Characterization of arsenic hepatobiliary transport using sandwich-cultured human hepatocytes

Toxicological Sciences

Volumn 145, Issue 2, 2015, Pages 307-320

  Roggenbeck, Barbara A ^a   Carew, Michael W ^a   Charrois, Gregory J ^a   Douglas, Donna N ^a   Kneteman, Norman M ^a   Lu, Xiufen ^a   Chris Le, X ^a   Leslie, Elaine M ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Arsenic; Glutathione; Multidrug resistance proteins (MRPs ABCCs); Primary human hepatocytes; Sandwich cultured hepatocytes

Indexed keywords

ARSENIC; GLUTATHIONE; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 4; MULTIDRUG RESISTANCE PROTEIN 4; OLTIPRAZ; ABCC4 PROTEIN, HUMAN; MULTIDRUG RESISTANCE PROTEIN; NFE2L2 PROTEIN, HUMAN; PROPIONIC ACID DERIVATIVE; PYRAZINE DERIVATIVE; QUINOLINE DERIVATIVE; TRANSCRIPTION FACTOR NRF2; VERLUKAST;

ADULT; ARTICLE; BASOLATERAL MEMBRANE; BILIARY EXCRETION; CELL CULTURE; CONTROLLED STUDY; DOSE RESPONSE; EFFUSION; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CELL; TEMPERATURE; AGONISTS; ANTAGONISTS AND INHIBITORS; BILE DUCT; CULTURE TECHNIQUE; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; KINETICS; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

RATTUS;

ARSENIC; BILE DUCTS; BIOLOGICAL TRANSPORT; CELL CULTURE TECHNIQUES; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTATHIONE; HEK293 CELLS; HEPATOCYTES; HUMANS; KINETICS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NF-E2-RELATED FACTOR 2; PROPIONATES; PYRAZINES; QUINOLINES; TEMPERATURE; TRANSFECTION;

EID: 84930744828     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfv051     Document Type: Article

References (45)

1. Banerjee, M., Carew, M. W., Roggenbeck, B. A., Whitlock, B. D., Naranmandura, H., Le, X. C., and Leslie, E. M. (2014). A novel pathway for arsenic elimination: Human multidrug resistance protein 4 (MRP4/ABCC4) mediates cellular export of dimethylarsinic acid (DMAV) and the diglutathione conjugate of monomethylarsonous acid (MMAIII). Mol. Pharmacol. 86, 168-179.
2. Carew, M. W., and Leslie, E. M. (2010). Selenium-dependent and -independent transport of arsenic by the human multidrug resistance protein 2 (MRP2/ABCC2): Implications for the mutual detoxification of arsenic and selenium. Carcinogenesis 31, 1450-1455.
3. Carew, M. W., Naranmandura, H., Shukalek, C. B., Le, X. C., and Leslie, E. M. (2011). Monomethylarsenic diglutathione transport by the human multidrug resistance protein 1 (MRP1/ABCC1). Drug Metab. Dispos. 39, 2298-2304.
4. Csanaky, I., and Gregus, Z. (2002). Species variations in the biliary and urinary excretion of arsenate, arsenite and their metabolites. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 131, 355-365.
5. Cui, X., Kobayashi, Y., Hayakawa, T., and Hirano, S. (2004). Arsenic speciation in bile and urine following oral and intravenous exposure to inorganic and organic arsenics in rats. Toxicol. Sci. 82, 478-487.
6. Cullen, W. R. (2014). Chemical mechanism of arsenic biomethylation. Chem. Res. Toxicol. 27, 457-461.
7. Dietrich, C. G., Ottenhoff, R., de Waart, D. R., and Oude Elferink, R. P. (2001). Role of MRP2 and GSH in intrahepatic cycling of toxins. Toxicology 167, 73-81.
8. Drobna, Z., Walton, F. S., Paul, D. S., Xing, W., Thomas, D. J., and Styblo, M. (2010). Metabolism of arsenic in human liver: The role of membrane transporters. Arch. Toxicol. 84, 3-16.
9. Drobna, Z., Waters, S. B., Walton, F. S., LeCluyse, E. L., Thomas, D.J., and Styblo, M. (2004). Interindividual variation in the metabolism of arsenic in cultured primary human hepatocytes. Toxicol. Appl. Pharmacol. 201, 166-177.
10. Ghibellini, G., Vasist, L. S., Leslie, E. M., Heizer, W. D., Kowalsky, R. J., Calvo, B. F., and Brouwer, K. L. (2007). In vitro-in vivo correlation of hepatobiliary drug clearance in humans. Clin. Pharmacol. Ther. 81, 406-413.
11. Hamilton, G. A., Jolley, S. L., Gilbert, D., Coon, D. J., Barros, S., and LeCluyse, E. L. (2001). Regulation of cell morphology and cytochrome P450 expression in human hepatocytes by extracellular matrix and cell-cell interactions. Cell Tissue Res. 306, 85-99.
12. Hipfner, D. R., Gauldie, S. D., Deeley, R. G., and Cole, S. P. (1994). Detection of the M(r) 190,000 multidrug resistance protein, MRP, with monoclonal antibodies. Cancer Res. 54, 5788-5792.
13. IARC. (2012). Arsenic, metals, fibres, and dusts. IARC Monogr. Eval. Carcinog Risks Hum. 100(Pt C), 11-465.
14. Ishihara, N., and Matsushiro, T. (1986). Biliary and urinary excretion of metals in humans. Arch. Environ. Health 41, 324-330.
15. Jigorel, E., Le Vee, M., Boursier-Neyret, C., Parmentier, Y., and Fardel, O. (2006). Differential regulation of sinusoidal and canalicular hepatic drug transporter expression by xenobiotics activating drug-sensing receptors in primary human hepatocytes. Drug Metab. Dispos. 34, 1756-1763.
16. Kala, S. V., Neely, M. W., Kala, G., Prater, C. I., Atwood, D. W., Rice, J. S., and Lieberman, M. W. (2000). The MRP2/cMOAT transporter and arsenic-glutathione complex formation are required for biliary excretion of arsenic. J. Biol. Chem. 275, 33404-33408.
17. Kostrubsky, V. E., Strom, S. C., Hanson, J., Urda, E., Rose, K., Burliegh, J., Zocharski, P., Cai, H., Sinclair, J. F., and Sahi, J. (2003). Evaluation of hepatotoxic potential of drugs by inhibition of bile-acid transport in cultured primary human hepatocytes and intact rats. Toxicol. Sci. 76, 220-228.
18. Krupka, R. M. (1985). Asymmetrical binding of phloretin to the glucose transport system of human erythrocytes. J. Membr. Biol. 83, 71-80.
19. Kwon, O., Eck, P., Chen, S., Corpe, C. P., Lee, J. H., Kruhlak, M., and Levine, M. (2007). Inhibition of the intestinal glucose transporter GLUT2 by flavonoids. FASEB J. 21, 366-377.
20. Lebeck, J. (2014). Metabolic impact of the glycerol channels AQP7 and AQP9 in adipose tissue and liver. J. Mol. Endocrinol. 52, R165-R178.
21. Lee, J. K., Leslie, E. M., Zamek-Gliszczynski, M. J., and Brouwer, K. L. (2008). Modulation of trabectedin (ET-743) hepatobiliary disposition by multidrug resistance-associated proteins (Mrps) may prevent hepatotoxicity. Toxicol. Appl. Pharmacol. 228, 17-23.
22. Leslie, E. M. (2012). Arsenic-glutathione conjugate transport by the human multidrug resistance proteins (MRPs/ABCCs). J. Inorg. Biochem. 108, 141-149.
23. Liu, X., Chism, J. P., LeCluyse, E. L., Brouwer, K. R., and Brouwer, K. L. (1999a). Correlation of biliary excretion in sandwich-cultured rat hepatocytes and in vivo in rats. Drug Metab. Dispos. 27, 637-644.
24. Liu, X., LeCluyse, E. L., Brouwer, K. R., Gan, L. S., Lemasters, J. J., Stieger, B., Meier, P. J., and Brouwer, K. L. (1999b). Biliary excretion in primary rat hepatocytes cultured in a collagensandwich configuration. Am. J. Physiol. 277(1 Pt 1), G12-G21.
25. 2+ modulation to evaluate biliary excretion in sandwich-cultured rat hepatocytes. J. Pharmacol. Exp. Ther. 289, 1592-1599.
26. Marion, T. L., Leslie, E. M., and Brouwer, K. L. (2007). Use of sandwich-cultured hepatocytes to evaluate impaired bile acid transport as a mechanism of drug-induced hepatotoxicity. Mol. Pharm. 4, 911-918.
27. McDermott, J. R., Jiang, X., Beene, L. C., Rosen, B. P., and Liu, Z. (2010). Pentavalent methylated arsenicals are substrates of human AQP9. Biometals 23, 119-127.
28. Mercer, D. F., Schiller, D. E., Elliott, J. F., Douglas, D. N., Hao, C., Rinfret, A., Addison, W. R., Fischer, K. P., Churchill, T. A., Lakey, J. R., et al. (2001). Hepatitis C virus replication in mice with chimeric human livers. Nat. Med. 7, 927-933.
29. Mukhopadhyay, R., Bhattacharjee, H., and Rosen, B. P. (2014). Aquaglyceroporins: Generalized metalloid channels. Biochim. Biophys. Acta 1840, 1583-1591.
30. Naujokas, M. F., Anderson, B., Ahsan, H., Aposhian, H. V., Graziano, J. H., Thompson, C., and Suk, W. A. (2013). The broad scope of health effects from chronic arsenic exposure:Update on a worldwide public health problem. Environ. Health Perspect. 121, 295-302.
31. Pomroy, C., Charbonneau, S. M., McCullough, R. S., and Tam, G. K. (1980). Human retention studies with 74As. Toxicol. Appl. Pharmacol. 53, 550-556.
32. Reay, P. F., and Asher, C. J. (1977). Preparation and purification of 74As-labeled arsenate and arsenite for use in biological experiments. Anal. Biochem. 78, 557-560.
33. Rius, M., Nies, A. T., Hummel-Eisenbeiss, J., Jedlitschky, G., and Keppler, D. (2003). Cotransport of reduced glutathione with bile salts by MRP4 (ABCC4) localized to the basolateral hepatocyte membrane. Hepatology 38, 374-384.
34. Sharma, S., Ellis, E. C., Gramignoli, R., Dorko, K., Tahan, V., Hansel, M., Mattison, D. R., Caritis, S. N., Hines, R. N., Venkataramanan, R., et al. (2013). Hepatobiliary disposition of 17-OHPC and taurocholate in fetal human hepatocytes: A comparison with adult human hepatocytes. Drug Metab. Dispos. 41, 296-304.
35. Shirasaka, Y., Shichiri, M., Mori, T., Nakanishi, T., and Tamai, I. (2013). Major active components in grapefruit, orange, and apple juices responsible for OATP2B1-mediated drug interactions. J. Pharm. Sci. 102, 280-288.
36. Smith, A. H., Lingas, E. O., and Rahman, M. (2000). Contamination of drinking-water by arsenic in Bangladesh:A public health emergency. Bull. World Health Organ. 78, 1093-1103.
37. Styblo, M., Del Razo, L. M., LeCluyse, E. L., Hamilton, G. A., Wang, C., Cullen, W. R., and Thomas, D. J. (1999). Metabolism of arsenic in primary cultures of human and rat hepatocytes. Chem. Res. Toxicol. 12, 560-565.
38. Suzuki, K. T., Tomita, T., Ogra, Y., and Ohmichi, M. (2001). Glutathione-conjugated arsenics in the potential hepato-enteric circulation in rats. Chem. Res. Toxicol. 14, 1604-1611.
39. Tokar, E. J., Benbrahim-Tallaa, L., Ward, J. M., Lunn, R., Sams, R. L., II, and Waalkes, M. P. (2010). Cancer in experimental animals exposed to arsenic and arsenic compounds. Crit. Rev. Toxicol. 40, 912-927.
40. Vernhet, L., Seite, M. P., Allain, N., Guillouzo, A., and Fardel, O. (2001). Arsenic induces expression of the multidrug resistance-associated protein 2 (MRP2) gene in primary rat and human hepatocytes. J. Pharmacol. Exp. Ther. 298, 234-239.
41. Villa-Bellosta, R., and Sorribas, V. (2010). Arsenate transport by sodium/phosphate cotransporter type IIb. Toxicol. Appl. Pharmacol. 247, 36-40.
42. Wang, Q., and Morris, M. E. (2007). Flavonoids modulate monocarboxylate transporter-1-mediated transport of gamma-hydroxybutyrate in vitro and in vivo. Drug Metab. Dispos. 35, 201-208.
43. Wu, C. P., Calcagno, A. M., Hladky, S. B., Ambudkar, S. V., and Barrand, M. A. (2005). Modulatory effects of plant phenols on human multidrug-resistance proteins 1, 4 and 5 (ABCC1, 4 and 5). FEBS J. 272, 4725-4740.
44. Xu, S., Weerachayaphorn, J., Cai, S. Y., Soroka, C. J., and Boyer, J. L. (2010). Aryl hydrocarbon receptor and NF-E2-related factor 2 are key regulators of human MRP4 expression. Am. J. Physiol. Gastrointest. Liver Physiol. 299, G126-G135.
45. Zamek-Gliszczynski, M. J., Xiong, H., Patel, N. J., Turncliff, R. Z., Pollack, G. M., and Brouwer, K. L. (2003). Pharmacokinetics of 5 (and 6)-carboxy-20,70-dichlorofluorescein and its diacetate promoiety in the liver. J. Pharmacol. Exp. Ther. 304, 801-809.