Enantioselective transport and biotransformation of chiral hydroxylated metabolites of polychlorinated biphenyls in whole poplar plants

Environmental Science and Technology

Volumn 48, Issue 20, 2014, Pages 12213-12220

  Zhai, Guangshu ^a   Gutowski, Sarah M ^a   Lehmler, Hans Joachim ^b   Schnoor, Jerald L ^a,b  

^a IA United States   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMOLECULES; COTTON; ENANTIOMERS; ENANTIOSELECTIVITY; HISTOLOGY; HYDROXYLATION; METABOLISM; METABOLITES; POLYCHLORINATED BIPHENYLS; TISSUE;

CHIRAL COMPOUNDS; ENANTIOMERIC FRACTIONS; HYDROPONIC SOLUTION; HYDROXYLATED METABOLITES; METABOLIC PROCESS; OXIDATIVE METABOLISM; PARENT COMPOUNDS; POPULUS DELTOIDES;

ORGANIC POLLUTANTS;

METHANOL; POLYCHLORINATED BIPHENYL; 2,2',3,5',6-PENTACHLOROBIPHENYL;

BIOTRANSFORMATION; CONIFEROUS TREE; ENVIRONMENTAL FATE; GENOMICS; METABOLISM; METABOLITE; NUMERICAL MODEL; PCB; POLLUTANT REMOVAL; TRANSLOCATION;

ARTICLE; BARK; BIOTRANSFORMATION; CONTROLLED STUDY; ENANTIOMER; ENANTIOSELECTIVITY; ENVIRONMENTAL EXPOSURE; EVAPOTRANSPIRATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ION MONITORING; MASS SPECTROMETRY; NONHUMAN; PLANT LEAF; PLANT METABOLISM; PLANT TISSUE; POPULUS; QUANTITATIVE ANALYSIS; RACEMIC MIXTURE; BIOREMEDIATION; DRUG EFFECTS; HYDROPONICS; HYDROXYLATION; METABOLISM; PLANT STEM; STEREOISOMERISM; TRANSPORT AT THE CELLULAR LEVEL;

BIODEGRADATION, ENVIRONMENTAL; BIOLOGICAL TRANSPORT; BIOTRANSFORMATION; HYDROPONICS; HYDROXYLATION; PLANT STEMS; PLANT TRANSPIRATION; POLYCHLORINATED BIPHENYLS; POPULUS; STEREOISOMERISM;

EID: 84908140594     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es503443e     Document Type: Article

References (61)

1. Safe, S. H. Polychlorinated biphenyls (PCBs): Environmental impact, biochemical and toxic responses, and implications for risk assessment Crit. Rev. Toxicol. 1994, 24, 87-149
2. Evans, M. S.; Noguchi, G. E.; Rice, C. P. The biomagnifications of polychlorinated biphenyls, toxaphene, and DDT compounds in a Lake Michigan offshore food web Arch. Environ. Contam. Toxicol. 1991, 20, 87-93
3. Hu, D.; Hornbuckle, K. C. Inadvertent polychlorinated biphenyls in commercial paint pigments Environ. Sci. Technol. 2009, 44, 2822-2827
4. Tehrani, R.; Van Aken, B. Hydroxylated polychlorinated biphenyls in the environment: Sources, fate, and toxicities Environ. Sci. Pollut. Res. 2014, 21, 6334-6345
5. Rezek, J.; Macek, T.; Mackova, M.; Triska, J.; Ruzickova, K. Hydroxy-PCBs, methoxy-PCBs and hydroxy-methoxy-PCBs: Metabolites of polychlorinated biphenyls formed in vitro by tobacco cells Environ. Sci. Technol. 2008, 42, 5746-5751
6. Weistrand, C.; Noren, K. Methylsulfonyl metabolites of PCBs and DDE in human tissues Environ. Health Perspect. 1997, 105, 644-649
7. Ueno, D.; Darling, C.; Alaee, M.; Campbell, L.; Pacepavicius, G.; Teixeira, C.; Muir, D. Detection of hydroxylated polychlorinated biphenyls (OH-PCBs) in the abiotic environment: surface water and precipitation from Ontario, Canada Environ. Sci. Technol. 2007, 41, 1841-1848
8. Marek, R. F.; Martinez, A.; Hornbuckle, K. C. Discovery of hydroxylated polychlorinated biphenyls (OH-PCBs) in sediment from a Lake Michigan waterway and original commercial Aroclors Environ. Sci. Technol. 2013, 47, 8204-8210
9. Zeng, Y.; Luo, X.; Zheng, X.; Tang, B.; Wu, J.; Mai, B. Species-specific bioaccumulation of halogenated organic pollutants and their metabolites in fish serum from an e-waste site, South China Arch. Environ. Contam. Toxicol. 2014, 10.1007/s00244-014-0040-8
10. Imaeda, D.; Nomiyama, K.; Kunisue, T.; Iwata, H.; Tsydenova, O.; Amano, M.; Petrov, E. A.; Batoev, V. B.; Tanabe, S. Blood levels of polychlorinated biphenyls and their hydroxylated metabolites in Baikal seals (Pusa sibirica): Emphasis on interspecies comparison, gender difference and association with blood thyroid hormone levels Chemosphere 2014, 114, 1-8
11. Kunisue, T.; Tanabe, S. Hydroxylated polychlorinated biphenyls (OH-PCBs) in the blood of mammals and birds from Japan: Lower chlorinated OH-PCBs and profiles Chemosphere 2009, 74, 950-961
12. Marek, R. F.; Thorne, P. S.; Wang, K.; DeWall, J.; Hornbuckle, K. C. PCBs and OH-PCBs in serum from children and mothers in urban and rural U.S. communities Environ. Sci. Technol. 2013, 47, 3353-3361
13. Guengerich, F. P. Cytochrome P450 oxidations in the generation of reactive electrophiles: Epoxidation and related reactions Arch. Biochem. Biophys. 2003, 409, 59-71
14. Forgue, S. T.; Preston, B. D.; Hargraves, W. A.; Reich, I. L.; Allen, J. R. Direct evidence that an arene oxide is a metabolic intermediate of 2,2′,5,5′-tetrachlorobiphenyl Biochem. Biophys. Res. Commun. 1979, 91, 475-483
15. Koga, N.; Kikuichinishimura, N.; Hara, T.; Harada, N.; Ishii, Y.; Yamada, H.; Oguri, K.; Yoshimura, H. Purification and characterization of a newly identified isoform of cytochrome-P450 responsible for 3-hydroxylation of 2,5,2′,5′-tetrachlorobiphenyl in hamster liver Arch. Biochem. Biophys. 1995, 317, 464-470
16. Ekuase, E. J.; Lehmler, H.-J.; Robertson, L. W.; Duffel, M. W. Binding interactions of hydroxylated polychlorinated biphenyls (OHPCBs) with human hydroxysteroid sulfotransferase hSULT2A1 Chem.-Biol. Interact. 2014, 212, 56-64
17. Wang, L.; Lehmler, H. J.; Robertson, L. W.; James, M. O. Polychlorobiphenylols are selective inhibitors of human phenol sulfotransferase 1A1 with 4-nitrophenol as a substrate Chem.-Biol. Interact. 2006, 159, 235-246
18. Maddox, C.; Wang, B.; Kirby, P. A.; Wang, K.; Ludewig, G. Mutagenicity of 3-methylcholanthrene, PCB3, and 4-OH-PCB3 in the lung of transgenic BigBlue® rats Environ. Toxicol. Pharmacol. 2008, 25, 260-266
19. Ptak, A.; Ludewig, G.; Lehmler, H.; Wojtowicz, A. K.; Robertson, L. W.; Gregoraszczuk, E. L. Comparison of the actions of 4-chlorobiphenyl and its hydroxylated metabolites on estradiol secretion by ovarian follicles in primary cells in culture Reprod. Toxicol. 2005, 20, 57-64
20. Kodavanti, P. R. S.; Ward, T. R.; Derr-Yellin, E. C.; McKinney, J. D.; Tilson, H. A. Increased [H-3] phorbol ester binding in rat cerebellar granule cells and inhibition of Ca-45(2+) buffering in rat cerebellum by hydroxylated polychlorinated biphenyls Neurotoxicology 2003, 24, 187-198
21. Londono, M.; Shimokawa, N.; Miyazaki, W.; Iwasaki, T.; Koibuchi, N. Hydroxylated PCB induces Ca2+ oscillations and alterations of membrane potential in cultured cortical cells J. Appl. Toxicol. 2010, 30, 334-342
22. Park, H. Y.; Park, J. S.; Sovcikova, E.; Kocan, A.; Linderholm, L.; Bergman, A.; Trnovec, T.; Hertz-Picciotto, I. Exposure to hydroxylated polychlorinated biphenyls (OH-PCBs) in the prenatal period and subsequent neurodevelopment in Eastern Slovakia Environ. Health Perspect. 2009, 117, 1600-1606
23. Braathen, M.; Mortensen, A. S.; Sandvik, M.; Skare, J. U.; Arukwe, A. Estrogenic effects of selected hydroxy polychlorinated biphenyl congeners in primary culture of Atlantic salmon (Salmo salar) hepatocytes Arch. Environ. Contam. Toxicol. 2009, 56, 111-122
24. Gabrielsen, K. M.; Villanger, G. D.; Lie, E.; Karimi, M.; Lydersen, C.; Kovacs, K. M.; Jenssen, B. M. Levels and patterns of hydroxylated polychlorinated biphenyls (OH-PCBs) and their associations with thyroid hormones in hooded seal (Cystophora cristata) mother-pup pairs Aquat. Toxicol. 2011, 105, 482-491
25. Otake, T.; Yoshinaga, J.; Enomoto, T.; Matsuda, M.; Wakimoto, T.; Ikegami, M.; Suzuki, E.; Naruse, H.; Yamanaka, T.; Shibuya, N.; Yasumizu, T.; Kato, N. Thyroid hormone status of newborns in relation to in utero exposure to PCBs and hydroxylated PCB metabolites Environ. Res. 2007, 105, 240-246
26. Ptak, A.; Ludewig, G.; Robertson, L.; Lehmler, H. J.; Gregoraszczuk, E. L. In vitro exposure of porcine prepubertal follicles to 4-chlorobiphenyl (PCB3) and its hydroxylated metabolites: Effects on sex hormone levels and aromatase activity Toxicol. Lett. 2006, 164, 113-122
27. Stadnicki, S. S.; Allen, J. R. Toxicity of 2,2′,5,5′-tetrachlorobiphenyl and its metabolites, 2,2′,5,5′-tetrachlorobiphenyl-3,4-oxide and 2,2′,5,5′-tetrachlorobiphenyl-4-O1 to cultured-cells in vitro Bull. Environ. Contam. Toxicol. 1979, 23, 788-796
28. Niknam, Y.; Feng, W.; Cherednichenko, G.; Dong, Y.; Joshi, S. N.; Vyas, S. M.; Lehmler, H.-J.; Pessah, I. N. Structure-activity relationship of selected meta- and para-hydroxylated non-dioxin like polychlorinated biphenyls: from single RyR1 channels to muscle dysfunction Toxicol. Sci. 2013, 136, 500-513
29. Kaiser, K. On the optical activity of polychlorinated biphenyls Environ. Pollut. 1974, 7, 93-101
30. Frame, G. M.; Wagner, R. E.; Carnahan, J. C.; Brown, J. F., Jr.; May, R. J.; Smullen, L. A.; Bedard, D. L. Comprehensive, quantitative congener-specific analyses of eight Aroclors and complete PCB congener assignments on DB-1 capillary GC columns Chemosphere 1996, 33, 603-623
31. Robson, M.; Harrad, S. Chiral PCB signatures in air and soil: Implications for atmospheric source apportionment Environ. Sci. Technol. 2004, 38, 1662-1666
32. Wong, F.; Robson, M.; Diamond, M.; Harrad, S.; Truong, J. Concentrations and chiral signatures of POPs in soil and sediments: A comparative urban versus rural study in Canada and UK Chemosphere 2009, 74, 404-411
33. Wong, C. S.; Garrison, A. W.; Foreman, W. T. Enantiomeric composition of chiral polychlorinated biphenyl atropisomers in aquatic bed sediment Environ. Sci. Technol. 2001, 35, 33-39
34. Wong, C. S.; Garrison, A. W.; Smith, P. D.; Foreman, W. T. Enantiomeric composition of chiral polychlorinated biphenyl atropisomers in aquatic and riparian biota Environ. Sci. Technol. 2001, 35, 2448-2454
35. Ross, M. S.; Verreault, J.; Letcher, R. J.; Gabrielsen, G. W.; Wong, C. S. Chiral organochlorine contaminants in blood and eggs of glaucous gulls (Larus hyperboreus) from the Norwegian Arctic Environ. Sci. Technol. 2008, 42, 7181-7186
36. Serrano, R.; Fernandez, M.; Rabanal, R.; Hernandez, L. M.; Gonzalez, M. J. Congener-specific determination of polychlorinated biphenyls in shark and grouper livers from the Northwest African Atlantic Ocean Arch. Environ. Contam. Toxicol. 2000, 38, 217-224
37. Reich, S.; Jimenez, B.; Marsili, L.; Hernández, L. M.; Schurig, V.; González, M. J. Congener specific determination and enantiomeric ratios of chiral polychlorinated biphenyls in striped dolphins (Stenella coeruleoalba) from the Mediterranean Sea Environ. Sci. Technol. 1999, 33, 1787-1793
38. Hoekstra, P. F.; Wong, C. S.; O'Hara, T. M.; Solomon, K. R.; Mabury, S. A.; Muir, D. C. G. Enantiomer-specific accumulation of PCB atropisomers in the bowhead whale (Balaena mysticetus) Environ. Sci. Technol. 2002, 36, 1419-1425
39. Harrad, S.; Ren, J.; Hazrati, S.; Robson, M. Chiral signatures of PCB#s 95 and 149 in indoor air, grass, duplicate diets and human faeces Chemosphere 2006, 63, 1368-1376
40. Chu, S.; Covaci, A.; Schepens, P. Levels and chiral signatures of persistent organochlorine pollutants in human tissues from Belgium Environ. Res. 2003, 93, 167-176
41. Lehmler, H.-J.; Harrad, S. J.; Hunerfuss, H.; Kania-Korwel, I.; Lee, C. M.; Lu, Z.; Wong, C. S. Chiral polychlorinated biphenyl transport, metabolism, and distribution: A review Environ. Sci. Technol. 2010, 44, 2757-2766
42. Nezel, T.; Muller-Plathe, F.; Muller, M. D.; Buser, H.-R. Theoretical considerations about chiral PCBs and their methylthio and methylsulfonyl metabolites being possibly present as stable enantiomers Chemosphere 1997, 35, 1895-1906
43. Kania-Korwel, I.; Barnhart, C. D.; Stamou, M.; Truong, K. M.; El-Komy, M. H. M. E.; Lein, P. J.; Veng-Pedersen, P.; Lehmler, H.-J. 2,2′,3,5′,6-Pentachlorobiphenyl (PCB 95) and its hydroxylated metabolites are enantiomerically enriched in female mice Environ. Sci. Technol. 2012, 46, 11393-11401
44. Kania-Korwel, I.; Duffel, M. W.; Lehmler, H.-J. Gas chromatographic analysis with chiral cyclodextrin phases reveals the enantioselective formation of hydroxylated polychlorinated biphenyls by rat liver microsomes Environ. Sci. Technol. 2011, 45, 9590-9596
45. Zhai, G.; Wu, X.; Lehmler, H.-J.; Schnoor, J. L. Atropisomeric determination of chiral hydroxylated metabolites of polychlorinated biphenyls using HPLC-MS Chem. Cent. J. 2013, 7, 183
46. Coleman, J.; Blake-Kalff, M.; Davies, E. Detoxification of xenobiotics by plants: Chemical modification and vacuolar compartmentation Trends Plant Sci. 1997, 2, 144-151
47. Sandermann, H. Higher-plant metabolism of xenobiotics - The green liver concept Pharmacogenet. Genomics 1994, 4, 225-241
48. Liu, J.; Schnoor, J. L. Uptake and translocation of lesser-chlorinated polychlorinated biphenyls (PCBs) in the whole hybrid poplar plants after hydroponic exposure Chemosphere 2008, 73, 1608-1616
49. Zhai, G.; Lehmler, H.-J.; Schnoor, J. L. Hydroxylated metabolites of 4-monochlorobiphenyl and its metabolic pathway in whole poplar plants Environ. Sci. Technol. 2010, 44, 3901-3907
50. Liu, J.; Hu, D.; Jiang, G.; Schnoor, J. L. In vivo biotransformation of 3,3′,4,4′-tetrachlorobiphenyl by whole plants-poplars and switchgrass Environ. Sci. Technol. 2009, 43, 7503-7509
51. Lehmler, H.-J.; Robertson, L. W. Synthesis of hydroxylated PCB metabolites with the Suzuki-coupling Chemosphere 2001, 45, 1119-1127
52. Bauer, U.; Amaro, A. R.; Robertson, L. W. A new strategy for the synthesis of polychlorinated biphenyl metabolites Chem. Res. Toxicol. 1995, 8, 92-95
53. Harner, T.; Wiberg, K.; Norstrom, R. Enantiomer fractions are preferred to enantiomer ratios for describing chiral signatures in environmental analysis Environ. Sci. Technol. 2000, 34, 218-220
54. Dietz, A. C.; Schnoor, J. L. Phytotoxicity of chlorinated aliphatics to hybrid poplar (Populus deltoides × nigra DN34) Environ. Toxicol. Chem. 2001, 20, 389-393
55. Zhai, G.; Hu, D.; Lehmler, H.-J.; Schnoor, J. L. Enantioselective biotransformation of chiral PCBs in whole poplar plants Environ. Sci. Technol. 2011, 45, 2308-2316
56. Warner, N. A.; Norstrom, R. J.; Wong, C. S.; Fisk, A. T. Enantiomeric fractions of chiral polychlorinated biphenyls provide insights on biotransformation capacity of arctic biota Environ. Toxicol. Chem. 2005, 24, 2763-2767
57. Krishnan, P. Spectral binding of multiple ortho substituted polychlorinated biphenyls and their 5-hydroxy metabolites to microsomal cytochrome P450 enzymes. M.S. (Master of Science) thesis, University of Iowa, Iowa City, 2011; http://ir.uiowa.edu/etd/2733.
58. Liu, Y.; Apak, T. I.; Lehmler, H.-J.; Robertson, L. W.; Duffel, M. W. Hydroxylated polychlorinated biphenyls are substrates and inhibitors of human hydroxysteroid sulfotransferase SULT2A1 Chem. Res. Toxicol. 2006, 19, 1420-1425
59. Dhakal, K.; He, X.; Lehmler, H.-J.; Teesch, L. M.; Duffel, M. W.; Robertson, L. W. Identification of sulfated metabolites of 4-chlorobiphenyl (PCB3) in the serum and urine of male rats Chem. Res. Toxicol. 2012, 25, 2796-2804
60. Zhai, G.; Lehmler, H.-J.; Schnoor, J. L. Sulfate metabolites of 4-monochlorobiphenyl in whole poplar plants Environ. Sci. Technol. 2013, 47, 557-562
61. Liu, Y.; Smart, J. T.; Song, Y.; Lehmler, H.-J.; Robertson, L. W.; Duffel, M. W. 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. 2009, 37, 1065-1072