A combined DNA-microarray and mechanism-specific toxicity approach with zebrafish embryos to investigate the pollution of river sediments

Reproductive Toxicology

Volumn 33, Issue 2, 2012, Pages 245-253

  Kosmehl, Thomas ^a   Otte, Jens C ^b   Yang, Lixin ^b   Legradi, Jessica ^b   Bluhm, Kerstin ^c   Zinsmeister, Christian ^b   Keiter, Steffen H ^c   Reifferscheid, Georg ^d   Manz, Werner ^e   Braunbeck, Thomas ^a   Strähle, Uwe ^b   Hollert, Henner ^c  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d FEDERAL INSTITUTE OF HYDROLOGY   (Germany)

^e University of Koblenz Landau ^*  (Germany)

Author keywords

Ames test; Comet assay; EROD assay; Microarray; Neutral red assay; Sediment extract; Transcriptomics; Zebrafish

Indexed keywords

COPPER; HEXACHLOROBENZENE; NICKEL; POLYCYCLIC AROMATIC HYDROCARBON; ZINC;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOASSAY; CHEMICAL ANALYSIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DNA MICROARRAY; ECOTOXICOLOGY; EMBRYO; EMBRYO MORTALITY; EMBRYOTOXICITY; EXPOSURE; GENE EXPRESSION PROFILING; GENETIC ANALYSIS; GENOTOXICITY; GERMANY; HEALTH HAZARD; MUTAGENICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; RIVER ECOSYSTEM; SEDIMENT; TOXICITY TESTING; TRANSCRIPTOMICS; WATER CONTAMINATION; ZEBRA FISH;

ANIMALS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GEOLOGIC SEDIMENTS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RIVERS; TERATOGENS; WATER POLLUTANTS, CHEMICAL; ZEBRAFISH;

DANIO RERIO;

EID: 84862828537     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2012.01.005     Document Type: Article

References (87)

1. Nuwaysir E.F., Bittner M., Trent J., Barrett J.C., Afshari C.A. Microarrays and toxicology: the advent of toxicogenomics. Mol Carcinogen 1999, 24:153-159.
2. Lettieri T. Recent applications of DNA microarray technology to toxicology and ecotoxicology. Environ Health Perspect 2006, 114:4-9.
3. van Straalen N.M. Ecotoxicology becomes stress ecology. Environ Sci Technol 2003, 37:324A-330A.
4. Linney E., Dobbs-McAuliffe B., Sajadi H., Malek R.L. Microarray gene expression profiling during the segmentation phase of zebrafish development. Comp Biochem Physiol C: Toxicol Pharmacol 2004, 138:351-362.
5. Smith L.L. Key challenges for toxicologists in the 21st century. Trends Pharmacol Sci 2001, 22:281-285.
6. Miracle A.L., Ankley G.T. Ecotoxicogenomics: linkages between exposure and effects in assessing risks of aquatic contaminants to fish. Reprod Toxicol 2005, 19:321-326.
7. Tice R.R., Agurell E., Anderson D., Burlinson B., Hartmann A., Kobayashi H., et al. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 2000, 35:206-221.
8. White P.A. The genotoxicity of priority polycyclic aromatic hydrocarbons in complex mixtures. Mutat Res 2002, 515:85-98.
9. Ames B.N., McCann J., Yamasaki E. Methods for detecting carcinogens and mutagens with the Salmonella/mammalian-microsome mutagenicity test. Mutat Res 1975, 31:347-364.
10. Bartlett J. Technology evaluation: SAGE, genzyme molecular oncology. Curr Opin Mol Ther 2001, 3:85-96.
11. Gallègue-Zouitina S., Bailleul B., Loucheux-Lefebyre M.H. Adducts from in vivo action of the carcinogen 4-hydroxyaminoquinoline 1-oxide in rats and from in vitro reaction of 4-acetoxyaminoquinoline 1-oxide with DNA and polynucleotides. Cancer Res 1985, 45:520-525.
12. He J.L., Chen W.L., Jin H.Y. Comparative evaluation of the in vitro micronuleus test and the comet assay for the detection of genotoxic effects of X-ray radiation. Mutat Res 2000, 469:223-231.
13. Hollstein M.J., McCann J., Angelsanto F.A., Nichols W.W. Short-term tests for carcinogens and mutagens. Mutat Res 1979, 65:133-226.
14. Sideris E.G., Charalambous S.C., Tsolomyty A., Katsaros N. Mutagenesis:carcinogenesis and the metal elements-DNA interaction. Prog Clin Biol Res 1988, 259:13-25.
15. Belpaeme K., Cooreman K., Kirsch-Volders M. Development and validation of the in vivo alkaline comet assay for detecting genomic damage in marine flatfish. Mutat Res 1998, 415:167-184.
16. Singh N.P., McCoy M.T., Tice R.R., Schneider E.L. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 1988, 175:184-191.
17. Sina J.F., Bean C.L., Dysart G.R., Taylor V.I., Bradley M.O. Evaluation of the alkaline elution/rat hepatocyte assay as a predictor of carcinogenic/mutagenic potential. Mutat Res 1983, 113:357-391.
18. Sanner T., Rivedal E. Studies of tumor promoters with the Syrian hamster embryo cell transformation assay. Carcinog Compr Surv 1985, 9:167-178.
19. Matter B., Schmid W. Trenimon-induced chromosomal damage in bone-marrow cells of six mammalian species, evaluated by the micronucleus test. Mutat Res 1971, 12:417-425.
20. Brewen J.G., Peacock W.J. The effect of triated thymidine on sister chromatid exchange in a ring chromosome. Mutat Res 1969, 7:433-440.
21. Furihata C., Yamawaki Y., Jin S.S., Moriva H., Kodama K., Matsushima T., et al. Induction of unscheduled DNA synthesis in rat stomach mucosa by glandular stomach carcinogens. J Natl Cancer Inst 1984, 72:1327-1334.
22. Hamadeh H.K., Bushel P.R., Jayadev S., Martin K., DiSorbo O., Sieber S., et al. Gene expression analysis reveals chemical-specific profiles. Toxicol Sci 2002, 67:219-231.
23. Hu T., Gibson D.P., Carr G.J., Torontali S.M., Tiesman J.P., Chaney J.G., et al. Identification of a gene expression profile that discriminates indirect-acting genotoxins from direct-acting genotoxins. Mutat Res 2004, 549:5-27.
24. Moens L.N., van der Ven K., van Remortel P., Del-Favero J., De Coen W.M. Expression profiling of endocrine-disrupting compounds using a customized Cyprinus carpio cDNA microarray. Toxicol Sci 2006, 93:298-310.
25. Yang L., Kemadjou J.R., Zinsmeister C., Bauer M., Legradi J., Müller F., et al. Transcriptional profiling reveals barcode-like toxicogenomic responses in the zebrafish embryo. Genome Biol 2007, 8:227-244.
26. Zhou J., Thompson D.K. Challenges in applying microarrays to environmental studies. Curr Opin Biotechnol 2002, 13:204-207.
27. DIN-38415-T6. DIN-AK Fischeitest DIN 38415 T6: Deutsche Einheitsverfahren zur Wasser-, Abwasser- und Schlammuntersuchung - Suborganismische Testverfahren (Gruppe T) - Bestimmung der nicht akut giftigen Wirkung von Abwasser auf die Entwicklung von Fischeiern (T6); 2000.
28. Braunbeck T., Boettcher M., Hollert H., Kosmehl T., Lammer E., Leist E., et al. Towards an alternative for the acute fish LC50 test in chemical assessment: the zebrafish (Danio rerio) embryo toxicity test -an update. ALTEX 2005, 22:87-102.
29. Lammer E., Carr G.J., Wendler K., Rawlings J.M., Belanger S.E., Braunbeck T. Is the fish embryo toxicity test (FET) with the zebrafish (Danio rerio) a potential alternative for the fish acute toxicity test?. Comp Biochem Physiol C: Toxicol Pharmacol 2009, 149:196-209.
30. Alberti M., Kausch U., Haindl S., Seifert M. Gene expression analysis for exposure to estrogenic substances. Acta Hydrochim Hydrobiol 2005, 33:38-44.
31. Handley-Goldstone H.M., Grow M.W., Stegeman J.J. Cardiovascular gene expression profiles of dioxin exposure in zebrafish embryos. Toxicol Sci 2005, 85:683-693.
32. Hoffmann J.L., Thomason R.G., Lee D.M., Brill J.L., Price B.B., Carr G.J., et al. Hepatic gene expression profiling using GeneChips in zebrafish exposed to 17alpha-methyldihydrotestosterone. Aquat Toxicol 2006, 87:69-80.
33. van der Ven K., De Wit M., Keil D., Moens L., Van Leemput K., Naudts B., et al. Development and application of a brain-specific cDNA microarray for effect evaluation of neuro-active pharmaceuticals in zebrafish (Danio rerio). Comp Biochem Physiol B: Biochem Mol Biol 2005, 141:408-417.
34. Wen C., Zhang Z., Ma W., Xu M., Wen Z., Peng J. Genome-wide identification of female-enriched genes in zebrafish. Dev Dyn 2005, 232:171-179.
35. Hollert H., Dürr M., Erdinger L., Braunbeck T. Cytotoxicity of settling particulate matter (SPM) and sediments of the Neckar River (Germany) during a winter flood. Environ Toxicol Chem 2000, 19:528-534.
36. Kosmehl T., Krebs F., Manz W., Erdinger L., Braunbeck T., Hollert H. Comparative genotoxicity testing of Rhine river sediment extracts using the permanent cell lines RTG-2 and RTL-W1 in the comet assay and ames assay. J Soils Sed 2004, 4:84-94.
37. Krebs F. ökotoxikologische Untersuchung und Bewertung von Baggergut mit Hilfe der pT-Wert-Methode. In: BfG, editor. Jahresbericht 1999. Koblenz: Bundesanstalt für Gewässerkunde; 2000. p. 51-6.
38. Kosmehl T., Krebs F., Manz W., Braunbeck T., Hollert H. Differentiation between bioavailable and total hazard potential of sediment-induced DNA fragmentation as measured by the comet assay with zebrafish embryos. J Soils Sed 2007, 7:377-387.
39. Lachmund C., Köcher B., Manz W., Heininger P. Chemical and microbiological in situ characterization of benthic communities in sediments with different contamination levels. J Soils Sed 2003, 3:188-196.
40. Kosmehl T., Hallare A.V., Reifferscheid G., Manz W., Braunbeck T., Hollert H. A novel contact assay for testing genotoxic of chemicals and whole sediments in zebrafish embryos. Environ Toxicol Chem 2006, 25:2097-2106.
41. Lee L.E.J., Clemons J.H., Bechtel D.G., Caldwell S.J., Han K., Pasitschniak-Arts M., et al. Development and characterization of a rainbow trout liver cell line expressing cytochrome P450-dependent monooxygenase activity. Cell Biol Toxicol 1993, 9:279-294.
42. Behrens A., Schirmer K., Bols N.C., Segner H. Polycyclic aromatic hydrocarbons as inducers of cytochrome P4501A enzyme activity in the rainbow trout liver cell line, RTL-W1, and in primary cultures of rainbow trout hepatocytes. Environ Toxicol Chem 2001, 20:632-643.
43. Klee N., Gustavsson L., Kosmehl T., Engwall M., Erdinger L., Braunbeck T., et al. Changes in toxicity and genotoxicity in an industrial sewage sludge containing nitro- and amino-aromatic compounds during treatment in bioreactors under different oxygen regimes. Environ Sci Pollut Res 2004, 11:313-320.
44. Keiter S., Grund S., van Bavel B., Engwall M., Hagberg J., Kammann U., et al. Activities and identification of Ah receptor agonists in sediments from the Danube River. Anal Bioanal Chem 2008, 390:2009-2020.
45. Hollert H., Keiter S., König N., Rudolf M., Ulrich M., Braunbeck T. A new sediment contact assay to assess particle-bound pollutants using zebrafish (Danio rerio). J Soils Sed 2003, 3:197-207.
46. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B: Method 1995, 57:289-300.
47. Altschul S.F., H.Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
48. Stajich J.E., Block D., Boulez K., Brenner S.E., Chervitz S.A., Dagdigian C., et al. The bioperl toolkit: perl modules for the life sciences. Genome Res 2002, 12:1611-1618.
49. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., et al. Gene ontology: tool for the unification of biology. Nat Genet 2000, 25:25-29.
50. Zhang B., Kirov S., Snoddy J. WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucl Acids Res 2005, 33:W741-W748.
51. Supek F., Škunca N., Repar J., Vlahoviček K., Šmuc T. Translational selection is ubiquitous in prokaryotes. PLOS Genetics 2010, 6:e1001004.
52. Schlicker A., Albrecht M. FunSimMat: a comprehensive functional similarity database. Nucl Acids Res 2008, 36:D434-D439.
53. Ahlf W., Hollert H., Neumann-Hense H., Ricking M. A guidance for the assessment and evaluation of sediment quality - a german approach based on ecotoxicological and chemical measurements. J Soils Sediments 2002, 2:37-42.
54. Heise S, Maaß V, Gratzer H, Ahlf W. Möglichkeiten und Leistungen einer ökotoxikologischen Sedimentklassifikation am Beispiel der Elbe. Mitteilungen der Bundesanstalt für Gewässerkunde. Koblenz: Bundesanstalt für Gewässerkunde; 2000. p. 96-104.
55. Rippen GH. Handbuch der Umweltchemikalien; 1994.
56. Greve P.A. Environmental and human exposure to hexachlorobenzene in the Netherlands. Hexachlorobenzene: proceedings of an international symposium 1986, 87-97. International Agency for Research on Cancer, Lyon. C.R. Morris, J.B.R. Cabral (Eds.).
57. Mizell M., Romig E.S. The aquatic vertebrate embryo as a sentinel for toxins: zebrafish embryo dechorionation and perivitelline space microinjection. Int J Dev Biol 1997, 41:411-423.
58. Canonero R., Campart G.B., Mattioli F., Robbiano L., Martelli A. Testing of p-dichlorobenzene and hexachlorobenzene for their ability to induce DNA damage and micronucleus formation in primary cultures of rat and human hepatocytes. Mutagenesis 1997, 12:35-39.
59. McKelvey-Martin V.J., Green M.H.L., Schmezer P., Pool-Zobel B.L., De Meo M.P., Collins A. The single cell gel electrophoresis (comet assay): a European review. Mutat Res 1993, 288:47-63.
60. Schnurstein A., Braunbeck T. Tail moment versus tail length-application of an in vitro version of the comet assay in biomonitoring for genotoxicity in native surface waters using primary hepatocytes and gill cells from zebrafish (Danio rerio). Ecotoxicol Environ Saf 2001, 49:187-196.
61. Schlezinger J.J., Struntz W.D.J., Goldstone J.V., Stegeman J.J. Uncoupling of cytochrome P450 1A and stimulation of reactive oxygen species production by co-planar polychlorinated biphenyl congeners. Aquat Toxicol 2006, 77:422-432.
62. Perdomo G., Dong H.H. Apolipoprotein D in lipid metabolism and its functional implication in atherosclerosis and aging. Aging 2009, 1:17-27.
63. Hunter S., Weiss S., Ou C.Y., Jaye D., Young A., Wilcox J., et al. Apolipoprotein D is down-regulated during malignant transformation of neurofibromas. Hum Pathol 2005, 36:987-993.
64. Langheinrich U., Hennen E., Stott G., Vacun G. Zebrafish as a model organism for the identification and characterization of drugs and genes affecting p53 signaling. Curr Biol 2002, 12:2023-2028.
65. Liu T.X., Howlett N.G., Deng M., Langenau D.M., Hsu K., Rhodes J., et al. Knockdown of zebrafish Fancd2 causes developmental abnormalities via p53-dependent apoptosis. Dev Cell 2003, 5:903-914.
66. Tamura K., Hua B., Adachi S., Guney I., Kawauchi J., Morioka M., et al. Stress response gene ATF3 is a target of c-myc in serum-induced cell proliferation. EMBO J 2005, 24:2590-2601.
67. Yan C., Boyd D.D. ATF3 regulates the stability of p53: a link to cancer. Cell Cycle 2006, 5:926-929.
68. Levy E., Ménard D., Delvin E., Montoudis A., Beaulieu J.F., Mailhot G., et al. Localization, function and regulation of the two intestinal fatty acid-binding protein types. Histochem Cell Biol 2009, 132:351-367.
69. Violante S., Ijlst L., van Lenthe H., de Almeida I.T., Wanders R.J., Ventura F.V. Carnitine palmitoyltransferase 2: new insights on the substrate specificity and implications for acylcarnitine profiling. Biochim Biophys Acta: Mol Basis Dis 2010, 1802:728-732.
70. Liu Y., Wang J., Wei Y., Zhang H., Xu M., Dai J. Induction of time-dependent oxidative stress and related transcriptional effects of perfluorododecanoic acid in zebrafish liver. Aquat Toxicol 2008, 89:242-250.
71. Zhang H., Shi Z., Liu Y., Wei Y., Dai J. Lipid homeostasis and oxidative stress in the liver of male rats exposed to perfluorododecanoic acid. Toxicol Appl Pharmacol 2008, 227:16-25.
72. Thisse B, Thisse C. Fast Release Clones: A High Throughput Expression Analysis. ZFIN Direct Data Submission (); 2004. http://zfinorg/.
73. Thompson P.A., Seyedi F., Lang N.P., MacLeod S.L., Wogan G.N., Anderson K.E., et al. Comparison of DNA adduct levels associated with exogenous and endogenous exposures in human pancreas in relation to metabolic genotype. Mutat Res 1999, 424:263-274.
74. Pour P.M. Toxicology of the pancreas: 2005, CRC - Taylor & Francis.
75. Jönsson M.E., Jenny M.J., Woodin B.R., Hahn M.E., Stegeman J.J. Role of AHR2 in the expression of novel cytochrome P450 1 family genes, cell cycle genes, and orphological defects in developing zebra fish exposed to 3,3',4,4',5-pentachlorobiphenyl or 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci 2007, 100:180-193.
76. Brunström B., Halldin K. EROD induction by environmental contaminants in avian embryo livers. Comp Biochem Physiol 1998, 121:213-219.
77. Brack W., Altenburger R., Ensenbach U., Möder M., Segner H., Schüürmann G. Bioassay-directed identification of organic toxicants in river sediment in the industrial region of Bitterfeld (Germany) - a contribution to hazard assessment. Arch Environ Contam Toxicol 1999, 37:164-174.
78. Brack W., Schirmer K., Erdinger L., Hollert H. Effect-directed analysis of mutagens and ethoxyresorufin-o-deethylase inducers in aquatic sediments. Environ Toxicol Chem 2005, 24:2445-2458.
79. Wölz J., Brack W., Möhlenkamp C., Claus E., Braunbeck T., Hollert H. Effect-directed analysis of Ah receptor-mediated activities caused by PAHs in suspended particulate matter sampled in flood events. Sci Tot Environ 2010, 408:3327-3333.
80. Wölz J., Engwall M., Maletz S., Olsman Takner H., Bavel B., Kammann U., et al. Changes in toxicity and Ah receptor agonist activity of suspended particulate matter during flood events at the rivers Neckar and Rhine - a mass balance approach using in vitro methods and chemical analysis. ESPR - Environ Sci Pollut Res 2008, 15:536-553.
81. Hallare A.V., Kosmehl T., Schulze T., Hollert H., Kohler H.R., Triebskorn R. Assessing contamination levels of Laguna Lake sediments (Philippines) using a contact assay with zebrafish (Danio rerio) embryos. Sci Tot Environ 2005, 347:254-271.
82. Mukhopadhyay I., Nazir A., Saxena D.K., Chowdhuri D.K. Heat shock response: hsp70 in environmental monitoring. J Biochem Mol Toxicol 2003, 17:249-254.
83. Triebskorn R., Kohler H-R., Honnen W., Schramm M., Adams S.M., Müller E.F. Induction of heat shock proteins, changes in liver ultrastructure, and alterations of fish behavior: are these biomarkers related and are they useful to reflect the state of pollution in the field. J Aquat Ecosys Stress Recov 1997, 6:57-73.
84. Gonzalez P., Baudrimont M., Boudou A., Bourdineaud J-P. Comparative effects of direct cadmium contamination on gene expression in gills, liver, skeletal muscles and brain of the zebrafish (Danio rerio). Biometals 2006, 19:225-235.
85. Airaksinen S., Rabergh C.M.I., Lahti A., Kaatrasalo A., Sistonen L., Nikinmaa M. Stressor-dependent regulation of the heat shock response in zebrafish, Danio rerio. Comp Bioch Physiol A: Mol Int Physiol 2003, 134:839-846.
86. Blechinger S.R., Kusch R.C., Haugo K., Matz C., Chivers D.P., Krone P.H. Brief embryonic cadmium exposure induces a stress response and cell death in the developing olfactory system followed by long-term olfactory deficits in juvenile zebrafish. Toxicol Appl Pharmacol 2007, 224:72-80.
87. Wahl M., Lahni B., Guenther R., Kuch B., Yang L., Straehle U., et al. A technical mixture of 2,2',4,4'-tetrabromo diphenyl ether (BDE47) and brominated furans triggers aryl hydrocarbon receptor (AhR) mediated gene expression and toxicity. Chemosphere 2008, 73:209-215.