Abstract
Alkylphenols are well-known endocrine disruptors and may cause developmental and reproductive disorders in aquatic organisms. Daphnia magna is commonly used in ecotoxicological studies as a promising model species to investigate the effects of endocrine distruptors. In the present study, transcriptional modulation of eleven potential molecular indicators related to detoxification, antioxidant, development, and cellular stress was analyzed in D. magna exposed to different concentrations of bisphenol A (BPA) and 4-nonylphenol (4-NP) for 24 h and 48 h, using real-time qPCR. A hierarchical clustering analysis was applied to investigate relations among molecular markers depending on the compound, exposure duration, and concentration. Our findings suggested that GSH-related systems and stress proteins may be involved in cellular defense against BPA and 4-NP-mediated toxicity with different modes of action. Furthermore, these compounds may interrupt molting and reproduction in daphnids. In particular, D. magna GSH-related genes seem to be strongly affected by 4-NP exposure, indicating their potential as molecular biomarkers.
Similar content being viewed by others
References
Barbosa IA, Martins RM, Sá e Melo ML, Soares AMVM (2003) Acute and chronic toxicity of dimethyl sulfoxide to Daphnia magna. Bull Environ Contam Toxicol 70:1264–1268
Bhattacharjee A, Chakraborty K, Shukla A (2017) Cellular copper homeostasis: current concepts on its interplay with glutathione homeostasis and its implication in physiology and human diseases. Metallomics 9:1376–1388
Brennan SJ, Brougham CA, Roche JJ, Fogarty AM (2006) Multi-generational effects of four selected environmental oestrogens on Daphnia magna. Chemosphere 64:49–55
Colbourne JK, Pfrender ME, Gilbert D et al. (2011) The ecoresponsive genome of Daphnia pulex. Science 331:555–561
Dagnino A, Allen JI, Moore MN, Broeg K, Canesi LV, iarengo A (2007) Development of an expert system for the integration of biomarker responses in mussels into an animal health index. Biomarkers 12:155–172
EN ISO 6341 (2012) Water quality—determination of the inhibition of the mobility of Daphnia magna Straus (Cladocera, Crustacea)—acute toxicity test. EN ISO 6341:2012. European Committee for Standardization, Brussels
Forget-Leray J, Landriau I, Minier C, Leboulenger F (2005) Impact of endocrine toxicants on survival, development, and reproduction of the estuarine copepod Eurytemora affinis (Poppe). Ecotoxicol Environ Saf 60:288–294
Grignard E, Lapenna S, Bremer S (2012) Weak estrogenic transcriptional activities of Bisphenol A and Bisphenol S. Toxicol Vitr 26:727–731
Gross MY, Maycock DS, Thorndyke MC, Morritt D, Crane M (2001) Abnormalities in sexual development of the amphipod Gammarus pulex (L.) found below sewage treatment works. Environ Toxicol Chem 20:1792–1797
Handler AM, Postlethwait JH (2005) Regulation of vitellogenin synthesis in Drosophila by ecdysterone and juvenile hormone. J Exp Zool 206:247–254
Hannas BR, Wang YH, Thomson S, Kwon G, Li H, LeBlanc GA (2011) Regulation and dysregulation of vitellogenin mRNA accumulation in daphnids (Daphnia magna). Aquat Toxicol 101:351–357
Holmgren A, Johansson C, Berndt C, Lonn ME, Hudemann C, Lillig CH (2005) Thiol redox control via thioredoxin and glutatredoxin systems. Biochem Soc Trans 33:1375–1377
Hwang DS, Lee JS, Lee KW et al. (2010) Cloning and expression of ecdysone receptor (EcR) from the intertidal copepod, Tigriopus japonicus. Comp Biochem Physiol C 151(3):303–312
Jeong SW, Lee SM, Yum SS, Iguchi T, Seo YR (2013) Genomic expression responses toward bisphenol-A toxicity in Daphnia magna in terms of reproductive activity. Mol Cell Toxicol 9:149–158
Kang Y, Yan X, Li L, Zhang Q, Zeng L, Luo J (2014) Daphnia magna may serve as a powerful tool in screening endocrine disruption chemicals (EDCs). Environ Sci Technol 48:881–882
Kato Y, Kobayashi K, Oda S, Tatarazako N, Watanabe H, Iguchi T (2007) Cloning and characterization of the ecdysone receptor and ultraspiracle protein from the water flea Daphnia magna. J Endocrinol 193:183–194
Kim H, Yim B, Bae C, Lee YM (2017) Acute toxicity and antioxidant responses in the water flea Daphnia magna to xenobiotics (cadmium, lead, mercury, bisphenol A, and 4-nonylphenol). Toxicol Environ Health Sci 9:41–49
Lauritano C, Procaccini G, Ianora A (2012) Gene expression patterns and stress response in marine copepods. Mar Environ Res 76:22–31
Li X, Lin L, Luan T, Yang L, Lan C (2008) Effects of landfill leachate effluent and bisphenol A on glutathione and glutathione-related enzymes in the gills and digestive glands of the freshwater snail Bellamya purificata. Chemosphere 70:1903–1909
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
Matozzo V, Gagné F, Marin MG, Ricciardi F, Blaise C (2008) Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates: a review. Environ Int 34:531–545
Moore MN, Depledge MH, Readman JW, Leonard DP (2004) An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management. Mutat Res Fund Mol M 552:247–268
Mu X, Rider CV, Hwang GS, Hoy H, LeBlanc GA (2005) Covert signal disruption: anti-ecdysteroidal activity of bisphenol A involves cross talk between signalling pathways. Environ Toxicol Chem 24:146–152
Nair PMG, Park SY, Choi J (2011) Expression of catalase and glutathione S-transferase genes in Chironomus riparius on exposure to cadmium and nonylphenol. Comp Biochem Physiol C 154(4):399–408
Park SY, Choi J (2009) Genotoxic effects of nonylphenol and bisphenol A exposure in aquatic biomonitoring species: freshwater crustacean, Daphnia magna, and aquatic midge, Chironomus riparius. Bull Environ Contam Toxicol 83:463–468
Park K, Kwak IS (2014) Characterize and Gene Expression of Heat Shock Protein 90 in Marine Crab Charybdis japonica following Bisphenol A and 4-Nonylphenol Exposures. Environ Health Toxicol 29:e2014002
Planelló R, Martinez-Guitarte JL, Morcillo G (2008) The endocrine disruptor bisphenol A increases the expression of HSP70 and ecdysone receptor genes in the aquatic larvae of Chironomus riparius. Chemosphere 71:1870–1876
Puinean AM, Rotchell JM (2006) Vitellogenin gene expression as a biomarker of endocrine disruption in the invertebrate. Mytilus edulis Mar Environ Res 62:S211–S214
Rhee JS, Raisuddin S, Lee KW et al. (2009) Heat shock protein (Hsp) gene responses of the intertidal copepod Tigriopus japonicus to environmental toxicants. Comp Biochem Physiol C 149(1):104–112
Rotchell J, Ostrander G (2003) Molecular markers of endocrine disruption in aquatic organisms. J Toxicol Environ Health B 6:453–496
Sharma VK, Anquandah GA, Yngard RA et al. (2009) Nonylphenol, octylphenol, and bisphenol-A in the aquatic environment: a review on occurrence, fate, and treatment. J Environ Sci Health A 44:423–442
Shaw JR, Pfrender ME, Eads BD et al (2008) Daphnia as an emerging model for toxicological genomics. Adv Exp Biol 2:165–328
Sheehan D, Meade G, Foley VM, Dowd CA (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem J 360:1–16
Soares A, Guieysse B, Jefferson B, Cartmell E, Lester JN (2008) Nonylphenol in the environment: a critical review on occurrence, fate, toxicity and treatment in wastewaters. Environ Int 34:1033–1049
Tokishita S, Kato Y, Kobayashi T, Nakamura S, Ohta T, Yamagata H (2006) Organization and repression by juvenile hormone of a vitellogenin gene cluster in the crustacean, Daphnia magna. Biochem Biophy Res Comm 345:362–370
Watts MM, Pascoe D, Carroll K (2003) Exposure to 17α-ethinylestradiol and bisphenol A—effects on larval moulting and mouthpart structure of Chironomus riparius. Ecotoxicol Environ Saf 54:207–215
Yao TP, Forman BM, Jiang Z et al. (1993) Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature 366:476–479
Yazdani M, Andresen AM, Gjøen T (2016) Short-term effect of bisphenol-a on oxidative stress responses in Atlantic salmon kidney cell line: a transcriptional study. Toxicol Mech Methods 26:295–300
Wu M, Xu H, Shen Y, Qiu W, Yang M (2011) Oxidative stress in zebrafish embryos induced by short‐term exposure to bisphenol A, nonylphenol, and their mixture. Environ Toxicol Chem 30:2335–2341
Yuan HX, Sima YH, Xu SQ (2013) Differential Effects of 4-n-Nonylphenol on Glutathione, Glutathione S-Transferase, and Glutathione Peroxidase on Gonads in Different Developmental Stages in the Bombyx mori (Lepidoptera: Bombycidae). Ann Entomol Soc Am 106:832–839
Zitka O, Skalickova S, Gumulec J et al. (2012) Redox status expressed as GSH: GSSG ratio as a marker for oxidative stress in paediatric tumour patients. Oncol Let 4:1247–1253
Acknowledgements
This work was supported by a grant from the National Research Foundation of Korea (NRF-2016R1A2B4009939) funded to Young-Mi Lee.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
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
Kim, RO., Kim, H. & Lee, YM. Evaluation of 4-nonylphenol and bisphenol A toxicity using multiple molecular biomarkers in the water flea Daphnia magna. Ecotoxicology 28, 167–174 (2019). https://doi.org/10.1007/s10646-018-2009-2
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-018-2009-2