A and phthalates and endometriosis: the Endometriosis: Natural History, Diagnosis and Outcomes Study. Fertil Ster 2013, 100:162-9.
- [64]Itoh H, Iwasaki M, Hanaoka T, Sasaki H, Tanaka T, Tsugane S: Urinary bisphenol-A concentration in infertile Japanese women and its association with endometriosis: A cross-sectional study. Environ Health Prev Med 2007, 12:258-64.