Toxicity of bisphenol A and its replacements in the mice Leydig cells in vitro

. 2023 Mar 08 ; 72 (1) : 71-86. [epub] 20221222

Jazyk angličtina Země Česko Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36545881

The aim of the study was to examine the potential impacts of bisphenol A (BPA) and its analogues BPB, BPF, and BPS on mice TM3 Leydig cells, with respect to basal cell viability parameters such as metabolic activity, cell membrane integrity, and lysosomal activity after 48-h exposure. In addition, monitoring of potential bisphenol´s actions included evaluation of ROS production and gap junctional intercellular communication (GJIC) complemented by determination of testosterone secretion. Obtained results revealed significant inhibition in mitochondrial activity started at 10 microg/ml of bisphenols after 48-h exposure. Cell membrane integrity was significantly decreased at 5 microg/ml of BPA and BPF and 10, 25, and 50 microg/ml of BPA and BPS. The lysosomal activity was significantly affected at 10, 25, and 50 microg/ml of applied bisphenols. A significant overproduction of ROS was recorded mainly at 5 and 10 microg/ml of tested compounds. In addition, significant inhibition of GJIC was observed at 5 microg/ml of BPB followed by a progressive decline at higher applied doses. In the case of testosterone production, a significant decline was confirmed at 10, 25 and 50 microg/ml.

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Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA) Reprod Toxicol. 2007;24:139–177. doi: 10.1016/j.reprotox.2007.07.010. PubMed DOI

Teeguarden JG, Twaddle NC, Churchwell MI, Doerge DR. Urine and serum biomonitoring of exposure to environmental estrogens I: Bisphenol A in pregnant women. Food Chem Toxicol. 2016;92:129–142. doi: 10.1016/j.fct.2016.03.023. PubMed DOI

Jambor T, Knizatova N, Lukac N. Men’s reproductive alterations caused by bisphenol A and its analogues: a review. Physiol Res. 2021;70(Suppl 4):S643–S656. doi: 10.33549/physiolres.934742. PubMed DOI PMC

Mustieles V, D’Cruz SC, Couderq S, Rodríguez-Carrillo A, Fini JB, Hofer T, Steffensen IL, et al. Bisphenol A and its analogues: A comprehensive review to identify and prioritize effect biomarkers for human biomonitoring. Environ Int. 2020;144:105811. doi: 10.1016/j.envint.2020.105811. PubMed DOI

Kolatorova L, Duskova M, Vitku J, Starka L. Prenatal exposure to bisphenols and parabens and impact on human physiology. Physiol Res. 2017;66(Suppl 3):S305–S315. doi: 10.33549/physiolres.933723. PubMed DOI

Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL. Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003–2004. Environ Health Perspect. 2008;116:39–44. doi: 10.1289/ehp.10753. PubMed DOI PMC

Becker K, Göen T, Seiwert M, Conrad A, Pick-Fuss H, Müller J, Wittassek M, Schulz C, Kolossa-Gehring M. GerES IV: phthalate metabolites and bisphenol A in urine of German children. Int J Hyg Environ Health. 2009;212:685–692. doi: 10.1016/j.ijheh.2009.08.002. PubMed DOI

ECHA. Member State Committee Support Document for Identification of 4, 4′-Isopropylidenediphenol (Bisphenol A) as a Substance of Very High Concern Because of its Toxic For Reproduction (Article 57 C), EC 201-245-8, CAS 80-05-7. 2016. https://echa.europa.eu/documents/10162/b10d6a00-8e47-9b14-4f61-c779a8dc8450 .

ECHA. Member State Committee Unanimously Agrees that Bisphenol A is an Endocrine Disruptor. 2017. https://echa.europa.eu/documents/10162/769b2777-19cd-9fff-33c4-54fe6d8290d5 .

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. 2016;50:5438–5453. doi: 10.1021/acs.est.5b05387. PubMed DOI

Cabaton N, Dumont C, Severin I, Perdu E, Zalko D, Cherkaoui-Malki M, Chagnon MC. Genotoxic and endocrine activities of bis(hydroxyphenyl)methane (bisphenol F) and its derivatives in the HepG2 cell line. Toxicology. 2009;255:15–24. doi: 10.1016/j.tox.2008.09.024. PubMed DOI

Yang Y, Guan J, Yin J, Shao B, Li H. Urinary levels of bisphenol analogues in residents living near a manufacturing plant in south China. Chemosphere. 2014;112:481–486. doi: 10.1016/j.chemosphere.2014.05.004. PubMed DOI

Ye X, Wong LY, Kramer J, Zhou X, Jia T, Calafat AM. Urinary concentrations of bisphenol A and three other bisphenols in convenience samples of U.S. adults during 2000–2014. Environ Sci Technol. 2015;49:11834–11839. doi: 10.1021/acs.est.5b02135. PubMed DOI PMC

Mann U, Shiff B, Patel P. Reasons for worldwide decline in male fertility. Curr Opin Urol. 2020;30:296–301. doi: 10.1097/MOU.0000000000000745. PubMed DOI

Santoro A, Chianese R, Troisi J, Richards S, Nori SL, Fasano S, Guida M, Plunk E, Viggiano A, Pierantoni R, Meccariello R. Neuro-toxic and Reproductive Effects of BPA. Curr Neropharmacol. 2019;17:1109–1132. doi: 10.2174/1570159X17666190726112101. PubMed DOI PMC

Yawer A, Sychrová E, Labohá P, Raška J, Jambor T, Babica P, Sovadinová I. Endocrine-disrupting chemicals rapidly affect intercellular signalling in Leydig cells. Toxicol Appl Pharmacol. 2020;404:115177. doi: 10.1016/j.taap.2020.115177. PubMed DOI

Zhang X, Chang H, Wiseman S, He Y, Higley E, Jones P, Wong CK, Al-Khedhairy A, Giesy JP, Hecker M. Bisphenol A disrupts steroidogenesis in human H295R cells. Toxicol Sci. 2011;121:320–327. doi: 10.1093/toxsci/kfr061. PubMed DOI

Bloom MS, Mok-Lin E, Fujimoto VY. Bisphenol A and ovarian steroidogenesis. Fertil Steril. 2016;106:857–863. doi: 10.1016/j.fertnstert.2016.08.021. PubMed DOI

Gassman NR. Induction of oxidative stress by bisphenol A and its pleiotropic effects. Environ Mol Mutagen. 2017;58:60–71. doi: 10.1002/em.22072. PubMed DOI PMC

Huang M, Huang M, Li X, Liu S, Fu L, Jiang X, Yang M. Bisphenol A induces apoptosis through GPER-dependent activation of the ROS/Ca2+-ASK1-JNK pathway in human granulosa cell line KGN. Ecotoxicol Environ Saf. 2021;208:111429. doi: 10.1016/j.ecoenv.2020.111429. PubMed DOI

Huang M, Liu S, Fu L, Jiang X, Yang M. Bisphenol A and its analogues bisphenol S, bisphenol F and bisphenol AF induce oxidative stress and biomacromolecular damage in human granulosa KGN cells. Chemosphere. 2020;253:126707. doi: 10.1016/j.chemosphere.2020.126707. PubMed DOI

Mesnil M, Crespin S, Avanzo JL, Zaidan-Dagli ML. Defective gap junctional intercellular communication in the carcinogenic process. Biochim Biophys Acta. 2005;1719:125–145. doi: 10.1016/j.bbamem.2005.11.004. PubMed DOI

Acuña-Hernández DG, Arreola-Mendoza L, Santacruz-Márquez R, García-Zepeda SP, Parra-Forero LY, Olivares-Reyes JA, Hernández-Ochoa I. Bisphenol A alters oocyte maturation by prematurely closing gap junctions in the cumulus cell-oocyte complex. TAAP. 2018;344:13–22. doi: 10.1016/j.taap.2018.02.011. PubMed DOI

Gingrich J, Pu Y, Upham BL, Hulse M, Pearl S, Martin D, Avry A, Veige-Lopez A. Bisphenol S enhances gap junction intercellular communication in ovarian theca cells. Chemosphere. 2021;263:128304. doi: 10.1016/j.chemosphere.2020.128304. PubMed DOI PMC

Lin TC, Wang KH, Chuang KH, Kao AP, Kuo TC. Downregulation of gap junctional intercellular communication and connexin 43 expression by bisphenol A in human granulosa cells. Biotechnolo Appl Biochem. 2021;68:676–682. doi: 10.1002/bab.1979. PubMed DOI

Jambor T, Kovacikova E, Greifova H, Kovacik A, Libova L, Lukac N. Assessment of the effective impact of bisphenols on mitochondrial activity and steroidogenesis in a dose-dependency in mice TM3 Leydig cells. Physiol Res. 2019;68:689–693. doi: 10.33549/physiolres.934200. PubMed DOI

Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65:55–63. doi: 10.1016/0022-1759(83)90303-4. PubMed DOI

Schreer A, Tinson CH, Sherry JP, Schirmer K. Application of Alamar blue/5-carboxyfluorescein diacetate acetoxymethyl ester as a non-invasive cell viability assay in primary hepatocytes from rainbow trout. Anal Biochem. 2005;344:76–85. doi: 10.1016/j.ab.2005.06.009. PubMed DOI

Repetto G, Del Peso A, Zurita JL. Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat Protoc. 2008;3:1125–1131. doi: 10.1038/nprot.2008.75. PubMed DOI

Choi HS, Kim JW, Cha YN, Kim C. A quantitative nitroblue tetrazolium assay for determining intracellular superoxide anion production in phagocytic cells. J Immunoassay Immunochem. 2006;27:31–44. doi: 10.1080/15321810500403722. PubMed DOI

Babica P, Sovadinová I, Upham BL. Scrape Loading/Dye Transfer Assay. Gap Junction Protocols. In: VINKEN M, JOHNSTONE S, editors. Methods in Molecular Biology. Humana Press; New York, NY: 2016. pp. 133–144. PubMed DOI

Schneider CA, Rasband WS, Eliceiri KW. NIH image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671–675. doi: 10.1038/nmeth.2089. PubMed DOI PMC

Li C, Zhang L, Ma T, Gao L, Yang L, Wu M, Pang Z, Wnag X, Yao Q, Wnag A, Jin Y, Chen H. Bisphenol A attenuates testosterone production in Leydig cells via the inhibition of NR1D1 signaling. Chemosphere. 2021;263:128020. doi: 10.1016/j.chemosphere.2020.128020. PubMed DOI

Rajkumar A, Luu T, Beal MA, Barton-Maclaren ST, Robaire B, Hales BF. Elucidation of the effects of bisphenol A and structural analogues on germ and steroidogenic cells using single cell high-content imaging. Toxicol Sci. 2021;180:224–238. doi: 10.1093/toxsci/kfab012. PubMed DOI PMC

Lan HCH, Wu KY, Lin IW, Yang ZJ, Chang AA, Hu MCH. Bisphenol A disrupts steroidogenesis and induces a sex hormone imbalance through c-Jun phosphorylation in Leydig cells. Chemosphere. 2017;185:237–246. doi: 10.1016/j.chemosphere.2017.07.004. PubMed DOI

Zhang W, Huan T, Sun Z, Kuang H, Yuan Y, Zou W, Liu F, Zhang F, Yang B, Wu L, Zhang D. Bisphenol S exposure induces cytotoxicity in mouse Leydig cells. Food Chem Toxicol. 2022;160:112805. doi: 10.1016/j.fct.2021.112805. PubMed DOI

Goncalves GD, Semprebon SC, Biazi BI, Mantovani MS, Fernandes GA. Bisphenol A reduces testosterone production in TM3 Leydig cells independently of its effects on cell death and mitochondrial membrane potential. Repro Toxicol. 2018;76:26–34. doi: 10.1016/j.reprotox.2017.12.002. PubMed DOI

Yin L, Siracusa JS, Measet E, Guan X, Edenfield C, Liang S, You X. High-content image-based single-cell phenotypic analysis for the testicular toxicity prediction induced by bisphenol A and its analogues bisphenol S, bisphenol AF, and tetrabromobisphenol A in a three-dimensional testicular cell co-culture model. Toxicol Sci. 2020;173:313–335. doi: 10.1093/toxsci/kfz233. PubMed DOI PMC

Shaha C, Tripathi R, Mishra DP. Male germ cell apoptosis: regulation and biology. Philos Trans R Soc Lond B Biol Sci. 2010;365:1501–1515. doi: 10.1098/rstb.2009.0124. PubMed DOI PMC

Yin L, Dai Y, Cui Z, Jian X, Liu W, Han F, Lin A, Cao J, Liu J. The regulation of cellular apoptosis by the ROS-triggered PERK/EIF2α/chop pathway plays a vital role in bisphenol A-induced male reproductive toxicity. Toxicol Appl Pharmacol. 2017;314:98–108. doi: 10.1016/j.taap.2016.11.013. PubMed DOI

Qu W, Zhao Z, Chen S, Zhang L, Wu D, Chen Z. Bisphenol A suppresses proliferation and induces apoptosis in colonic epithelial cells through mitochondrial and MAPK/AKT pathways. Life Sci. 2018;208:167–174. doi: 10.1016/j.lfs.2018.07.040. PubMed DOI

De Toni L, De Rocco Ponce M, Petre GC, Rtibi K, Di Nisio A, Foresta C. Bisphenols and male reproductive health: from toxicological models to therapeutic hypotheses. Front Endocrinol. 2020;11:301–309. doi: 10.3389/fendo.2020.00301. PubMed DOI PMC

Ullah A, Pirzada M, Jahan S, Ullah H, Shaheen G, Rehman H, Siddiqui FM, Butt AM. Bisphenol A and its analogues bisphenol B, bisphenol F, and bisphenol S: Comparative in vitro and in vivo studies on the sperms and testicular tissues of rats. Chemosphere. 2018;209:508–516. doi: 10.1016/j.chemosphere.2018.06.089. PubMed DOI

Zhang Y, Yan M, Kuang S, Lou Y, Wu S, Li Y, Wang Z, Mao H. Bisphenol A induces apoptosis and autophagy in murine osteocytes MLO-Y4: Involvement of ROS-mediated mTOR/ULK1 pathway. Ecotoxicol Environ Saf. 2021;230:113119. doi: 10.1016/j.ecoenv.2021.113119. PubMed DOI

Ullah A, Pirzada M, Afsar T, Razak S, Almajwal A, Jahan S. Effect of bisphenol F, an analog of bisphenol A, on the reproductive functions of male rats. Environ Health Prev Med. 2019;24:2–11. doi: 10.1186/s12199-019-0797-5. PubMed DOI PMC

Iwase Y, Fukata H, Mori CJ. Estrogenic compounds inhibit gap junctional intercellular communication in mouse Leydig TM3 cells. Toxicol Appl Phamacol. 2006;212:237–246. doi: 10.1016/j.taap.2005.08.005. PubMed DOI

Goldenberg RC, Fortes FA, Christancho JM, Morales MM, Franci CR, Varanda WA, Campos de Cervalho CAC. Modulation of gap junction mediated intercellular communication in TM3 Leydig cells. J Endocrinol. 2003;177:327–335. doi: 10.1677/joe.0.1770327. PubMed DOI

Yawer A, Sychrová E, Raška J, Babica P, Sovadinová I. Endocrine-disrupting chemicals affect Sertoli TM4 cell functionality through dysregulation of gap junctional intercellular communication in vitro. Food Chem Toxicol. 2022;164:113004. doi: 10.1016/j.fct.2022.113004. PubMed DOI

Schuhaibar LC, Egbert JR, Norris RP, Lampe DP, Nikolaev VO, Thunemann M, Wen L, Feil R, Jaffe LA. Intercellular signalling via cyclic GMP diffusion through gap junctions restarts meiosis in mouse ovarian follicles. Proc Natl Acad Sci U S A. 2015;112:5527–5532. doi: 10.1073/pnas.1423598112. PubMed DOI PMC

Richards JS, Ascoli M. Endocrine, paracrine, and autocrine signalling pathways that regulate ovulation. Trends Endocrinol Metab. 2018;29:313–325. doi: 10.1016/j.tem.2018.02.012. PubMed DOI

Koepple CH, Zhou Z, Huber L, Shulte M, Schmidt K, Gloe T, Kneser U, Schmidt VJ, de Wit C. Expression of connexin43 stimulates endothelial angiogenesis independently of gap junctional communication in vitro. Int J Mol Sci. 2021;22:7400. doi: 10.3390/ijms22147400. PubMed DOI PMC

Sabry R, Apps CH, Saunders JA, Saleh AC, Balachandran S, St John EJ, Favetta LA. BPA and BPS affect connexin 37 in bovine cumulus cells. Genes (Basel) 2021;12:321. doi: 10.3390/genes12020321. PubMed DOI PMC

Gao Z, Liu S, Tan L, Gao X, Fan W, Ding CH, Li M, Tang Z, Shi X, Luo Y, Song S. Testicular toxicity of bisphenol compounds: Homeostasis disruption of cholesterol/testosterone via PPARα activation. Sci Total Environ. 2022;836:555628. doi: 10.1016/j.scitotenv.2022.155628. PubMed DOI

Roelofs ME, Van den Berg M, Bovee TH, Piersma AH, Van Duursen MM. Structural bisphenol analogues differentially target steroidogenesis in murine MA-10 Leydig cells as well as the glucocorticoid receptor. Toxicology. 2015;329:10–20. doi: 10.1016/j.tox.2015.01.003. PubMed DOI

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