Induction of cytochrome P450 1A5 mRNA, protein and enzymatic activities by dioxin-like compounds, and congener-specific metabolism and sequestration in the liver of wild jungle crow (Corvus macrorhynchos) from Tokyo, Japan

Toxicological Sciences

Volumn 88, Issue 2, 2005, Pages 384-399

  Watanabe, Michio X ^a   Iwata, Hisato ^a   Okamoto, Mio ^a   Kim, Eun Young ^a   Yoneda, Kumiko ^b   Hashimoto, Takuma ^b   Tanabe, Shinsuke ^a  

^a EHIME UNIVERSITY   (Japan)

^b JAPAN WILDLIFE RESEARCH CENTER   (Japan)

Author keywords

Alkoxyresorufin O dealkylation activities; CYP1A5 mRNA; Dioxin like compounds; Hepatic sequestration; Jungle crow; Metabolism

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AMINO ACID; COMPLEMENTARY DNA; CYTOCHROME P450; CYTOCHROME P450 1A; CYTOCHROME P450 1A5; CYTOCHROME P450 2B; CYTOCHROME P450 2C; CYTOCHROME P450 3A; DIBENZOFURAN; DIOXIN; MESSENGER RNA; POLYCHLORINATED BIPHENYL; POLYCHLORINATED DIBENZODIOXIN; POLYCLONAL ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BIRD; BREAST; CATALYSIS; CHICKEN; CONTAMINATION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; ENZYME INDUCTION; EXPOSURE; JAPAN; LIVER; LIVER MICROSOME; METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PROTEIN EXPRESSION;

AMINO ACID SEQUENCE; ANIMALS; ARYL HYDROCARBON HYDROXYLASES; BASE SEQUENCE; BENZOFURANS; CROWS; DIOXINS; ENZYME INDUCTION; GENE EXPRESSION; LIVER; MALE; MICROSOMES, LIVER; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; OXIDOREDUCTASES; POLYCHLORINATED BIPHENYLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TETRACHLORODIBENZODIOXIN; TRANSCRIPTION, GENETIC;

ANIMALIA; AVES; CORVUS MACRORHYNCHOS;

EID: 27944431747     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfi326     Document Type: Article

References (44)

1. Bosveld, A. T. C., Grandener, J., Murk, A. J., Brouwer, A., Van Kampen, M., Evers, E. H. G., and Van den Berg, M. (1995). Effects of PCDDs, PCDFs and PCBs in common tern (Sterna hirundo) breeding in estuarine and coastal colonies in the Netherlands and Belgium. Environ. Toxicol. Chem. 14, 99-115.
2. Bosveld, A. T. C., Nieboer, R., De Bout, A., Mennen, J., Murk, A. J., Feyk, L. A., Giesy, J. P., and Van den Berg, M. (2000). Biochemical and developmental effects of dietary exposure to polychlorinated biphenyls 126 and 153 in common tern chicks (Sterna hirundo). Environ. Toxicol. Chem. 19, 719-730.
3. Burke, M. D., Thompson, S., Weaver, R. J., Wolf, C. R., and Mayer, R. T. (1994). Cytochrome P450 specificities of alkoxyresorufin O-dealkylation in human and rat liver. Biochem. Pharmacol. 48, 923-936.
4. Chen, C. Y., Hamm, J. T., Hass, J. R., and Birnbaum, L. S. (2001). Distribution of polychlorinated dibenzo-p-dioxins, dibenzofurans, and non-ortho polychlorinated biphenyls in pregnant Long Evans rats and the transfer to offspring. Toxicol. Appl. Pharmacol. 173, 65-88.
5. DeVito, M. J., Ross, D. G., Dupuy, A. E., Jr., Ferrario, J., McDaniel, D., and Birnbaum, L. S. (1998). Dose-response relationships for disposition and hepatic sequestration of polyhalogenated dibenzo-p-dioxins, dibenzofurans, and biphenyls following subchronic treatment in mice. Toxicol. Sci. 46, 223-234.
6. Diliberto, J. J., Burgin, D. E., and Birnbaum, L. S. (1999). Effects of CYP1A2 on disposition of 2,3,7,8-tetrachlorodibenzo-p-dioxin, 2,3,4,7,8-pentachlorodibenzofuran, and 2,2′,4,4′,5,5′-hexachlorobiphenyl in CYP1A2 knockout and parental (C57BL/6N and 129/Sv) strains of mice. Toxicol. Appl. Pharmacol. 159, 52-64.
7. Edwards, R. J., Murray, B. P., Boobis, A. R., and Davies, D. S. (1989). Identification and location of α-helices in mammalian cytochrome P450. Biochemistry 28, 3762-3770.
8. Giesy, J. P., Ludwig, J. P., and Tillitt, D. E. (1994). Deformites in birds of the great lakes region. Environ. Sci. Technol. 28, 128A-135A.
9. Gilday, D., Gannon, M., Yutzey, K., Bader, D,, and Rifkind, A. B. (1996). Molecular cloning and expression of two novel avian cytochrome P450 1A enzymes induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin. J. Bio. Chem. 271, 33054-33059.
10. Guengerich, F. P. (1982). Microsomal enzymes involved in toxicology: Analysis and separation. In Principles and Methods of Toxicology (A. W. Hayes, Ed.), pp. 609-634. Raven Press, New York.
11. Guruge, K. S., and Tanabe, S. (1997). Congener specific accumulation and toxic assessment of polychlorinated biphenyls in common cormorants, Phalacrocorax carbo, from Lake Biwa, Japan. Environ. Pollut. 96, 425-433.
12. Guruge, K. S., Tanabe, S., and Fukuda, M. (2000). Toxic assessment of PCBs by the 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalent in common cormorant (Phalacrocorax carbo) from Japan. Arch. Environ. Contam. Toxicol. 38, 509-521.
13. Handly-Goldstone, H. M., and Stegeman, J. J. (in press). Evidence of a single gene duplication and gene conversion in tetrapod CYP1As. J. Mol. Evol.
14. Hu, K., and Bunce, N. J. (1999). Metabolism of polychlorinated dibenzo-p-dioxins by rat liver microsomes. J. Biochem. Mol. Tox. 13, 307-315.
15. Imai, M., Shimada, H., Watanabe, Y., Matsushima-Hibiya, Y., Makino, R., Koga, H., Horiuchi, T., and Ishimura, Y. (1989). Uncoupling of the cytochrome P-450cam monooxygenase reaction by a single mutation, threonine-252 to alanine or valine: A possible role of the hydroxyl amino acid in oxygen activation. Proc. Natl. Acad. Sci. U.S.A. 86, 7823-7827.
16. Iwata, H., Watanabe, M., Okajima, Y., Tanabe, S., Amano, M., Miyazaki, N., and Petrov, E. A. (2004). Toxicokinetics of PCDD, PCDF, and coplanar PCB congeners in Baikal seals, Pusa sibirica: Age-related accumulation, maternal transfer, and hepatic sequestration. Environ. Sci. Technol. 38, 3505-3513.
17. Iwata, H., Yoshinari, K., Negishi, M., and Stegeman, J. J. (2002). Species-specific responses of constitutively active receptor (CAR) - CYP2B coupling: Lack of CYP2B inducer-responsive nuclear translocation of CAR in marine teleost, scup (Stenotomus chrysops). Comp. Biochem. Physiol. 131C, 501-510.
18. Jacobs, J. M., Sinclair, P. R., Bement, W. J., Lambrecht, R. W., Sinclair, J. F., and Goldstein, J. A. (1989). Oxidation of uroporphyrinogen by methylcholanthrene-induced cytochrome P-450d. Essential role of cytochrome P-450d. Biochem. J. 258, 247-253.
19. Jones, P. D., Giesy, J. P., Newsted, J. L., Verbrugge, D. A., Beaver, D. L., Ankley, G. T., Tillitt, D. E., Lodge, K. B., and Niemi, G. J. (1993). 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents in tissues of birds at Green Bay, Wisconsin, USA. Arch. Environ. Contam. Toxicol. 24, 345-354.
20. Kennedy, S. W., Lorenzen, A., Jones, S. P., Hahn, M. E., and Stegeman, J. J. (1996). Cytochrome P4501A induction in avian hepatocyte cultures: A promising approach for predicting the sensitivity of avian species to toxic effects of halogenated aromatic hydrocarbons. Toxicol. Appl. Pharmacol. 141, 214-230.
21. Koistinen, J., Koivusaari, J., Nuuja, I., Vuorinen, P. J., Paasivirta, J., and Giesy, J. P. (1997). 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents in extracts of Baltic white-tailed sea eagles. Environ. Toxicol. Chem. 16, 1533-1544.
22. Körner, W., Golor, G., Schulz, T., Wiesmüller, T., Hagenmaier, H., and Neubert, D. (2002). Tissue concentrations and induction of a hepatic monooxygenase in male Wister rats after repeated doses of defined polychlorinated dibenzo-p-dioxin and dibenzofuran (PCDDs and PCDFs) mixtures. Arch. Toxicol. 75, 653-664.
23. Kubota, A., Iwata, H., Tanabe, S., Yoneda, K., and Tobata, S. (2004). Levels and toxicokinetic behaviors of PCDD, PCDF, and coplanar PCB congeners in common cormorants from Lake Biwa, Japan. Environ. Sci. Technol. 38, 3853-3859.
24. Kubota, A., Iwata, H., Tanabe, S., Yoneda, K., and Tobata, S. (2005). Hepatic CYP1A induction by dioxin-like compounds, and congener-specific metabolism and sequestration in wild common cormorants from Lake Biwa, Japan. Environ. Sci. Technol. 39, 3611-3619.
25. Lambrecht, R. W., Sinclair, P. R., Gorman, N., and Sinclair, J. F. (1992). Uroporphyrinogen oxidation catalyzed by reconstituted cytochrome P4501A2. Arch. Biochem. Biophys. 294, 504-510.
26. Leffin, M., and Riviere, J. L. (1992). Effects of some inducers on hepatic and extrahepatic drug metabolism in the mallard duck (Anas platyrhynchos). Comp. Biochem. Phys. 102C, 471-476.
27. Murk, A., Morse, D., Boon, J., and Brouwer, A. (1994). In vitro metabolism of 3,3′,4,4′-tetrachlorobiphenyl in relation to ethoxyresorufin-O-deethylase activity in liver microsomes of some wildlife species and rat. Eur. J. Pharmacol. 270, 253-261.
28. Nakai, K., Ward, A. M., Gannon, M., and Rifkind, A. B. (1992). β-naphthoflavone induction of a cytochrome P-450 arachidonic acid epoxygenase in chick embryo liver distinct from the aryl hydrocarbon hydroxylase and from phenobarbital-induced arachidonate epoxygenase. J. Biol. Chem. 267, 19503-19512.
29. Poland, A., and Glover, E. (1973). Chlorinated dibenzo-p-dioxins: Potent inducers of δ-aminolevulinic acid synthetase and aryl hydrocarbon hydroxylase. Mol. Pharmacol. 9, 736-747.
30. Rattner, B. A., Melancon, M. J., Custer, T. W., Hothem, R. L., King, K. A., LeCaptain, L. J., Spann, J. W., Woodin, B. R., and Stegeman, J. J. (1993). Biomonitoring environmental contamination with pipping black-crowned night heron embryos: Induction of cytochrome P450. Environ. Toxicol. Chem. 12, 1719-1732.
31. Rifkind, A. B., Kanetoshi, A., Orlinick, J., Capdevila, J. H., and Lee, C. (1994). Purification and biochemical characterization of two major cytochrome P-450 isoforms induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin in chick embryo liver. J. Biol. Chem. 269, 3387-3396.
32. Sanderson, J. T., and Bellward, G. D. (1995). Hepatic microsomal ethoxyresorufin O-deethylase-inducing potency in ovo and cytosolic Ah receptor binding affinity of 2,3,7,8-tetrachlorodibenzo-p-dioxin: Comparison of four avian species. Toxicol. Appl. Pharmacol. 132, 131-145.
33. Senthilkumar, K., Iseki, N., Hayama, S., Nakanishi, J., and Masunaga, S. (2002a). Polychlorinated dibenzo-p-dioxins, dibenzofurans, and dioxin-like polychlorinated biphenyls in livers of birds from Japan. Arch. Environ. Contam. Toxicol. 42, 244-255.
34. Senthilkumar, K., Kannan, K., Giesy, J. P., and Masunaga, S. (2002b). Distribution and elimination of polychlorinated dibenzo-p-dioxins, dibenzofurans, biphenyls, and p,p′-DDE in tissues of bald eagles from the upper peninsula of Michigan. Environ. Sci. Technol. 36, 2789-2796.
35. Senthilkumar, K., Watanabe, K., Takemori, H., Iseki, N., Masunaga, S., and Takasuga, T. (2005). Analysis of UNEP priority POPs using HRGC-HRMS and their contamination profiles in livers and eggs of great cormorants (Phalacrocorax carbo) from Japan. Arch. Environ. Contam. Toxicol. 48, 538-551.
36. Smith, P. K., Krohn, R. I., and Hermanson, G. T. (1985). Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.
37. Tai, H. L., McReynolds, J. H., Goldstein, J. A., Eugster, H. P., Sengstag, C., Alworth, W. L., and Olson, J. R. (1993). Cytochrome P4501A1 mediates the metabolism of 2,3,7,8-tetrachlorodibenzofuran in the rat and human. Toxicol. Appl. Pharmacol. 123, 34-42.
38. Uno, S., Dalton, T. P., Sinclair, P. R., Gorman, N., Wang, B., Smith, A. D., Miller, M. L., Shertzer, H. G., and Nebert, D. W. (2004). Cyp1a1(-/ -) male mice: Protection against high-dose TCDD-induced lethality and wasting syndrome, and resistance to intrahepatocyte lipid accumulation and uroporphyria. Toxicol. Appl. Pharmacol. 196, 410-421.
39. Van den Berg, M., Birnbaum, L., Bosveld, A. T. C., Brunström, B., Cook, P., Feeley, M., Giesy, J. P., Hanberg, A., Hasegawa, R., Kennedy, S. W., et al. (1998). Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environ. Health Perspect. 106, 775-792.
40. Van den Berg, M., De Jongh, J., Poiger, H., and Olson, J. R. (1994). The toxicokinetics and metabolism of polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs) and their relevance for toxicity. Crit. Rev. Toxicol. 24, 1-74.
41. Verbrugge, L. A., Giesy, J. P., Verbrugge, D. A., Woodin, B. R., and Stegeman, J. J. (2001). Catalytic and immunochemical properties of hepatic cytochrome P450 1A in three avian species treated with β-naphthoflavone or isosafrole. Comp. Biochem. Phys. 130C, 67-83.
42. Wan, Y., Hu, J., Yang, M., An, L., An, W., Jin, X., Hattori, T., and Itoh, M. (2005). Characterization of trophic transfer for polychlorinated dibenzo-p-dioxins, dibenzofurans, non- and mono-ortho polychlorinated biphenyls in the marine food web of Bohai Bay, North China. Environ. Sci. Technol. 39, 2417-2425.
43. Watanabe, M. X., Iwata, H., Watanabe, M., Tanabe, S., Subramanian, An., Yoneda, K., and Hashimoto, T. (2005). Bioaccumulation of organochlorines in crows from Indian open waste dumping site: Evidence for direct transfer of dioxin-like congeners from the contaminated soil. Environ. Sci. Technol. 39, 4421-4430.
44. BM-3. Biochemistry 34, 14733-14740.