2,2′,3,3′,6,6′-hexachlorobiphenyl (PCB 136) atropisomers interact enantioselectively with hepatic microsomal cytochrome P450 enzymes

Chemical Research in Toxicology

Volumn 21, Issue 6, 2008, Pages 1295-1303

  Kania Korwel, Izabela ^a   Hrycay, Eugene G ^b   Bandiera, Stelvio M ^b   Lehmler, Hans Joachim ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2,2,3,3,6,6 HEXACHLOROBIPHENYL; 3 METHYLCHOLANTHRENE; BETA NAPHTHOFLAVONE; CYTOCHROME P450; CYTOCHROME P450 1A; CYTOCHROME P450 2B; CYTOCHROME P450 3A; DEXAMETHASONE; PHENOBARBITAL; POLYCHLORINATED BIPHENYL; 2,3,6,2',3',6' HEXACHLOROBIPHENYL; 2,3,6,2',3',6'-HEXACHLOROBIPHENYL; ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING KINETICS; C57BL 6 MOUSE; CHEMICAL INTERACTION; CONTROLLED STUDY; ENANTIOSELECTIVITY; ENZYME BINDING; FEMALE; ISOMER; LIVER MICROSOME; LONG EVANS RAT; MALE; MOUSE; NONHUMAN; RAT; ANIMAL; C57BL MOUSE; CHEMISTRY; CLASSIFICATION; DRUG EFFECT; ENZYMOLOGY; IMMUNOLOGY; METABOLISM; STEREOISOMERISM;

MUS; RATTUS;

ANIMALS; ANTIBODIES; CYTOCHROME P-450 ENZYME SYSTEM; FEMALE; MICE; MICE, INBRED C57BL; MICROSOMES, LIVER; POLYCHLORINATED BIPHENYLS; RATS; STEREOISOMERISM;

EID: 47049092256     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx800059j     Document Type: Article

References (53)

1. Robertson, L. W. and Hansen, L. G. (2001) PCBs: Recent Advances in Environmental Toxicology and Health Effects, University Press of Kentucky, Lexington, KY.
2. Hornbuckle, K. C., Carlson, D. L., Swackhamer, D. L., Baker, J. E. and Eisenreich, S. J. (2006) Polychlorinated Biphenyls in the Great Lakes, in Handbook of Environmental Chemistry (Hites, R., Ed.) pp 13-70, Springer Verlag, Berlin/Heidelberg, Germany.
3. Kodavanti, P. R. S. (2004) Intracellular Signaling and Developmental Neurotoxicity, in Molecular Neurotoxicology: Environmental Agents and Transcription-Transduction Coupling (Zawia, N. H., Ed.) pp 151-182, CRC press, Boca Roton, FL.
4. Schantz, S. L., Widholm, J. J., and Rice, D. C. (2003) Effects of PCB exposure on neuropsychological function in children. Environ. Health Perspect. 111, 357-376.
5. Lehmler, H.-J. and Robertson, L. W. (2001) Atropisomers of PCBs, in PCBs: Recent Advances in Environmental Toxicology and Health Effects (Robertson, L. W., and Hansen, L. G., Eds.) pp 61-65, University Press of Kentucky, Lexington, KY.
6. Kania-Korwel, I., Hornbuckle, K. C., Robertson, L. W., and Lehmler, H. J. (2007) Dose-dependent enantiomeric enrichment of 2,2′,3,3′,6, 6′-hexachlorobiphenyl in female mice. Environ. Toxicol. Chem. 27, 299-305.
7. Rodman, L. E., Shedlofsky, S. I., Mannschreck, A., Puttmann, M., Swim, A. T., and Robertson, L. W. (1991) Differential potency of atropisomers of polychlorinated biphenyls on cytochrome P450 induction and uroporphyrin accumulation in the chick embryo hepatocyte culture. Biochem. Pharmacol. 41, 915-922.
8. 45Ca2+-uptake in rat cerebellum. Toxicol. Lett. 156, 391-400.
9. Feng, W., Lehmler, H.-J., Allen, P. D., and Pessah, I. N. (2007) Chiral PCB 136 enantioselectively activates RyR1 and RyR2. Biophysical Society Meeting Abstracts. Biophys. J. 87A, 403-Pos.
10. Wiberg, K., Andersson, P. L., Berg, H., Olsson, P.-E., and Haglund, P. (2006) The fate of chiral organochlorine compounds and selected metabolites in intraperitoneally exposed Arctic char (Salvelinus Alpinus). Environ. Toxicol. Chem. 25, 1465-1473.
11. Gomara, B., and Gonzalez, M. J. (2006) Enantiomeric fractions and congener specific determination of polychlorinated biphenyls in eggs of predatory birds from Donana National Park (Spain). Chemosphere 63, 662-669.
12. Buckman, A. H., Wong, C. S., Chow, E. A., Brown, S. B., Solomon, K. R., and Fisk, A. T. (2006) Biotransformation of polychlorinated biphenyls (PCBs) and bioformation of hydroxylated PCBs in fish. Aquat. Toxicol. 78, 176-185.
13. Wong, C. S., Lau, F., Clark, M., Mabury, S. A., and Muir, D. C. G. (2002) Rainbow Trout (Oncorhynchus mykiss) can eliminate chiral organochlorine compound enantioselectively. Environ. Sci. Technol. 36, 1257-1262.
14. Hoekstra, P. F., Braune, B. M., Wong, C. S., Wiliamson, M., Elkin, B., and Muir, D. C. G. (2003) Profile of persistent chlorinated contaminants, including selected chiral compounds, in wolverine (Gulo gulo) livers from Canadian Arctic. Chemosphere 53, 551-560.
15. Warner, N. A., and Wong, C. S. (2006) The freshwater invertebrate Mysis relicta can eliminate chiral organochlorine compounds enantioselectively. Environ. Sci. Technol. 40, 4158-4164.
16. Hoekstra, P. F., Wong, C. S., O'Hara, T. M., Solomon, K. R., Mabury, S. A., and Muir, D. C. G. (2002) Enantiomer-specific accumulation of PCB atropisomers in the bowhead whale (Balaena mysticetus). Environ. Sci. Technol. 36, 1419-1425.
17. Jimenez, O., Jimenez, B., and Gonzales, M. J. (2000) Isomer-specific polychlorinated biphenyl determination in cetaceans from the Mediterranean Sea: enantioselective occurrence of chiral polychlorinated biphenyl congeners. Environ. Toxicol. Chem. 19, 2653-2660.
18. Reich, S., Jimenez, B., Marsili, L., Hernandez, L. M., Schurig, V., and Gonzales, M. J. (1999) Congener specific determination and enantiomeric ratios of chiral polychlorinated biphenyl in striped dolphins (Stanella coeruleoalba) from Mediterranean Sea. Environ. Sci. Technol. 33, 1787-1793.
19. Kania-Korwel, I., Shaikh, N., Hornbuckle, K. C., Robertson, L. W., and Lehmler, H.-J. (2007) Enantioselective disposition of PCB 136 (2,2′,3,3′,6,6′-hexachlorobiphenyl) in C57BL/6 mice after oral and intraperitoneal administration. Chirality 19, 56-66.
20. Kania-Korwel, I., Hornbuckle, K. C., Robertson, L. W., and Lehmler, H. J. (2008) Influence of dietary fat on the enantioselective disposition of 2,2′,3,3′,6,6′-hexachlorobiphenyl (PCB 136) in female mice. Food Chem. Toxicol. 46, 637-644.
21. Kania-Korwel, I., Garrison, A. W., Avants, J. K., Hornbuckle, K. C., Robertson, L. W., Sulkowski, W. W., and Lehmler, H.-J. (2006) Distribution of chiral PCBs in selected tissues in the laboratory rat. Environ. Sci. Technol. 40, 3704-3710.
22. Kania-Korwel, I., Xie, W., Hornbuckle, K. C., Robertson, L. W. and Lehmler, H.-J. (2008) Enantiomeric enrichment of 2,2′,3,3′,6, 6′-hexachlorobiphenyl (PCB 136) in mice after induction of CYP enzymes. Arch. Environ. Contam. Toxicol., in press.
23. Harrad, S., Ren, J., Hazrati, S., and Robson, M. (2006) Chiral signatures of PCB#s 95 and 149 in indoor air, grass, duplicate diets and human faeces. Chemosphere 63, 1368-1376.
24. Lehmler, H.-J., Price, D. J., Garrison, A. W., Birge, W. J., and Robertson, L. W. (2003) Distribution of PCB 84 enantiomers in C57B1/6 mice. Fresenius' Environ. Bulk 12, 254-260.
25. Norström, K., Eriksson, J., Haglund, J., Silvari, V., and Bergman, A. (2006) Enantioselective formation of methyl sulfone metabolites of 2,2′,3,3′,4,6′-hexachlorobiphenyl in rat. Environ. Sci. Technol. 40, 7649-7655.
26. Matthews, H. B., and Tuey, D. B. (1980) The effect of chlorine position on the distribution and excretion of four hexachlorobiphenyl isomers. Toxicol. Appl. Pharmacol. 53, 377-388.
27. Kato, S., McKinney, J. D., and Matthews, H. B. (1980) Metabolism of symmetrical hexachlorobiphenyl isomers in the rat. Toxicol. Appl. Pharmacol. 53, 389-398.
28. Mizutani, T., Hidaka, K., Ohe, T., Matsumoto, M., Yamamoto, K., and Tajima, K. (1980) Comparative study on accumulation and elimination of hexachlorobiphenyls and decachlorobiphenyl in mice. Bull. Environ. Contam. Toxicol. 25, 181-187.
29. Schnellmann, R., Putnam, C., and Sipes, I. (1983) Metabolism of 2,2′,3,3′,6,6′-hexachlorobiphenyl and 2,2′,4,4′,5, 5′-hexachlorobiphenyl by human hepatic microsomes. Biochem. Pharmacol. 32, 3233-3239.
30. Bandiera, S. (2001) Cytochrome P450 Enzymes As Biomarkers of PCB Exposure and Modulators of Toxicity, in PCBs: Recent Advances in Environmental Toxicology and Health Effects (Robertson, L. W., and Hansen, L. G., Eds.) pp 61-65, University Press of Kentucky, Lexington, KY.
31. Shaikh, N., Parkin, S., and Lehmler, H.-J. (2006) The Ullmann coupling reaction: A new approach to tetraarylstannanes. Organometallics 25, 4207-4214.
32. Haglund, P. (1996) Isolation and characterization of polychlorinated biphenyl (PCB) atropisomers. Chemosphere 32, 2133-2140.
33. Harner, T., Wiberg, K., and Norstrom, R. (2000) Enantiomer fractions are preferred to enantiomer ratios for describing chiral signatures in environmental analysis. Environ. Sci. Technol. 34, 218-220.
34. Thomas, P. E., Reik, L. M., Ryan, D. E., and Levin, W. (1983) Induction of two immunochemically related rat liver cytochrome P-450 isozymes, cytochromes P-450c and P-450d, by structurally diverse xenobiotics. J. Biol. Chem. 258, 4590-4598.
35. Lowry, O. H., Rosenbrough, N. J., Rarr, A. L., and Randall, R. J. (1951) Protein measurement with Folin Phenol reagent. J. Biol. Chem. 193, 265-275.
36. Omura, T., and Sato, R. (1964) The carbon monoxide-binding pigment of liver microsomes I. Evidence for its haemoprotein nature. J. Biol. Chem. 239, 2370-2378.
37. Hrycay, E. G., and Bandiera, S. M. (2003) Spectral interactions of tetrachlorobiphenyls with hepatic microsomal cytochrome P450 enzymes. Chem.-Biol. Interact. 146, 285-296.
38. Vatsis, K. P., and Coon, M. J. (2002) Ipso-substitution by cytochrome P450 with conversion of p-hydroxybenzene derivatives to hydroquinone: evidence for hydroperoxo-iron as the active oxygen species. Arch. Biochem. Biophys. 397, 119-129.
39. Murray, M., and Reidy, G. (1989) In vitro inhibition of hepatic drug oxidation by thioridazine. Kinetic analysis of the inhibition of cytochrome P-450 isoform-specific reactions. Biochem. Pharmacol. 38, 4359-4365.
40. Lewis, D. F. V. (1996) Cytochromes P450: structure, function and mechanism, Taylor and Francis, London.
41. Ryan, D. E., and Levin, W. (1990) Purification and characterization of hepatic microsomal cytochrome P-450. Pharmacol. Ther. 45, 153-239.
42. Schenkman, J. B. and Griem, H. (1993) Cytochrome P450, Springer-Verlag, Berlin, Germany.
43. Schenkman, J. B., Frey, I., Remmer, H., and Estabrook, R. W. (1967) Sex differences in drug metabolism by rat liver microsomes. Mol. Pharmacol. 3, 516-525.
44. Schenkman, J. B., Sligar, S. G., and Cinti, D. L. (1981) Substrate interaction with cytochrome P-450. Pharmacol. Ther. 12, 43-71.
45. Blanck, H., Rein, H., Sommer, M., Ristau, O., Smettan, G., and Ruckpaul, K. (1984) Correlations between spin equilibrium shift, reduction rate, and N-demethylation activity in liver microsomal cytochrome P450 and series of benzphetamine analogues as substrates. Biochem. Pharmacol. 32, 1683-1688.
46. Tamburini, P. P., Gibson, G. G., Backes, W. L., Sligar, S. G., and Schenkman, J. B. (1984) Reduction kinetics of purified rat liver cytochrome P-450. Evidence for sequential reaction mechanism dependent on the hemoprotein spin state. Biochemistry 23, 4526-4533.
47. Kennedy, M. W., Carpentier, N. K., Dymerski, P. D., Adams, S. M., and Kaminsky, L. S. (1980) Metabolism of monochlorobiphenyl by hepatic microsomal cytochrome P-450. Biochem. Pharmacol. 29, 727-736.
48. Waller, S. C., He, Y. A., Harlow, G. R., He, Y. Q., Mash, E. A., and Halpert, J. R. (1999) 2,2′,3,3′,6,6′-Hexachlorobiphenyl hydroxylation by active site mutants of cytochrome P450 2B1 and 2B11. Chem. Res. Toxicol. 12, 690-699.
49. Duignan, D., Sipes, I., Leonard, T., and Halpert, J. (1987) Purification and characterization of the dog hepatic cytochrome P-450 isozyme responsible for the metabolism of 2,2′,4,4′,5,5′-hexachlorobiphenyl. Arch. Biochem. Biophys. 255, 290-303.
50. Duignan, D., Sipes, I. G., Ciaccio, P. J., and Halpert, J. R. (1988) The metabolism of xenobiotics and endogenous compounds by the constitutive dog liver cytochrome P450 PBD-2. Arch. Biochem. Biophys. 267, 106-115.
51. 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.
52. Sakuma, T., Takai, M., Endo, Y., Kuroiwa, M., Ohara, A., Jarukamjorn, K., Honma, R., and Nemoto, N. (2000) A novel female-specific member of the CYP3A gene subfamily in the mouse liver. Arch. Biochem. Biophys. 377, 153-162.
53. Jan, Y.-H., Mishin, V., Busch, C. M., and Thomas, P. E. (2006) Generation of specific antibodies and their use to characterize sex differences in four rat P450 3A enzymes following vehicle and pregnenolone 16α-carbonitrile treatment. Arch. Biochem. Biophys. 446, 101-110.