1. bookVolume 54 (2020): Issue 4 (October 2020)
Journal Details
License
Format
Journal
eISSN
1336-0329
First Published
30 Mar 2016
Publication timeframe
4 times per year
Languages
English
access type Open Access

Effect of selected bisphenol derivatives on nuclear receptor expression in ovarian cell line COV434

Published Online: 24 Nov 2020
Volume & Issue: Volume 54 (2020) - Issue 4 (October 2020)
Page range: 275 - 283
Journal Details
License
Format
Journal
eISSN
1336-0329
First Published
30 Mar 2016
Publication timeframe
4 times per year
Languages
English
Abstract

Objectives. Bisphenol A (BPA), as an indispensable plastic additive, has also been proven as an endocrine disruptor associated with adverse health effects including impaired ovarian function and cancer. Due to the restrictions of its usage, several analogs have been employed to replace BPA. Although many studies revealed a harmfulness in the biological effects of BPA analogs, their specific targets remain largely unknown. Nuclear receptors (NRs) may be one of the most important targets of bisphenols. Therefore, in this study, our attention was directed to explore the effect of BPA and its analogs, AF and S, on the mRNA expression of selected NRs involved in the steroidogenic and carcinogenic pathways in the human granulosa cell line COV434. The NRs investigated included: thyroid hormone receptor α (THRA), peroxisome proliferator activating receptor β/δ (PPARD), retinoid X receptor α (RXRA), chicken ovalbumin upstream promoter-transcription factor II (COUPTFII), nuclear receptor-related protein 1 (NURR1), and liver receptor homolog-1 (LRH1).

Methods. COV434 cells were treated with the bisphenols at the concentrations of 10−9 M, 10−7 M, and 10−5 M, and after 24 and 48 h, cell viability was monitored by the MTS assay and gene expressions were analyzed using RT-qPCR.

Results. Bisphenol treatment did not alter the COV434 cell viability. After 24 h, the expression of neither of the NRs was changed. Likewise, after 48 h, the expression of the selected genes was not altered. However, both BPAF and BPS increased, at the highest concentration (10−5 M) used, the mRNA levels of both PPARD and NURR1 NRs after 48 h of the treatment. In the BPA-treated groups, no significant upregulation was observed.

Conclusions. In the present study, the effect of bisphenols on COUP-TFII, Nurr1, and LRH-1 NRs was investigated for the first time. Although generally we did not observe that BPs provoked any alterations in the expression of the selected NRs in COV434 cells, at specific concentrations and time points they might alter mRNA expression of certain NRs (NURR1, PPARD).

Keywords

Alexiadis M, Eriksson N, Jamieson S, Davis M, Drummond AE, Chu S, Clyne CD, Muscat GE, Fuller PJ. Nuclear receptor profiling of ovarian granulosa cell tumors. Horm Cancer 2, 157–169, 2011.10.1007/s12672-011-0069-321761343Search in Google Scholar

Bassett MH, Suzuki T, Sasano H, De Vries CJ, Jimenez PT, Carr BR, Rainey WE. The orphan nuclear receptor NGFIB regulates transcription of 3beta-hydroxysteroid dehydrogenase. Implications for the control of adrenal functional zonation. J Biol Chem 279, 37622–37630, 2004.10.1074/jbc.M40543120015208301Search in Google Scholar

Beard JA, Tenga A, Chen T. The interplay of NR4A receptors and the oncogene-tumor suppressor networks in cancer. Cell Signal 27, 257–266, 2015.10.1016/j.cellsig.2014.11.009427644125446259Search in Google Scholar

Cao Y, Qu X, Ming Z, Yao Y, Zhang Y. The correlation between exposure to BPA and the decrease of the ovarian reserve. Int J Clin Exp Pathol 11, 3375–3382, 2018.Search in Google Scholar

Castellini C, Totaro M, Parisi A, D’Andrea S, Lucente L, Cordeschi G, Francavilla S, Francavilla F, Barbonetti A. Bisphenol A and Male Fertility: Myths and Realities. Front Endocrinol (Lausanne) 11, 353, 2020.10.3389/fendo.2020.00353730433732595601Search in Google Scholar

Castillo Sanchez R, Gomez R, Perez Salazar E. Bisphenol A induces migration through a GPER-, FAK-, Src-, and ERK2-dependent pathway in MDA-MB-231 breast cancer cells. Chem Res Toxicol 29, 285–295, 2016.10.1021/acs.chemrestox.5b0045726914403Search in Google Scholar

Chand AL, Pathirage N, Lazarus K, Chu S, Drummond AE, Fuller PJ, Clyne CD. Liver receptor homologue-1 expression in ovarian epithelial and granulosa cell tumours. Steroids 78, 700–706, 2013.10.1016/j.steroids.2013.03.00123537609Search in Google Scholar

Chen D, Kannan K, Tan H, Zheng Z, Feng YL, Wu Y, Widelka M. Bisphenol analogues other than BPA: environmental occurrence, human exposure, and toxicity-a review. Environ Sci Technol 50, 5438–5453, 2016.10.1021/acs.est.5b0538727143250Search in Google Scholar

Ciucci A, Ferrandina G, Mascilini F, Filippetti F, Scambia G, Zannoni GF, Gallo D. Estrogen receptor β: Potential target for therapy in adult granulosa cell tumors? Gynecol Oncol 150, 158–165, 2018.10.1016/j.ygyno.2018.05.01329786517Search in Google Scholar

Ditsch N, Heublein S, Jeschke U, Sattler C, Kuhn C, Hester A, Czogalla B, Trillsch F, Mahner S, Engel J, Mayr D, Schmoeckel E. Cytoplasmic versus nuclear THR alpha expression determines survival of ovarian cancer patients. J Cancer Res Clin Oncol 146, 1923–1932, 2020.10.1007/s00432-020-03241-7732441532533406Search in Google Scholar

Gerona RR, Pan J, Zota AR, Schwartz JM, Friesen M, Taylor JA, Hunt PA, Woodruff TJ. Direct measurement of Bisphenol A (BPA), BPA glucuronide and BPA sulfate in a diverse and low-income population of pregnant women reveals high exposure, with potential implications for previous exposure estimates: a cross-sectional study. Environ Health 15, 50, 2016.10.1186/s12940-016-0131-2482888827071747Search in Google Scholar

Gorowska-Wojtowicz E, Duliban M, Kudrycka M, Dutka P, Pawlicki P, Milon A, Zarzycka M, Placha W, Kotula-Balak M, Ptak A, Wolski JK, Bilinska B. Leydig cell tumorigenesis - implication of G-protein coupled membrane estrogen receptor, peroxisome proliferator-activated receptor and xenoestrogen exposure. In vivo and in vitro appraisal. Tissue Cell 61, 51–60, 2019.10.1016/j.tice.2019.08.00131759407Search in Google Scholar

Grimaldi M, Boulahtouf A, Toporova L, Balaguer P. Functional profiling of bisphenols for nuclear receptors. Toxicology 420, 39–45, 2019.10.1016/j.tox.2019.04.00330951782Search in Google Scholar

Hui L, Li H, Lu G, Chen Z, Sun W, Shi Y, Fu Z, Huang B, Zhu X, Lu W, Xia D, Wu Y. Low dose of bisphenol A modulates ovarian cancer gene expression profile and promotes epithelial to mesenchymal transition via canonical Wnt pathway. Toxicol Sci 164, 527–538, 2018.10.1093/toxsci/kfy10729718440Search in Google Scholar

Hunakova L, Macejova D, Toporova L, Brtko J. Anticancer effects of tributyltin chloride and triphenyltin chloride in human breast cancer cell lines MCF-7 and MDA-MB-231. Tumour Biol 37, 6701–6708, 2016.10.1007/s13277-015-4524-626662104Search in Google Scholar

Inoue T, Kohro T, Tanaka T, Kanki Y, Li G, Poh HM, Mimura I, Kobayashi M, Taguchi A, Maejima T, Suehiro J, Sugiyama A, Kaneki K, Aruga H, Dong S, Stevens JF, Yamamoto S, Tsutsumi S, Fujita T, Ruan X, Aburatani H, Nangaku M, Ruan Y, Kodama T, Wada Y. Cross-enhancement of ANGPTL4 transcription by HIF1 alpha and PPAR beta/delta is the result of the conformational proximity of two response elements. Genome Biol, 15, R63, 2014.10.1186/gb-2014-15-4-r63405374924721177Search in Google Scholar

Kulus M, Kranc W, Sujka-Kordowska P, Celichowski P, Konwerska A, Jankowski M, Jeseta M, Skowronski MT, Piotrowska-Kempisty H, Bukowska D, Zabel M, Bruska M, Mozdziak P, Kempisty B, Antosik P. Transcriptomic analysis of expression of genes regulating cell cycle progression in porcine ovarian granulosa cells during short-term in vitro primary culture. Histochem Cell Biol 153, 397–412, 2020.10.1007/s00418-020-01860-2729992632157392Search in Google Scholar

Lammel Lindemann JA, Angajala A, Engler DA, Webb P, Ayers SD. Thyroid hormone induction of human cholesterol 7 alpha-hydroxylase (Cyp7a1) in vitro. Mol Cell Endocrinol 388, 32–40, 2014.10.1016/j.mce.2014.02.003418072024582860Search in Google Scholar

Lathi RB, Liebert CA, Brookfield KF, Taylor JA, vom Saal FS, Fujimoto VY, Baker VL. Conjugated bisphenol A in maternal serum in relation to miscarriage risk. Fertil Steril 102, 123–128, 2014.10.1016/j.fertnstert.2014.03.024471126324746738Search in Google Scholar

Lee S, Kim C, Youn H, Choi K. Thyroid hormone disrupting potentials of bisphenol A and its analogues - in vitro comparison study employing rat pituitary (GH3) and thyroid follicular (FRTL-5) cells. Toxicol In Vitro 40, 297–304, 2017.10.1016/j.tiv.2017.02.00428167136Search in Google Scholar

Lefevre L, Authier H, Stein S, Majorel C, Couderc B, Dardenne C, Eddine MA, Meunier E, Bernad J, Valentin A, Pipy B, Schoonjans K, Coste A. LRH-1 mediates anti-inflammatory and antifungal phenotype of IL-13-activated macrophages through the PPARγ ligand synthesis. Nat Commun 6, 6801, 2015.10.1038/ncomms7801441063825873311Search in Google Scholar

Leung DTH, Nguyen T, Oliver EM, Matti J, Alexiadis M, Silke J, Jobling TW, Fuller PJ, Chu S. Combined PPARγ activation and XIAP inhibition as a potential therapeutic strategy for ovarian granulosa cell tumors. Mol Cancer Ther 18, 364–375, 2019.10.1158/1535-7163.MCT-18-007830530769Search in Google Scholar

Liu Y, Deguchi Y, Tian R, Wei D, Wu L, Chen W, Xu W, Xu M, Liu F, Gao S, Jaoude JC, Chrieki SP, Moussalli MJ, Gagea M, Morris J, Broaddus RR, Zuo X, Shureiqi I. Pleiotropic Effects of PPARD Accelerate colorectal tumorigenesis, progression, and invasion. Cancer Res 79, 954–969, 2019.10.1158/0008-5472.CAN-18-1790639766330679176Search in Google Scholar

Livak KJ, Schmittgen TC. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402–408, 2001.10.1006/meth.2001.126211846609Search in Google Scholar

Martin-Martin N, Zabala-Letona A, Fernandez-Ruiz S, Arreal L, Camacho L, Castillo-Martin M, Cortazar AR, Torrano V, Astobiza I, Zuniga-Garcia P, Ugalde-Olano A, Loizaga-Iriarte A, Unda M, Valcarcel-Jimenez L, Arruabarrena-Aristorena A, Piva M, Sanchez-Mosquera P, Aransay AM, Gomez-Munoz A, Barrio R, Sutherland JD, Carracedo A. PPARδ elicits ligand-independent repression of trefoil factor family to limit prostate cancer growth. Cancer Res 78, 399–409, 2018.10.1158/0008-5472.CAN-17-090829187400Search in Google Scholar

Meinsohn MC, Smith OE, Bertolin K, Murphy BD. The orphan nuclear receptors steroidogenic factor-1 and liver receptor homolog-1: structure, regulation, and essential roles in mammalian reproduction. Physiol Rev 99, 1249–1279, 2019.10.1152/physrev.00019.201830810078Search in Google Scholar

Nishizawa H, Morita M, Sugimoto M, Imanishi S, Manabe N. Effects of in utero exposure to bisphenol A on mRNA expression of arylhydrocarbon and retinoid receptors in murine embryos. J Reprod Dev 51, 315–324, 2005.10.1262/jrd.1600815738621Search in Google Scholar

Nomiri S, Hoshyar R, Ambrosino C, Tyler CR, Mansouri B. A minireview of bisphenol A (BPA) effects on cancer-related cellular signaling pathways. Environ Sci Pollut Res Int 26, 8459–8467, 2019.10.1007/s11356-019-04228-930712204Search in Google Scholar

Pei F, Jiang J, Bai S, Cao H, Tian L, Zhao Y, Yang C, Dong H, Ma Y. Chemical-defined and albumin-free generation of human atrial and ventricular myocytes from human pluripotent stem cells. Stem Cell Res 19, 94–103, 2017.10.1016/j.scr.2017.01.00628110125Search in Google Scholar

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 122, 775–786, 2014.10.1289/ehp.1307728412303124896072Search in Google Scholar

Renaud L, Huff M, da Silveira WA, Angert M, Haas M, Hardiman G. Genome-wide analysis of low dose bisphenol-A (BPA) exposure in human prostate cells. Curr Genomics 20, 260–274, 2019.10.2174/1389202920666190603123040698395532030086Search in Google Scholar

Rochester J, Bolden A. Bisphenol S and F: A systematic review and comparison of the hormonal activity of bisphenol A substitutes. Environ Health Perspect 123, 643–650, 2015.10.1289/ehp.1408989449227025775505Search in Google Scholar

Safe S, Jin UH, Hedrick E, Reeder A, Lee SO. Minireview: role of orphan nuclear receptors in cancer and potential as drug targets. Mol Endocrinol 28, 157–172, 2014.10.1210/me.2013-1291389663824295738Search in Google Scholar

Sauer SJ, Tarpley M, Shah I, Save AV, Lyerly HK, Patierno SR, Williams KP, Devi GR. Bisphenol A activates EGFR and ERK promoting proliferation, tumor spheroid formation and resistance to EGFR pathway inhibition in estrogen receptor-negative inflammatory breast cancer cells. Carcinogenesis 38, 252–260, 2017.10.1093/carcin/bgx003596374228426875Search in Google Scholar

Scsukova S, Rollerova E, Bujnakova Mlynarcikova A. Impact of endocrine disrupting chemicals on onset and development of female reproductive disorders and hormone-related cancer. Reprod Biol 16, 243–254, 2016.10.1016/j.repbio.2016.09.00127692877Search in Google Scholar

Shah K, Faridi J. Estrogen, tamoxifen, and Akt modulate expression of putative housekeeping genes in breast cancer cells. J Steroid Biochem Mol Biol 125, 219–225, 2011.10.1016/j.jsbmb.2011.03.00521420492Search in Google Scholar

Sharma S, Ahmad S, Khan MF, Parvez S, Raisuddin S. In silico molecular interaction of bisphenol analogues with human nuclear receptors reveals their stronger affinity vs. classical bisphenol A. Toxicol Mech Methods 28, 660–669, 2018.10.1080/15376516.2018.149166329925285Search in Google Scholar

Toporova L, Balaguer P. Nuclear receptors are the major targets of endocrine disrupting chemicals. Mol Cell Endocrinol 502, 110665, 2020.10.1016/j.mce.2019.11066531760044Search in Google Scholar

Vissenberg R, Manders VD, Mastenbroek S, Fliers E, Afink GB, Ris-Stalpers C, Goddijn M, Bisschop PH. Patho-physiological aspects of thyroid hormone disorders/thyroid peroxidase autoantibodies and reproduction. Hum Reprod Update 21, 378–387, 2015.10.1093/humupd/dmv00425634660Search in Google Scholar

Wu F, Zhao J, Zhang E, Wu Q, Wu X, Zhang D, Liu Y, Wang R, Li W. Bisphenol A affects ovarian development in adolescent mice caused by genes expression change. Gene 740, 144535, 2020.10.1016/j.gene.2020.14453532156529Search in Google Scholar

Wu S, Zhang D, Zhang ZP, Soprano DR, Soprano KJ. Critical role of both retinoid nuclear receptors and retinoid-X-receptors in mediating growth inhibition of ovarian cancer cells by all-trans retinoic acid. Oncogene 17, 2839–2849, 1998.10.1038/sj.onc.12022089879990Search in Google Scholar

Wu S, Sun H, Zhang Q, Jiang Y, Fang T, Cui I, Yan G, Hu Y. MicroRNA-132 promotes estradiol synthesis in ovarian granulosa cells via translational repression of Nurr1. Reprod Biol Endocrinol 13, 94, 2015.10.1186/s12958-015-0095-zSearch in Google Scholar

Wu Y, Ghosh S, Nishi Y, Yanase T, Nawata H, Hu T. The orphan nuclear receptors NURR1 and NGFI-B modulate aromatase gene expression in ovarian granulosa cells: a possible mechanism for repression of aromatase expression upon luteinizing hormone surge. Endocrinology 146, 237–246, 2005.10.1210/en.2004-0889Search in Google Scholar

Yanase T, Mu YM, Nishi Y, Goto K, Nomura M, Okabe T, Takayanagi R, Nawata H. Regulation of aromatase by nuclear receptors. J Steroid Biochem Mol Biol 79, 187–192, 2001.10.1016/S0960-0760(01)00161-3Search in Google Scholar

Yoo SW, Savchev S, Sergott L, Rezai T, Lopez MF, Von Wald T, Eaton JL, Reindollar R, Usheva A. A large network of interconnected signaling pathways in human ovarian follicles is supported by the gene expression activity of the granulosa cells. Reprod Sci 18, 476–484, 2011.10.1177/193371911038884821558463Search in Google Scholar

Ziv-Gal A, Flaws JA. Evidence for bisphenol A-induced female infertility: a review (2007-2016). Fertil Steril 106, 827–856, 2016.10.1016/j.fertnstert.2016.06.027502690827417731Search in Google Scholar

Recommended articles from Trend MD

Plan your remote conference with Sciendo