ABCG2 functions as a general phytoestrogen sulfate transporter in vivo

FASEB Journal

Volumn 26, Issue 10, 2012, Pages 4014-4024

  Van De Wetering, Koen ^a   Sapthu, Sunny ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

BCRP; Metabolomics; Phase II metabolism; Vesicular transport

Indexed keywords

BILE ACID; BREAST CANCER RESISTANCE PROTEIN; PHYTOESTROGEN; PHYTOESTROGEN SULFATE; UNCLASSIFIED DRUG; VESICULAR TRANSPORT PROTEIN;

ARTICLE; BLOOD SAMPLING; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; URINALYSIS; WILD TYPE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; FEMALE; MALE; MASS SPECTROMETRY; MEMBRANE TRANSPORT PROTEINS; METABOLOMICS; MICE; MICE, KNOCKOUT; PHYTOESTROGENS;

MAMMALIA; MUS;

EID: 84868134869     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-210039     Document Type: Article

References (30)

1. Borst, P., and Oude Elferink, R. P. (2002) Mammalian ABC transporters in health and disease. Annu. Rev. Biochem. 71, 537-592
2. Vlaming, M. L., Lagas, J. S., and Schinkel, A. H. (2009) Physiological and pharmacological roles of ABCG2 (BCRP): recent findings in Abcg2 knockout mice. Adv. Drug Deliv. Rev. 61, 14-25
3. Krishnamurthy, P., and Schuetz, J. D. (2006) Role of ABCG2/ BCRP in biology and medicine. Annu. Rev. Pharmacol. Toxicol. 46, 381-410
4. Robey, R. W., To, K. K., Polgar, O., Dohse, M., Fetsch, P., Dean, M., and Bates, S. E. (2009) ABCG2: a perspective. Adv. Drug Deliv. Rev. 61, 3-13
5. Van de Wetering, K., Burkon, A., Feddema, W., Bot, A., de Jonge, H., Somoza, V., and Borst, P. (2008) Intestinal BCRP/ Bcrp1 and MRP3/Mrp3 are involved in the pharmacokinetics of resveratrol. Mol. Pharmacol. 75, 876-885
6. Pal, A., Mehn, D., Molnar, E., Gedey, S., Meszaros, P., Nagy, T., Glavinas, H., Janaky, T., von Richter, O., Bathori, G., Szente, L., and Krajcsi, P. (2007) Cholesterol potentiates ABCG2 activity in a heterologous expression system: improved in vitro model to study function of human ABCG2. J. Pharmacol. Exp. Ther. 321, 1085-1094
7. Suzuki, M., Suzuki, H., Sugimoto, Y., and Sugiyama, Y. (2003) ABCG2 transports sulfated conjugates of steroids and xenobiotics. J. Biol. Chem. 278, 22644-22649
8. Lindsay, J., Wang, L. L., Li, Y., and Zhou, S. F. (2008) Structure, function and polymorphism of human cytosolic sulfotransferases. Curr. Drug Metab. 9, 99-105
9. Enokizono, J., Kusuhara, H., and Sugiyama, Y. (2007) Regional expression and activity of breast cancer resistance protein (Bcrp/Abcg2) in mouse intestine: overlapping distribution with sulfotransferases. Drug Metab. Dispos. 35, 922-928
10. Adachi, Y., Suzuki, H., Schinkel, A. H., and Sugiyama, Y. (2005) Role of breast cancer resistance protein (Bcrp1/Abcg2) in the extrusion of glucuronide and sulfate conjugates from enterocytes to intestinal lumen. Mol. Pharmacol. 67, 923-928
11. Alvarez, A. I., Vallejo, F., Barrera, B., Merino, G., Prieto, J. G., Tomas-Barberan, F., and Espin, J. C. (2011) Bioavailability of the glucuronide and sulfate conjugates of genistein and daidzein in breast cancer resistance protein 1 knockout mice. Drug Metab. Dispos. 39, 2008-2012
12. Zamek-Gliszczynski, M. J., Nezasa, K., Tian, X., Kalvass, J. C., Patel, N. J., Raub, T. J., and Brouwer, K. L. (2006) 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, 2127-2133
13. Krumpochova, P., Sapthu, S., Brouwers, J. F., de Haas, M., de Vos, R., Borst, P., and van de Wetering, K. (2011) Transportomics: screening for substrates of ABC transporters in body fluids using vesicular transport assays. FASEB J. 26, 738-747
14. Jonker, J. W., Buitelaar, M., Wagenaar, E., van der Valk, M. A., Scheffer, G. L., Scheper, R. J., Plosch, T., Kuipers, F., Elferink, R. P., Rosing, H., Beijnen, J. H., and Schinkel, A. H. (2002) The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria. Proc. Natl. Acad. Sci. U. S. A. 99, 15649-15654
15. Van de Wetering, K., Feddema, W., Helms, J. B., Brouwers, J. F., and Borst, P. (2009) Targeted metabolomics identifies glucuronides of dietary phytoestrogens as a major class of MRP3 substrates in vivo. Gastroenterology 137, 1725-1735
16. Lafaye, A., Junot, C., Ramounet-Le Gall, B., Fritsch, P., Ezan, E., and Tabet, J. C. (2004) Profiling of sulfoconjugates in urine by using precursor ion and neutral loss scans in tandem mass spectrometry. Application to the investigation of heavy metal toxicity in rats. J. Mass Spectrom. 39, 655-664
17. Breedveld, P., Pluim, D., Cipriani, G., Dahlhaus, F., van Eijndhoven, M. A., de Wolf, C. J., Kuil, A., Beijnen, J. H., Scheffer, G. L., Jansen, G., Borst, P., and Schellens, J. H. (2007) The effect of low pH on breast cancer resistance protein (ABCG2)-mediated transport of methotrexate, 7-hydroxymethotrexate, methotrexate diglutamate, folic acid, mitoxantrone, topotecan, and resveratrol in in vitro drug transport models. Mol. Pharmacol. 71, 240-249
18. Van de Wetering, K., Zelcer, N., Kuil, A., Feddema, W., Hillebrand, M., Vlaming, M. L., Schinkel, A. H., Beijnen, J. H., and Borst, P. (2007) Multidrug resistance protein 2 and 3 provide alternative routes for hepatic excretion of morphine-glucuronides. Mol. Pharmacol. 72, 387-394
19. Lee, J. K., Abe, K., Bridges, A. S., Patel, N. J., Raub, T. J., Pollack, G. M., and Brouwer, K. L. (2009) Sex-dependent disposition of acetaminophen sulfate and glucuronide in the in situ perfused mouse liver. Drug Metab. Dispos. 37, 1916-1921
20. Eeckhaut, E., Struijs, K., Possemiers, S., Vincken, J. P., Keukeleire, D. D., and Verstraete, W. (2008) Metabolism of the lignan macromolecule into enterolignans in the gastrointestinal lumen as determined in the simulator of the human intestinal microbial ecosystem. J. Agric. Food Chem. 56, 4806-4812
21. Dixon, R. A. (2004) Phytoestrogens. Annu. Rev. Plant Biol. 55, 225-261
22. Jansen, G. H., Arts, I. C., Nielen, M. W., Muller, M., Hollman, P. C., and Keijer, J. (2005) Uptake and metabolism of enterolactone and enterodiol by human colon epithelial cells. Arch. Biochem. Biophys. 435, 74-82
23. De Loor, H., Bammens, B., Evenepoel, P., De Preter, V., and Verbeke, K. (2005) Gas chromatographic-mass spectrometric analysis for measurement of p-cresol and its conjugated metabolites in uremic and normal serum. Clin. Chem. 51, 1535-1538
24. Setchell, K. D., Gosselin, S. J., Welsh, M. B., Johnston, J. O., Balistreri, W. F., Kramer, L. W., Dresser, B. L., and Tarr, M. J. (1987) Dietary estrogens-a probable cause of infertility and liver disease in captive cheetahs. Gastroenterology 93, 225-233
25. Adams, N. R. (1990) Permanent infertility in ewes exposed to plant oestrogens. Aust. Vet. J. 67, 197-201
26. Whitten, P. L., Lewis, C., and Naftolin, F. (1993) A phytoestrogen diet induces the premature anovulatory syndrome in lactationally exposed female rats. Biol. Reprod. 49, 1117-1121
27. Lewis, R. W., Brooks, N., Milburn, G. M., Soames, A., Stone, S., Hall, M., and Ashby, J. (2003) The effects of the phytoestrogen genistein on the postnatal development of the rat. Toxicol. Sci. 71, 74-83
28. D'Alessandro, T. L., Boersma-Maland, B. J., Peterson, T. G., Sfakianos, J., Prasain, J. K., Patel, R. P., Darley-Usmar, V. M., Botting, N. P., and Barnes, S. (2005) Metabolism of phytoestrogen conjugates. Methods Enzymol. 400, 316-342
29. Zhu, W., Xu, H., Wang, S. W., and Hu, M. (2010) Breast cancer resistance protein (BCRP) and sulfotransferases contribute significantly to the disposition of genistein in mouse intestine. AAPS J. 12, 525-536
30. Roth, M., Obaidat, A., and Hagenbuch, B. (2012) OATPs, OATs and OCTs: the organic anion and cation transporters of the SLCO and SLC22A gene superfamilies. Br. J. Pharmacol. 165, 1260-1287