Effects of hydroxy-polychlorinated biphenyl (OH-PCB) congeners on the xenobiotic biotransformation gene expression patterns in primary culture of Atlantic salmon (Salmo salar) hepatocytes

Ecotoxicology and Environmental Safety

Volumn 68, Issue 3, 2007, Pages 351-360

  Mortensen, Anne S ^a   Braathen, Marte ^b   Sandvik, Morten ^c   Arukwe, Augustine ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^c NORWEGIAN VETERINARY INSTITUTE   (Norway)

Author keywords

AhR; Biotransformation; Fish; Hepatocytes; Hydroxylated PCBs; Suppression

Indexed keywords

CYTOCHROME P450 1A1; CYTOCHROME P450 3A; ESTROGEN; ETHINYLESTRADIOL; GLUCURONOSYLTRANSFERASE; GLUTATHIONE; HYPOXIA INDUCIBLE FACTOR 1BETA; POLYCHLORINATED BIPHENYL;

BIOTRANSFORMATION; ESTROGENIC COMPOUND; GENE EXPRESSION; PCB; POLLUTION EFFECT; POLLUTION EXPOSURE; SALMONID; XENOBIOTICS;

ANIMAL CELL; ARTICLE; ATLANTIC SALMON; BIOTRANSFORMATION; CLEARANCE; CONTROLLED STUDY; ESTROGEN ACTIVITY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE SEQUENCE; GENETIC TRANSCRIPTION; IN VITRO STUDY; LIVER CELL; LIVER CELL CULTURE; MOLECULE; NONHUMAN; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; XENOBIOTIC METABOLISM;

ANIMALS; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; BIOTRANSFORMATION; CELLS, CULTURED; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 CYP3A; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTROGENS; ETHINYL ESTRADIOL; FISH PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCURONOSYLTRANSFERASE; GLUTATHIONE TRANSFERASE; HEPATOCYTES; HYDROXYLATION; POLYCHLORINATED BIPHENYLS; RECEPTORS, ARYL HYDROCARBON; RNA, MESSENGER; SALMO SALAR; SIGNAL TRANSDUCTION; WATER POLLUTANTS, CHEMICAL; XENOBIOTICS;

SALMO SALAR;

EID: 34848923326     PISSN: 01476513     EISSN: 10902414     Source Type: Journal    
DOI: 10.1016/j.ecoenv.2006.11.019     Document Type: Article

References (61)

1. Ahlborg U.G., Lipworth L., Titus-Ernstoff L., Hsieh C.C., Hanberg A., Baron J., Trichopoulos D., and Adami H.O. Organochlorine compounds in relation to breast cancer, endometrial cancer, and endometriosis: an assessment of the biological and epidomiological evidence. Crit. Rev. Toxicol. 25 (1995) 463-531
2. Anderson M.J., Miller M.R., and Hinton D.E. In vitro modulation of 17ß-estradiol-induced vitellogenin synthesis: effects of cytochrome P4501A1 inducing compounds on rainbow trout (Oncorhychus mykiss) liver cells. Aquat. Toxicol. 34 (1996) 327-350
3. Anderson M.J., Olsen H., Matsumura F., and Hinton D.E. In vivo modulation of 17β-estradiol-induced vitellogenin synthesis and estrogen receptor in rainbow trout (Oncorhynchus mykiss) liver cells by β-naphthoflavone. Toxicol. Appl. Pharmacol. 137 (1996) 210-218
4. Andersson T., Förlin L., and Hansson T. Biotransformation of 7- ethoxycoumarin in isolated perfused rainbow trout liver. Drug Metab. Dispos. 11 (1983) 494-498
5. Andersson P.L., Blom A., Johannisson A., Pesonen M., Tysklind M., Berg A.H., Olsson P.E., and Norrgren L. Assessment of PCBs and hydroxylated PCBs as potential xenoestrogens: in vitro studies based on MCF-7 cell proliferation and induction of vitellogenin in primary culture of rainbow trout hepatocytes. Arch. Environ. Contam. Toxicol. 37 (1999) 145-150
6. Aoki Y. Polychlorinated biphenyls, polychlorinated dibenzo-p-dioxins, and polychlorinated dibenzofurans as endocrine disrupters-what we have learned from Yusho disease. Environ. Res. 86 (2001) 2-11
7. Arukwe A. Modulation of brain steroidogenesis by affecting transcriptional changes of steroidogenic acute regulatory (StAR) protein and cholesterol side chain cleavage (P450scc) in Juvenile Atlantic salmon (Salmo salar) is a novel aspect of nonylphenol toxicity. Environ. Sci. Technol. 39 (2005) 9791-9798
8. Arukwe A., and Goksøyr A. Changes in three hepatic cytochrome P450 subfamilies during a reproductive cycle in Turbot (Scophthalmus maximus L.). J. Exp. Zool. 277 (1997) 313-325
9. Arukwe A., Forlin L., and Goksøyr A. Xenobiotic and steroid biotransformation enzymes in Atlantic salmon (Salmo salar) liver treated with an estrogenic compound, 4-nonylphenol. Environ. Toxicol, Chem. 16 (1997) 2576-2583
10. Arukwe A., Celius T., Walther B.T., and Goksoyr A. Effects of xenoestrogen treatment on zona radiata protein and vitellogenin expression in Atlantic salmon (Salmo salar). Aquat. Toxicol. 49 (2000) 159-170
11. Arukwe A., Yadetie F., Male R., and Goksoyr A. In vivo modulation of nonylphenol-induced zonagenesis and vitellogenesis by the antiestrogen, 3,3′4,4′-tetrachlorobiphenyl (PCB-77) in juvenile fish. Environ. Toxicol. Pharmacol. 10 (2001) 5-15
12. Aubry E., Rime H., and Monod G. Beta-naphthoflavone inhibits the induction of hepatic oestrogen-dependent proteins by 17alpha-ethynylestradiol in mosquitofish (Gambusia holbrooki). Biomarkers 10 (2005) 439-455
13. Berry M.N., and Friend D.S. High-yield preparations of isolated rat liver parenchymal cells. A biocemical and fine structural study. J. Cell Biol. 43 (1969) 506-520
14. Besselink H.T., Denison M.S., Hahn M.E., Karchner S.I., Vethaak A.D., Koeman J.H., and Brouwer A. Low inducibility of CYP1A activity by polychlorinated biphenyls (PCBs) in flounder (Platichthys flesus): characterization of the Ah receptor and the role of CYP1A inhibition. Toxicol. Sci. 43 (1998) 161-171
15. Buckman A.H., Brown S.B., Hoekstra P.F., Solomon K.R., and Fisk A.T. Toxicokinetics of three polychlorinated biphenyl technical mixtures in rainbow trout (Oncorhynchus mykiss). Environ. Toxicol. Chem. 23 (2004) 1725-1736
16. Buhler D.R., Miranda C.L., Henderson M.C., Yang Y.H., Lee S.J., and Wang-Buhler J.L. Effects of 17β-estradiol and testosterone on hepatic mRNA/protein levels and catalytic activities of CYP2M1, CYP2K1, and CYP3A27 in rainbow trout (Oncorhynchus mykiss). Toxicol. Appl. Pharmacol. 168 (2000) 91-101
17. Carlson D.B., and Williams D.E. 4-hydroxy-2′,4′,6′-trichlorobiphenyl and 4-hydroxy-2′,3′,4′,5′-tetrachlorobiphenyl are estrogenic in rainbow trout. Environ. Toxicol. Chem. 20 (2001) 351-358
18. Chan Z., and Hollebone B. A QSAR for steroidal compound interaction with cytochrome P4501A1. Environ. Toxicol. Chem. 14 (1995) 597-603
19. Cheek A.O., Kow K., Chen J., and McLachlan J.A. Potential mechanisms of thyroid disruption in humans: interaction of organochlorine compounds with thyroid receptor, transthyretin, and thyroid-binding globulin. Environ. Health Perspect. 107 (1999) 273-278
20. Connor K., Ramamoorthy K., Moore M., Mustain M., Chen I., Safe S., Zacharewski T., Gillesby B., Joyeux A., and Balaguer P. Hydroxylated polychlorinated biphenyls (PCBs) as estrogens and antiestrogens: structure-activity relationships. Toxicol. Appl. Pharmacol. 145 (1997) 111-123
21. Crews D., Bergeron J.M., and McLachlan J.A. The role of estrogens in turtle sex determination and the effects of PCBs. Environ. Health Perspect. 103 (1995) 73-77
22. Dalton T.P., Dieter M.Z., Matlib R.S., Childs N.L., Shertzer H.G., Genter M.B., and Nebert D.W. Targeted knockout of CYP1A1 gene does not alter hepatic constitutive expression of other genes in the mouse [Ah] battery. Biochem. Biophys. Res. Commun. 267 (2000) 184-189
23. Elizondo G., Fernandez-Salguero P., Sheikh M.S., Kim G.Y., Fornace A.J., Lee K.S., and Gonzalez F.J. Altered cell cycle control at the G(2)/M phases in aryl hydrocarbon receptor-null embryo fibroblast. Mol. Pharmacol. 57 (2000) 1056-1063
24. Fangstrom B., Athanasiadou M., Grandjean P., Weihe P., and Bergman A. Hydroxylated PCB metabolites and PCBs in serum from pregnant Faroese women. Environ. Health Perspect. 110 (2002) 895-899
25. Fernandez-Salguero P., Pineau T., Hilbert D.M., McPhail T., Lee S.S., Kimura S., Nebert D.W., Rudikoff S., Ward J.M., and Gonzalez F.J. Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 268 (1995) 722-726
26. FitzGerald C.T., Fernandez-Salguero P., Gonzalez F.J., Nebert D.W., and Puga A. Differential regulation of mouse Ah receptor gene expression in cell lines of different tissue origins. Arch. Biochem. Biophys. 333 (1996) 170-178
27. Förlin L., and Haux C. Sex differences in hepatic cytochrome P-450 monooxygenase activities in rainbow trout during an annual reproductive cycle. J. Endocrinol. 124 (1990) 207-213
28. George S.G. Enzymology and molecular biology of phase II xenobiotic-conjugating enzymes in fish. In: Malins D.C., and Ostrander G.K. (Eds). Aquatic Toxicology: Molecular, Biochemical, and Cellular Perspectives (1994), Lewis Publisher Inc., Boca Raton, Florida, USA 37-85
29. Gonzalez F.J., and Fernandez-Salguero P. The aryl hydrocarbon receptor: studies using the AHR-null mice. Drug Metab. Dispos. 26 (1998) 1194-1198
30. Hahn M.E. Dioxin toxicology and the aryl hydrocarbon receptor: insights from fish and other non-traditional models. Mar. Biotechnol. 3 (2001) S224-S238
31. Hasselberg L., Meier S., Svardal A., Hegelund T., and Celander M.C. Effects of alkylphenols on CYP1A and CYP3A expression in first spawning Atlantic cod (Gadus morhua). Aquat. Toxicol. 67 (2004) 303-313
32. Ko H.P., Okino S.T., Ma Q., and Whitlock Jr. J.P. Dioxin-induced CYP1A1 transcription in vivo: the aromatic hydrocarbon receptor mediates transactivation, enhancer-promoter communication, and changes in chromatin structure. Mol. Cell Biol. 16 (1996) 430-436
33. Koivusaari U., Harri M., and Hanninen O. Seasonal variation of hepatic biotransformation in female and male rainbow trout (Salmo gairdneri). Comp. Biochem. Physiol. 70 (1981) 149-157
34. Kramer V.J., and Giesy J.P. Specific binding of hydroxylated polychlorinated biphenyl metabolites and other substances to bovine calf uterine estrogen receptor: structure-binding relationships. Sci. Total Environ. 233 (1999) 141-161
35. Letcher R.J., Lemmen J.G., van der Burg B., Brouwer A., Bergman A., Giesy J.P., and van den Berg M. In vitro antiestrogenic effects of aryl methyl sulfone metabolites of polychlorinated biphenyls and 2,2-bis(4-chlorophenyl)-1,1-dichloroethene on 17beta-estradiol-induced gene expression in several bioassay systems. Toxicol. Sci. 69 (2002) 362-372
36. Lin H.L., Kent U.M., and Hollenberg P.F. Mechanism-based inactivation of cytochrome P450 3A4 by 17α-ethynylestradiol: evidence for heme destruction and covalent binding to protein. J. Pharmacol. Exp. Ther. 301 (2002) 160-167
37. Malmberg T., Hoogstraate J., Bergman A., and Klasson Wehler E. Pharmacokinetics of two major hydroxylated polychlorinated biphenyl metabolites with specific retention in rat blood. Xenobiotica 34 (2004) 581-589
38. Maradonna F., Polzonetti V., Bandiera S.M., Migliarini B., and Carnevali O. Modulation of the hepatic CYP1A1 system in the marine fish Gobius niger, exposed to xenobiotic compounds. Environ. Sci. Technol. 38 (2004) 6277-6282
39. Meerts I.A., Hoving S., Van Den Berg J.H., Weijers B.M., Swarts H.J., Van Der Beek E.M., Bergman A., Koeman J.H., and Brouwer A. Effects of in utero exposure to 4-hydroxy-2,3,3′,4′,5-pentachlorobiphenyl (4-OH-CB107) on developmental landmarks, steroid hormone levels and female estrous cyclicity in rats. Toxicol. Sci. 82 (2004) 258-267
40. Moore M., Mustain M., Daniel K., Chen I., Safe S., Zacharewski T., Gillesby B., Joyeux A., and Balaguer P. Antiestrogenic activity of hydroxylated polychlorinated biphenyl congeners identified in human serum. Toxicol. Appl. Pharmacol. 142 (1997) 160-168
41. Mortensen A.S., Tolfsen C.C., and Arukwe A. Gene expression patterns in estrogen (Nonylphenol) and Aryl hydrocarbon receptor agonists (PCB-77) interaction using rainbow trout (Oncorhynchus Mykiss) primary Hepatocyte culture. J. Toxicol. Environ. Health A 69 (2006) 1-19
42. Navas J.M., and Segner H. Antiestrogenicity of beta-naphthoflavone and PAHs in cultured rainbow trout hepatocytes: evidence for a role of the arylhydrocarbon receptor. Aquat. Toxicol. 51 (2000) 79-92
43. Navas J.M., and Segner H. Modulation of trout 7-ethoxyresorufin-O-deethylase (EROD) activity by estradiol and octylphenol. Mar. Environ. Res. 50 (2000) 157-162
44. Navas J.M., and Segner H. Estrogen-mediated suppression of cytochrome P4501A (CYP1A) expression in rainbow trout hepatocytes: role of estrogen receptor. Chem. Biol. Interact. 138 (2001) 285-298
45. Nebert D.W., Roe A.L., Dieter M.Z., Solis W.A., Yang Y., and Dalton T.P. Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem. Pharmacol. 59 (2000) 65-85
46. Nebert D.W., Dalton T.P., Okey A.B., and Gonzalez F.J. Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J. Biol. Chem. 279 (2004) 23847-23850
47. Riedel R., Schlenk D., Frank D., and Costa-Pierce B. Analyses of organic and inorganic contaminants in Salton Sea fish. Mar. Pollut. Bull. 44 (2002) 403-411
48. Safe S. Limitations of the toxic equivalency factor approach for risk assessment of TCDD and related compounds. Teratog. Carcinog. Mutagen. 17 (1997) 285-304
49. Safe S., Astroff B., Harris M., Zacharewski T., Dickerson R., Romkes M., and Biegel. I. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) and related compounds as antiestrogens: charaterization and mechanism of action. Pharmacol. Toxicol. 69 (1991) 400-409
50. Smeets J.M.W., van Holsteijn I., Giesy J.P., and van den Berg M. The anti-estrogenicity of Ah receptor agonists in carp (Cyprinus carpio) hepatocytes. Toxicol. Sci, 52 (1999) 178-188
51. Sogawa K., Iwabuchi K., Abe H., and Fujii-Kuriyama Y. Transcriptional activation domains of the Ah receptor and Ah receptor nuclear translocator. J. Cancer Res. Clin. Oncol. 121 (1995) 612-620
52. Spink B.C., Fasco M.J., Gierthy J.F., and Spink D.C. 12-O-tetradecanoylphorbol-13-acetate upregulates the Ah receptor and differentially alters CYP1B1 and CYP1A1 expression in MCF-7 breast cancer cells. J. Cell Biochem. 70 (1998) 289-296
53. Thurmond T.S., and Gasiewicz T.A. A single dose of 2,3,7,8-tetrachlorodibenzo-p-dioxin produces a time- and dose-dependent alteration in the murine bone marrow B-lymphocyte maturation profile. Toxicol. Sci. 58 (2000) 88-95
54. Thurmond L.M., Lauer L.D., House R.V., Cook J.C., and Dean J.H. Immunosuppression following exposure to 7,12-dimethylbenz[a]anthracene (DMBA) in Ah-responsive and Ah-nonresponsive mice. Toxicol. Appl. Pharmacol. 91 (1987) 450-460
55. van Lipzig M.M., ter Laak A.M., Jongejan A., Vermeulen N.P., Wamelink M., Geerke D., and Meerman J.H. Prediction of ligand binding affinity and orientation of xenoestrogens to the estrogen receptor by molecular dynamics simulations and the linear interaction energy method. J. Med. Chem. 47 (2004) 1018-1030
56. Vasseur P., and Cossu-Leguille C. Linking molecular interactions to consequent effects of persistent organic pollutants (POPs) upon populations. Chemosphere 62 (2006) 1033-1042
57. Vaziri C., Schneider A., Sherr D.H., and Faller D.V. Expression of the aryl hydrocarbon receptor is regulated by serum and mitogenic growth factors in murine 3T3 fibroblasts. J. Biol. Chem. 271 (1996) 25921-25927
58. Whitelaw M.L., Gustafsson J.A., and Poellinger L. Identification of transactivation and repression functions of the dioxin receptor and its basic helix-loop-helix/PAS partner factor Arnt: inducible versus constitutive modes of regulation. Mol. Cell Biol. 14 (1994) 8343-8355
59. Wilson C.L., and Safe S. Mechanisms of ligand-induced aryl hydrocarbon receptor-mediated biochemical and toxic responses. Toxicol. Pathol. 26 (1998) 657-671
60. Wolff S., Harper P.A., Wong J.M., Mostert V., Wang Y., and Abel J. Cell-specific regulation of human aryl hydrocarbon receptor expression by transforming growth factor-β1. Mol. Pharmacol. 59 (2001) 716-724
61. Zaher H., Fernandez-Salguero P.M., Letterio J., Sheikh M.S., Fornace Jr. A.J., Roberts A.B., and Gonzalez F.J. The involvement of aryl hydrocarbon receptor in the activation of transforming growth factor-β and apoptosis. Mol. Pharmacol. 54 (1998) 313-321