Embryonic Exposure to Low Concentrations of Bisphenol A and S Altered Genes Related to Pancreatic β-Cell Development and DNA Methyltransferase in Zebrafish

Springer Science and Business Media LLC - 2021
Eric Gyimah1, Xing Dong1, Hai Xu1, Zhen Zhang1, John Kenneth Mensah2
1Institute of Environmental Health and Ecological Security, School of Environment and Safety Engineering, Jiangsu University, Zhenjiang, China
2Department of Chemistry, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana

Tóm tắt

Bisphenol A (BPA) and bisphenol S (BPS) are implicated in the development of metabolic disorders, such diabetes mellitus. However, the epigenetic mechanism underlying the pancreatic β-cell dysregulation for both BPA/BPS needs clarification. This exploratory study was designed to investigate whether embryonic exposure to low BPA/BPS concentrations impair early pancreatic β-cell differentiation as well as DNA methylation in its gene expression profile using an in vivo model, zebrafish. Zebrafish embryos were exposed to 0, 0.01, 0.03, 0.1, 0.3, and 1.0 µM BPA/BPS at 4-h post fertilization (hpf) until 120 hpf. BPA/BPS-induced effects on pancreatic-related genes, insulin gene, and DNA methylation-associated genes were assessed at developmental stages (24–120 hpf), while glucose level was measure at the 120 hpf. The insulin expression levels decreased at 72–120 hpf for 1.0 µM BPA, while 0.32 and 0.24-fold of insulin expression were elicited by 0.3 and 1 µM BPS respectively at 72 hpf. Significant elevation of glucose levels; 16.3% (for 1.0 µM BPA), 7.20% (for 0.3 µM BPS), and 74.09% (for 1.0 µM BPS) higher than the control groups were observed. In addition, pancreatic-related genes pdx-1, foxa2, ptfla, and isl1 were significantly interfered compared with the untreated group. Moreover, the maintenance methylation gene, dnmt1, was monotonically and significantly decreased at early stage of development following BPA exposure but remained constant for BPS treatment relative to the control group. DNMT3a and DNMT3b orthologs were distinctively altered following BPA/BPS embryonic exposure. Our data indicated that embryonic exposure to low concentration of BPA/BPS can impair the normal expressions of pancreatic-associated genes and DNA methylation pattern of selected genes in zebrafish early development.

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Tài liệu tham khảo

Aluru N, Kuo E, Helfrich LW, Karchner SI, Linney EA, Pais JE, Franks DG (2015) Developmental exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin alters DNA methyltransferase (dnmt) expression in zebrafish (Danio rerio). Toxicol Appl Pharmacol 284:142–151. https://doi.org/10.1016/j.taap.2015.02.016

Anderson IS, Lindeman LC, Reiner AH, Ostrup O, Aanes H, Alestrom P, Collas P (2013) Epegenetic marking of the zebrafish developmental program. Curr Top Dev Biol 104:85–112. https://doi.org/10.1016/B978-0-12-416027-9.00003-6

Aris A (2014) Estiamation of bisphenol A (BPA) concentrations in pregnant women, fetuses and nonpregnant women in Eastern Townships of Canada. Reprod Toxicol 45:8–13. https://doi.org/10.1016/j.reprotox.2013.12.006

Borowa-Mazgaj B, De Conti A, Tryndyak V, Steward CR, Jimenez L, Melnyk S, Seneshaw M, Mirshahi F, Rusyn I, Beland FA, Sanyani AJ, Pogribny IP (2019) Gene expression and DNA methylation alterations in the glycine N-methyltransferase gene in diet-induced nonalcoholic fatty liver disease-associated carcinogenesis. Toxicol Sci 170:273–282. https://doi.org/10.1093/toxsci/kfz110

Chakrabarti SK, Mirmira RG (2003) Transcription factors direct the development and function of pancreatic beta cells. Trends Endocrinol Metab 14:78–84. https://doi.org/10.1016/s1043-2760(02)00039-5

Chung ST, Hsia DS, Chacko SK, Rodriguez LM, Haymond MW (2015) Increased gluconeogenesis in youth with newly diagnosed type 2 diabetes. Diabetologia 58:596–603. https://doi.org/10.1007/s00125-104-3455x

Dassaye R, Naidoo S, Cerf ME (2016) Transcription factor regulation of pancreatic organogenesis, differentiation and maturation. Islets 8:13–34. https://doi.org/10.1080/19382014.2015.1075687

Davegårdh C, García-Calzón S, Bacos K, Ling C (2018) DNA methylation in the pathogenesis of type 2 diabetes in humans. Mol Metab 14:12–25. https://doi.org/10.1016/j.molmet.2018.01.022

Deng X, Liu Z, Li X, Zhou Y, Hu Z (2019) Generation of new hair cells by DNA methyltransferase (Dnmt) inhibitor 5-azacytidine in a chemically-deafened mouse model. Sci Rep 9:7997. https://doi.org/10.1038/s41598-019-44313-0

Dong X, Zhang Z, Meng S, Pan C, Yang M, Wu X, Yang L, Xu H (2018) Parental exposure to bisphenol A and its analogs influences zebrafish offspring immunity. Sci Total Environ 610–611:291–297. https://doi.org/10.1016/j.scitotenv.2017.08.057

Fang X, Corrales J, Thornton C, Scheffler BE, Willett KL (2013) Global and gene specific DNA methylation changes during zebrafish development. Comp Biochem Physiol B Biochem Mol Biol 166:99–108. https://doi.org/10.1016/j.cbpb.2013.07.007

Gut P, Baeza-Raja B, Andersson O, Hasenkamp L, Hsiao J, Hesselson D, Akassoglou K, Verdin E, Hirschey DM, Stainier DYR (2013) Whole-organism screening for gluconeogenesis identifies activators of fasting metabolism. Nat Chem Biol 9:97–104. https://doi.org/10.1038/nchembio.1136

Hesselson D, Anderson RM, Stainier DYR (2011) Suppression of Ptf1a activity induces acinar-to-endocrine conversion. Curr Biol 21:712–717. https://doi.org/10.1016/j.cub.2011.03.041

Jacobs HM, Sant KE, Basnet A, Williams LM, Moss JB, Timme-Laragy AR (2018) Embryonic exposure to Mono (2-ethylhexyl) phthalate (MEHP) disrupts pancreatic organogenesis in zebrafish (Danio rerio). Chemosphere 195:498–507. https://doi.org/10.1016/j.chemosphere.2017.12.094

Jin H, Zhu J, Chen Z, Hong Y, Cai Z (2018) Occurrence and partitioning of bisphenol analogues in adults’ blood from China. Environ Sci Technol 52:812–820. https://doi.org/10.1021/acs.est.7b03958

Jurczyk A, Roy N, Bajwa R, Gut P, Lipson K, Yang C, Covassin L, Racki WJ, Rossini AA, Nancy P, Stainier DYR, Greiner DL, Brehm MA, Bortell R, Dilorio P (2011) Dynamic glucoregulation and mammalian-like responses to metabolic and developmental disruption in zebrafish. Gen Comp Endocrinol 170:334–345. https://doi.org/10.1016/j.ygcen.2010.10.010

Kaestner KH (2015) An epigenomic road map for endoderm development. Cell Stem Cell 16:343–344. https://doi.org/10.1016/j.stem.2015.03.006

Kamel M, Ninov N (2017) Catching new targets in metabolic disease with a zebrafish. Curr Opin Pharmacol 37:41–50. https://doi.org/10.1016/j.coph.2017.08.007

Kamstra JH, Alestrom P, Kooter JM, Legler J (2015) Zebrafish as a model to study the role of DNA methylation in environmental toxicology. Environ Sci Pollut Res 22:16262–16276. https://doi.org/10.1007/s11356-014-3466-7

Kimmel RA, Dobler S, Schmitner N, Walsen T, Freudenblum J, Meyer D (2015) Diabetic pdx1-mutant zebrafish show conserved responses to nutrient overload and anti-glycemic treatment. Sci Rep 5:14241. https://doi.org/10.1038/srep14241

Liu Y, Zhang Y, Tao S, Guan Y, Zhang T, Wang Z (2016) Global DNA methylation in gonads of adult zebrafish (Danio rerio) under bisphenol A exposure. Ecotox Environ Saf 130:124–132. https://doi.org/10.1016/j.ecoenv.2016.04.012

Moreman J, Lee O, Trznadel M, David A, Kudoh T, Tyler CR (2017) Acute toxicity, teratogenic, and estrogenic effects of bisphenol A and its alternative replacements bisphenol S, bisphenol F, and bisphenol AF in zebrafish embryo-larvae. Environ Sci Technol 51:12796–12805. https://doi.org/10.1021/acs.est.7b03283

Mu X, Huang Y, Li X, Lei Y, Teng M, Li X, Wang C, Li Y (2018) Developmental effects and estrogenicity of bisphenol A alternatives in a zebrafish embryo model. Environ Sci Technol 52:3222–3231. https://doi.org/10.1021/acs.est.7b06255

National Research Counsil US (2011) Guide for the care and use of laboratiry animals, 8th edn. National Academies Press (US), Washington, DC

Nielsen JH, Haase TN, Jaksch C, Nalla A, Sostrup B, Nalla AA, Louise L, Rasmussen M, Dalgaard LT, Gaarn LW, Thams P, Kofood H, Billestrup N (2014) Impact of fetal and neonatal environment on beta cell function and development of diabetes. Acta Obstet Gynecol Scand 93:1109–1122. https://doi.org/10.1111/aogs.12504

Nilsson EE, Sadler-Riggleman I, Skinner MK (2018) Environmentally induced epigenetic transgenerational inheritance of disease. Environ Epigenetics 4:1–13. https://doi.org/10.1093/eep/dvy016

OECD (1998) Fish short-term toxicity test on embryo and sac-fry stages

Pelch K, Wignall JA, Goldstone AE, Ross PK, Blain RB, Shapiro AJ, Holmgren DS, Hsieh J-H, Svoboda D, Auerbach SS, Parham MF, Masten AS, Walker V, Rooney A, Thayner AK (2019) A scoping review of the health and toxicological activity of bisphenol A (BPA) structural analogues and functional alternatives. Toxicology 424:152235. https://doi.org/10.1016/j.tox.2019.06.006

Perera BPU, Faulk C, Svoboda LK, Goodrich JM, Dolinoy DC (2020) The role of environmental exposures and the epigenome in health and disease. Environ Mol Mutagen 61:176–192. https://doi.org/10.1002/em.22311

Qiu W, Zhan H, Hu J, Zhang T, Xu H, Wong M, Xu B, Zheng C (2019) The occurrence, potential toxicity, and toxicity mechanism of bisphenol S, a substitute of bisphenol A: a critical review of recent progress. Ecotoxicol Environ Saf 173:192–202. https://doi.org/10.1016/j.ecoenv.2019.01.114

Rai K, Nadauld LD, Chidester S, Manos EJ, James SR, Karpf AR, Cairns BR, Jones DA (2006) Zebrafish Dnmt1 and Suv39h1 regulate organ-specific terminal differentiation during development. Mol Cell Biol 26:7077–7085. https://doi.org/10.1128/MCB.00312-06

Rocha F, Dias J, Engrola S, Gavaia P, Geurden I, Dinis MT, Panserat S (2015) Glucose metabolism and gene expression in juvenile zebrafish (Danio rerio) challenged with a high carbohydrate diet: effects of an acute glucose stimulus during late embryonic life. Br J Nutr 113:403–413. https://doi.org/10.1017/s0007114514003869

Sanchez OF, Lee J, Hing NYK, Kim S-E, Freeman JL, Yuan C (2017) Lead (Pb) exposure reduces global DNA methylation level by non-competitive inhibition and alteration of dnmt expression. Metallomics 9:149–160. https://doi.org/10.1039/c6mt00198j

Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C T method. Nat protoc 3:1101–1108. https://doi.org/10.1038/nprot.2008.73

Sipione S, Eshpeter A, Lyon J, Korbutt G, Bleackley RJ (2004) Insulin expressing cells from differentiated embryonic stem cells are not beta cells. Diabetologia 47:499–508

Strömqvist M, Tooke N, Brunström B (2010) DNA methylation levels in the 5′ flanking region of the vitellogenin I gene in liver and brain of adult zebrafish (Danio rerio)—sex and tissue differences and effects of 17α-ethinylestradiol exposure. Aquat Toxicol 98:275–281. https://doi.org/10.1016/j.aquatox.2010.02.023

Tiso N, Moro E, Argenton F (2009) Zebrafish pancreas development. Mol Cell Endocrinol 312:24–30. https://doi.org/10.1016/j.mce.2009.04.018

Vaiserman A, Lushchak O (2019) Developmental origins of type 2 diabetes: focus on epigenetics. Ageing Res Rev 55:100957. https://doi.org/10.1016/j.arr.2019.100957

Wirbisky-Hershberger SE, Sanchez OF, Horzmann KA, Thanki D, Yuan C, Freeman JL (2017) Atrazine exposure decreases the activity of DNMTs, a global DNA methylation levels, and dnmt expression. Food Chem Toxicol 109:727–734. https://doi.org/10.1016/j.fct.2017.08.041

Wu X, Li Y, Zhu X, He C, Wang Q, Liu S (2017) Dummy molecular imprited magnetic nanoparticles for dispersive solid-phase extraction and determination of bisphenol A in water samples and orange juice. Talanta 162:57–64. https://doi.org/10.1016/j.talanta.2016.10.007

Wu LH, Zhang XM, Wang F, Gao CJ, Chen D, Palumbo JR, Guo Y, Zheng EY (2018) Occurrence of bisphenol S in the environment and implications for human exposure: a short review. Sci Total Environ 615:87–98. https://doi.org/10.1016/j.scitotenv.2017.09.194

Xue J, Wan Y, Kannan K (2016) Occurrence of bisphenols, bisphenol A diglycidyl ethers (BADGEs), and novolac glycidyl ethers (NOGEs) in indoor air from Albany, New York, USA, and its implications for inhalation exposure. Chemosphere 151:1–8. https://doi.org/10.1016/j.chemosphere.2016.02.038

Yao Y, Shao Y, Zhan M, Zou X, Qu W, Zhou Y (2018) Rapid and sensitive determination of nine bisphenol analogues, three amphenicol antibiotics, and six phthalate metabolites in human urine samples uning UHPLC-MS/MS. Anal Bioanal Chem 410:3871–3883. https://doi.org/10.1007/s00216-018-1062-2

Yun Y, Zhang Y, Li G, Chen S, Sang N (2019) Embryonic exposure to oxy-polycyclic aromatic hydrocarbon interfere with pancreatic beta-cell development in zebrafish via altering DNA methylation and gene expression. Sci Total Environ 660:1602–1609. https://doi.org/10.1016/j.scitotenv.2018.12.476

Zhao Y, Shi H, Xie C, Chen J, Laue H, Zhang Y (2015) Prenatal phthalate exposure, infant growth, and global DNA methylation of human placenta. Environ Mol Mutagen 56:286–292. https://doi.org/10.1002/em.21916

Zhao F, Jiang G, Wei P, Wang H, Ru S (2018) Bisphenol S exposure impairs glucose homeostasis in male zebrafish (Danio rerio). Ecotoxicol Environ Saf 147:794–802. https://doi.org/10.1016/j.ecoenv.2017.09.048

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