Effect of bisphenol-A (BPA) on placental biomarkers for inflammation, neurodevelopment and oxidative stress

Journal of Perinatal Medicine - Tập 47 Số 7 - Trang 741-749 - 2019
Yuko Arita1, Hyeon Jeong Park1, Aisling Cantillon1, Darios Getahun2, Ramkumar Menon3, Morgan R. Peltier1,4
1Department of Foundations of Medicine, NYU-Long Island School of Medicine , Mineola, NY , USA
2Department of Research and Evaluation , Kaiser-Permanente Southern California , Pasadena, CA , USA
3Department of Obstetrics and Gynecology, UTMB-Galveston, Galveston, TX, USA
4Department of Obstetric and Gynecology, NYU-Winthrop Hospital, 101 Mineola Blvd Rm. 4-040 , Mineola, NY , USA

Tóm tắt

Abstract Background Bisphenol-A (BPA) is a widespread pollutant whose effects on pregnant women are poorly understood. Therefore, we investigated the effects of BPA on basal and bacteria-stimulated production of proinflammatory cytokines [interleukin (IL)-1β, tumor necrosis factor-α (TNF-α) and IL-6], anti-inflammatory mediators [soluble glycoprotein 130 (sgp) 130, heme oxidase-1 (HO-1) and IL-10] and biomarkers for neurodevelopment [brain-derived neurotrophic factor (BDNF)], and oxidative stress [8-isoprostane (8-IsoP)] by the placenta. Methods Placental explant cultures were treated with BPA (0–10,000 nM) in the presence or absence of 107 colony-forming unit (CFU)/mL heat-killed Escherichia coli for 24 h. Biomarker concentrations in conditioned medium were quantified by the enzyme-linked immunosorbent assay (ELISA). Results Under basal conditions, IL-1β and IL-6 production was enhanced by BPA in a dose-dependent manner. Sgp130, a soluble receptor that reduces IL-6 bioactivity, was suppressed by BPA at 1000–10,000 nM. BPA also enhanced BDNF production at 1000 and 10,000 nM, and 8-IsoP expression at 10 and 100 nM. For bacteria-treated cultures, BPA increased IL-6 production at 100 nM and reduced sgp130 at 1000 nM but had no effect on IL-1β, TNF-α, BDNF, HO-1, 8-IsoP or IL-10 production. Conclusion BPA may increase placental inflammation by promoting IL-1β and IL-6 but inhibiting sgp130. It may also disrupt oxidative balance and neurodevelopment by increasing 8-IsoP and BDNF production.

Từ khóa


Tài liệu tham khảo

Schecter A, Malik N, Haffner D, Smith S, Harris TR, Paepke O, et al. Bisphenol A (BPA) in U.S. food. Environ Sci Technol 2010;44: 9425–30.

Troisi J, Mikelson C, Richards S, Symes S, Adair D, Zullo F, et al. Placental concentrations of bisphenol A and birth weight from births in the Southeastern U.S. Placenta 2014;35:947–52.

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:A703–7.

Cao XL, Zhang J, Goodyer CG, Hayward S, Cooke GM, Curran IH. Bisphenol A in human placental and fetal liver tissues collected from Greater Montreal area (Quebec) during 1998–2008. Chemosphere 2012;89:505–11.

Zhang J, Cooke GM, Curran IH, Goodyer CG, Cao XL. GC-MS analysis of bisphenol A in human placental and fetal liver samples. J Chromatogr B Analyt Technol Biomed Life Sci 2011;879:209–14.

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;17:2839–41.

Cantonwine D, Meeker JD, Hu H, Sanchez BN, Lamadrid-Figueroa H, Mercado-Garcia A, et al. Bisphenol a exposure in Mexico City and risk of prematurity: a pilot nested case control study. Environ Health 2010;9:62.

Behnia F, Peltier M, Getahun D, Watson C, Saade G, Menon R. High bisphenol A (BPA) concentration in the maternal, but not fetal, compartment increases the risk of spontaneous preterm delivery. J Matern Fetal Neonatal Med 2016;29:3583–9.

Chou WC, Chen JL, Lin CF, Chen YC, Shih FC, Chuang CY. Biomonitoring of bisphenol A concentrations in maternal and umbilical cord blood in regard to birth outcomes and adipokine expression: a birth cohort study in Taiwan. Environ Health 2011;10:94.

Leclerc F, Dubois MF, Aris A. Maternal, placental and fetal exposure to bisphenol A in women with and without preeclampsia. Hypertens Pregnancy 2014;33:341–8.

de Cock M, Maas YG, van de Bor M. Does perinatal exposure to endocrine disruptors induce autism spectrum and attention deficit hyperactivity disorders? Review. Acta Paediatr 2012;101:811–8.

Arita Y, Yeh C, Thoma T, Getahun D, Menon R, Peltier MR. Effect of polybrominated diphenyl ether congeners on placental cytokine production. J Reprod Immunol 2018;125:72–9.

Behnia F, Peltier MR, Saade GR, Menon R. Environmental pollutant polybrominated diphenyl ether, a flame retardant, induces primary amnion cell senescence. Am J Reprod Immunol 2015;74:398–406.

Tetz LM, Aronoff DM, Loch-Caruso R. Mono-ethylhexyl phthalate stimulates prostaglandin secretion in human placental macrophages and THP-1 cells. Reprod Biol Endocrinol 2015;13:56.

Arita Y, Kirk M, Gupta N, Menon R, Getahun D, Peltier MR. Effects of tributyltin on placental cytokine production. J Perinat Med 2018;46:867–75.

Peltier MR, Arita Y, Klimova NG, Gurzenda EM, Koo HC, Murthy A, et al. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) enhances placental inflammation. J Reprod Immunol 2013;98:10–20.

Peltier MR. Immunology of term and preterm labor. Reprod Biol Endocrinol 2003;1:122.

Hsiao EY, Patterson PH. Placental regulation of maternal-fetal interactions and brain development. Dev Neurobiol 2012;72:1317–26.

Alizadeh M, Ota F, Hosoi K, Kato M, Sakai T, Satter MA. Altered allergic cytokine and antibody response in mice treated with Bisphenol A. J Med Invest 2006;53:70–80.

Youn JY, Park HY, Lee JW, Jung IO, Choi KH, Kim K, et al. Evaluation of the immune response following exposure of mice to bisphenol A: induction of Th1 cytokine and prolactin by BPA exposure in the mouse spleen cells. Arch Pharm Res 2002;25:946–53.

Watanabe H, Adachi R, Kusui K, Hirayama A, Kasahara T, Suzuki K. Bisphenol A significantly enhances the neutrophilic differentiation of promyelocytic HL-60 cells. Int Immunopharmacol 2003;3:1601–8.

Lee MH, Chung SW, Kang BY, Park J, Lee CH, Hwang SY, et al. Enhanced interleukin-4 production in CD4+ T cells and elevated immunoglobulin E levels in antigen-primed mice by bisphenol A and nonylphenol, endocrine disruptors: involvement of nuclear factor-AT and Ca2+. Immunology 2003;109:76–86.

Sugita-Konishi Y, Shimura S, Nishikawa T, Sunaga F, Naito H, Suzuki Y. Effect of Bisphenol A on non-specific immunodefenses against non-pathogenic Escherichia coli. Toxicol Lett 2003;136:217–27.

Savastano S, Tarantino G, D’Esposito V, Passaretti F, Cabaro S, Liotti A, et al. Bisphenol-A plasma levels are related to inflammatory markers, visceral obesity and insulin-resistance: a cross-sectional study on adult male population. J Transl Med. 2015;13:169.

Stein TP, Schluter MD, Steer RA, Guo L, Ming X. Bisphenol A exposure in children with autism spectrum disorders. Autism Res 2015;8:272–83.

Couleau N, Falla J, Beillerot A, Battaglia E, D’Innocenzo M, Plancon S, et al. Effects of endocrine disruptor compounds, alone or in combination, on human macrophage-like THP-1 cell Response. PLoS One 2015;10:e0131428.

Liu Y, Mei C, Liu H, Wang H, Zeng G, Lin J, et al. Modulation of cytokine expression in human macrophages by endocrine-disrupting chemical Bisphenol-A. Biochem Biophys Res Commun 2014;451:592–8.

Ben-Jonathan N, Hugo ER, Brandebourg TD. Effects of bisphenol A on adipokine release from human adipose tissue: implications for the metabolic syndrome. Mol Cell Endocrinol 2009;304:49–54.

Zhu J, Jiang L, Liu Y, Qian W, Liu J, Zhou J, et al. MAPK and NF-kappaB pathways are involved in bisphenol A-induced TNF-alpha and IL-6 production in BV2 microglial cells. Inflammation 2015;38:637–48.

Romero R, Sepulveda W, Kenney JS, Archer LE, Allison AC, Sehgal PB. Interleukin 6 determination in the detection of microbial invasion of the amniotic cavity. Ciba Found Symp 1992;167:205–20; discussion 20–3.

Yoshimura K, Hirsch E. Interleukin-6 is neither necessary nor sufficient for preterm labor in a murine infection model. J Soc Gynecol Investig 2003;10:423–7.

Smith SE, Li J, Garbett K, Mirnics K, Patterson PH. Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci 2007;27:10695–702.

Jang YJ, Park HR, Kim TH, Yang WJ, Lee JJ, Choi SY, et al. High dose bisphenol A impairs hippocampal neurogenesis in female mice across generations. Toxicology 2012;296:73–82.

Acconcia F, Pallottini V, Marino M. Molecular mechanisms of action of BPA. Dose Response 2015;13:1559325815610582.

Hiroi H, Tsutsumi O, Momoeda M, Takai Y, Osuga Y, Taketani Y. Differential interactions of bisphenol A and 17beta-estradiol with estrogen receptor alpha (ERalpha) and ERbeta. Endocr J 1999;46:773–8.

Sui Y, Ai N, Park SH, Rios-Pilier J, Perkins JT, Welsh WJ, et al. Bisphenol A and its analogues activate human pregnane X receptor. Environ Health Perspect 2012;120:399–405.

Ferguson KK, Cantonwine DE, McElrath TF, Mukherjee B, Meeker JD. Repeated measures analysis of associations between urinary bisphenol-A concentrations and biomarkers of inflammation and oxidative stress in pregnancy. Reprod Toxicol 2016;66:93–8.

Watkins DJ, Ferguson KK, Anzalota Del Toro LV, Alshawabkeh AN, Cordero JF, Meeker JD. Associations between urinary phenol and paraben concentrations and markers of oxidative stress and inflammation among pregnant women in Puerto Rico. Int J Hyg Environ Health 2015;218:212–9.

Hong CC, Shimomura-Shimizu M, Muroi M, Tanamoto K. Effect of endocrine disrupting chemicals on lipopolysaccharide-induced tumor necrosis factor-alpha and nitric oxide production by mouse macrophages. Biol Pharm Bull 2004;27:1136–9.

Teixeira D, Marques C, Pestana D, Faria A, Norberto S, Calhau C, et al. Effects of xenoestrogens in human M1 and M2 macrophage migration, cytokine release, and estrogen-related signaling pathways. Environ Toxicol 2016;31:1496–509.