MRP isoforms and BCRP mediate sulfate conjugate efflux out of BeWo cells

International Journal of Pharmaceutics

Volumn 384, Issue 1-2, 2010, Pages 15-23

  Mitra, Pallabi ^a   Audus, Kenneth L ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

BODIPY FL prazosin; Breast cancer resistance protein (BCRP); Mitoxantrone; Multidrug resistance associated protein (MRP); Sulfate conjugate; Trophoblast

Indexed keywords

4 NITROPHENOL; 4 NITROPHENYL SULFATE; BREAST CANCER RESISTANCE PROTEIN; FUMITREMORGIN C; INDOMETACIN; LEUKOTRIENE C4; MITOXANTRONE; MULTIDRUG RESISTANCE PROTEIN; ORGANIC ANION TRANSPORTER; PARACETAMOL; PARACETAMOL SULFATE; PRAZOSIN; SULFATE; UNCLASSIFIED DRUG; VERLUKAST;

APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG CONJUGATION; DRUG ELIMINATION; DRUG TRANSPORT; HUMAN; HUMAN CELL; MEMBRANE TRANSPORT; PRIORITY JOURNAL; SULFATION; TROPHOBLAST;

ACETAMINOPHEN; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT, ACTIVE; CELL LINE, TUMOR; CELL MEMBRANE; HUMANS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NEOPLASM PROTEINS; NITROBENZENES; PROTEIN ISOFORMS; PROTEIN TRANSPORT; SULFATES; TROPHOBLASTS;

EID: 70649112175     PISSN: 03785173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2009.09.033     Document Type: Article

References (47)

1. Adachi Y., Suzuki H., Schinkel A.H., and Sugiyama Y. Role of breast cancer resistance protein (Bcrp1/Abcg2) in the extrusion of glucuronide and sulfate conjugates from enterocytes to intestinal lumen. Mol. Pharmacol. 67 (2005) 923-928
2. Atkinson D.E., Greenwood S.L., Sibley C.P., Glazier J.D., and Fairbairn L.J. Role of MDR1 and MRP1 in trophoblast cells, elucidated using retroviral gene transfer. Am. J. Physiol. Cell. Physiol. 285 (2003) C584-C591
3. Azzaroli F., Mennone A., Feletti V., Simoni P., Baglivo E., Montagnani M., Rizzo N., Pelusi G.D.D.E.A., Lodato F., Festi D., Colecchia A., Roda E., Boyer J.L., and Mazzella G. Clinical trial: modulation of human placental multidrug resistance proteins in cholestasis of pregnancy by ursodeoxycholic acid. Aliment. Pharmacol. Ther. 26 (2007) 1139-1146
4. Bode C.J., Jin H., Rytting E., Silverstein P.S., Young A.M., and Audus K.L. In vitro models for studying trophoblast transcellular transport. Methods Mol. Med. 122 (2006) 225-239
5. Brand W., Van Der Wel P.A., Rein M.J., Barron D., Williamson G., Van Bladeren P.J., and Rietjens I.M. Metabolism and transport of the citrus flavonoid hesperetin in Caco-2 cell monolayers. Drug Metab. Dispos. 36 (2008) 1794-1802
6. Cerveny L., Pavek P., Malakova J., Staud F., and Fendrich Z. Lack of interactions between breast cancer resistance protein (bcrp/abcg2) and selected antiepileptic agents. Epilepsia 47 (2006) 461-468
7. Chen J., Lin H., and Hu M. Absorption and metabolism of genistein and its five isoflavone analogs in the human intestinal Caco-2 model. Cancer Chemother. Pharmacol. 55 (2005) 159-169
8. Deeley R.G., and Cole S.P. Substrate recognition and transport by multidrug resistance protein 1 (ABCC1). FEBS Lett. 580 (2006) 1103-1111
9. Enokizono J., Kusuhara H., and Sugiyama Y. Involvement of breast cancer resistance protein (BCRP/ABCG2) in the biliary excretion and intestinal efflux of troglitazone sulfate, the major metabolite of troglitazone with a cholestatic effect. Drug Metab. Dispos. 35 (2007) 209-214
10. Evseenko D.A., Murthi P., Paxton J.W., Reid G., Emerald B.S., Mohankumar K.M., Lobie P.E., Brennecke S.P., Kalionis B., and Keelan J.A. The ABC transporter BCRP/ABCG2 is a placental survival factor, and its expression is reduced in idiopathic human fetal growth restriction. FASEB J. 21 (2007) 3592-3605
11. Evseenko D.A., Paxton J.W., and Keelan J.A. ABC drug transporter expression and functional activity in trophoblast-like cell lines and differentiating primary trophoblast. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290 (2006) R1357-R1365
12. Falany C.N. Enzymology of human cytosolic sulfotransferases. FASEB J. 11 (1997) 206-216
13. Friedman S.J., and Skehan P. Morphological differentiation of human choriocarcinoma cells induced by methotrexate. Cancer Res. 39 (1979) 1960-1967
14. Funk C., Ponelle C., Scheuermann G., and Pantze M. Cholestatic potential of troglitazone as a possible factor contributing to troglitazone-induced hepatotoxicity: in vivo and in vitro interaction at the canalicular bile salt export pump (Bsep) in the rat. Mol. Pharmacol. 59 (2001) 627-635
15. Grube M., Reuther S., Meyer Zu Schwabedissen H., Kock K., Draber K., Ritter C.A., Fusch C., Jedlitschky G., and Kroemer H.K. Organic anion transporting polypeptide 2B1 and breast cancer resistance protein interact in the transepithelial transport of steroid sulfates in human placenta. Drug Metab. Dispos. 35 (2007) 30-35
16. Gyemant N., Tanaka M., Antus S., Hohmann J., Csuka O., Mandoky L., and Molnar J. In vitro search for synergy between flavonoids and epirubicin on multidrug-resistant cancer cells. In Vivo 19 (2005) 367-374
17. Hanson S.R., Best M.D., and Wong C.H. Sulfatases: structure, mechanism, biological activity, inhibition, and synthetic utility. Angew. Chem. Int. Ed. Engl. 43 (2004) 5736-5763
18. Higaki K., Ishii M., Esumi H., Kanayama M., Ogawara K.I., and Kimura T. Pharmacokinetic analysis of factors determining elimination pathways for sulfate and glucuronide metabolites of xenobiotics II: studies with isolated perfused rat liver. Xenobiotica 33 (2003) 1097-1108
19. Hu M., Chen J., and Lin H. Metabolism of flavonoids via enteric recycling: mechanistic studies of disposition of apigenin in the Caco-2 cell culture model. J. Pharmacol. Exp. Ther. 307 (2003) 314-321
20. Imai Y., Asada S., Tsukahara S., Ishikawa E., Tsuruo T., and Sugimoto Y. Breast cancer resistance protein exports sulfated estrogens but not free estrogens. Mol. Pharmacol. 64 (2003) 610-618
21. Jeong E.J., Lin H., and Hu M. Disposition mechanisms of raloxifene in the human intestinal Caco-2 model. J. Pharmacol. Exp. Ther. 310 (2004) 376-385
22. Kallen C.B. Steroid hormone synthesis in pregnancy. Obstet. Gynecol. Clin. North Am. 31 (2004) 795-816 x
23. Konig J., Seithel A., Gradhand U., and Fromm M.F. Pharmacogenomics of human OATP transporters. Naunyn Schmiedebergs Arch. Pharmacol. 372 (2006) 432-443
24. Kostrubsky V.E., Vore M., Kindt E., Burliegh J., Rogers K., Peter G., Altrogge D., and Sinz M.W. The effect of troglitazone biliary excretion on metabolite distribution and cholestasis in transporter-deficient rats. Drug Metab. Dispos. 29 (2001) 1561-1566
25. Lee G., Babakhanian K., Ramaswamy M., Prat A., Wosik K., and Bendayan R. Expression of the ATP-binding cassette membrane transporter, ABCG2, in human and rodent brain microvessel endothelial and glial cell culture systems. Pharm. Res. 24 (2007) 1262-1274
26. Liu F., Soares M.J., and Audus K.L. Permeability properties of monolayers of the human trophoblast cell line BeWo. Am. J. Physiol. 273 (1997) C1596-C1604
27. Meyer Zu Schwabedissen H.E., Grube M., Heydrich B., Linnemann K., Fusch C., Kroemer H.K., and Jedlitschky G. Expression, localization, and function of MRP5 (ABCC5), a transporter for cyclic nucleotides, in human placenta and cultured human trophoblasts: effects of gestational age and cellular differentiation. Am. J. Pathol. 166 (2005) 39-48
28. Mitra P., and Audus K.L. Expression and functional activities of selected sulfotransferase isoforms in BeWo cells and primary cytotrophoblast cells. Biochem. Pharmacol. (2009)
29. Pascolo L., Fernetti C., Pirulli D., Crovella S., Amoroso A., and Tiribelli C. Effects of maturation on RNA transcription and protein expression of four MRP genes in human placenta and in BeWo cells. Biochem. Biophys. Res. Commun. 303 (2003) 259-265
30. Rao S.I., and Duffel M.W. Benzylic alcohols as stereospecific substrates and inhibitors for aryl sulfotransferase. Chirality 3 (1991) 104-111
31. Sakuma-Sawada N., Iida S., Mizuma T., Hayashi M., and Awazu S. Hepatic uptake of p-nitrophenyl sulfate by transporter that acetaminophen sulfate shares for uptake: sulfate moiety as a vector for metabolite transport. Res. Commun. Mol. Pathol. Pharmacol. 97 (1997) 131-138
32. Sakuma-Sawada N., Iida S., Mizuma T., Hayashi M., and Awazu S. Inhibition of the hepatic uptake of paracetamol sulphate by anionic compounds. J. Pharm. Pharmacol. 49 (1997) 743-746
33. Serrano M.A., Macias R.I., Briz O., Monte M.J., Blazquez A.G., Williamson C., Kubitz R., and Marin J.J. Expression in human trophoblast and choriocarcinoma cell lines, BeWo, Jeg-3 and JAr of genes involved in the hepatobiliary-like excretory function of the placenta. Placenta 28 (2007) 107-117
34. Sharom F.J. Shedding light on drug transport: structure and function of the P-glycoprotein multidrug transporter (ABCB1). Biochem. Cell. Biol. 84 (2006) 979-992
35. Sodha R.J., and Schneider H. Sulphate conjugation of beta 2-adrenoceptor stimulating drugs by platelet and placental phenol sulphotransferase. Br. J. Clin. Pharmacol. 17 (1984) 106-108
36. St-Pierre M.V., Serrano M.A., Macias R.I., Dubs U., Hoechli M., Lauper U., Meier P.J., and Marin J.J. Expression of members of the multidrug resistance protein family in human term placenta. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279 (2000) R1495-R1503
37. Stanley E.L., Hume R., Visser T.J., and Coughtrie M.W. Differential expression of sulfotransferase enzymes involved in thyroid hormone metabolism during human placental development. J. Clin. Endocrinol. Metab. 86 (2001) 5944-5955
38. Suzuki M., Suzuki H., Sugimoto Y., and Sugiyama Y. ABCG2 transports sulfated conjugates of steroids and xenobiotics. J. Biol. Chem. 278 (2003) 22644-22649
39. Ugele B., Bahn A., and Rex-Haffner M. Functional differences in steroid sulfate uptake of organic anion transporter 4 (OAT4) and organic anion transporting polypeptide 2B1 (OATP2B1) in human placenta. J. Steroid Biochem. Mol. Biol. 111 (2008) 1-6
40. Walle T., Otake Y., Brubaker J.A., Walle U.K., and Halushka P.V. Disposition and metabolism of the flavonoid chrysin in normal volunteers. Br. J. Clin. Pharmacol. 51 (2001) 143-146
41. Walle U.K., Galijatovic A., and Walle T. Transport of the flavonoid chrysin and its conjugated metabolites by the human intestinal cell line Caco-2. Biochem. Pharmacol. 58 (1999) 431-438
42. Young A.M. Characterization of efflux transporters of the human trophoblast using BeWo as a model. Pharmaceutical Chemistry (2005), University of Kansas, Lawrence
43. Zamek-Gliszczynski M.J., Hoffmaster K.A., Nezasa K., Tallman M.N., and Brouwer K.L. Integration of hepatic drug transporters and phase II metabolizing enzymes: mechanisms of hepatic excretion of sulfate, glucuronide, and glutathione metabolites. Eur. J. Pharm. Sci. 27 (2006) 447-486
44. Zamek-Gliszczynski M.J., Hoffmaster K.A., Tian X., Zhao R., Polli J.W., Humphreys J.E., Webster L.O., Bridges A.S., Kalvass J.C., and Brouwer K.L. Multiple mechanisms are involved in the biliary excretion of acetaminophen sulfate in the rat: role of Mrp2 and Bcrp1. Drug Metab. Dispos. 33 (2005) 1158-1165
45. Zamek-Gliszczynski M.J., Nezasa K., Tian X., Bridges A.S., Lee K., Belinsky M.G., Kruh G.D., and Brouwer K.L. Evaluation of the role of multidrug resistance-associated protein (Mrp) 3 and Mrp4 in hepatic basolateral excretion of sulfate and glucuronide metabolites of acetaminophen, 4-methylumbelliferone, and harmol in Abcc3-/- and Abcc4-/-mice. J. Pharmacol. Exp. Ther. 319 (2006) 1485-1491
46. Zamek-Gliszczynski M.J., Nezasa K., Tian X., Kalvass J.C., Patel N.J., Raub T.J., and Brouwer K.L. The important role of Bcrp (Abcg2) in the biliary excretion of sulfate and glucuronide metabolites of acetaminophen, 4-methylumbelliferone, and harmol in mice. Mol. Pharmacol. 70 (2006) 2127-2133
47. Zhang L., Lin G., Kovacs B., Jani M., Krajcsi P., and Zuo Z. Mechanistic study on the intestinal absorption and disposition of baicalein. Eur. J. Pharm. Sci. 31 (2007) 221-231