Volume 19, Issue 2 (February 2021)                   IJRM 2021, 19(2): 129-136 | Back to browse issues page

XML Persian Abstract Print

Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
Jamali Khaghani A, Farrokh P, Zavareh S. Epigenetic effects of Bisphenol A on granulosa cells of mouse follicles during in vitro culture: An experimental study. IJRM 2021; 19 (2) :129-136
URL: http://ijrm.ir/article-1-1737-en.html
Epigenetic effects of Bisphenol A on granulosa cells of mouse follicles during in vitro culture: An experimental study
Aylin Jamali Khaghani1 , Parisa Farrokh * 2, Saeed Zavareh3
1- School of Biology, Damghan University, Damghan, Iran.
2- School of Biology, Damghan University, Damghan, Iran. Institute of Biological Sciences, Damghan University, Damghan, Iran. , farrokh@du.ac.ir
3- School of Biology, Damghan University, Damghan, Iran. Institute of Biological Sciences, Damghan University, Damghan, Iran.
Abstract:   (1550 Views)

Background: Bisphenol A (BPA), a synthetic endocrine-disrupting chemical, is a reproductive toxicant. Granulosa cells have significant roles in follicle development, and KIT ligand (KITL) and Anti-Müllerian hormone (AMH) are essential biomolecules produced by them during folliculogenesis.
Objective: Due to the widespread use of BPA and its potential epigenetic effects, this study examined the impact of BPA on promoter methylation of amh and kitl genes in mouse granulosa cells.
Materials and Methods: Preantral follicles were isolated from ovaries of immature mice and cultured for eight days. Then, follicles were treated with 50 and 100 μM of BPA, and 0.01% (v/v) ethanol for 24 and 72 hr. Growth and degeneration of follicles and antrum formation were analyzed. The granulosa cells were isolated mechanically, and their extracted DNA was treated with sodium bisulfite. The promoter regions of the amh and kitl were analyzed with PCR and sequencing.
Results: BPA did not change follicle survival and antrum formation significantly (p = 0.41). However, the culture in the presence of 100 μM BPA had an inhibitory effect on growth. Before BPA treatment, the CpG of the kitl and amh promoters were unmethylated and partially methylated, respectively. While the percent of 5mC in the amh promoter reduced at 100 μM of BPA, it did not alter the kitl promoter methylation.
Conclusion: BPA at higher concentrations has an inhibitory effect on follicle growth. Moreover, it seems that the epigenetic impact of BPA restricts to the demethylation of CpG sites.

Keywords: Bisphenol A, DNA methylation, Granulosa cells
Full-Text [PDF 574 kb]   (486 Downloads) |   |   Full-Text (HTML)  (270 Views)  
Type of Study: Original Article | Subject: Reproductive Genetics
References
1. Maqbool F, Mostafalou S, Bahadar H, Abdollahi M. Review of endocrine disorders associated with environmental toxicants and possible involved mechanisms. Life Sci 2016; 145: 265-273. [DOI:10.1016/j.lfs.2015.10.022] [PMID]
2. Swedenborg E, Rüegg J, Mӓkelӓ S, Pongratz I. Endocrine disruptive chemicals: Mechanisms of action and involvement in metabolic disorders. J Mol Endocrinol 2009; 43: 1-10. [DOI:10.1677/JME-08-0132] [PMID]
3. Kundakovic M, Champagne FA. Epigenetic perspective on the developmental effects of bisphenol A. Brain Behav Immun 2011; 25: 1084-1093. [DOI:10.1016/j.bbi.2011.02.005] [PMID] [PMCID]
4. Matuszczak E, Komarowska MD, Debek W, Hermanowicz A. The impact of bisphenol A on fertility, reproductive system, and development: A review of the literature. Int J Endocrinol 2019; 2019: 4068717. [DOI:10.1155/2019/4068717] [PMID] [PMCID]
5. Chianese R, Troisi J, Richards S, Scafuro M, Fasano S, Guida M, et al. Bisphenol A in reproduction: Epigenetic effects. Curr Med Chem 2018, 25: 748-770. [DOI:10.2174/0929867324666171009121001] [PMID]
6. Huo X, Chen D, He Y, Zhu W, Zhou W, Zhang J. Bisphenol-A and female infertility: A possible role of gene-environment interactions. Int J Environ Res Public Health 2015; 12: 11101-11116. [DOI:10.3390/ijerph120911101] [PMID] [PMCID]
7. Mansur A, Israel A, Combelles CMH, Adir M, Racowsky C, Hauser R, et al. Bisphenol-A exposure and gene expression in human luteinized membrana granulosa cells in vitro. Hum Reprod 2017; 32: 409-417. [DOI:10.1093/humrep/dew316] [PMID] [PMCID]
8. Ideta-Otsuka M, Igarashi K, Narita M, Hirabayashi Y. Epigenetic toxicity of environmental chemicals upon exposure during development - Bisphenol A and valproic acid may have epigenetic effects. Food Chem Toxicol 2017; 109: 812-816. [DOI:10.1016/j.fct.2017.09.014] [PMID]
9. Laing LV, Viana J, Dempster EL, Trznadel M, Trunkfield LA, Uren Webster TM, et al. Bisphenol A causes reproductive toxicity, decreases dnmt1 transcription, and reduces global DNA methylation in breeding zebrafish (Danio rerio). Epigenetics 2016, 11: 526-538. [DOI:10.1080/15592294.2016.1182272] [PMID] [PMCID]
10. Ruiz-Hernandez A, Kuo CC, Rentero-Garrido P, Tang WY, Redon J, Ordovas JM, et al. Environmental chemicals and DNA methylation in adults: A systematic review of the epidemiologic evidence. Clin Epigenetics 2015; 7: 55. [DOI:10.1186/s13148-015-0055-7] [PMID] [PMCID]
11. Jiang JY, Xiong H, Cao M, Xia X, Sirard MA, Tsang BK. Mural granulosa cell gene expression associated with oocyte developmental competence. J Ovarian Res 2010; 3: 6. [DOI:10.1186/1757-2215-3-6] [PMID] [PMCID]
12. Cuiling L, Wei Y, Zhaoyuan H, Yixun L. Granulosa cell proliferation differentiation and its role in follicular development. Chin Sci Bull 2005; 50: 2665-2671. https://doi.org/10.1360/982005-983 [DOI:10.1007/BF02899632]
13. Grasselli F, Baratta L, Baioni L, Bussolati S, Ramoni R, Grolli S, et al. Bisphenol A disrupts granulosa cell function. Domest Anim Endocrinol 2010; 39: 34-39. [DOI:10.1016/j.domaniend.2010.01.004] [PMID]
14. Kidder GM, Vanderhyden BC. Bidirectional communication between oocytes and follicle cells: Ensuring oocyte developmental competence. Can J Physiol Pharmacol 2010; 88: 399-413. [DOI:10.1139/Y10-009] [PMID] [PMCID]
15. Driancourt M, Reynaud K, Cortvrindt R, Smitz J. Roles of KIT and KIT ligand in ovarian function. Rev Reprod 2000; 5: 143-152. [DOI:10.1530/ror.0.0050143] [PMID]
16. van Houten ELAF, Themmen APN, Visser JA. Anti-Müllerian hormone (AMH): Regulator and marker of ovarian function. Ann Endocrinol 2010; 71: 191-197. [DOI:10.1016/j.ando.2010.02.016] [PMID]
17. Knight PG, Glister C. TGF-β superfamily members and ovarian follicle development. Reproduction 2006; 132: 191-206. [DOI:10.1530/rep.1.01074] [PMID]
18. 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. [DOI:10.1016/j.reprotox.2013.07.022] [PMID] [PMCID]
19. 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: 63-74. [DOI:10.1095/biolreprod.112.101899] [PMID] [PMCID]
20. Wang X, Jiang SW, Wang L, Sun Y, Xu F, He H, et al. Interfering effects of bisphenol A on in vitro growth of preantral follicles and maturation of oocyes. Clin Chim Acta 2018; 485: 119-125. [DOI:10.1016/j.cca.2018.06.041] [PMID]
21. Xu J, Osuga Y, Yano T, Morita Y, Tang X, Fujiwara T, et al. Bisphenol A induces apoptosis and G2-to-M arrest of ovarian granulosa cells. Biochem Biophys Res Commun 2002; 292: 456-462. [DOI:10.1006/bbrc.2002.6644] [PMID]
22. Council NR. Guide for the care and use of laboratory animals. 8th Ed. Washington, DC: The National Academies Press, 2011.
23. Vafere Koohestani N, Zavareh S, Lashkarbolouki T, Azimipour F. Exposure to cell phone induce oxidative stress in mice preantral follicles during in vitro cultivation: An experimental study. Int J Reprod Biomed 2019; 17: 637-646. [DOI:10.18502/ijrm.v17i9.5099] [PMID] [PMCID]
24. Karolchik D, Hinrichs AS, Furey TS, Roskin KM, Sugnet CW, Haussler D, et al. The UCSC Table Browser data retrieval tool. Nucleic Acids Res 2004; 32: 493-496. [DOI:10.1093/nar/gkh103] [PMID] [PMCID]
25. LC L-Ch, Dahiya R. MethPrimer: Designing primers for methylation PCRs. Bioinformatics 2002; 18: 1427-1431. [DOI:10.1093/bioinformatics/18.11.1427] [PMID]
26. Uslu B, Dioguardi CC, Haynes M, Miao DQ, Kurus M, Hoffman G, et al. Quantifying growing versus non-growing ovarian follicles in the mouse. J Ovarian Res 2017; 10: 3-13. [DOI:10.1186/s13048-016-0296-x] [PMID] [PMCID]
27. Parrish RR, Day JJ, Lubin FD. Direct bisulfite sequencing for examination of DNA methylation with gene and nucleotide resolution from brain tissues. Curr Protoc Neurosci 2012; 7: 24. [DOI:10.1002/0471142301.ns0724s60] [PMID] [PMCID]
28. Caserta D, Di Segni N, Mallozzi M, Giovanale V, Mantovani A, Marci R, et al. Bisphenol A and the female reproductive tract: An overview of recent laboratory evidence and epidemiological studies. Reprod Biol Endocrinol 2014; 12: 37. [DOI:10.1186/1477-7827-12-37] [PMID] [PMCID]
29. Drummond AE, Fuller PJ. Ovarian actions of estrogen receptor-β: an update. Semin Reprod Med 2012; 30: 32-38. [DOI:10.1055/s-0031-1299595] [PMID]
30. Peretz J, Gupta RK, Singh J, Hernández-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: 209-217. [DOI:10.1093/toxsci/kfq319] [PMID] [PMCID]
31. Lenie S, Cortvrindt R, Eichenlaub-Ritter U, Smitz J. Continuous exposure to bisphenol A during in vitro follicular development induces meiotic abnormalities. Mutat Res 2008; 651: 71-81. [DOI:10.1016/j.mrgentox.2007.10.017] [PMID]
32. Wang T, Han J, Duan X, Xiong B, Cui XS, Kim NH, et al. The toxic effects and possible mechanisms of Bisphenol A on oocyte maturation of porcine in vitro. Oncotarget 2016; 7: 32554-32565. [DOI:10.18632/oncotarget.8689] [PMID] [PMCID]
33. Chao HH, Zhang XF, Chen B, Pan B, Zhang LJ, Li L, et al. Bisphenol A exposure modifies methylation of imprinted genes in mouse oocytes via the estrogen receptor signaling pathway. Histochem Cell Biol 2012; 137: 249-259. [DOI:10.1007/s00418-011-0894-z] [PMID]
34. Li Y, Tollefsbol TO. DNA methylation detection: Bisulfite genomic sequencing analysis. Methods Mol Biol 2011; 791: 11-21. [DOI:10.1007/978-1-61779-316-5_2] [PMID] [PMCID]
35. Zhang T, Li L, Qin XS, Zhou Y, Zhang XF, Wang LQ, et al. Di-(2-ethylhexyl) phthalate and bisphenol A exposure impairs mouse primordial follicle assembly in vitro. Environ Mol Mutagen 2014; 55: 343-353. [DOI:10.1002/em.21847] [PMID]
36. Trapphoff T, 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. [DOI:10.1016/j.fertnstert.2013.08.021] [PMID]
Send email to the article author

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Designed & Developed by : Yektaweb