Identification of sulfated metabolites of 4-chlorobiphenyl (PCB3) in the serum and urine of male rats

Chemical Research in Toxicology

Volumn 25, Issue 12, 2012, Pages 2796-2804

  Dhakal, Kiran ^a   He, Xianran ^a   Lehmler, Hans Joachim ^a   Teesch, Lynn M ^a   Duffel, Michael W ^a   Robertson, Larry W ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 CHLOROBIPHENYL; ACETYLCYSTEINE; BETA GLUCURONIDASE; GLUCURONIDE; POLYCHLORINATED BIPHENYL DERIVATIVE; SULFATASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD ANALYSIS; CONJUGATION; CONTROLLED STUDY; EXCRETION; FECES ANALYSIS; HYDROXYLATION; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; METABOLITE; NONHUMAN; QUANTITATIVE ANALYSIS; RAT; SULFATION; URINALYSIS;

ANIMALS; BIOTRANSFORMATION; BIPHENYL COMPOUNDS; ENVIRONMENTAL POLLUTANTS; FECES; MALE; RATS; RATS, SPRAGUE-DAWLEY; SULFATES;

RATTUS;

EID: 84871248973     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx300416v     Document Type: Article

References (73)

1. Jones, K. C. and de Voogt, P. (1999) Persistent organic pollutants (POPs): state of the science Environ. Pollut. 100, 209-221 (Pubitemid 29435515)
2. Burreau, S., Zebuhr, Y., Broman, D., and Ishaq, R. (2006) Biomagnification of PBDEs and PCBs in food webs from the Baltic Sea and the northern Atlantic ocean Sci. Total Environ. 366, 659-672 (Pubitemid 44037701)
3. Nisbet, I. C. and Sarofim, A. F. (1972) Rates and routes of transport of PCBs in the environment Environ. Health Perspect. 1, 21-38
4. Breivik, K., Sweetman, A., Pacyna, J. M., and Jones, K. C. (2002) Towards a global historical emission inventory for selected PCB congeners: A mass balance approach. 1. Global production and consumption Sci. Total Environ. 290, 181-198 (Pubitemid 34450978)
5. Consonni, D., Sindaco, R., and Bertazzi, P. A. (2012) Blood levels of dioxins, furans, dioxin-like PCBs, and TEQs in general populations: A review, 1989-2010 Environ. Int. 44, 151-162
6. Wania, F. and Mackay, D. (1996) Peer reviewed: tracking the distribution of persistent organic pollutants Environ. Sci. Technol. 30, 390A-396A (Pubitemid 27127765)
7. Iwata, H., Tanabe, S., Sakai, N., Nishimura, A., and Tatsukawa, R. (1994) Geographical distribution of persistent organochlorines in air, water and sediments from Asia and Oceania, and their implications for global redistribution from lower latitudes Environ. Pollut. 85, 15-33
8. Arellano, L., Fernandez, P., Tatosova, J., Stuchlik, E., and Grimalt, J. O. (2011) Long-range transported atmospheric pollutants in snowpacks accumulated at different altitudes in the Tatra mountains (Slovakia) Environ. Sci. Technol. 45, 9268-9275
9. Feinberg, M., Soler, L., Contenot, S., and Verger, P. (2011) Assessment of seasonality in exposure to dioxins, furans and dioxin-like PCBs by using long-term food-consumption data Food Addit. Contam., Part A 28, 502-512
10. Currado, G. M. and Harrad, S. (1998) Comparison of polychlorinated biphenyl concentrations in indoor and outdoor air and the potential significance of inhalation as a human exposure pathway Environ. Sci. Technol. 32, 3043-3047 (Pubitemid 28485235)
11. Ludewig, G., Lehmann, L., Esch, H., and Robertson, L. W. (2008) Metabolic activation of PCBs to carcinogens in vivo: A review Environ. Toxicol. Pharmacol. 25, 241-246
12. Persoon, C., Peters, T. M., Kumar, N., and Hornbuckle, K. C. (2010) Spatial distribution of airborne polychlorinated biphenyls in Cleveland, Ohio and Chicago, Illinois Environ. Sci. Technol. 44, 2797-2802
13. Hu, D., Lehmler, H. J., Martinez, A., Wang, K., and Hornbuckle, K. C. (2010) Atmospheric PCB congeners across Chicago Atmos. Environ. 44, 1550-1557
14. U.S. Environmental Protection Agency (2011) Public health levels for PCBs in indoor school air, available at http://www.epa.gov/pcbsincaulk.
15. Hu, D., Martinez, A., and Hornbuckle, K. C. (2008) Discovery of non-aroclor PCB (3,3′-dichlorobiphenyl) in Chicago air Environ. Sci. Technol. 42, 7873-7877
16. Ishikawa, Y., Noma, Y., Mori, Y., and Sakai, S. (2007) Congener profiles of PCB and a proposed new set of indicator congeners Chemosphere 67, 1838-1851 (Pubitemid 46367135)
17. Block, W. D. and Cornish, H. H. (1959) Metabolism of biphenyl and 4-chlorobiphenyl in the rabbit J. Biol. Chem. 234, 3301-3302
18. Safe, S. and Ruzo, L. O. (1975) The metabolism of 4-chlorobiphenyl in the pig Can. J. Physiol. Pharmacol. 53, 392-396
19. Safe, S., Hutzinger, O., Ecobichon, D. J., and Grey, A. A. (1975) The metabolism of 4′chloro-4-biphenylol in the rat Can. J. Biochem. 53, 415-420
20. Hass, J. R., Jao, L. T., Wilson, N. K., and Matthews, H. B. (1977) Metabolism of 4-chlorobiphenyl and 4,4′-dichlorobiphenyl in the rat: qualitative and quantitative aspects J. Agric. Food Chem. 25, 1330-1333 (Pubitemid 8243877)
21. Wyndham, C. and Safe, S. (1978) In vitro metabolism of 4-chlorobiphenyl by control and induced rat liver microsomes Biochem. 17, 208-215 (Pubitemid 8270202)
22. McLean, M. R., Bauer, U., Amaro, A. R., and Robertson, L. W. (1996) Identification of catechol and hydroquinone metabolites of 4-monochlorobiphenyl Chem. Res. Toxicol. 9, 158-164 (Pubitemid 26041283)
23. Parkinson, A. and Safe, S. (1982) Cytochrome P-450-mediated metabolism of biphenyl and the 4-halobiphenyls Biochem. Pharmacol. 31, 1849-1856
24. Song, Y., Wagner, B. A., Lehmler, H. J., and Buettner, G. R. (2008) Semiquinone radicals from oxygenated polychlorinated biphenyls: Electron paramagnetic resonance studies Chem. Res. Toxicol. 21, 1359-1367
25. Wangpradit, O., Mariappan, S. V. S., Teesch, L. M., Duffel, M. W., Norstrom, K., Robertson, L. W., and Luthe, G. (2009) Oxidation of 4-chlorobiphenyl metabolites to electrophilic species by prostaglandin H synthase Chem. Res. Toxicol. 22, 64-71
26. Amaro, A. R., Oakley, G. G., Bauer, U., Spielmann, H. P., and Robertson, L. W. (1996) Metabolic activation of PCBs to quinones: reactivity toward nitrogen and sulfur nucleophiles and influence of superoxide dismutase Chem. Res. Toxicol. 9, 623-629 (Pubitemid 26123964)
27. Zhao, S., Narang, A., Ding, X., and Eadon, G. (2004) Characterization and quantitative analysis of DNA adducts formed from lower chlorinated PCB-derived quinones Chem. Res. Toxicol. 17, 502-511 (Pubitemid 38506984)
28. Oakley, G. G., Robertson, L. W., and Gupta, R. C. (1996) Analysis of polychlorinated biphenyl-DNA adducts by 32P-postlabeling Carcinogenesis 17, 109-114
29. Srinivasan, A., Robertson, L. W., and Ludewig, G. (2002) Sulfhydryl binding and topoisomerase inhibition by PCB metabolites Chem. Res. Toxicol. 15, 497-505 (Pubitemid 34326931)
30. Srinivasan, A., Lehmler, H. J., Robertson, L. W., and Ludewig, G. (2001) Production of DNA strand breaks in vitro and reactive oxygen species in vitro and in HL-60 cells by PCB metabolites Toxicol. Sci. 60, 92-102 (Pubitemid 32229830)
31. Bender, R. P., Lehmler, H. J., Robertson, L. W., Ludewig, G., and Osheroff, N. (2006) Polychlorinated biphenyl quinone metabolites poison human topoisomerase IIalpha: altering enzyme function by blocking the N-terminal protein gate Biochem. 45, 10140-10152 (Pubitemid 44257408)
32. Flor, S. and Ludewig, G. (2010) Polyploidy-induction by dihydroxylated monochlorobiphenyls: Structure-activity-relationships Environ. Int. 36, 962-969
33. Chaudhuri, L., Sarsour, E. H., and Goswami, P. C. (2010) 2-(4-Chlorophenyl)benzo-1,4-quinone induced ROS-signaling inhibits proliferation in human non-malignant prostate epithelial cells Environ. Int. 36, 924-930
34. Jacobus, J. A., Flor, S., Klingelhutz, A., Robertson, L. W., and Ludewig, G. (2008) 2-(4′-Chlorophenyl)-1,4-benzoquinone increases the frequency of micronuclei and shortens telomeres Environ. Toxicol. Pharmacol. 25, 267-272
35. Pereg, D., Tampal, N., Espandiari, P., and Robertson, L. W. (2001) Distribution and macromolecular binding of benzo[a]pyrene and two polychlorinated biphenyl congeners in female mice Chem.-Biol. Interact. 137, 243-258 (Pubitemid 32879339)
36. Espandiari, P., Glauert, H. P., Lehmler, H. J., Lee, E. Y., Srinivasan, C., and Robertson, L. W. (2004) Initiating activity of 4-chlorobiphenyl metabolites in the resistant hepatocyte model Toxicol. Sci. 79, 41-46 (Pubitemid 38660246)
37. Lehmann, L., Esch, H. L., Kirby, P. A., Robertson, L. W., and Ludewig, G. (2007) 4-Monochlorobiphenyl (PCB3) induces mutations in the livers of transgenic Fisher 344 rats Carcinogenesis 28, 471-478 (Pubitemid 46321865)
38. Maddox, C., Wang, B., Kirby, P. A., Wang, K., and Ludewig, G. (2008) Mutagenicity of 3-methylcholanthrene, PCB3, and 4-OH-PCB3 in the lung of transgenic BigBlue (R) rats Environ. Toxicol. Pharmacol. 25, 260-266
39. Jacobus, J. A., Wang, B., Maddox, C., Esch, H., Lehmann, L., Robertson, L. W., Wang, K., Kirby, P., and Ludewig, G. (2010) 3-Methylcholanthrene (3-MC) and 4-chlorobiphenyl (PCB3) genotoxicity is gender-related in Fischer 344 transgenic rats Environ. Int. 36, 970-979
40. Hovander, L., Malmberg, T., Athanasiadou, M., Athanassiadis, I., Rahm, S., Bergman, A., and Wehler, E. K. (2002) Identification of hydroxylated PCB metabolites and other phenolic halogenated pollutants in human blood plasma Arch. Environ. Contam. Toxicol. 42, 105-117 (Pubitemid 34260160)
41. Dirtu, A. C., Jaspers, V. L., Cernat, R., Neels, H., and Covaci, A. (2010) Distribution of PCBs, their hydroxylated metabolites, and other phenolic contaminants in human serum from two European countries Environ. Sci. Technol. 44, 2876-2883
42. Bergman, A., Klasson-Wehler, E., and Kuroki, H. (1994) Selective retention of hydroxylated PCB metabolites in blood Environ. Health Perspect. 102, 464-469 (Pubitemid 24200106)
43. Herrick, R. F., Meeker, J. D., and Altshul, L. (2011) Serum PCB levels and congener profiles among teachers in PCB-containing schools: a pilot study Environ. Health 10, 56
44. Tampal, N., Lehmler, H. J., Espandiari, P., Mahnberg, T., and Robertson, L. W. (2002) Glucuronidation of hydroxylated polychlorinated biphenyls (PCBs) Chem. Res. Toxicol. 15, 1259-1266 (Pubitemid 35222194)
45. Volp, R. P. (1988) Glucuronidation in 4-chlorobiphenyl metabolism by rat and human liver microsomes Drug Metab. Dispos. 16, 650-652
46. Wang, L. Q., Lehmler, H. J., Robertson, L. W., and James, M. O. (2006) Polychlorobiphenylols are selective inhibitors of human phenol sulfotransferase 1A1 with 4-nitrophenol as a substrate Chem.-Biol. Interact. 159, 235-246 (Pubitemid 43112434)
47. Liu, Y., Apak, T. I., Lehmler, H. J., Robertson, L. W., and Duffel, M. W. (2006) Hydroxylated polychlorinated biphenyls are substrates and inhibitors of human hydroxysteroid sulfotransferase SULT2A1 Chem. Res. Toxicol. 19, 1420-1425 (Pubitemid 44863483)
48. Liu, Y., Smart, J. T., Song, Y., Lehmler, H. J., Robertson, L. W., and Duffel, M. W. (2009) Structure-activity relationships for hydroxylated polychlorinated biphenyls as substrates and inhibitors of rat sulfotransferases and modification of these relationships by changes in thiol status Drug Metab. Dispos. 37, 1065-1072
49. Oikari, A. and Anas, E. (1985) Chlorinated phenolics and their conjugates in the bile of trout (Salmo-Gairdneri) exposed to contaminated waters Bull. Environ. Contam. Toxicol. 35, 802-809 (Pubitemid 16210067)
50. Li, X., Parkin, S., Duffel, M. W., Robertson, L. W., and Lehmler, H. J. (2010) An efficient approach to sulfate metabolites of polychlorinated biphenyls Environ. Int. 36, 843-848
51. Joshi, S. N., Vyas, S. M., Duffel, M. W., Parkin, S., and Lehmler, H. J. (2011) Synthesis of sterically hindered polychlorinated biphenyl derivatives Synthesis 7, 1045-1054
52. Shelnutt, S. R., Cimino, C. O., Wiggins, P. A., Ronis, M. J., and Badger, T. M. (2002) Pharmacokinetics of the glucuronide and sulfate conjugates of genistein and daidzein in men and women after consumption of a soy beverage Am. J. Clin. Nutr. 76, 588-594 (Pubitemid 34920836)
53. Daidoji, T., Gozu, K., Iwano, H., Inoue, H., and Yokota, H. (2005) UDP-glucuronosyltransferase isoforms catalyzing glucuronidation of hydroxy-polychlorinated biphenyls in rat Drug Metab. Dispos. 33, 1466-1476 (Pubitemid 41323994)
54. Zhai, G. S., Lehmler, H. J., and Schnoor, J. L. (2010) Hydroxylated metabolites of 4-monochlorobiphenyl and its metabolic pathway in whole poplar plants Environ. Sci. Technol. 44, 3901-3907
55. St'avova, J., Stahl, D. C., Seames, W. S., and Kubatova, A. (2012) Method development for the characterization of biofuel intermediate products using gas chromatography with simultaneous mass spectrometric and flame ionization detections J. Chromatogr., A 1224, 79-88
56. University of North Dakota, Chemistry Department, How to Use Linest Function to Calculate LOD, available at http://www.und.edu/dept/chromatography/ Docs/Determination%20of%20LODs.pdf.
57. Tomaszewski, J. E., Jerina, D. M., and Daly, J. W. (1975) Deuterium isotope effects during formation of phenols by hepatic monoxygenases. Evidence for an alternative to arene oxide pathway Biochemistry 14, 2024-2031
58. Jerina, D. M. and Daly, J. W. (1974) Arene oxides: a new aspect of drug metabolism Science 185, 573-582
59. Klaassen, C. D., Liu, L., and Dunn, R. T., II. (1998) Regulation of sulfotransferase mRNA expression in male and female rats of various ages Chem.-Biol. Interact. 109, 299-313 (Pubitemid 28161122)
60. Chen, G., Baron, J., and Duffel, M. W. (1995) Enzyme- and sex-specific differences in the intralobular localizations and distributions of aryl sulfotransferase IV (tyrosine-ester sulfotransferase) and alcohol (hydroxysteroid) sulfotransferase a in rat liver Drug Metab. Dispos. 23, 1346-1353 (Pubitemid 26007841)
61. Berger, I., Guttman, C., Amar, D., Zarivach, R., and Aharoni, A. (2011) The molecular basis for the broad substrate specificity of human sulfotransferase 1A1 PLoS One 6, e26794
62. Hempel, N., Gamage, N., Martin, J. L., and McManus, M. E. (2007) Human cytosolic sulfotransferase SULT1A1 Int. J. Biochem. Cell Biol. 39, 685-689 (Pubitemid 46366795)
63. Webb, L., Miles, K., Kessler, F., and Ritter, J. K. (2006) Activity of rat UGT1A1 towards benzo[a]pyrene phenols and dihydrodiols Environ. Toxicol. Pharmacol. 21, 224-230
64. Hinchman, C. A. and Ballatori, N. (1994) Glutathione conjugation and conversion to mercapturic acids can occur as an intrahepatic process J. Toxicol. Environ. Health 41, 387-409 (Pubitemid 24119819)
65. Bakke, J. E., Bergman, A. L., and Larsen, G. L. (1982) Metabolism of 2,4′,5-trichlorobiphenyl by the mercapturic acid pathway Science 217, 645-647 (Pubitemid 12041292)
66. Letcher, R., Klasson-Wehler, E., and Bergman, A. (2000) Methyl Sulfone and Hydroxylated Metabolites of Polychlorinated Biphenyls (Hutzinger, O. and Paasivirta, J., Eds.) Vol. 3, Anthropogenic Compounds Part K, pp 315-359, Springer, Berlin, Germany.
67. Gustafsson, J. A., Rafter, J. J., Bakke, J. E., and Gustafsson, B. E. (1981) The effect of intestinal microflora on the enterohepatic circulation of mercapturic acid pathway metabolites Nutr. Cancer 2, 224-231 (Pubitemid 12110599)
68. Bergman, A., Larsen, G. L., and Bakke, J. E. (1982) Biliary-secretion, retention and excretion of 5 C-14-labeled polychlorinated-biphenyls in the rat Chemosphere 11, 249-253 (Pubitemid 12121670)
69. Jurewicz, J., Hanke, W., Sobala, W., and Ligocka, D. (2012) Exposure to phenoxyacetic acid herbicides and predictors of exposure among spouses of farmers Ann. Agric. Environ. Med. 19, 51-56
70. Hovander, L., Athanasiadou, M., Asplund, L., Jensen, S., and Wehler, E. K. (2000) Extraction and cleanup methods for analysis of phenolic and neutral organohalogens in plasma J. Anal. Toxicol. 24, 696-703 (Pubitemid 32171217)
71. van't Erve, T. J., Rautiainen, R. H., Robertson, L. W., and Luthe, G. (2010) Trimethylsilyldiazomethane: a safe non-explosive, cost effective and less-toxic reagent for phenol derivatization in GC applications Environ. Int. 36, 835-842
72. Sundström, G. and Jansson, B. (1975) The metabolism of 2,2′,3,5′,6-pentachlorobiphenyl in rats, mice and quails Chemosphere 4, 361-370
73. Kania-Korwel, I., Zhao, H., Norstrom, K., Li, X., Hornbuckle, K. C., and Lehmler, H. J. (2008) Simultaneous extraction and clean-up of polychlorinated biphenyls and their metabolites from small tissue samples using pressurized liquid extraction J. Chromatogr., A 1214, 37-46