Genotoxic and teratogenic effect of freshwater sediment samples from the Rhine and Elbe River (Germany) in zebrafish embryo using a multi-endpoint testing strategy

Environmental Science and Pollution Research

Volumn 22, Issue 21, 2014, Pages 16341-16357

  Garcia Kaufer M ^a,b,c   Gartiser, S ^a   Hafner, C ^a   Schiwy, S ^b   Keiter, S ^b,g   Grundemann C ^c   Hollert, H ^b,d,e,f  

^a Hydrotox GmbH   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d NANJING UNIVERSITY   (China)

^e Tongji University   (China)

^f CHONGQING UNIVERSITY   (China)

^g ÖREBRO UNIVERSITY   (Sweden)

Author keywords

Apoptosis; Comet assay; Cytotoxicity; Dioxin like toxicity; Embryotoxicity; Freshwater sediment; Genotoxicity; Zebrafish

Indexed keywords

APOPTOSIS; BIOAVAILABILITY; BIOMARKER; CYPRINID; DIOXIN; ECOTOXICOLOGY; EMBRYO; FRESHWATER SEDIMENT; GENOTOXICITY; RISK ASSESSMENT; XENOBIOTICS;

ELBE BASIN; GERMANY; RHINE BASIN;

DANIO RERIO;

WATER POLLUTANT;

ANIMAL; CHEMISTRY; COMET ASSAY; DNA DAMAGE; DRUG EFFECTS; ECOTOXICOLOGY; EMBRYO DEVELOPMENT; GERMANY; NONMAMMALIAN EMBRYO; RISK ASSESSMENT; RIVER; SEDIMENT; TOXICITY; WATER POLLUTANT; WATER QUALITY; ZEBRA FISH;

ANIMALS; COMET ASSAY; DNA DAMAGE; ECOTOXICOLOGY; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; GEOLOGIC SEDIMENTS; GERMANY; RISK ASSESSMENT; RIVERS; WATER POLLUTANTS, CHEMICAL; WATER QUALITY; ZEBRAFISH;

EID: 84945462680     PISSN: 09441344     EISSN: 16147499     Source Type: Journal    
DOI: 10.1007/s11356-014-3894-4     Document Type: Article

References (65)

1. Billiard SM, Meyer JN, Wassenberg DM et al (2008) Nonadditive effects of PAHs on early vertebrate development: mechanisms and implications for risk assessment. Toxicol Sci Off J Soc Toxicol 105:5–23. doi:10.1093/toxsci/kfm303
2. Brannen KC, Panzica-Kelly JM, Danberry TL, Augustine-Rauch KA (2010) Development of a zebrafish embryo teratogenicity assay and quantitative prediction model. Birth Defects Res B Dev Reprod Toxicol 89:66–77. doi:10.1002/bdrb.20223
3. Braunbeck T, Boettcher M, Hollert H et al (2005) Towards an alternative for the acute fish LC(50) test in chemical assessment: the fish embryo toxicity test goes multi-species—an update. ALTEX 22:87–102
4. Burlinson B, Tice RR, Speit G et al (2007) Fourth International Workgroup on Genotoxicity testing: results of the in vivo Comet assay workgroup. Mutat Res 627:31–35. doi:10.1016/j.mrgentox.2006.08.011
5. Calabrese EJ, Blain RB (2011) The hormesis database: the occurrence of hormetic dose responses in the toxicological literature. Regul Toxicol Pharmacol RTP 61:73–81. doi:10.1016/j.yrtph.2011.06.003
6. Carls MG, Holland L, Larsen M et al (2008) Fish embryos are damaged by dissolved PAHs, not oil particles. Aquat Toxicol Amst Neth 88:121–127. doi:10.1016/j.aquatox.2008.03.014
7. Cole LK, Ross LS (2001) Apoptosis in the developing zebrafish embryo. Dev Biol 240:123–142. doi:10.1006/dbio.2001.0432
8. Collins AR, Oscoz AA, Brunborg G et al (2008) The comet assay: topical issues. Mutagenesis 23:143–151. doi:10.1093/mutage/gem051
9. David RM, Jones HS, Panter GH et al (2012) Interference with xenobiotic metabolic activity by the commonly used vehicle solvents dimethylsulfoxide and methanol in zebrafish (Danio rerio) larvae but not Daphnia magna. Chemosphere 88:912–917. doi:10.1016/j.chemosphere.2012.03.018
10. Doak SH, Jenkins GJS, Johnson GE et al (2007) Mechanistic influences for mutation induction curves after exposure to DNA-reactive carcinogens. Cancer Res 67:3904–3911. doi:10.1158/0008-5472.CAN-06-4061
11. EFSA (2009) Guidance of the scientific comitee on a request from EFSA on the use of the benchmark dose approach in risk assessment. EFSA J 1150:1–72
12. Feiler U, Höss S, Ahlf W et al (2013) Sediment contact tests as a tool for the assessment of sediment quality in German waters. Environ Toxicol Chem SETAC 32:144–155. doi:10.1002/etc.2024
13. Fischer S, Klüver N, Burkhardt-Medicke K et al (2013) Abcb4 acts as multixenobiotic transporter and active barrier against chemical uptake in zebrafish (Danio rerio) embryos. BMC Biol 11:69. doi:10.1186/1741-7007-11-69
14. Fleming CR, Di Giulio RT (2011) The role of CYP1A inhibition in the embryotoxic interactions between hypoxia and polycyclic aromatic hydrocarbons (PAHs) and PAH mixtures in zebrafish (Danio rerio). Ecotoxicol Lond Engl 20:1300–1314. doi:10.1007/s10646-011-0686-1
15. Franco R, Panayiotidis MI (2010) Cell death or survival: the double-edged sword of environmental and occupational toxicity. Chem Biol Interact 188:265–266. doi:10.1016/j.cbi.2010.06.002
16. Garner LVT, Di Giulio RT (2012) Glutathione transferase pi class 2 (GSTp2) protects against the cardiac deformities caused by exposure to PAHs but not PCB-126 in zebrafish embryos. Comp Biochem Physiol Toxicol Pharmacol CBP 155:573–579. doi:10.1016/j.cbpc.2012.01.007
17. Gollapudi BB, Johnson GE, Hernandez LG et al (2013) Quantitative approaches for assessing dose–response relationships in genetic toxicology studies. Environ Mol Mutagen 54:8–18. doi:10.1002/em.21727
18. Grummt T, Kuckelkorn J, Bahlmann A et al (2013) Tox-Box: securing drops of life—an enhanced health-related approach for risk assessment of drinking water in Germany. Environ Sci Eur 25:27. doi:10.1186/2190-4715-25-27
19. Häfeli N, Schwartz P, Burkhardt-Holm P (2011) Embryotoxic and genotoxic potential of sewage system biofilm and river sediment in the catchment area of a sewage treatment plant in Switzerland. Ecotoxicol Environ Saf 74:1271–1279. doi:10.1016/j.ecoenv.2011.03.008
20. Hafner C, Gartiser S, Garcia-Käufer M et al. (2015) Investigations on sediment toxicity of German rivers applying a standardized bioassay battery. DanTox Project. (in this issue)
21. Hartmann A, Schumacher M, Plappert-Helbig U et al (2004) Use of the alkaline in vivo Comet assay for mechanistic genotoxicity investigations. Mutagenesis 19:51–59
22. Helma C, Uhl M (2000) A public domain image-analysis program for the single-cell gel-electrophoresis (comet) assay. Mutat Res 466:9–15
23. Hermsen SAB, van den Brandhof E-J, van der Ven LTM, Piersma AH (2011) Relative embryotoxicity of two classes of chemicals in a modified zebrafish embryotoxicity test and comparison with their in vivo potencies. Toxicol Vitro Int J Publ Assoc BIBRA 25:745–753. doi:10.1016/j.tiv.2011.01.005
24. Hernandez LG, Slob W, van SH, van BJ (2011) Can carcinogenic potency be predicted from in vivo genotoxicity data?: a meta-analysis of historical data. Env Mol Mutagen 52:518–528. doi:10.1002/em.20651
25. Hollert H, Keiter S, König N et al (2003) A new sediment contact assay to assess particle-bound pollutants using zebrafish (danio rerio) embryos. J Soils Sediments 3:197–207. doi:10.1065/jss2003.09.085
26. Hornung MW, Cook PM, Fitzsimmons PN et al (2007) Tissue distribution and metabolism of benzo[a]pyrene in embryonic and larval medaka (Oryzias latipes). Toxicol Sci Off J Soc Toxicol 100:393–405. doi:10.1093/toxsci/kfm231
27. Höss S, Ahlf W, Fahnenstich C et al (2010) Variability of sediment-contact tests in freshwater sediments with low-level anthropogenic contamination—determination of toxicity thresholds. Environ Pollut 158:2999–3010. doi:10.1016/j.envpol.2010.05.013
28. Incardona JP, Carls MG, Teraoka H et al (2005) Aryl hydrocarbon receptor-independent toxicity of weathered crude oil during fish development. Environ Health Perspect 113:1755–1762
29. Incardona JP, Linbo TL, Scholz NL (2011) Cardiac toxicity of 5-ring polycyclic aromatic hydrocarbons is differentially dependent on the aryl hydrocarbon receptor 2 isoform during zebrafish development. Toxicol Appl Pharmacol 257:242–249. doi:10.1016/j.taap.2011.09.010
30. ISO 7346–3 (1996) ISO 7346–3:1996 - Water quality -- Determination of the acute lethal toxicity of substances to a freshwater fish [Brachydanio rerio Hamilton-Buchanan (Teleostei, Cyprinidae)] -- Part 3: flow-through method. http://www.iso.org/iso/catalogue_detail.htm?csnumber=14030
31. Kais B, Schneider KE, Keiter S et al (2013) DMSO modifies the permeability of the zebrafish (Danio rerio) chorion—implications for the fish embryo test (FET). Aquat Toxicol Amst Neth 140–141:229–238. doi:10.1016/j.aquatox.2013.05.022
32. Keiter S, Rastall A, Kosmehl T et al (2006) Ecotoxicological assessment of sediment, suspended matter and water samples in the upper Danube River. A pilot study in search for the causes for the decline of fish catches. Environ Sci Pollut Res Int 13:308–319
33. Keiter S, Peddinghaus S, Feiler U et al (2010) DanTox—a novel joint research project using zebrafish (Danio rerio) to identify specific toxicity and molecular modes of action of sediment-bound pollutants. J Soils Sediments 10:714–717. doi:10.1007/s11368-010-0221-7
34. Kimmel CB, Ballard WW, Kimmel SR et al (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310
35. Kosmehl T, Hallare AV, Reifferscheid G et al (2006) A novel contact assay for testing genotoxicity of chemicals and whole sediments in zebrafish embryos. Env Toxicol Chem 25:2097–2106
36. Kosmehl T, Krebs F, Manz W et al (2007) Differentiation between bioavailable and total hazard potential of sediment-induced DNA fragmentation as measured by the comet assay with Zebrafish embryos. J Soils Sediments 7:377–387. doi:10.1065/jss2007.11.261
37. Lee KJ, Nallathamby PD, Browning LM et al (2007) In vivo imaging of transport and biocompatibility of single silver nanoparticles in early development of zebrafish embryos. ACS Nano 1:133–143. doi:10.1021/nn700048y
38. Lin S, Zhao Y, Nel AE, Lin S (2013) Zebrafish: an in vivo model for nano EHS studies. Small 9:1608–1618
39. Lo KH, Hui MNY, Yu RMK et al (2011) Hypoxia impairs primordial germ cell migration in zebrafish (Danio rerio) embryos. PLoS One 6:e24540. doi:10.1371/journal.pone.0024540
40. McElroy A, Clark C, Duffy T et al (2012) Interactions between hypoxia and sewage-derived contaminants on gene expression in fish embryos. Aquat Toxicol Amst Neth 108:60–69. doi:10.1016/j.aquatox.2011.10.017
41. Meyer J, Di Giulio R (2002) Patterns of heritability of decreased EROD activity and resistance to PCB 126-induced teratogenesis in laboratory-reared offspring of killifish (Fundulus heteroclitus) from a creosote-contaminated site in the Elizabeth River, VA, USA. Mar Environ Res 54:621–626
42. Nagel R (2002) DarT: the embryo test with the Zebrafish Danio rerio—a general model in ecotoxicology and toxicology. ALTEX 19(Suppl 1):38–48
43. OECD (2004) Test no. 218: sediment-water chironomid toxicity using spiked sediment. OECD Publishing. doi:10.1787/9789264070264-en
44. OECD (2014) Test no. 489: in vivo mammalian alkaline comet assay. OECD Publishing. doi:10.1787/9789264091016-en
45. Rocha PS, Bernecker C, Strecker R, et al (2011) Sediment-contact fish embryo toxicity assay with Danio rerio to assess particle-bound pollutants in the Tietê River Basin (São Paulo, Brazil). Ecotoxicol Environ Saf 74:1951–1959. doi:10.1016/j.ecoenv.2011.07.009
46. Schiwy S, Bräunig J, Alert H et al (2014) A novel contact assay for testing aryl hydrocarbon receptor (AhR)-mediated toxicity of chemicals and whole sediments in zebrafish (Danio rerio) embryos. Environ Sci Pollut Res Int. doi:10.1007/s11356-014-3185-0
47. Scholz S, Fischer S, Gündel U, et al (2008) The zebrafish embryo model in environmental risk assessment--applications beyond acute toxicity testing. Environ Sci Pollut Res Int 15:394–404. doi:10.1007/s11356-008-0018-z
48. Seitz N, Böttcher M, Keiter S et al (2008) A novel statistical approach for the evaluation of comet assay data. Mutat Res 652:38–45. doi:10.1016/j.mrgentox.2007.12.004
49. Selderslaghs IWT, Blust R, Witters HE (2012) Feasibility study of the zebrafish assay as an alternative method to screen for developmental toxicity and embryotoxicity using a training set of 27 compounds. Reprod Toxicol Elmsford N 33:142–154. doi:10.1016/j.reprotox.2011.08.003
50. Sipes NS, Padilla S, Knudsen TB (2011) Zebrafish: as an integrative model for twenty-first century toxicity testing. Birth Defect Res Part C Embryo Today Rev 93:256–267. doi:10.1002/bdrc.20214
51. Strähle U, Scholz S, Geisler R et al (2012) Zebrafish embryos as an alternative to animal experiments—a commentary on the definition of the onset of protected life stages in animal welfare regulations. Reprod Toxicol Elmsford N 33:128–132. doi:10.1016/j.reprotox.2011.06.121
52. Strecker R, Seiler T-B, Hollert H, Braunbeck T (2011) Oxygen requirements of zebrafish (Danio rerio) embryos in embryo toxicity tests with environmental samples. Comp Biochem Physiol Toxicol Pharmacol CBP 153:318–327. doi:10.1016/j.cbpc.2010.12.002
53. Swenberg JA, Lu K, Moeller BC et al (2011) Endogenous versus exogenous DNA adducts: their role in carcinogenesis, epidemiology, and risk assessment. Toxicol Sci Off J Soc Toxicol 120(Suppl 1):S130–S145. doi:10.1093/toxsci/kfq371
54. Teixidó E, Piqué E, Gómez-Catalán J, Llobet JM (2013) Assessment of developmental delay in the zebrafish embryo teratogenicity assay. Toxicol Vitro Int J Publ Assoc BIBRA 27:469–478. doi:10.1016/j.tiv.2012.07.010
55. Tice RR, Agurell E, Anderson D et al (2000) Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35:206–221
56. Tuikka AI, Schmitt C, Hoss S et al (2011) Toxicity assessment of sediments from three European river basins using a sediment contact test battery. Ecotoxicol Environ Saf 74:123–131
57. Vasquez MZ (2010) Combining the in vivo comet and micronucleus assays: a practical approach to genotoxicity testing and data interpretation. Mutagenesis 25:187–199. doi:10.1093/mutage/gep060
58. Vasquez MZ (2012) Recommendations for safety testing with the in vivo comet assay. Mutat Res 747:142–156. doi:10.1016/j.mrgentox.2012.05.002
59. Vincze K, Graf K, Scheil V et al (2014) Embryotoxic and proteotoxic effects of water and sediment from the Neckar River (Southern Germany) to zebrafish (Danio rerio) embryos. Environ Sci Eur 26:3. doi:10.1186/2190-4715-26-3
60. Weigt S, Huebler N, Strecker R et al (2011) Zebrafish (Danio rerio) embryos as a model for testing proteratogens. Toxicology 281:25–36. doi:10.1016/j.tox.2011.01.004
61. Wills LP, Zhu S, Willett KL, Di Giulio RT (2009) Effect of CYP1A inhibition on the biotransformation of benzo[a]pyrene in two populations of Fundulus heteroclitus with different exposure histories. Aquat Toxicol Amst Neth 92:195–201. doi:10.1016/j.aquatox.2009.01.009
62. Wölz J, Brack W, Moehlenkamp C et al (2010) Effect-directed analysis of Ah receptor-mediated activities caused by PAHs in suspended particulate matter sampled in flood events. Sci Total Environ 408:3327–3333. doi:10.1016/j.scitotenv.2010.03.029
63. Woo S, Kim S, Yum S et al (2006) Comet assay for the detection of genotoxicity in blood cells of flounder (Paralichthys olivaceus) exposed to sediments and polycyclic aromatic hydrocarbons. Mar Pollut Bull 52:1768–1775. doi:10.1016/j.marpolbul.2006.08.027
64. Yu KN, Tung MMT, Choi VWY, Cheng SH (2012) Alpha radiation exposure decreases apoptotic cells in zebrafish embryos subsequently exposed to the chemical stressor, Cd. Environ Sci Pollut Res Int 19:3831–3839. doi:10.1007/s11356-012-1032-8
65. Zielke H, Seiler T-B, Niebergall S et al (2011) The impact of extraction methodologies on the toxicity of sediments in the zebrafish (Danio rerio) embryo test. J Soils Sediments 11:352–363. doi:10.1007/s11368-010-0317-0