Mechanism of polybrominated diphenyl ether uptake into the liver: PBDE congeners are substrates of human hepatic OATP transporters

Toxicological Sciences

Volumn 115, Issue 2, 2010, Pages 344-353

  Pacyniak, Erik ^a   Roth, Megan ^a   Hagenbuch, Bruno ^a,b   Guo, Grace L ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KANSAS CANCER CENTER   (United States)

Author keywords

Kinetics; Liver; Organic anion transporting polypeptides; Polybrominated diphenyl ethers; Uptake assay

Indexed keywords

2,2',4,4' TETRABROMODIPHENYL ETHER; 2,2',4,4',5 PENTABROMODIPHENYL ETHER; 2,2',4,4',5,5', HEXABROMODIPHENYL ETHER; ORGANIC ANION TRANSPORTER; ORGANIC ANION TRANSPORTER 1B3; ORGANIC ANION TRANSPORTER 2; ORGANIC ANION TRANSPORTER 2B1; POLYBROMINATED DIPHENYL ETHER; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOTRANSFORMATION; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; CONTROLLED STUDY; ENZYME SPECIFICITY; KINETICS; LIVER CELL; MOLECULAR WEIGHT; NONHUMAN; PROTEIN EXPRESSION;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; ESTRADIOL; ESTRONE; FLAME RETARDANTS; HALOGENATED DIPHENYL ETHERS; HEPATOCYTES; HUMANS; LIVER; ORGANIC ANION TRANSPORTERS;

CRICETULUS GRISEUS;

EID: 77954046372     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq059     Document Type: Article

References (62)

1. Abe, T., Kakyo, M., Tokui, T., Nakagomi, R., Nishio, T., Nakai, D., Nomura, H., Unno, M., Suzuki, M., Naitoh, T., et al. (1999). Identification of a novel gene family encoding human liver-specific organic anion transporter LST-1. J. Biol. Chem. 274, 17159-17163.
2. Allen, J. G., McClean, M. D., Stapleton, H. M., Nelson, J. W., and Webster, T. F. (2007). Personal exposure to polybrominated diphenyl ethers (PBDEs) in residential indoor air. Environ. Sci. Technol. 41, 4574-4579.
3. Allen, J. G., McClean, M. D., Stapleton, H. M., and Webster, T. F. (2008). Critical factors in assessing exposure to PBDEs via house dust. Environ. Int. 34, 1085-1091.
4. Athanasiadou, M., Cuadra, S. N., Marsh, G., Bergman, A., and Jakobsson, K. (2008). Polybrominated diphenyl ethers (PBDEs) and bioaccumulative hydroxylated PBDE metabolites in young humans from Managua, Nicaragua. Environ. Health Perspect. 116, 400-408.
5. Birnbaum, L. S., and Cohen Hubal, E. A. (2006). Polybrominated diphenyl ethers: a case study for using biomonitoring data to address risk assessment questions. Environ. Health Perspect. 114, 1770-1775.
6. Bronger, H., Konig, J., Kopplow, K., Steiner, H. H., Ahmadi, R., Herold-Mende, C., Keppler, D., and Nies, A. T. (2005). ABCC drug efflux pumps and organic anion uptake transporters in human gliomas and the blood-tumor barrier. Cancer Res. 65, 11419-11428.
7. Chen, L. J., Lebetkin, E. H., Sanders, J. M., and Burka, L. T. (2006). Metabolism and disposition of 2,2',4,4',5-pentabromodiphenyl ether (BDE99) following a single or repeated administration to rats or mice. Xenobiotica 36, 515-534.
8. Costa, L. G., Giordano, G., Tagliaferri, S., Caglieri, A., and Mutti, A. (2008). Polybrominated diphenyl ether (PBDE) flame retardants: environmental contamination, human body burden and potential adverse health effects. Acta Biomed. 79, 172-183.
9. Covaci, A., Voorspoels, S., Roosens, L., Jacobs, W., Blust, R., and Neels, H. (2008). Polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) in human liver and adipose tissue samples from Belgium. Chemosphere 73, 170-175.
10. Cui, Y., Konig, J., Leier, I., Buchholz, U., and Keppler, D. (2001). Hepatic uptake of bilirubin and its conjugates by the human organic anion transporter SLC21A6. J. Biol. Chem. 276, 9626-9630.
11. Darnerud, P. O., Aune, M., Larsson, L., and Hallgren, S. (2007). Plasma PBDE and thyroxine levels in rats exposed to Bromkal or BDE-47. Chemosphere 67, S386-S392.
12. Darnerud, P. O., Eriksen, G. S., Johannesson, T., Larsen, P. B., and Viluksela, M. (2001). Polybrominated diphenyl ethers: occurrence, dietary exposure, and toxicology. Environ. Health Perspect. 109(Suppl. 1), 49-68.
13. Darnerud, P. O., and Risberg, S. (2006). Tissue localisation of tetra- and pentabromodiphenyl ether congeners (BDE-47, -85 and -99) in perinatal and adult C57BL mice. Chemosphere 62, 485-493.
14. Ganapathy, V., Balkovetz, D. F., Ganapathy, M. E., Mahesh, V. B., Devoe, L. D., and Leibach, F. H. (1987). Evidence for histidyl and carboxy groups at the active site of the human placental Na+-H+ exchanger. Biochem. J. 245, 473-477.
15. Grillo, F. G., and Aronson, P. S. (1986). Inactivation of the renal microvillus membrane Na+-H+ exchanger by histidine-specific reagents. J. Biol. Chem. 261, 1120-1125.
16. Grube, M., Kock, K., Oswald, S., Draber, K., Meissner, K., Eckel, L., Bohm, M., Felix, S. B., Vogelgesang, S., Jedlitschky, G., et al. (2006). Organic anion transporting polypeptide 2B1 is a high-affinity transporter for atorvastatin and is expressed in the human heart. Clin. Pharmacol. Ther. 80, 607-620.
17. Gui, C., Miao, Y., Thompson, L., Wahlgren, B., Mock, M., Stieger, B., and Hagenbuch, B. (2008). Effect of pregnane X receptor ligands on transport mediated by human OATP1B1 and OATP1B3. Eur. J. Pharmacol. 584, 57-65.
18. Hagenbuch, B. (2010). Drug uptake systems in liver and kidney: a historic perspective. Clin. Pharmacol. Ther. 87, 39-47.
19. Hagenbuch, B., and Gui, C. (2008). Xenobiotic transporters of the human organic anion transporting polypeptides (OATP) family. Xenobiotica 38, 778-801.
20. Hagenbuch, B., and Meier, P. J. (2003). The superfamily of organic anion transporting polypeptides. Biochim. Biophys. Acta 1609, 1-18.
21. Hagenbuch, B., and Meier, P. J. (2004). Organic anion transporting polypeptides of the OATP/SLC21 family: phylogenetic classification as OATP/SLCO superfamily, new nomenclature and molecular/functional properties. Pflugers Arch. 447, 653-665.
22. Hakk, H., Larsen, G., and Klasson-Wehler, E. (2002). Tissue disposition, excretion and metabolism of 2,2',4,4',5-pentabromodiphenyl ether (BDE-99) in the male Sprague-Dawley rat. Xenobiotica 32, 369-382.
23. Hamers, T., Kamstra, J. H., Sonneveld, E., Murk, A. J., Visser, T. J., Van Velzen, M. J., Brouwer, A., and Bergman, A. (2008). Biotransformation of brominated flame retardants into potentially endocrine-disrupting metabolites, with special attention to 2,2',4,4'-tetrabromodiphenyl ether (BDE-47). Mol. Nutr. Food Res. 52, 284-298.
24. Hirano, M., Maeda, K., Shitara, Y., and Sugiyama, Y. (2004). Contribution of OATP2 (OATP1B1) and OATP8 (OATP1B3) to the hepatic uptake of pitavastatin in humans. J. Pharmacol. Exp. Ther. 311, 139-146.
25. Hites, R. A. (2004). Polybrominated diphenyl ethers in the environment and in people: a meta-analysis of concentrations. Environ. Sci. Technol. 38, 945-956.
26. Hsiang, B., Zhu, Y., Wang, Z., Wu, Y., Sasseville, V., Yang, W. P., and Kirchgessner, T. G. (1999). A novel human hepatic organic anion transporting polypeptide (OATP2). Identification of a liver-specific human organic anion transporting polypeptide and identification of rat and human hydroxymethylglutaryl-CoA reductase inhibitor transporters. J. Biol. Chem. 274, 37161-37168.
27. Kalliokoski, A., and Niemi, M. (2009). Impact of OATP transporters on pharmacokinetics. Br. J. Pharmacol. 158, 693-705.
28. Kato, M., Maegawa, H., Okano, T., Inui, K., and Hori, R. (1989). Effect of various chemical modifiers on H+ coupled transport of cephradine via dipeptide carriers in rabbit intestinal brush-border membranes: role of histidine residues. J. Pharmacol. Exp. Ther. 251, 745-749.
29. Kobayashi, D., Nozawa, T., Imai, K., Nezu, J., Tsuji, A., and Tamai, I. (2003). Involvement of human organic anion transporting polypeptide OATP-B (SLC21A9) in pH-dependent transport across intestinal apical membrane. J. Pharmacol. Exp. Ther. 306, 703-708.
30. Konig, J., Cui, Y., Nies, A. T., and Keppler, D. (2000a). A novel human organic anion transporting polypeptide localized to the basolateral hepatocyte membrane. Am. J. Physiol. Gastrointest. Liver Physiol. 278, G156-G164.
31. Konig, J., Cui, Y., Nies, A. T., and Keppler, D. (2000b). Localization and genomic organization of a new hepatocellular organic anion transporting polypeptide. J. Biol. Chem. 275, 23161-23168.
32. Kullak-Ublick, G. A., Ismair, M. G., Stieger, B., Landmann, L., Huber, R., Pizzagalli, F., Fattinger, K., Meier, P. J., and Hagenbuch, B. (2001). Organic anion-transporting polypeptide B (OATP-B) and its functional comparison with three other OATPs of human liver. Gastroenterology 120, 525-533.
33. Leuthold, S., Hagenbuch, B., Mohebbi, N., Wagner, C. A., Meier, P. J., and Stieger, B. (2009). Mechanisms of pH-gradient driven transport mediated by organic anion polypeptide transporters. Am. J. Physiol. Cell Physiol. 296, C570-582.
34. Lorber, M. (2008). Exposure of Americans to polybrominated diphenyl ethers. J. Expo. Sci. Environ. Epidemiol. 18, 2-19.
35. Lupton, S. J., McGarrigle, B. P., Olson, J. R., Wood, T. D., and Aga, D. S. (2009). Human liver microsome-mediated metabolism of brominated diphenyl ethers 47, 99, and 153 and identification of their major metabolites. Chem. Res. Toxicol. 22, 1802-1809.
36. Mazdai, A., Dodder, N. G., Abernathy, M. P., Hites, R. A., and Bigsby, R. M. (2003). Polybrominated diphenyl ethers in maternal and fetal blood samples. Environ. Health Perspect. 111, 1249-1252.
37. Meerts, I. A., Letcher, R. J., Hoving, S., Marsh, G., Bergman, A., Lemmen, J. G., van der Burg, B., and Brouwer, A. (2001). In vitro estrogenicity of polybrominated diphenyl ethers, hydroxylated PDBEs, and polybrominated bisphenol A compounds. Environ. Health Perspect. 109, 399-407.
38. Meerts, I. A., van Zanden, J. J., Luijks, E. A., van Leeuwen-Bol, I., Marsh, G., Jakobsson, E., Bergman, A., and Brouwer, A. (2000). Potent competitive interactions of some brominated flame retardants and related compounds with human transthyretin in vitro. Toxicol. Sci. 56, 95-104.
39. Meier-Abt, F., Mokrab, Y., and Mizuguchi, K. (2005). Organic anion transporting polypeptides of the OATP/SLCO superfamily: identification of new members in nonmammalian species, comparative modeling and a potential transport mode. J. Membr. Biol. 208, 213-227.
40. Meironyte Guvenius, D., Bergman, A., and Noren, K. (2001). Polybrominated diphenyl ethers in Swedish human liver and adipose tissue. Arch. Environ. Contam. Toxicol. 40, 564-570.
41. Miles, E. W. (1977). Modification of histidyl residues in proteins by diethylpyrocarbonate. Methods Enzymol. 47, 431-442.
42. Nozawa, T., Imai, K., Nezu, J., Tsuji, A., and Tamai, I. (2004). Functional characterization of pH-sensitive organic anion transporting polypeptide OATP-B in human. J. Pharmacol. Exp. Ther. 308, 438-445.
43. Nozawa, T., Nakajima, M., Tamai, I., Noda, K., Nezu, J., Sai, Y., Tsuji, A., and Yokoi, T. (2002). Genetic polymorphisms of human organic anion transporters OATP-C (SLC21A6) and OATP-B (SLC21A9): allele frequencies in the Japanese population and functional analysis. J. Pharmacol. Exp. Ther. 302, 804-813.
44. Palermo, D. P., DeGraaf, M. E., Marotti, K. R., Rehberg, E., and Post, L. E. (1991). Production of analytical quantities of recombinant proteins in Chinese hamster ovary cells using sodium butyrate to elevate gene expression. J. Biotechnol. 19, 35-47.
45. Petreas, M., She, J., Brown, F. R., Winkler, J., Windham, G., Rogers, E., Zhao, G., Bhatia, R., and Charles, M. J. (2003). High body burdens of 2,2',4,4'-tetrabromodiphenyl ether (BDE-47) in California women. Environ. Health Perspect. 111, 1175-1179.
46. Qiu, X., Bigsby, R. M., and Hites, R. A. (2009). Hydroxylated metabolites of polybrominated diphenyl ethers in human blood samples from the United States. Environ. Health Perspect. 117, 93-98.
47. Sai, Y., Kaneko, Y., Ito, S., Mitsuoka, K., Kato, Y., Tamai, I., Artursson, P., and Tsuji, A. (2006). Predominant contribution of organic anion transporting polypeptide OATP-B (OATP2B1) to apical uptake of estrone-3-sulfate by human intestinal Caco-2 cells. Drug Metab. Dispos. 34, 1423-1431.
48. Sandanger, T. M., Sinotte, M., Dumas, P., Marchand, M., Sandau, C. D., Pereg, D., Berube, S., Brisson, J., and Ayotte, P. (2007). Plasma concentrations of selected organobromine compounds and polychlorinated biphenyls in postmenopausal women of Quebec, Canada. Environ. Health Perspect. 115, 1429-1434.
49. Sanders, J. M., Chen, L. J., Lebetkin, E. H., and Burka, L. T. (2006a). Metabolism and disposition of 2,2',4,4'-tetrabromodiphenyl ether following administration of single or multiple doses to rats and mice. Xenobiotica 36, 103-117.
50. Sanders, J. M., Lebetkin, E. H., Chen, L. J., and Burka, L. T. (2006b). Disposition of 2,2',4,4',5,5'-hexabromodiphenyl ether (BDE153) and its interaction with other polybrominated diphenyl ethers (PBDEs) in rodents. Xenobiotica 36, 824-837.
51. Schecter, A., Johnson-Welch, S., Tung, K. C., Harris, T. R., Papke, O., and Rosen, R. (2007). Polybrominated diphenyl ether (PBDE) levels in livers of U.S. human fetuses and newborns. J. Toxicol. Environ. Health A 70, 1-6.
52. Schecter, A., Papke, O., Harris, T. R., Tung, K. C., Musumba, A., Olson, J., and Birnbaum, L. (2006). Polybrominated diphenyl ether (PBDE) levels in an expanded market basket survey of U.S. food and estimated PBDE dietary intake by age and sex. Environ. Health Perspect. 114, 1515-1520.
53. Schecter, A., Papke, O., Joseph, J. E., and Tung, K. C. (2005a). Polybrominated diphenyl ethers (PBDEs) in U.S. computers and domestic carpet vacuuming: possible sources of human exposure. J. Toxicol. Environ. Health A 68, 501-513.
54. Schecter, A., Papke, O., Tung, K. C., Joseph, J., Harris, T. R., and Dahlgren, J. (2005b). Polybrominated diphenyl ether flame retardants in the U.S. population: current levels, temporal trends, and comparison with dioxins, dibenzofurans, and polychlorinated biphenyls. J. Occup. Environ. Med. 47, 199-211.
55. Schecter, A., Papke, O., Tung, K. C., Staskal, D., and Birnbaum, L. (2004). Polybrominated diphenyl ethers contamination of United States food. Environ. Sci. Technol. 38, 5306-5311.
56. Sjodin, A., Wong, L. Y., Jones, R. S., Park, A., Zhang, Y., Hodge, C., Dipietro, E., McClure, C., Turner, W., Needham, L. L., et al. (2008). Serum concentrations of polybrominated diphenyl ethers (PBDEs) and polybrominated biphenyl (PBB) in the United States population: 2003-2004. Environ. Sci. Technol. 42, 1377-1384.
57. Stapleton, H. M., Kelly, S. M., Pei, R., Letcher, R. J., and Gunsch, C. (2009). Metabolism of polybrominated diphenyl ethers (PBDEs) by human hepatocytes in vitro. Environ. Health Perspect. 117, 197-202.
58. Staskal, D. F., Diliberto, J. J., DeVito, M. J., and Birnbaum, L. S. (2005). Toxicokinetics of BDE 47 in female mice: effect of dose, route of exposure, and time. Toxicol. Sci. 83, 215-223.
59. St-Pierre, M. V., Hagenbuch, B., Ugele, B., Meier, P. J., and Stallmach, T. (2002). Characterization of an organic anion-transporting polypeptide (OATP-B) in human placenta. J. Clin. Endocrinol. Metab. 87, 1856-1863.
60. Tamai, I., Nezu, J., Uchino, H., Sai, Y., Oku, A., Shimane, M., and Tsuji, A. (2000). Molecular identification and characterization of novel members of the human organic anion transporter (OATP) family. Biochem. Biophys. Res. Commun. 273, 251-260.
61. Tamai, I., Nozawa, T., Koshida, M., Nezu, J., Sai, Y., and Tsuji, A. (2001). Functional characterization of human organic anion transporting polypeptide B (OATP-B) in comparison with liver-specific OATP-C. Pharm. Res. 18, 1262-1269.
62. Zhou, T., Taylor, M. M., DeVito, M. J., and Crofton, K. M. (2002). Developmental exposure to brominated diphenyl ethers results in thyroid hormone disruption. Toxicol. Sci. 66, 105-116.