Skip to main content
SpringerLink
Log in

Bisphenol B induces developmental toxicity in zebrafish via oxidative stress

  • Integrative approach to various environmental toxins: Effects and interactions
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Bisphenol A (BPA) is a typical endocrine disruptor, and the use of bisphenol B (BPB) as a substitute is gradually increasing. Some studies have shown that BPB also has endocrine disrupting effects, but its effects on the early stages of fish growth and development have not been reported. In this paper, zebrafish embryos were exposed to different concentrations of BPB until the 6th day post fertilization (dpf), and the toxic effects of BPB on the early development of zebrafish and the possible molecular mechanisms were investigated. The results showed that BPB exposure at 10, 100, and 1000 μg/L induced developmental toxic effects such as early neurotoxicity and cardiovascular toxicity in zebrafish, and the toxic effects were positively correlated with the degree of oxidative damage. These adverse results were ameliorated by the classical antioxidant N-acetyl-L-cysteine (NAC), suggesting the involvement of oxidative stress in BPB-induced early developmental toxicity. The above data suggest that BPB exposure increases oxidative damage and suppresses the expression of genes critical for early neurological and cardiovascular development, ultimately leading to early developmental toxicity in juvenile zebrafish. This study contributes to broadening our understanding of the toxic effects of BPB and provides a basic theoretical basis for the next management support of bisphenol analogs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arnich N, Canivenc-Lavier MC, Kolf-Clauw M, Coffigny H, Cravedi JP, Grob K, Macherey AC, Masset D, Maximilien R, Narbonne JF, Nesslany F, Stadler J, Tulliez J (2011) Conclusions of the French Food Safety Agency on the toxicity of bisphenol A. Int J Hyg Environ Health 214:271–275

    Article  CAS  Google Scholar 

  • Caballero-Casero N, Lunar L, Rubio S (2016) Analytical methods for the determination of mixtures of bisphenols and derivatives in human and environmental exposure sources and biological fluids. A review. Anal Chim Acta 908:22–53

    Article  CAS  Google Scholar 

  • Chang BV, Liu JH, Liao CS (2014) Aerobic degradation of bisphenol-A and its derivatives in river sediment. Environ Technol 35:416–424

    Article  CAS  Google Scholar 

  • Cobellis L, Colacurci N, Trabucco E, Carpentiero C, Grumetto L (2009) Measurement of bisphenol A and bisphenol B levels in human blood sera from healthy and endometriotic women. Biomed chromatogr 23:1186–1190

    Article  CAS  Google Scholar 

  • Cunha SC, Almeida C, Mendes E, Fernandes JO (2011) Simultaneous determination of bisphenol A and bisphenol B in beverages and powdered infant formula by dispersive liquid-liquid micro-extraction and heart-cutting multidimensional gas chromatography-mass spectrometry. Food Addit Contam 28:513–526

    Article  CAS  Google Scholar 

  • Cunha SC, Fernandes JO (2010) Quantification of free and total bisphenol A and bisphenol B in human urine by dispersive liquid-liquid microextraction (DLLME) and heart-cutting multidimensional gas chromatography-mass spectrometry (MD-GC/MS). Talanta 83:117–125

    Article  CAS  Google Scholar 

  • Gu J, Guo L, Zhu Y, Qian L, Shi L, Zhang H, Ji G (2023) Neurodevelopmental Toxicity of emamectin benzoate to the early life stage of zebrafish larvae (Danio rerio). Int J Mol Sci 24

  • Gu J, Guo M, Huang C, Wang X, Zhu Y, Wang L, Wang Z, Zhou L, Fan D, Shi L, Ji G (2021) Titanium dioxide nanoparticle affects motor behavior, neurodevelopment and axonal growth in zebrafish (Danio rerio) larvae. Sci Total Environ 754:142315

    Article  CAS  Google Scholar 

  • Gu J, Guo M, Yin X, Huang C, Qian L, Zhou L, Wang Z, Wang L, Shi L, Ji G (2022) A systematic comparison of neurotoxicity of bisphenol A and its derivatives in zebrafish. Sci Total Environ 805:150210

    Article  CAS  Google Scholar 

  • Gu J, Wang H, Zhou L, Fan D, Shi L, Ji G, Gu A (2020) Oxidative stress in bisphenol AF-induced cardiotoxicity in zebrafish and the protective role of N-acetyl N-cysteine. Sci Total Environ 731:139190

    Article  CAS  Google Scholar 

  • Gu J, Zhang J, Chen Y, Wang H, Guo M, Wang L, Wang Z, Wu S, Shi L, Gu A, Ji G (2019) Neurobehavioral effects of bisphenol S exposure in early life stages of zebrafish larvae (Danio rerio). Chemosphere 217:629–635

    Article  CAS  Google Scholar 

  • Huang M, Liu S, Fu L, Jiang X, Yang M (2020) Bisphenol A and its analogues bisphenol S, bisphenol F and bisphenol AF induce oxidative stress and biomacromolecular damage in human granulosa KGN cells. Chemosphere 253:126707

    Article  CAS  Google Scholar 

  • Huang Y, Tao Y, Cai C, Chen J, Ji C, Aniagu S, Jiang Y, Chen T (2021) Using immunofluorescence to detect PM2.5-induced DNA damage in zebrafish embryo hearts. J V Exp

  • Ike M, Chen MY, Danzl E, Sei K, Fujita M (2006) Biodegradation of a variety of bisphenols under aerobic and anaerobic conditions. Water Sci Technol 53:153–159

    Article  CAS  Google Scholar 

  • Ji G, Gu J, Guo M, Zhou L, Wang Z, Shi L, Gu A (2022) A systematic comparison of the developmental vascular toxicity of bisphenol A and its alternatives in vivo and in vitro. Chemosphere 291:132936

    Article  CAS  Google Scholar 

  • Kitamura S, Suzuki T, Sanoh S, Kohta R, Jinno N, Sugihara K, Yoshihara S, Fujimoto N, Watanabe H, Ohta S (2005) Comparative study of the endocrine-disrupting activity of bisphenol A and 19 related compounds. Toxicol Sci 84:249–259

    Article  CAS  Google Scholar 

  • Lai KP, Gong Z, Tse WKF (2021) Zebrafish as the toxicant screening model: Transgenic and omics approaches. Aquat Toxicol 234:105813

    Article  CAS  Google Scholar 

  • Li A, Zhuang T, Shi W, Liang Y, Liao C, Song M, Jiang G (2020) Serum concentration of bisphenol analogues in pregnant women in China. Sci Total Environ 707:136100

    Article  CAS  Google Scholar 

  • Li S, Dang YY, Oi Lam Che G, Kwan YW, Chan SW, Leung GP, Lee SM, Hoi MP (2014) VEGFR tyrosine kinase inhibitor II (VRI) induced vascular insufficiency in zebrafish as a model for studying vascular toxicity and vascular preservation. Toxicol Appl Pharmacol 280:408–420

    Article  CAS  Google Scholar 

  • Liao C, Kannan K (2013) Concentrations and profiles of bisphenol A and other bisphenol analogues in foodstuffs from the United States and their implications for human exposure. J Agric Food Chem 61:4655–4662

    Article  CAS  Google Scholar 

  • Liao C, Kannan K (2014) A survey of alkylphenols, bisphenols, and triclosan in personal care products from China and the United States. Arch Environ Contam Toxicol 67:50–59

    Article  CAS  Google Scholar 

  • Liu Y, Zhang S, Song N, Guo R, Chen M, Mai D, Yan Z, Han Z, Chen J (2017) Occurrence, distribution and sources of bisphenol analogues in a shallow Chinese freshwater lake (Taihu Lake): implications for ecological and human health risk. Sci Total Environ 599-600:1090–1098

    Article  CAS  Google Scholar 

  • Mocelin R, Herrmann AP, Marcon M, Rambo CL, Rohden A, Bevilaqua F, de Abreu MS, Zanatta L, Elisabetsky E, Barcellos LJ, Lara DR, Piato AL (2015) N-acetylcysteine prevents stress-induced anxiety behavior in zebrafish. Pharmacol Biochem Behav 139:121–126

    Article  CAS  Google Scholar 

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

  • Oggier DM, Lenard A, Küry M, Hoeger B, Affolter M, Fent K (2011) Effects of the protein kinase inhibitor PKC412 on gene expression and link to physiological effects in zebrafish Danio rerio eleuthero-embryos. Toxicol Sci 119:104–115

    Article  CAS  Google Scholar 

  • Ren F, Ji C, Huang Y, Aniagu S, Jiang Y, Chen T (2020) AHR-mediated ROS production contributes to the cardiac developmental toxicity of PM2.5 in zebrafish embryos. Sci Total Environ 719:135097

    Article  CAS  Google Scholar 

  • Salahinejad A, Attaran A, Naderi M, Meuthen D, Niyogi S, Chivers DP (2021) Chronic exposure to bisphenol S induces oxidative stress, abnormal anxiety, and fear responses in adult zebrafish (Danio rerio). Sci Total Environ 750:141633

    Article  CAS  Google Scholar 

  • Salim S (2017) Oxidative stress and the central nervous system. J Pharmacol Exp Ther 360:201–205

    Article  CAS  Google Scholar 

  • Serra H, Beausoleil C, Habert R, Minier C, Picard-Hagen N, Michel C (2019) Evidence for bisphenol B endocrine properties: scientific and regulatory perspectives. Environ Health Perspect 127:106001

    Article  Google Scholar 

  • Sun Y, Cao Y, Tong L, Tao F, Wang X, Wu H, Wang M (2020) Exposure to prothioconazole induces developmental toxicity and cardiovascular effects on zebrafish embryo. Chemosphere 251:126418

    Article  CAS  Google Scholar 

  • Tesoriero C, Greco F, Cannone E, Ghirotto F, Facchinello N, Schiavone M, Vettori A (2023) Modeling Human Muscular Dystrophies in Zebrafish: Mutant Lines, Transgenic Fluorescent Biosensors, and Phenotyping Assays. Int J Mol Sci 24(9):8314

    Article  CAS  Google Scholar 

  • Ullah A, Pirzada M, Jahan S, Ullah H, Turi N, Ullah W, Siddiqui MF, Zakria M, Lodhi KZ, Khan MM (2018) Impact of low-dose chronic exposure to bisphenol A and its analogue bisphenol B, bisphenol F and bisphenol S on hypothalamo-pituitary-testicular activities in adult rats: a focus on the possible hormonal mode of action. Food Chem Toxicol 121:24–36

    Article  CAS  Google Scholar 

  • Wang C, He J, Xu T, Han H, Zhu Z, Meng L, Pang Q, Fan R (2021) Bisphenol A(BPA), BPS and BPB-induced oxidative stress and apoptosis mediated by mitochondria in human neuroblastoma cell lines. Ecotoxicol Environ Saf 207:111299

    Article  CAS  Google Scholar 

  • Xia M, Wang X, Xu J, Qian Q, Gao M, Wang H (2021) Tris (1-chloro-2-propyl) phosphate exposure to zebrafish causes neurodevelopmental toxicity and abnormal locomotor behavior. Sci Total Environ 758:143694

    Article  CAS  Google Scholar 

  • Yan Z, Liu Y, Yan K, Wu S, Han Z, Guo R, Chen M, Yang Q, Zhang S, Chen J (2017) Bisphenol analogues in surface water and sediment from the shallow Chinese freshwater lakes: occurrence, distribution, source apportionment, and ecological and human health risk. Chemosphere 184:318–328

    Article  CAS  Google Scholar 

  • Yang L, Guo H, Kuang Y, Yang H, Zhang X, Tang R, Li D, Li L (2022) Neurotoxicity induced by combined exposure of microcystin-LR and nitrite in male zebrafish (Danio rerio): effects of oxidant-antioxidant system and neurotransmitter system. Comp Biochem Physiol C Toxicol Pharmacol 253:109248

    Article  CAS  Google Scholar 

  • Yang M, Huang J, Zhang S, Zhao X, Feng D, Feng X (2021a) Melatonin mitigated circadian disruption and cardiovascular toxicity caused by 6-benzylaminopurine exposure in zebrafish. Ecotoxicol Environ Saf 223:112555

    Article  CAS  Google Scholar 

  • Yang Q, Zhu Z, Liu Q, Chen L (2021b) Adverse effects of bisphenol B exposure on the thyroid and nervous system in early life stages of zebrafish. Comp Biochem Physiol C Toxicol Pharmacol 250:109167

    Article  CAS  Google Scholar 

  • Yang X, Liu H, Yang Q, Liu J, Chen J, Shi L (2016) Predicting anti-androgenic activity of bisphenols using molecular docking and quantitative structure-activity relationships. Chemosphere 163:373–381

    Article  CAS  Google Scholar 

  • Zhu J, Liu C, Wang J, Liang Y, Gong X, You L, Ji C, Wang SL, Wang C, Chi X (2021) Difenoconazole induces cardiovascular toxicity through oxidative stress-mediated apoptosis in early life stages of zebrafish (Danio rerio). Ecotoxicol Environ Saf 216:112227

    Article  CAS  Google Scholar 

  • Zhu XY, Wu YY, Xia B, Dai MZ, Huang YF, Yang H, Li CQ, Li P (2020) Fenobucarb-induced developmental neurotoxicity and mechanisms in zebrafish. Neurotoxicology 79:11–19

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (Grant No. NSFC82100340), the Scientific and Technological Projects of Henan Province (212102310439), the Medical Science and Technique Program of Henan (Grant No. LHGJ20210633, LHGJ2018020617), and the Henan Provincial Key Laboratory of Children’s Genetics and Metabolic Diseases Foundation (SS202203).

Author information

Author notes

  1. Fangjie Wang, Xiaocui Ma, and Qiqing Sun contributed equally to this work.

Authors and Affiliations

  1. Children’s Hospital Affiliated to Zhengzhou University, Henan Key Laboratory of Children’s Genetics and Metabolic Diseases, Zhengzhou Engineering Research Center of Zebrafish Models for Pediatric Diseases and Drug Screening, Henan Children’s Hospital, Zhengzhou Children’s Hospital, Zhengzhou, 450018, China

    Fangjie Wang, Xiaocui Ma, Qiqing Sun, Yaodong Zhang & Longfei Wang

  2. Nanjing Institute of Environmental Sciences, Key Laboratory of Pesticide Environmental Assessment and Pollution Control, Ministry of Ecology and Environment, Nanjing, 210042, China

    Jie Gu

  3. Woman & Infants Hospital of Zhengzhou, Zhengzhou Maternity Hospital Affiliated to Henan University, Zhengzhou, 450012, China

    Yanjie Liu & Longfei Wang

Authors
  1. Fangjie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaocui Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qiqing Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yaodong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yanjie Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jie Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Longfei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization, L.W.; methodology, L.W., J.G., and F.W.; software, Q.S., Y.Z., and Y.L.; formal analysis, investigation, F.W., X.M., and Y.L.; resources, L.W. and Y.Z.; data curation, writing—original draft preparation, F.W., X.M., and Q.S.; writing—review and editing, L.W. and J.G.; visualization F.W., L.W., and J.G; supervision, project administration, L.W.; All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Longfei Wang.

Ethics declarations

Ethical approval

All animal experiments were conducted in accordance with the regulations of the relevant laws and approved by the Ethics Committee of the Children’s Hospital Affiliated to Zhengzhou University with approval/protocol number (2022-k-071).

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Bruno Nunes

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, ., Ma, X., Sun, Q. et al. Bisphenol B induces developmental toxicity in zebrafish via oxidative stress. Environ Sci Pollut Res (2023). https://doi.org/10.1007/s11356-023-31161-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11356-023-31161-9

Keywords

Search

Navigation