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Aryl hydrocarbon receptor (AhR) inducers and estrogen receptor (ER) activities in surface sediments of Three Gorges Reservoir, China evaluated with in vitro cell bioassays

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Abstract

Two types of biological tests were employed for monitoring the toxicological profile of sediment cores in the Three Gorges Reservoir (TGR), China. In the present study, sediments collected in June 2010 from TGR were analyzed for estrogen receptor (ER)- and aryl hydrocarbon receptor (AhR)-mediated activities. The estrogenic activity was assessed using a rapid yeast estrogen bioassay, based on the expression of a green fluorescent reporter protein. Weak anti-estrogenic activity was detected in sediments from an area close to the dam of the reservoir, and weak estrogenic activities ranging from 0.3 to 1 ng 17β-estradiol (E2) equivalents (EQ) g−1 dry weight sediment (dw) were detected in sediments from the Wanzhou to Guojiaba areas. In the upstream areas Wanzhou and Wushan, sediments demonstrated additive effects in co-administration of 1 nM E2 in the yeast test system, while sediments from the downstream Badong and Guojiaba areas showed estrogenic activities which seemed to be more than additive (synergistic activity). There was an increasing tendency in estrogenic activity from upstream of TGR to downstream, while this tendency terminated and converted into anti-estrogenic activity in the area close to the dam. The AhR activity was detected employing rat hepatoma cell line (H4IIE). EROD activities were found homogenously distributed in sediments in TGR ranging from 200 to 311 pg 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) EQ g−1 dw for total AhR agonists and from 45 to 76 pg TCDD EQ g−1 dw for more persistent AhR agonists. The known AhR agonists polycyclic aromatic hydrocarbon, polychlorinated biphenyl, and PCDD/F only explained up to 8 % of the more persistent AhR agonist activity in the samples, which suggests that unidentified AhR-active compounds represented a great proportion of the TCDD EQ in sediments from TGR. These findings of estrogenic potential and dioxin-like activity in TGR sediments provide possible weight-of-evidence of potential ecotoxicological causes for the declines in fish populations which have been observed during the past decades in TGR.

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References

  • Ahlf W, Heise S (2005) Sediment toxicity assessment. Rationale for effect classes. J Soils Sediments 5:16–20

    Article  CAS  Google Scholar 

  • Ahlf W, Hollert H, Neumann-Hensel H, Ricking M (2002) A guidance for the assessment and evaluation of sediment quality: a German approach based on ecotoxicological and chemical measurements. J Soils Sediments 2:37–42

    Article  CAS  Google Scholar 

  • Andersen AG, Jensen TK, Carlsen E, Jorgensen N, Andersson AM, Krarup T et al (2000) High frequency of sub-optimal semen quality in an unselected population of young men. Hum Reprod 15:366–372

    Article  CAS  Google Scholar 

  • Bovee TFH, Pikkemaat MG (2009) Bioactivity-based screening of antibiotics and hormones. J Chrom A 1216:8035–8050

    Article  CAS  Google Scholar 

  • Bovee TFH, Helsdingen RJR, Koks PD, Kuiper HA, Hoogenboom RLAP, Keijer J (2004) Development of a rapid yeast estrogen bioassay, based on the expression of green fluorescent protein. Gene 325:187–200

    Article  CAS  Google Scholar 

  • Bovee TFH, Heskamp HH, Hamers ARM, Hoogenboom LAP, Nielen MWF (2005) Validation of a rapid yeast estrogen bioassay, based on the expression of green fluorescent protein, for the screening of estrogenic activity in calf urine. Anal Chim Acta 529:57–64

    Article  CAS  Google Scholar 

  • Bovee TFH, Bor G, Heskamp HH, Hoogenboom LAP, Nielen MWF (2006) Validation and application of a robust yeast estrogen bioassay for the screening of estrogenic activity in animal feed. Food Addit Contam 23:556–568

    Article  CAS  Google Scholar 

  • Bovee TFH, Thevis M, Hamers ARM, Peijnenburg AACM, Nielen MWF, Schoonen WGEJ (2010) SERMs and SARMs: detection of their activities with yeast based bioassays. JSBMB 118:85–92

    CAS  Google Scholar 

  • Brack W (2003) Effect-directed analysis: a promising tool for the identification of organic toxicants in complex mixtures? Anal Bioanal Chem 377:397–407

    Article  CAS  Google Scholar 

  • CCME (2002) Canadian soil quality guidelines for the protection of environmental and human health: dioxins and furans. Canada, Winnipeg

  • CCME (2010) Canadian soil quality guidelines for the protection of environmental and human health: carcinogenic and other PAHs. Canada, Winnipeg

  • Chen L, Shen C, Tang X, Chen C, Chen Y (2012) Estrogenic effects of dissolved matter and its impact on the activity of 17β-estradiol. Environ Sci Pollut Res 19:522–528

    Article  CAS  Google Scholar 

  • Chen L, Bi Y, Zhu K, Hu Z, Zhao W, Henkelmann B, Bernhöft S, Temoka C, Schramm K-W (2013) Contamination status of dioxins in sediment cores from the Three Gorges Dam area, China. Environ Sci Pollut Res 20:4268–4277

    Article  CAS  Google Scholar 

  • Conroy O, Sáez AE, Quanrud D, Ela W, Arnold RG (2007) Changes in estrogen/anti-estrogen activities in ponded secondary effluent. Sci Tot Environ 382:311–323

    Article  CAS  Google Scholar 

  • Den Besten PJ, de Deckere E, Babut MP, Power B, DelValls TA, Zago C, Oen AMP, Heise S (2003) Biological effects-based sediment quality in ecological risk assessment for European waters. J Soils Sediments 3:144–162

    Article  Google Scholar 

  • Denison MS, Zhao B, Baston DS, Clark GC, Murata H, Han D (2004) Recombinant cell bioassay systems for the detection and relative quantitation of halogenated dioxins and related chemicals. Talanta 63:1123–1133

    Article  CAS  Google Scholar 

  • DeVito M, Birnbaum LS (1994) Toxicology of the dioxins and related chemicals. In: Schecter A (ed) Dioxins and health. Plenum, New York, pp 139–162

    Chapter  Google Scholar 

  • Donato MT, Gomez-Lechon MJ, Castell JV (1993) A micro assay for measuring cytochrome P450IA1 and P450IIB1 activities in intact human and rat hepatocytes cultured on 96-well plates. Anal Biochem 213:29–33

    Article  CAS  Google Scholar 

  • Forstner U, Westrich B (2005) BMBF coordinated research project SEDYMO (2002-2006): sediment dynamics and pollutant mobility in river basins. J Soils Sediments 5:134–138

    Article  Google Scholar 

  • Garcia-Reyero N, Pina B, Grimalt JO (2005) Estrogenic activity in sediments from European mountain lakes. Environ Sci Technol 39:1427–1436

    Article  CAS  Google Scholar 

  • Giesy JP, Hilscherova K, Jones PD, Kannan K, Machala M (2002) Cell bioassays for detection of aryl hydrocarbon (AhR) and estrogen receptor (ER) mediated activity in environmental samples. Mar Pollut Bull 45:3–16

    Article  CAS  Google Scholar 

  • Grund S, Higley E, Schönenberger R, Suter MJ-F, Giesy JP, Braunbeck T, Hecker M, Hollert H (2011) The endocrine disrupting potential of sediments from the Upper Danube River (Germany) as revealed by in vitro bioassays and chemical analysis. Environ Sci Pollut Res 18:446–460

    Article  CAS  Google Scholar 

  • Hankinson O (1995) The aryl hydrocarbon receptor complex. Ann Rev Pharmacol Toxicol 35:307–340

    Article  CAS  Google Scholar 

  • Hong S, Khim JS, Naile JE, Park J, Kwon B-O, Wang T, Lu Y, Shim WJ, Jones PD, Giesy JP (2012) AhR-mediated potency of sediments and soils in estuarine and coastal areas of the Yellow Sea region: a comparison between Korea and China. Environ Pollut 171:216–225

    Article  CAS  Google Scholar 

  • Houtman CJ, Booij P, Jover E, Pascual del Rio D, Swart K, van Velzen M, Vreuls R, Legler J, Brouwer A, Lamoree MH (2006) Estrogenic and dioxin-like compounds in sediment from Zierikzee harbor identified with CALUX assay-directed fractionation combined with one and two dimensional gas chromatography analyses. Chemosphere 65:2244–2252

    Article  CAS  Google Scholar 

  • Huang L (2006) Impacts of hydraulic works on fish biodiversity in the Yangtze River valley and countermeasures. J Lake Sci 18:553–556

    Google Scholar 

  • Jacobs MN, Laws SC, Willett K, Schmieder P, Odum J, Bovee TF (2013) In vitro metabolism and bioavailability tests for endocrine active substances: what is needed next for regulatory purposes? ALTEX 30:331–351

    Article  Google Scholar 

  • Jeffries MKS, Conoan NH, Cox MB, Sangster JL, Balsiger HA, Bridges AA, Cowman T, Knight LA, Bartelt-Hunt SL, Kolok AS (2011) The anti-estrogenic activity of sediments from agriculturally intense watersheds: assessment using in vivo and in vitro assays. Aquat Toxicol 105:189–198

    Article  Google Scholar 

  • Jones JM, Anderson JW, Tukey RH (2000) Using the metabolism of PAHs in a human cell line to characterize environmental samples. Environ Toxicol Pharmacol 8:119–126

    Article  CAS  Google Scholar 

  • Karlsson J, Sundberg H, Åkerman G, Grunder K, Eklund B, Breitholtz M (2008) Hazard identification of contaminated sites-ranking potential toxicity of organic sediment extracts in crustacean and fish. J Soils Sediments 8:263–274

    Article  CAS  Google Scholar 

  • Kinani S, Bouchonnet S, Creusot N, Bourcier S, Balaguer P, Porcher JM et al (2010) Bioanalytical characterization of multiple endocrine- and dioxin-like activities in sediments from reference and impacted small rivers. Environ Pollut 158:74–83

    Article  CAS  Google Scholar 

  • Koh C-H, Khim JS (2005) Instrumental and bioanalytical measures of dioxin-like and estrogenic compounds and activities associated with sediment from the Korean coast. Ecotox Environ Safe 61:366–379

    Article  CAS  Google Scholar 

  • Koh C-H, Khim JS, Villeneuve DL, Kannan K, Giesy JP (2006) Characterization of trace organic contaminants in marine sediment from Yeongi Bay, Korea: 2. Dioxin-like and estrogenic activities. Environ Pollut 142:48–57

    Article  CAS  Google Scholar 

  • Labadie P, Cundy AB, Stone K, Andrews M, Valbonesi S, Hill EM (2007) Evidence for the migration of steroidal estrogens through river bed sediments. Environ Sci Technol 41:4299–4304

    Article  CAS  Google Scholar 

  • Lee CJ, Rasmussen TJ (2006) Occurrence of organic wastewater compounds in effluent-dominated streams in Northeastern Kansas. Sci Tot Environ 371:258–269

    Article  CAS  Google Scholar 

  • Legler J, Dennekamp M, Vethaak AD, Brouwer A, Koeman JH, van der Burg B, Murk AJ (2002) Detection of estrogenic activity in sediment-associated compounds using in vitro reporter gene assays. Sci Tot Environ 293:69–83

    Article  CAS  Google Scholar 

  • Levy W, Henkelmann B, Bernhöft S, Bovee T, Buegger F, Jakobi G, Kirchner M, Bassan R, Kräuchi N, Moche W, Offenthaler I, Simončič P, Weiss P, Schramm K-W (2011) Persistent aryl hydrocarbon receptor inducers increase with altitude, and estrogen-like disrupters are low in soils of the Alps. Environ Sci Pollut Res 18:99–110

    Article  CAS  Google Scholar 

  • Lu GH, Song WT, Wang C, Yan ZH (2010) Assessment of in vivo estrogenic response and the identification of environmental estrogens in the Yangtze River (Nanjing section). Chemosphere 80:982–990

    Article  CAS  Google Scholar 

  • Luo J, Ma M, Zha J, Wang Z (2009) Characterization of aryl hydrocarbon receptor agonists in sediments of Wenyu River, Beijing, China. Water Res 43:2441–2448

    Article  CAS  Google Scholar 

  • Maenpaa K, Kukkonen JV (2006) Bioaccumulation and toxicity of 4-nonylphenol (4-NP) and 4-(2-dodecyl)-benzene sulfonate (LAS) in Lumbriculus variegatus (Oligochaeta) and Chironomus riparius (Insecta). Aquat Toxicol 77:329–338

    Article  CAS  Google Scholar 

  • Maenpaa K, Sorsa K, Lyytikainen M, Leppanen MT, Kukkonen JVK (2008) Bioaccumulation, sublethal toxicity, and biotransformation of sediment-associated pentachlorophenol in Lumbriculus variegates (Oligochaeta). Ecotoxicol Environ Safety 69:121–129

    Article  CAS  Google Scholar 

  • Meerts IATM, Letcher RJ, Hoving S, Lemmen JG, van der Burg B, Brouwer A (2001) In vitro estrogenicity of polybrominated diphenyl ethers, hydroxylated PBDEs, and polybrominated bisphenol a compounds. Environ Health Perspect 109:399–407

    Article  CAS  Google Scholar 

  • Ministry of Environmental Protection of China (2012) Bulletin on the ecological and environmental monitoring results of the Three Gorges Project. http://english.mep.gov.cn/down-load/Documents/. Accessed 12 April 2012

  • Nelson J, Bishay F, van Roodselaar A, Ikonomou M, Law FCP (2007) The use of in vitro bioassays to quantify endocrine disrupting chemicals in municipal wastewater treatment plant effluents. Sci Tot Environ 374:80–90

    Article  CAS  Google Scholar 

  • Oh S-M, Park K, Chung K-H (2006) Combination of in vitro bioassays encompassing different mechanisms to determine the endocrine-disrupting effects of river water. Sci Tot Environ 354:252–264

    Article  CAS  Google Scholar 

  • Peck M, Gibson RW, Kortenkamp A, Hill EM (2004) Sediments are major sinks of steroidal estrogens in two United Kingdom rivers. Environ Toxicol Chem 23:945–952

    Article  CAS  Google Scholar 

  • Peck MR, Labadie P, Minier C, Hill EM (2007) Profiles of environmental and endogenous in the zebra mussel Dreissena polymorpha. Chemosphere 69:1–8

    Article  CAS  Google Scholar 

  • Pedersen KH, Pedersen SN, Pedersen KI, Korsgaard B, Bjerregard P (2003) Estrogenic effects of dietary 4-tert-octylphenol in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 62:295–303

    Article  CAS  Google Scholar 

  • Peng G (2006) Present state and protection countermeasure for fishery resources in the Yangtze River in Jiangsu section. Fish Eco Res 23:18–21

    Google Scholar 

  • Pickford KA, Thomas-Jones RE, Wheals B, Tyler CR, Sumpter JP (2003) Route of exposure affects the oestrogenic response of fish to 4-tert-nonylphenol. Aquat Toxicol 65:267–279

    Article  CAS  Google Scholar 

  • Qiao M, Huang S-B, Wang Z (2009) Evaluation of chronic toxicities from sediments before and after ecological project in Meiliang Bay, Lake Taihu, using cell bioassays. Ecol Eng 35:1631–1636

    Article  Google Scholar 

  • Rijk JCW, Bovee TFH, Wang S, Van Poucke C, Van Peteghem C, Nielen MWF (2009) Detection of anabolic steroids in dietary supplements: the added value of an androgen yeast bioassay in parallel with a chromatography-tandem mass spectrometry screening method. Anal Chim Acta 637:305–314

    Article  CAS  Google Scholar 

  • Rodgers-Gray TP, Jobling S, Kelly C, Morris S, Brighty G, Waldock MJ et al (2001) Exposure of juvenile roach (Rutilus rutilus) to treated sewage effluent induces dose-dependent and persistent disruption in gonadal duct development. Environ Sci Technol 35:462–470

    Article  CAS  Google Scholar 

  • Schwirzer SMG, Hofmaier AM, Kettrup A, Nerdinger PE, Schramm K-W, Thoma H, Wegenke M, Wiebel FJ (1999) Establishment of a simple cleanup procedure and bioassay for determining 2,3,7,8-tetrachlorodibenzo-p-dioxin toxicity equivalents of environmental samples. Ecotoxicol Environ Safe 41:77–82

    Article  Google Scholar 

  • Shi W, Wang X, Hu G, Hao Y, Zhang X, Liu H, Wei S, Wang X, Yu H (2011) Bioanalytical and instrumental analysis of thyroid hormone disrupting compounds in water sources along the Yangtze River. Environ Pollut 159:441–448

    Article  CAS  Google Scholar 

  • Simons R, Vincken J-P, Mol LAM, The SAM, Bovee TFH, Luijendijk TJC, Verbruggen MA, Gruppen H (2011) Agonistic and antagonistic estrogens in licorice root (Glycyrrhiza glabra). Anal Bioanal Chem 401:305–313

    Article  CAS  Google Scholar 

  • Stasinakis AS, Gatidou G, Mamais D, Thomaidis NS, Lekkas TD (2008) Occurrence and fate of endocrine disrupters in Greek sewage treatment plants. Water Res 42:1796–1804

    Article  CAS  Google Scholar 

  • Stronkhorst J, Leonards P, Murk AJ (2002) Using the dioxin receptor-CALUX in vitro bioassay to screen marine harbor sediments for compounds with a dioxin-like mode of action. Environ Toxicol Chem 21:2552–2561

    CAS  Google Scholar 

  • Takigami T, Sakai S, Brouwer A (2005) Bio/chemical analysis of dioxin-like compounds in sediment samples from Osaka Bay, Japan. Environ Technol 26:459–469

    Article  CAS  Google Scholar 

  • Thomas KV, Balaam J, Hurst M, Nedyalkova Z, Mekenyan O (2004) Potency and characterization of estrogen-receptor agonists in United Kingdom estuarine sediments. Environ Toxicol Chem 23:471–479

    Article  CAS  Google Scholar 

  • Toppari J, Larsen JC, Christiansen P, Giwercman A, Grandjean P, Guillette LJ, Jegou J, Bernard JTK, Jouannet P, Keiding N, Leffers H, McLachlan JA, Meyer O, Muller J, Rajpert-De ME, Scheike T, Sharpe R, Sumper J, Skakkebaek NE (1996) Male reproductive health and environmental xenoestrogens. Environ Health Perspect 104:741–803

    CAS  Google Scholar 

  • Ulrich B, Stahlmann R (2004) Developmental toxicity of polychlorinated biphenyls (PCBs): a systematic review of experimental data. Arch Toxicol 78:252–268

    Google Scholar 

  • Vigano L, Mandich A, Benfenati E, Bertolotti R, Bottero S, Porazzi E, Agradi E (2006) Investigating the estrogenic risk along the river Po and its intermediate section. Arch Environ Contam Toxicol 51:641–651

    Article  CAS  Google Scholar 

  • Villeneuve DL, Blankenship AL, Giesy JP (2000) Derivation and application of relative potency estimates based on in vitro bioassay results. Environ Toxicol Chem 19:2835–2843

    Article  CAS  Google Scholar 

  • Wang J, Bi Y, Pfister G, Henkelmann B, Zhu K, Schramm K-W (2009) Determination of PAH, PCB, and OCP in water from the Three Gorges Reservoir accumulated by semipermeable membrane devices (SPMD). Chemosphere 75:1119–1127

    Article  CAS  Google Scholar 

  • Wang L, Ying GG, Zhao JL, Liu S, Yang B, Zhou LJ, Tao R, Su HC (2011) Assessing estrogenic activity in surface water and sediment of the Liao River system in northeast China using combined chemical and biological tools. Environ Pollut 159:148–156

    Article  CAS  Google Scholar 

  • Wang J, Henkelmann B, Bi Y, Zhu K, Pfister G, Hu W, Temoka C, Westrich B, Schamm K-W (2013) Temporal variation and spatial distribution of PAH in water of Three Gorges Reservoir during the complete impoundment period. Environ Sci Pollut Res 20:7071–7079

    Google Scholar 

  • Weiss JM, Hamers T, Thomas KV, Linden S, Leonards PEG, Lamoree MH (2009) Masking effect of anti-androgens on androgenic activity in European river sediment unveiled by effect-directed analysis. Anal Bioanal Chem 394:1385–1397

    Article  CAS  Google Scholar 

  • Williams RJ, Johnson AC, Smith JJL, Kanda R (2003) Steroid estrogen profiles along river stretches arising from sewage treatment works discharges. Environ Sci Technol 37:1744–1750

    Article  CAS  Google Scholar 

  • Xiao R, Wang Z, Wang C, Yu G (2006) Soil screening for identifying ecological risk stressors using a battery of in vitro cell bioassays. Chemosphere 64:71–78

    Article  CAS  Google Scholar 

  • Xie SQ, Li ZJ, Liu JS, Xie SQ, Wang HZ, Murphy BR (2007) Fisheries of the Yangtze River show immediate impacts of the Three Gorges Dam. Fisheries 32:343–344

    Google Scholar 

  • Xu K, Milliman JD (2009) Seasonal variations of sediment discharge from the Yangtze River before and after impoundment of the Three Gorges Dam. Geomorphology 104:276–283

    Article  Google Scholar 

  • Yin S-Y, Lou B-F, Liu H, Lan J, Yuan L, Zhang Q, Zhang X-P (2011) Analysis of water quality of the Yangtze River within the Three Gorges Reservoir area during construction period. Res Environ Yangtze Basin 20:305–310

    Google Scholar 

  • Yoo H, Khim JS, Giesy JP (2006) Receptor-mediated in vitro bioassay for characterization of AhR-active compounds and activities in sediment from Korea. Chemosphere 62:1261–1271

    Article  CAS  Google Scholar 

  • Zhang J (1995) Geochemistry of trace metals from Chinese river/estuary systems: an overview. Estuar Coast Shelf Sci 41:631–658

    Article  CAS  Google Scholar 

  • Zhang Y, Zhou JL (2008) Occurrence and removal of endocrine disrupting chemicals in wastewater. Chemosphere 73:848–853

    Article  CAS  Google Scholar 

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Acknowledgments

This project was funded by the German Ministry of Education and Research (BMBF 02WT1132).

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Authors and Affiliations

  1. Department for Biosciences, Center for Life & Food Sciences, Land Use and Environment, Technical University of Munich, Weihenstephaner Steig 23, 85350, Freising, Germany

    Jingxian Wang & Karl-Werner Schramm

  2. Molecular EXposomics (MEX), Helmholtz Center Munich-German Research Center for Environmental Health (GmbH), Ingolstädter Landstr.1, 85764, Neuherberg, Germany

    Jingxian Wang, Silke Bernhöft & Karl-Werner Schramm

  3. The State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, People’s Republic of China

    Jingxian Wang & Yonghong Bi

  4. Department of Toxicology & Bioassays, RIKILT, Institute of Food Safety, WUR, P.O. Box 230, 6700 AE, Wageningen, The Netherlands

    Toine F. H. Bovee

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  1. Jingxian Wang
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Wang, J., Bovee, T.F.H., Bi, Y. et al. Aryl hydrocarbon receptor (AhR) inducers and estrogen receptor (ER) activities in surface sediments of Three Gorges Reservoir, China evaluated with in vitro cell bioassays. Environ Sci Pollut Res 21, 3145–3155 (2014). https://doi.org/10.1007/s11356-013-2260-2

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