Factorial design applied for multiple endpoint toxicity evaluation in Atlantic salmon (Salmo salar L.) hepatocytes

Toxicology in Vitro

Volumn 23, Issue 8, 2009, Pages 1455-1464

  Søfteland, Liv ^a   Eide, Ingvar ^b   Olsvik, Pål A ^a  

^a INSTITUTE OF MARINE RESEARCH   (Norway)

^b STATOIL   (Norway)

Author keywords

Atlantic salmon hepatocytes; CYP1A; Dioxins; Factorial design; Gene expression; PCB 138; TEQ; UDPGT

Indexed keywords

1,2,3,7,8 PENTACHLORODIBENZO 4 DIOXIN; 2,2',3,4,4',5' HEXACHLOROBIPHENYL; 2,3,7,8 TETRACHLORODIBENZOFURAN; CHEMICAL COMPOUND; CYTOCHROME P450 1A; GLUCURONOSYLTRANSFERASE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; HEAT SHOCK PROTEIN 70; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; POLYCHLORINATED BIPHENYL; POLYCHLORINATED BIPHENYL DERIVATIVE; PROTEIN P53; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ATLANTIC SALMON; CHEMICAL INTERACTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FACTORIAL DESIGN; GENE EXPRESSION; GENETIC TRANSCRIPTION; IN VITRO STUDY; LIVER CELL CULTURE; LIVER TOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARTIAL LEAST SQUARES REGRESSION; PRINCIPAL COMPONENT ANALYSIS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TOXICOKINETICS; TOXIN ANALYSIS;

ANIMALS; BENZOFURANS; CELLS, CULTURED; CYTOCHROME P-450 CYP1A1; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDPOINT DETERMINATION; GLUCURONOSYLTRANSFERASE; HEPATOCYTES; POLYCHLORINATED BIPHENYLS; PRINCIPAL COMPONENT ANALYSIS; RNA, MESSENGER; SALMO SALAR; TETRACHLORODIBENZODIOXIN;

SALMO SALAR;

EID: 70350707747     PISSN: 08872333     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tiv.2009.07.014     Document Type: Article

References (71)

1. AMAP. AMAP Assessment Report: Arctic Pollution Issues. Arctic Monitoring and Assessment Programme (AMAP) (1998), Oslo, Norway
2. Aruckwe A., and Nordbø B. Hepatic biotransformation responses in Atlantic salmon exposed to retinoic acid and 3,3′,4,4′-tetrachlorobiphenyl (PCB congener 77). Comparative Biochemistry and Physiology 147C (2008) 470-482
3. Baerson S.R., Sanchez-Moreiras A., Pedrol-Bonjoch N., Schulz M., Kagan I.A., Agarwal A.K., Reigosa M.J., and Duke S.O. Detoxification and transcriptome response in arabidopsis seedlings exposed to the allelochemical benzoxazolin-2(3H9-one. The Journal of Biological Chemistry 280 23 (2005) 21867-21881
4. Bemanin V., Male R., and Goksøyr A. The aryl hydrocarbon receptor-mediated disruption of vitellogenin synthesis in the fish liver: cross-talk between AHR- and ERα-signalling pathways. Comparative Hepatology 3 2 (2004) 1-14
5. Berenbaum M.C. What is synergy?. Pharmacological Reviews 41 (1989) 93-141
6. Berntssen M.H.G., Lundebye A.K., and Torstensen B.E. Reducing the levels of dioxins and dioxin-like PCBs in farmed Atlantic salmon by substitution of fish oil with vegetable oil in the feed. Aquaculture Nutrition 11 (2005) 219-231
7. Bock K.W., and Köhle C. Ah receptor: dioxin-mediated toxic responses as hints to deregulated physiologic functions. Biochemical Pharmacology 72 (2006) 393-404
8. Boström C.E., Gerde P., Hanberg A., Jernström B., Johansson C., Kyrklund T., Rannug A., Törnquist M., Victorin K., and Westerholm R. Cancer risk assessment, indicators, and guidelines for polycyclic aromatic hydrocarbons in the ambient air. Environmental Health Perspectives 110 3 (2002) 451-489
9. Brüschweiler B.J., Würgler F.E., and Fent K. An ELISA assay for cytochrome P4501A in fish liver cells. Environmental Toxicology and Chemistry 15 4 (1996) 592-596
10. Cao Z., Hong J., Peterson R.E., and Aiken J.M. Characterization of CYP1A1 and CYP1A3 gene expression in rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 49 (2000) 101-109
11. Carpenter D.O., Arcaro K., and Spink D.C. Understanding the human health effects of chemical mixtures. Environmental Health Perspectives 110 1 (2002) 25-42
12. Carver L.A., and Bradfield C.A. Ligand-dependent interaction of the aryl hydrocarbon receptor with a novel immunophilin homolog in vivo. Journal of Biological Chemistry 272 17 (1997) 11452-11456
13. Cherng S.H., Lin P., Yang J.L., Hsu S.L., and Lee H. Benzo[g,h,i]perylene synergistically transactivates benzo[a]pyrene-induced CYP1A1 gene expression by aryl hydrocarbon receptor pathway. Toxicology and Applied Pharmacology 170 (2001) 63-68
14. Chu I., Lecavalier P., Håkansson H., Yagminas A., Valli V.E., Poon P., and Freeley M. Mixture effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin and polychlorinated biphenyl congeners in rats. Chemosphere 43 (2001) 807-814
15. Clemons J.H., Myers C.R., Lee L.E.J., Dixon D.G., and Bols N.C. Induction of cytochrome P4501A by binary mixtures of polychlorinated biphenyls (PCBs) and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in liver cell lines from rat and trout. Aquatic Toxicology 43 (1998) 179-194
16. Corsolini S., Ademollo N., Romeo T., Greco S., and Focardi S. Persistent organic pollutants in edible fish: a human and environmental health problem. Microchemical Journal 79 (2005) 115-123
17. Coumoul X., Diry M., Robillot C., and Barouki R. Differential regulation of cytochrome P450 1A1 and 1B1 by a combination of dioxin and pesticides in the breast tumor cell line MCF-7. Cancer Research 61 (2001) 3942-3948
18. Dannevig B.H., and Berg T. Endocytosis of galactose-terminated glycoproteins by isolated liver cells of the rainbow trout (Salmo gairdneri). Comparative Biochemistry and Physiology 82B 4 (1985) 683-688
19. de Jongh J., Wondergem F., Seinen W., and van den Berg M. Toxicokinetic interactions between chlorinated aromatic hydrocarbons in the liver of the C57BL/6J mouse: I. Polychlorinated biphenyls (PCBs). Archives of Toxicology 67 (1993) 453-460
20. Denison M.S., Zhao B., Baston D.S., Clark G.C., Murata H., and Han D. Recombinant cell bioassay systems for the detection and relative quantification of halogenated dioxins and related chemicals. Talanta 63 (2004) 1123-1133
21. Eide I. Strategies for toxicological evaluation of mixtures. Food and Chemical Toxicology 34 (1996) 1147-1149
22. Eide I., and Johnsen H.G. Mixture design and multivariate analysis in mixture research. Environmental Health Perspectives 106 6 (1998) 1373-1376
23. Elonen G.E., Spehar R.L., Holcombe G.W., Johnson R.D., Fernandez J.D., Erickson R.J., Tietge J.E., and Cook P.M. Comparative toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin to seven freshwater fish species during early life-stage development. Environmental Toxicology and Chemistry 17 (1998) 472-483
24. Fent K., and Bätscher R. Cytochrome P4501A induction potencies of polycyclic aromatic hydrocarbons in a fish hepatoma cell line: demonstration of additive interactions. Environmental Toxicology and Chemistry 19 8 (2000) 2047-2058
25. Finne E.F., Cooper G.A., Koop B.F., Hylland K., and Tollefsen K.E. Toxicogenomic responses in rainbow trout (Oncorhynchus mykiss) hepatocytes exposed to model chemicals and a synthetic mixture. Aquatic Toxicology 81 (2007) 293-303
26. Fischer L.J., Seegal R.F., Ganey P.E., Pessah I.N., and Kodavanti P.R.S. Symposium overview: toxicity of non-coplanar PCBs. Toxicological Sciences 41 (1998) 49-61
27. Gooch J.W., Elskus A.A., Kloepper-Sams P.J., Hahn M.E., and Stegeman J.J. Effects of ortho- and non-ortho-substituted polychlorinated biphenyl congeners on the hepatic monooxygenase system in scup (Stenotumos chrysops). Toxicology and Applied Pharmacology 98 (1989) 422-433
28. Hahn M.E. Aryl hydrocarbon receptors: diversity and evolution. Chemico-Biological Interactions 141 (2002) 131-160
29. Hahn M.E. Biomarkers and bioassays for detecting dioxin-like compounds in the marine environment. The Science of the Total Environment 289 (2002) 49-69
30. Hahn M.E., Woodward B.L., Stegeman J.J., and Kennedy S.W. Rapid assessment of induced cytochrome P4501A protein and catalytic activity in fish hepatoma cells grown in multiwell plates: response to TCDD, TCDF, and two planar PCBs. Environmental Toxicology and Chemistry 15 4 (1996) 582-591
31. Henry E.C., Kende A.S., Rucci G., Totleben M.J., Willey J.J., Dertinger S.D., Pollenz R.S., Jones J.P., and Gasiewicz T.A. Flavone antagonists bind competitively with 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) to the aryl hydrocarbon receptor but inhibit nuclear uptake and transformation. Molecular Pharmacology 55 (1999) 716-725
32. Henry T.R., and DeVito M.J. Non-Dioxin-Like PCBs: Effects and Consideration in Ecological Risk Assessment (2003), Cincinnati, OH, USA
33. Henry T.R., Nesbit D.J., Heideman W., and Peterson R.E. Relative potencies of polychlorinated dibenzo-p-dioxin, dibenzofuran, and biphenyl congeners to induce cytochrome P4501A mRNA in a zebrafish liver cell line. Environmental Toxicology and Chemistry 20 5 (2001) 1053-1058
34. Huuskonen S.E., Tuvikene A., Trapido M., Fent K., and Hahn M.E. Cytochrome P4501A induction and porphyrin accumulation in PLHC-1 fish cells exposed to sediment and oil shale extracts. Archives of Environmental Contamination and Toxicology 38 (2000) 59-69
35. Ikuta T., Eguchi H., Tachibana T., Yoneda Y., and Kawajiri K. Nuclear localization and export signals of the human aryl hydrocarbon receptor. Journal of Biological Chemistry 273 5 (1998) 2895-2904
36. Jackson J.E. A User's Guide to Principal Components (1991), John Wiley, New York
37. Kodell R.L., and Pounds J.G. Assessing the toxicty of mixtures of chemicals. In: Krewsky D., and Franklin C. (Eds). Statistical Methods in Toxicological Research (1990), Gordon and Breach, New York 559-591
38. Kubista M., and Sindelka R. The prime technique; real-time PCR data analysis. G:I:T: Laboratory Journal 9-10 (2007) 33-35
39. Könemann W.H., and Pieters M.N. Confusion of concepts in mixture toxicology. Food and Chemical Toxicology 34 (1996) 1025-1031
40. Lundstedt T., Seifert E., Abramo L., Thelin B., Nyström A., Pettersen J., and Bergman R. Experimental design and optimization. Chemometrics and Intelligent Laboratory Systems 42 (1998) 3-40
41. Mandal P.K. Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology. Journal of Comparative Physiology 175B (2005) 221-230
42. Matthews J., and Gustafsson J. Estrogen receptor and aryl hydrocarbon receptor signalling pathways. Journal of the Nuclear Receptor Signaling Atlas 4 (2006) 1-4
43. Matthews J., Wihlen B., Thomsen J., and Gustafsson J. Aryl hydrocarbon receptor-mediated transcription: ligand-dependent recruitment of estrogen receptor α to 2,3,7,8-tretrachlorodibenzo-p-dioxin-responsive promoters. Molecular and Cellular Biology 25 13 (2005) 5317-5328
44. Mimura J., and Fujii-Kuriyama Y. Functional role of AhR in the expression of toxic effects by TCDD. Biochimica et Biophysica Acta 1619 (2003) 263-268
45. Moon J.Y., Kim Y.B., Lee S.I., Song H., Choi K., and Jeong G.H. Distribution characteristics of polychlorinated biphenyls in crucian carp (Carassius auratus) from major rivers in Korea. Chemosphere 62 (2006) 430-439
46. Myers R.H., and Montgomery D.C. Response Surface Methodology (2002), John Wiley and Sons Inc, New York
47. Nebert D.W., Roe A.L., Dieter M.Z., Solis W.A., Yang L., and Dalton T.P. Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochemical Pharmacology 59 (2000) 65-85
48. Østby L., and Krøkje A. Cytochrome P450 (CYP1A) induction and DNA adducts in a rat hepatoma cell line (Fao), exposed to environmentally relevant concentrations of organic compounds, singly and in combinations. Environmental Toxicology and Pharmacology 12 (2002) 15-26
49. Pinto B., Garritano S.L., Cristofani R., Ortaggi G., Giuliano A., Amodio-Cocchoero R., Cirillo T., De Giusti M., Boccia A., and Reali D. Monitoring of polychlorinated biphenyl contamination and estrogenic activity in water, commercial feed and farmed seafood. Environmental Monitoring and Assessment 144 (2008) 445-453
50. Rees C.B., McCormick S.D., and Heuvel V. Quantitative PCR analysis of CYP1A induction in Atlantic salmon (Salmo salar). Aquatic Toxicology 62 (2003) 67-78
51. Risso-de Faverney C., Girard Lafaurie J.P., and Rahmani R. Toxic effects of wastewaters collected at upstream and downstream sites of a purification station in cultures of rainbow trout hepatocytes. Archives of Environmental Contamination and Toxicology 41 (2001) 129-141
52. Safe S.H. Development validation and problems with the toxic equivalency factor approach for risk assessment of dioxins and related compounds. Journal of Animal Science 76 (1998) 134-141
53. Safe S.H. Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implications for risk assessment. Critical Reviews in Toxicology 24 2 (1994) 87-149
54. Sarkar S., Jana N.R., Yonemoto J., Tohyama C., and Sone H. Estrogen enhances induction of cytochrome P-4501A1 by 2,3,7,8-tetrachlorodibenzo-p-dioxin in liver of female Long-Evans rats. International Journal of Oncology 16 1 (2000) 141-147
55. Schlezinger J.J., Keller J., Verbrugge L.A., and Stegeman J.J. 3,3′,4,4′-tetrachlorobiphenyl oxidation in fish, bird and reptile species: relationship to cytochrome P4501A inactivation and reactive oxygen production. Comparative Biochemistry and Physiology 125C (2000) 273-386
56. Schlezinger J.J., White R.D., and Stegeman J.J. Oxidative inactivation of cytochrome P4501A (CYP1A) stimulated by 3,3′,4,4′-tetrachlorobiphenyl: production of reactive oxygen by vertebrate CYP1As. Molecular Pharmacology 56 (1999) 588-597
57. Schmitz H.J., Behnisch P., Hagenmaier A., Hagenmaier H., Bock K.W., and Schrenk D. CYP1A1-inducing potency in H4IIE cells and chemical composition of technical mixtures of polychlorinated biphenyls. Environmental Toxicology and Pharmacology 1 (1996) 73-79
58. Schmitz H.J., Hagenmaier A., Hagenmaier H.P., Bock K.W., and Schrenk D. Potency of mixtures of polychlorinated biphenyls as inducers of dioxin receptor-regulated CYP1A activity in rat hepatocytes and H4IIE cells. Toxicology 99 (1995) 47-54
59. Schroeder A., Mueller O., Stocker S., Salowsky R., Leiber M., Gassmann M., Lightfoot S., Menzel W., Granzow M., and Ragg T. The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Molecular Biology 7 (2006) 3
60. Seed J., Brown R.P., Olin S.S., and Foran J.A. Chemical mixtures: current risk assessment methodologies and future directions. Regulatory Toxicology and Pharmacology 22 (1995) 76-94
61. Seglen P.O. Preparation of isolated liver cells. Methods in Cell Biology 13 (1976) 29-83
62. Simmons J.E., and Gennings C. Experimental designs, statistics and interpretation. Food and Chemical Toxicology 34 (1996) 1169-1171
63. Till M., Riebniger D., Schmitz H.J., and Schrenk D. Potency of various polycyclic aromatic hydrocarbons as inducers of CYP1A1 in rat hepatocyte cultures. Chemico-Biological Interactions 117 (1999) 135-150
64. Toyoshiba H., Walker N.J., Bailer A.J., and Portier C.J. Evaluation of toxic equivalency factors for induction of cytochrome P450 CYP1A1 and CYP1A2 enzyme activity by dioxin-like compounds. Toxicology and Applied Pharmacology 194 (2004) 156-168
65. Vamvakas A., Keller J., and Dufresne M. In vitro induction of CYP1A1-associated activities in human and rodent cell lines by commercial and tissue-extracted halogenated aromatic hydrocarbons. Environmental Toxicology and Chemistry 15 6 (1996) 814-823
66. van der Oost R., Beyer J., and Vermeulen N.P.E. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology 13 (2003) 57-149
67. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., and Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3 7 (2002) RESEARCH0034
68. Walker N.J. Toxicological highlight: unraveling the complexities of the mechanism of action of dioxins. Toxicological Sciences 95 2 (2007) 297-299
69. Wold S. Cross-validatory estimation of the number of components in factor and principal components models. Technometrics 20 4 (1978) 397-405
70. Wold S., Ruhe A., Wold H., and Dunn III W.J. SIAM Journal on Scientific Computing 5 (1984) 735-743
71. Zabel E.W., Pollenz R., and Peterson R.E. Relative potencies of individual polychlorinated dibenzo-p-dioxin, dibenzofuran, and biphenyl congeners and congener mixtures based on induction of cytochrome P4501A mRNA in a rainbow trout gonadal cell line (RTG-2). Environmental Toxicology and Chemistry 15 12 (1996) 2310-2318