Abstract
Benzophenone-3 (BP-3) is one of the most used UV filters. The present study aimed to evaluate the toxic effects of BP-3 during embryo stages of zebrafish four hours post-fertilization (4hpf). Embryos were exposed to 0, 1, and 10 µg L−1 of BP-3 for 72 h. We investigated biochemical and molecular biomarkers of neurotoxicity (AChE) and the antioxidant system (gene expression of catalase, CAT, superoxide dismutase, SOD, glutathione peroxidase, GPX, the concentration of total glutathione, GSH, and lipid hydroperoxides, LPO). Results indicated that the acute exposure to BP-3 in zebrafish embryos did not show significant differences in survival, hatching rate, or antioxidant system biomarkers. In contrast, there were significant differences associated with AChE gene expression and activity.
Similar content being viewed by others
References
Bae J, Kim S, Kannan K, Louis GMB (2016) Couples’ urinary concentrations of benzophenone-type ultraviolet filters and the secondary sex ratio. Sci Total Environ 543:28–36. https://doi.org/10.1016/j.scitotenv.2015.11.019
Balmer ME, Buser HR, Müller MD, Poiger T (2005) Occurrence of some organic UV filters in wastewater, surface waters and in fish from Swiss lakes. Environ Sci Technol 39:953–962. https://doi.org/10.1021/es040055r
Belluti F, Bartolini M, Bottegoni G, Bisi A, Cavalli A, AndrisanoV RA (2011) Benzophenone-based derivatives: a novel series of potent and selective dual inhibitors of acetylcholinesterase and acetylcholinesterase-induced beta-amyloid aggregation. Eur J Med Chem 46:1682–1693. https://doi.org/10.1016/j.ejmech.2011.02.019
Blüthgen N, Zucchi S, Fent K (2012) Effects of the UV filter benzophenone-3 (oxybenzone) at low concentrations in zebrafish (Danio rerio). Toxicol Apl Pharmacol 263:184–194. https://doi.org/10.1016/j.taap.2012.06.008
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Broniowska Z, Bystrowska B, Starek-Swiechowicz B, Pomierny B, Krzyżanowska W, Walczak M, Budziszewska B (2019) Benzophenone-2 concentration and its effect on oxidative stress and apoptosis markers in rat brain. Neurotox Res 36:39–48. https://doi.org/10.1007/s12640-019-0011-y
Campos D, Gravato C, Fedorova G, Burkina V, Soares AMVM, Pestana JLT (2017) Ecotoxicity of two organic UV-filters to the freshwater caddisfly Sericostoma vittatum. Environ Pollut 228:370–377. https://doi.org/10.1016/j.envpol.2017.05.021
Cao F, Liu X, Wang Ch, Zheng M, Li X, Qiu L (2016) Acute and short-term developmental toxicity of cyhalofop-butyl to zebrafish (Danio rerio). Environ Sci Pollut Res 23:10080–10089. https://doi.org/10.1007/s11356-016-6236-x
Colović MB, Krstić DZ, Lazarević-Pašti TD, Bondžić AM, Vasić VM (2013) Acetylcholinesterase inhibitors: pharmacology and toxicology. Curr Neuropharmacol 11(3):315–335. https://doi.org/10.2174/1570159X11311030006
Ellman GL, Courtney D, Valentino A Jr, Featherstone RF (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. https://doi.org/10.1016/0006-2952(61)90145-9
Feduik DJ, Wang T, Raizman JE, Parkinson FE, Gu X (2010) Tissue deposition of the insect repellent DEET and the sunscreen oxybenzone from repeated topical skin applications in rats. Int J Toxicol 29:594–603. https://doi.org/10.1177/1091581810380147
Frikeche J, Couteau C, Roussakis C, Coiffard LJM (2015) Research on the immunosuppressive activity of ingredients contained in sunscreens. Arch Dermatol Res 307:211–218. https://doi.org/10.1007/s00403-014-1528-9
Gonzalez P, Baudrimont M, Boudou A, Bourdineaud JP (2006) Comparative effects of direct cadmium contamination on gene expression in gills, liver, skeletal muscles and brain of the zebrafish (Danio rerio). Biometals 19:225–235. https://doi.org/10.1007/s10534-005-5670-x
He T, Tsui MMP, Tan CJ, Ng KY, Guo FW, Wang LH, Chen TH, Fan TY, Lam PKS, Murphy MB (2019) Comparative toxicities of four benzophenone ultraviolet filters to two life stages of two coral species. STOTEN 651:2391–2399. https://doi.org/10.1016/j.scitotenv.2018.10.148
Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310. https://doi.org/10.1002/aja.1002030302
Krause M, Klit A, Blomberg-Jensen M, Søeborg T, Frederiksen H, Schlumpf M, Lichtensteiger W, Skakkebaek NE, Drzewiecki KT (2012) Sunscreens: are they beneficial for health? An overview of endocrine disrupting properties of UV-filters. Int J Androl 35:424–436. https://doi.org/10.1111/j.1365-2605.2012.01280.x
Le Fol V, Brion F, Hillenweck A, Perdu E, Bruel S, Aït-Aïssa S, Cravedi JP, Zalko D (2017) Comparison of the in vivo biotransformation of two emerging estrogenic contaminants, BP2 and BPs, in zebrafish embryos and adults. Int J Mol Sci 18:704. https://doi.org/10.3390/ijms18040704
Legendre P, Legendre L (1998) Numerical ecology, 2nd English edn. Elsevier, Amsterdam, p 853
Lei M, Zhang L, Lei J, Zong L, Li J, Wu Z, Wang Z (2015) Overview of emerging contaminants and associated human health effects. BioMed Res Int 2015:404796. https://doi.org/10.1155/2015/404796
Li AJ, Law JC, Chow C, Huang Y, Li K, Leung KS (2018) Joint effects of multiple UV filters on zebrafish embryo development. Environ Sci Technol 52:9460–9467. https://doi.org/10.1021/acs.est.8b02418
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Mihaljević B, Katušin-Ražem B, Ražem D (1996) The reevaluation of the ferric thiocyanate assay for lipid hydroperoxides with special considerations of the mechanism aspects of the response. Free Radic Biol Med 21:53–63. https://doi.org/10.1016/0891-5849(95)02224-4
Mu X, Pang S, Sun X, Gao J, Chen J, Chen X, Li X, Wang C (2013) Evaluation of acute and developmental effects of difenoconazole via multiple stage zebrafish assays. Environ Pollut 175:147–157. https://doi.org/10.1016/j.envpol.2012.12.029
Muñiz-González AB, Martínez-Guitarte JL (2018) Effects of single exposure and binary mixtures of ultraviolet filters octocrylene and 2-ethylhexyl 4-(dimethylamino) benzoate on gene expression in the freshwater insect Chironomus riparius. Environ Sci Pollut Res Int 25:35501–35514. https://doi.org/10.1007/s11356-018-3516-7
Negro CL, Senkman LE, Marino F, Lorenzatti E, Collins P (2014) Effects of chlorpyrifos and endosulfan on different life stages of the freshwater burrowing crab Zilchiopsis collastinensis P.: protective role of chorion. Bull Environ Contam Toxicol 92:625–630. https://doi.org/10.1007/s00128-014-1239-0
OECD (1998) Test No. 212: fish, short-term toxicity test on embryo and sac-fry stages, OECD Guidelines for the Testing of Chemicals, Section 2, OECD Publishing
Praskova E, Plhalova L, Chromcova L, Stepanova S, Bedanova I, Blahova J, Hostovsky M, Skoric M, Maršálek P, Voslarova E, Svobodova Z (2014) Effects of subchronic exposure of diclofenac on growth, histopathological changes, and oxidative stress in zebrafish (Danio rerio). Sci World J. https://doi.org/10.1155/2014/645737
Ramos S, Homem V, Alves A, Santos L (2016) A review of organic UV-filters in wastewater treatment plants. Environ Int 86:24–44. https://doi.org/10.1016/j.envint.2015.10.004
Rodríguez-Fuentes G, Sandoval-Gío JJ, Arroyo-Silva A, Noreña-Barroso E, Escalante-Herrera KS, Olvera-Espinosa F (2015a) Evaluation of the estrogenic and oxidative stress effects of the UV filter 3-benzophenone in zebrafish (Danio rerio) eleuthero-embryos. Ecotox Environ Safe 115:14–18. https://doi.org/10.1016/j.ecoenv.2015.01.033
Rodríguez-Fuentes G, Rubio-Escalante FJ, Noreña-Barroso E, Escalante-Herrera KS, Schlenk D (2015b) Impacts of oxidative stress on acetylcholinesterase transcription, and activity in embryos of zebrafish (Danio rerio) following Chlorpyrifos exposure. Comp Biochem Phys C 172–173:19–25. https://doi.org/10.1016/j.cbpc.2015.04.003
Ruszkiewicz JA, Pinkas A, Ferrer B, PeresTV TA, Aschner M (2017) Neurotoxic effect of active ingredients in sunscreen products, a contemporary review. Toxicol Rep 4:245–259. https://doi.org/10.1016/j.toxrep.2017.05.006
Sharifan H, Klein D, Morse AN (2016) UV filters are an environmental threat in the Gulf of Mexico: a case study of Texas coastal zones. Oceanologia 58:327–335. https://doi.org/10.1016/j.oceano.2016.07.002
Acknowledgements
This project was funded by the Postdoctoral Fellowship Program of the Mexican National Council of Science and Technology (CONACyT) and by the National Autonomous University of Mexico IACOD Grant # IC200111.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Sandoval-Gío, J.J., Noreña-Barroso, E., Escalante-Herrera, K. et al. Effect of Benzophenone-3 to Acetylcholinesterase and Antioxidant System in Zebrafish (Danio rerio) Embryos. Bull Environ Contam Toxicol 107, 814–819 (2021). https://doi.org/10.1007/s00128-021-03277-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00128-021-03277-6