Molecular characterization of cytochrome P450 1A1, 1A2, and 1B1, and Effects of polychlorinated dibenzo-p-dioxin, dibenzofuran, and biphenyl congeners on their hepatic expression in baikal seal (pusa sibirica)

Toxicological Sciences

Volumn 97, Issue 2, 2007, Pages 318-335

  Hirakawa, Shusaku ^a   Iwata, Hisato ^a   Takeshita, Yoko ^a   Kim, Eun Young ^a   Sakamoto, Tomohiro ^a   Okajima, Yuka ^a   Amano, Masao ^b   Miyazaki, Nobuyuki ^c   Petrov, Evgeny A ^d   Tanabe, Shinsuke ^a  

^a EHIME UNIVERSITY   (Japan)

^b TEIKYO UNIVERSITY OF SCIENCE   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d The Eastern Siberian Scientific and Production Fisheries Center   (Russian Federation)

Author keywords

Baikal seal; Catalytic inhibition; Cytochrome P450 1A; Cytochrome P450 1B; Toxic equivalent

Indexed keywords

AMINO ACID; COMPLEMENTARY DNA; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 1B1; ETHOXYRESORUFIN DEETHYLASE; MESSENGER RNA; POLYCHLORINATED BIPHENYL DERIVATIVE; POLYCHLORINATED DIBENZODIOXIN; POLYCHLORINATED DIBENZOFURAN;

ANIMAL TISSUE; ARTICLE; CANCER RISK; CARCINOGENICITY; CATALYSIS; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; IMMUNOCHEMISTRY; LIVER; LIVER MICROSOME; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN INDUCTION; PUSA SIBIRICA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RUSSIAN FEDERATION; SEAL; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, BLOCKING; ARYL HYDROCARBON HYDROXYLASES; BENZOFURANS; BIPHENYL COMPOUNDS; BLOTTING, WESTERN; CATALYSIS; CLONING, MOLECULAR; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 CYP1A2; DNA, COMPLEMENTARY; ENVIRONMENTAL POLLUTANTS; ISOENZYMES; LIVER; MICROSOMES, LIVER; MOLECULAR SEQUENCE DATA; PHYLOGENY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; SEALS, EARLESS; TETRACHLORODIBENZODIOXIN;

PHOCA SIBIRICA; RATTUS;

EID: 34447558488     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfm066     Document Type: Article

References (61)

1. Blobaum, A. L., Kent, U. M., Alworth, W. L., and Hollenberg P. F. (2004). Novel reversible inactivation of cytochrome P450 2E1 T303A by tert-butyl acetylene: The role of threonine 303 in proton delivery to the active site of cytochrome P450 2E1. J. Pharmacol. Exp. Ther. 310, 281-290.
2. 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.
3. Cavalieri, E. L., Stack, D. E., Devanesan, P. D., Todorovic, R., Dwivedy, I., Higginbotham, S., Johansson, S. L., Patil, K. D., Gross, M. L., Gooden, J. K., et al. (1997). Molecular origin of cancer: Catechol estrogen-3, 4-quinones as endogenous tumor initiators. Proc. Natl. Acad. Sci. USA 94, 10937-10942.
4. Chiba, I., Sakakibara, A., Iwata, H., Ishizuka, M., Tanabe, S., Akahori, F., Kazusaka, A., and Fujita, S. (2002). Hepatic microsomal cytochrome p450s and chlorinated hydrocarbons in largha and ribbon seals from Hokkaido, Japan: Differential response of seal species to Ah receptor agonist exposure. Environ. Toxicol. Chem. 21, 794-806.
5. Coumoul, X., Diry, M., Robillot, C., and Barouki, R. (2001). Differential regulation of cytochrome P450 1A1 and 1B1 by a combination of dioxin and pesticides in the breast tumor cell line MCF-7. Cancer Res. 61, 3942-3948.
6. de Swart, R. L., Harder, T. C., Ross, P. S., Vos, H. W., and Osterhaus, A. D. M. E. (1995). Morbilliviruses and morbillivirus diseases of marine mammals. Infect. Agents Dis. 4, 125-130.
7. Fernandez-Salguero, P. M., Hilbert, D. M., Rudikoff, S., Ward, J. M., and Gonzalez, F. J. (1996). Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity. Toxicol. Appl. Pharmacol. 140, 173-179.
8. Guengerrich, 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.
9. Hayes, C. L., Spink, D. C., Spink, B. C., Cao, J. Q., Walker, N. J., and Sutter, T. R. (1996). 17β-estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc. Natl. Acad. Sci. USA 93, 9776-9781.
10. Hiroya, K., Murakami, Y., Shimizu, T., Hatano, M., and Ortiz de Montellano, P. R. (1994). Differential roles of Glu318 and Thr319 in cytochrome P450 1A2 catalysis supported by NADPH-cytochrome P450 reductase and tert-butyl hydroperoxide. Arch. Biochem. Biophys. 310, 397-401.
11. Ishida, C., Koga, N., Hanioka, N., Saeki, H.K., and Yoshimura, H. (1991). Metabolism in vitro of 3,4,3′,4′- and 2,5,2′,5′-tetrachlorobiphenyl by rat liver microsomes and highly purified cytochrome P-450. J. Pharmacobio-Dyn. 14, 276-284.
12. 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.
13. 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. C Toxicol. Pharmacol. 131, 501-510.
14. Jensen, B. A., and Hahn, M. E. (2001). cDNA cloning and characterization of a high affinity aryl hydrocarbon receptor in a cetacean, the beluga, Delphinapterus leucas. Toxicol. Sci. 64, 41-56.
15. Kim, E. Y., and Hahn, M. E. (2002). cDNA cloning and characterization of an aryl hydrocarbon receptor from the harbor seal (Phoca vitulina): A biomarker of dioxin susceptibility? Aquat. Toxicol. 58 57-73.
16. Kim, E. Y., Hahn, M. E., Iwata, H., Tanabe, S., and Miyazaki, N. (2002). cDNA cloning of an aryl hydrocarbon receptor from Baikal seals (Phoca sibirica). Mar. Environ. Res. 54, 285-289.
17. Kim, E. Y., Iwata, H., Suda, T., Tanabe, S., Amano, M., Miyazaki, N., and Petrov, E. A. (2005). Aryl hydrocarbon receptor (AHR) and AHR nuclear translocator (ARNT) expression in Baikal seal (Pusa sibirica and association with 2,3,7,8-TCDD toxic equivalents and CYP1 expression levels. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 141, 281-291.
18. Kloepper-Sams, P. J., Park, S. S, Gelboin, H. V., and Stegeman, J. J. (1987). Specificity and cross-reactivity of monoclonal and polyclonal antibodies against cytochrome P-450E of the marine fish scup. Arch. Biochem. Biophys. 253, 268-278.
19. Kubota, A., Iwata, H., Goldstone, H. M. H., Kim, E. Y., Stegeman, J. J., and Tanabe, S. (2006). Cytochrome P450 1A4 and 1A5 in common cormorant (Phalacrocorax carbo): Evolutionary relationships and functional implications associated with dioxin and related compounds. Toxicol. Sci. 92, 394-408.
20. 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.
21. Kusano, K., Sakaguchi, M., Kagawa, N., Waterman, M. R., and Omura, T. (2001). Microsomal p450s use specific proline-rich sequences for efficient folding, but not for maintenance of the folded structure. J. Biochem. 129, 259-269.
22. Letcher, R. J., Norstrom, R. J., Lin, S., Ramsay, M. A., and Bandiera, S. M. (1996). Immunoquantitation and microsomal monooxygenase activities of hepatic cytochromes P4501A and P4502B and chlorinated hydrocarbon contaminant levels in polar bear (Ursus maritimus). Toxicol. Appl. Pharmacol. 137, 127-140.
23. Liehr, J. G., and Ricci, M. J. (1996). 4-hydroxylation of estrogens as marker of human mammary tumors. Proc. Natl. Acad. Sci. USA 93 3294-3296.
24. Liu, J., Ericksen, S. S., Besspiata, D., Fisher, C. W., and Szklarz, G. D. (2003). Characterization of substrate binding to cytochrome P450 1A1 using molecular modeling and kinetic analyses: Case of residue 382. Drug Metab. Dispos. 31, 412-420.
25. Liu, J., Ericksen, S. S., Sivaneri, M., Besspiata, D., Fisher, C. W., and Szklarz, G. D. (2004). The effect of reciprocal active site mutations in human cytochromes P450 1A1 and 1A2 on alkoxyresorufin metabolism. Arch. Biochem. Biophys. 424, 33-43.
26. Martucci, C. P., and Fishman, J. (1993). P450 enzymes of estrogen metabolism. Pharmacol. Ther. 57, 237-257.
27. McKinley, M. K., Kedderis, L. B., and Birnbaum, L. S. (1993). The effect of pretreatment on the biliary excretion of 2,3,7,8-tetrachlorodibenzo-p-dioxin, 2,3,7,8-tetrachlorodibenzofuran, and 3,3′,4,4′-tetrachlorobiphenyl in the rat. Fundam. Appl. Toxicol. 21, 425-432.
28. 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.
29. Nakata, H., Tanabe, S., Tatsukawa, R., Amano, M., Miyazaki, N., and Petrov, E. A. (1995). Persistent organochlorine residues and their accumulation kinetics in Baikal seal (Phoca sibirica) from Lake Baikal, Russia. Environ. Sci. Technol. 29, 2877-2885.
30. Nelson, D. R., Koymans, L., Kamataki, T., Stegeman, J. J., Feyereisen, R., Waxman, D. J., Waterman, M. R., Gotoh, O., Coon, M. J., Estabrook, R. W., et al. (1996). P450 superfamily: Update on new sequences, gene mapping, accession numbers and nomenclature. Pharmacogenetics 6, 1-42.
31. Niimi, S.,Watanabe, M. X., Kim, E. Y., Iwata, H., Yasunaga, G., Fujise, Y., and Tanabe, S. (2005). Molecular cloning and mRNA expression of cytochrome P4501A1 and 1A2 in the liver of common minke whales ( Balaenoptera acutorostrata). Mar. Pollut. Bull. 51, 784-793.
32. Ohtake, F., Takeyama, K., Matsumoto, T., Kitagawa, H., Yamamoto, Y., Nohara, K., Tohyama, C., Krust, A., Mimura, J., Chambon, P., et al. (2003). Modulation of oestrogen receptor signalling by association with the activated dioxin receptor. Nature 423, 545-550.
33. Okino, S. T., and Whitlock, J. P., Jr. (2000). The aromatic hydrocarbon receptor, transcription, and endocrine aspects of dioxin action. Vitam. Horm. 59, 241-264.
34. Olson, J. R., McGarrigle, B. P., Gigliotti, P. J., Kumar, S., and McReynolds, J. H. (1994). Hepatic uptake and metabolism of 2,3,7,8-tetrachlorodibenzop-dioxin and 2,3,7,8-tetrachlorodibenzofuran. Fundam. Appl. Toxicol. 22, 631-640.
35. Omura, T., and Sato, R. (1964). The carbon monoide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J. Biol. Chem. 239, 2370-2378.
36. Poland, A., and Knutson, J. C. (1982). 2,3,7,8-tetrachlorodibenzo-p dioxin and related halogenated aromatic hydrocarbons: Examination of the mechanism of toxicity. Annu. Rev. Pharmacol. Toxicol. 22 517-554.
37. Porter, T. D., and Coon, M. J. (1991). Cytochrome P450. Multiplicity of isoforms, substrates, and catalytic and regulatory mechanisms. J. Biol. Chem. 266, 13469-13472.
38. Safe, S. (1990). Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and related compounds: Environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). Crit. Rev. Toxicol. 21, 51-88.
39. Schlezinger, J. J., Keller, J., Verbrugge, L. A., and Stegeman, J. J. (2000). 3,3′,4,4′-Tetrachlorobiphenyl oxidation in fish, bird and reptile species: Relationship to cytochrome P450 1A inactivation and reactive oxygen production. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 125, 276-286.
40. Schlezinger, J. J., White, R. D., and Stegeman, J. J. (1999). Oxidative inactivation of cytochrome P-450 1A (CYP1A) stimulated by 3,3′,4,4′-tetrachlorobiphenyl: Production of reactive oxygen by vertebrate CYP1As. Mol. Pharmacol. 56, 588-597.
41. Shimada, T., Gillam, E. M., Sutter, T. R., Strickland, P. T., Guengerich, F. P., and Yamazaki, H. (1997). Oxidation of xenobiotics by recombinant human cytochrome P450 1B1. Drug Metab. Dispos. 29 617-622.
42. Shimada, T., Inoue, K., Suzuki, Y., Kawai, T., Azuma, E., Nakajima, T., Shindo, M., Kurose, K., Sugie, A, Yamagishi, Y., et al. (2002). Arylhydrocarbon receptor-dependent induction of liver and lung cytochromes P450 1A1, 1A2, and 1B1 by polycyclic aromatic hydrocarbons and polychlorinated biphenyls in genetically engineered C57BL/6J mice. Carcinogenesis 23, 1199-1207.
43. Smith, A. G., Clothier, B., Carthew, P., Childs, N. L., Sinclair, P. R., Nebert, D. W., and Dalton, T. P. (2001). Protection of the Cyp1a2(-/-) null mouse against uroporphyria and hepatic injury following exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Appl. Pharmacol. 173, 89-98.
44. Smith, P. K., Krohn, R. I., and Hermanson, G. T. (1985). Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.
45. Spink, D. C., Eugster, H. P., Lincoln, D. W., II, Schuetz, J. D., Schuetz, E. G., Johnson, J. A., Kaminsky, L. S., and Gierthy, J. F. (1992). 17β-estradiol hydroxylation catalyzed by human cytochrome P450 1A1: A comparison of the activities induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin in MCF-7 cells with those from heterologous expression of the cDNA. Arch. Biochem. Biophys. 293, 342-348.
46. Stegeman, J. J., Hahn, M. E., Weisbrod, R., Woodin, B. R., Joy, J. S., Najibi, S., and Cohen, R. A. (1995). Induction of cytochrome P4501A1 by aryl hydrocarbon receptor agonists in porcine aorta endothelial cells in culture and cytochrome P4501A1 activity in intact cells. Mol. Pharmacol. 47, 296-306.
47. 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.
48. Tanabe, S., Iwata, H., and Tatsukawa, R. (1994). Global contamination by persistent organochlorines and their ecotoxicological impact on marine mammals. Sci. Total. Environ. 154, 163-177.
49. Teramitsu, I., Yamamoto, Y., Chiba, I., Iwata, H., Tanabe, S., Fujise, Y., Kazusaka, A., Akahori, F., and Fujita, S. (2000). Identification of novel cytochrome P450 1A genes from five marine mammal species. Aquat. Toxicol. 51, 145-153.
50. Teraoka, H., Dong, W., Tsujimoto, Y., Iwasa, H., Endoh, D., Ueno, N., Stegeman, J. J., Peterson, R.E., and Hiraga, T. (2003). Induction of cytochrome P450 1A is required for circulation failure and edema by 2,3,7,8-tetrachlorodibenzo-p-dioxin in zebrafish. Biochem. Biophys. Res. Commun. 304, 223-228.
51. Tilley, R. E., Kemp, G. D., Teramitsu, I., and Hall, A. J. (2002). Isolation of two cytochrome P450 cDNAs, CYP1A1 and CYP1A2, from harp seal (Phoca groenlandica) and grey seal (Halichoerus grypus. Comp. Biochem. Physiol. Part C 132, 181-191.
52. Tudzynski, B., and Hölter, K. (1998). Gibberellin biosynthetic pathway in Gibberella fujikuroi: Evidence for a gene cluster. Fungal Genet. Biol. 25, 157-170.
53. Uno, S., Dalton, T. P., Sinclair, P. R., Gorman, N., Wang, B., Smith, A. G., 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.
54. Van den Berg, M., Birnbaum, L., Bosveld, A. T. C., Brunstorom, 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.
55. Vaz, A. D. N., McGinnity, D. F., and Coon, M. J. (1998). Epoxidation of olefins by cytochrome P450: Evidence from site-specific mutagenesis for hydroperoxo-iron as an electrophilic oxidant. Proc. Natl. Acad. Sci. USA 95, 3555-3560.
56. Vaz, A. D. N., Pernecky, S. J., Raner, G. M., and Coon, M. J. (1996). Peroxoiron and oxenoid-iron species as alternative oxygenating agents in cytochrome P450-catalyzed reactions: Switching by threonine-302 to alanine mutagenesis of cytochrome P450 2B4. Proc. Natl. Acad. Sci. USA 93, 4644-4648.
57. Vezina, C. M., Walker, N. J., and Olson, J. R. (2004). Subcronic exposure to TCDD, PeCDF, PCB126, and PCB153: Effect on hepatic gene expression. Environ. Health. Perspect. 112, 1636-1644.
58. Watanabe, M. X., Iwata, H., Okamoto, M., Kim, E.Y., Yoneda, K., Hashimoto, T., and Tanabe, S. (2005). Induction of cytochrome P450 1A5mRNA, 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. Toxicol. Sci. 88, 384-399.
59. White, R. D., Hahn, M. E., Lockhart, W. L., and Stegeman, J. J. (1994). Catalytic and immunochemical characterization of hepatic microsomal cytochromes P450 in beluga whale (Delphinapterus leucas). Toxicol. Appl. Pharmacol. 126, 45-57.
60. Yager, J. D. (2000). Endogenous estrogens as carcinogens through metabolic activation. J. Natl. Cancer Inst. Monogr. 27, 67-73.
61. Yager, J. D., and Liehr, J. G. (1996). Molecular mechanisms of estrogen carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 36, 203-232.