Transport of the soy isoflavone daidzein and its conjugative metabolites by the carriers SOAT, NTCP, OAT4, and OATP2B1

Archives of Toxicology

Volumn 89, Issue 12, 2015, Pages 2253-2263

  Grosser, Gary ^a   Döring, Barbara ^a   Ugele, Bernhard ^b   Geyer, Joachim ^a   Kulling, Sabine E ^c   Soukup, Sebastian T ^c  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c FEDERAL RESEARCH INSTITUTE OF NUTRITION AND FOOD   (Germany)

Author keywords

Carrier; Glucuronides; Soy isoflavones; Sulfates; Sulfoglucuronides; Transport

Indexed keywords

APICAL SODIUM DEPENDENT BILE ACID TRANSPORTER; DAIDZEIN; DAIDZEIN 7 GLUCURONIDE; DAIDZEIN 7 GLUCURONIDE 4' SULFATE; DAIDZEIN 7,4' DISULFATE; DAIDZIN; ESTRONE SULFATE; ORGANIC ANION TRANSPORTER 4; ORGANIC ANION TRANSPORTER B; SODIUM BILE ACID COTRANSPORTER; SODIUM DEPENDENT ORGANIC ANION TRANSPORTER; UNCLASSIFIED DRUG; CHOLESTEROL ACYLTRANSFERASE; COTRANSPORTER; ISOFLAVONE DERIVATIVE; ORGANIC ANION TRANSPORTER; PHYTOESTROGEN; SLC22A11 PROTEIN, HUMAN; SLCO2B1 PROTEIN, HUMAN; SODIUM-BILE ACID COTRANSPORTER;

ARTICLE; CONTROLLED STUDY; DRUG CONJUGATION; DRUG TRANSPORT; ENTEROHEPATIC CIRCULATION; HEK293 CELL LINE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; TRANSPORT ASSAY; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; PROCEDURES; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; HEK293 CELLS; HUMANS; ISOFLAVONES; ORGANIC ANION TRANSPORTERS; ORGANIC ANION TRANSPORTERS, SODIUM-DEPENDENT; ORGANIC ANION TRANSPORTERS, SODIUM-INDEPENDENT; PHYTOESTROGENS; STEROL O-ACYLTRANSFERASE; SYMPORTERS;

EID: 84949318043     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-014-1379-3     Document Type: Article

References (53)

1. Al Sarakbi W, Mokbel R, Salhab M, Jiang WG, Reed MJ, Mokbel K (2006) The role of STS and OATP-B mRNA expression in predicting the clinical outcome in human breast cancer. Anticancer Res 26:4985–4990
2. Allred CD, Ju YH, Allred KF, Chang J, Helferich WG (2001) Dietary genistin stimulates growth of estrogen-dependent breast cancer tumors similar to that observed with genistein. Carcinogenesis 22:1667–1673
3. Bolca S, Urpi-Sarda M, Blondeel P, Roche N, Vanhaecke L, Possemiers S, Al-Maharik N, Botting N, De Keukeleire D, Bracke M, Heyerick A, Manach C, Depypere H (2010) Disposition of soy isoflavones in normal human breast tissue. Am J Clin Nutr 91:976–984
4. + exchanger isoform, NHE3. Am J Physiol 269:C198–C206
5. Cha SH, Sekine T, Kusuhara H, Yu E, Kim JY, Kim DK, Sugiyama Y, Kanai Y, Endou H (2000) Molecular cloning and characterization of multispecific organic anion transporter 4 expressed in the placenta. J Biol Chem 275:4507–4512
6. Craddock AL, Love MW, Daniel RW, Kirby LC, Walters HC, Wong MH, Dawson PA (1998) Expression and transport properties of the human ileal and renal sodium-dependent bile acid transporter. Am J Physiol 274:G157–G169
7. Fietz D, Bakhaus K, Wapelhorst B, Grosser G, Gunther S, Alber J, Doring B, Kliesch S, Weidner W, Galuska CE, Hartmann MF, Wudy SA, Bergmann M, Geyer J (2013) Membrane transporters for sulfated steroids in the human testis—cellular localization, expression pattern and functional analysis. PLoS One 8:e62638
8. Geisler J (2003) Breast cancer tissue estrogens and their manipulation with aromatase inhibitors and inactivators. J Steroid Biochem Mol Biol 86:245–253
9. Geyer J, Wilke T, Petzinger E (2006) The solute carrier family SLC10: more than a family of bile acid transporters regarding function and phylogenetic relationships. Naunyn Schmiedebergs Arch Pharmacol 372:413–431
10. Geyer J, Doring B, Meerkamp K, Ugele B, Bakhiya N, Fernandes CF, Godoy JR, Glatt H, Petzinger E (2007) Cloning and functional characterization of human sodium-dependent organic anion transporter (SLC10A6). J Biol Chem 282:19728–19741
11. Grosser G, Fietz D, Gunther S, Bakhaus K, Schweigmann H, Ugele B, Brehm R, Petzinger E, Bergmann M, Geyer J (2013) Cloning and functional characterization of the mouse sodium-dependent organic anion transporter Soat (Slc10a6). J Steroid Biochem Mol Biol 138:90–99
12. Grube M, Kock K, Karner S, Reuther S, Ritter CA, Jedlitschky G, Kroemer HK (2006) Modification of OATP2B1-mediated transport by steroid hormones. Mol Pharmacol 70:1735–1741
13. Grube M, Reuther S, Meyer Zu Schwabedissen H, Kock K, Draber K, Ritter CA, Fusch C, Jedlitschky G, Kroemer HK (2007) Organic anion transporting polypeptide 2B1 and breast cancer resistance protein interact in the transepithelial transport of steroid sulfates in human placenta. Drug Metab Dispos 35:30–35
14. +/bile acid cotransporter. J Clin Investig 93:1326–1331
15. Hagos Y, Stein D, Ugele B, Burckhardt G, Bahn A (2007) Human renal organic anion transporter 4 operates as an asymmetric urate transporter. J Am Soc Nephrol 18:430–439
16. Hilakivi-Clarke L, Andrade JE, Helferich W (2010) Is soy consumption good or bad for the breast? J Nutr 140:2326S–2334S
17. Hosoda K, Furuta T, Ishii K (2011) Metabolism and disposition of isoflavone conjugated metabolites in humans after ingestion of kinako. Drug Metab Dispos 39:1762–1767
18. Imai Y, Tsukahara S, Asada S, Sugimoto Y (2004) Phytoestrogens/flavonoids reverse breast cancer resistance protein/ABCG2-mediated multidrug resistance. Cancer Res 64:4346–4352
19. Kijkuokool P, Parhar IS, Malaivijitnond S (2006) Genistein enhances N-nitrosomethylurea-induced rat mammary tumorigenesis. Cancer Lett 242:53–59
20. Kinjo J, Tsuchihashi R, Morito K, Hirose T, Aomori T, Nagao T, Okabe H, Nohara T, Masamune Y (2004) Interactions of phytoestrogens with estrogen receptors a and b (III). Estrogenic activities of soy isoflavone aglycones and their metabolites isolated from human urine. Biol Pharm Bull 27:185–188
21. Kobayashi D, Nozawa T, Imai K, Nezu J, Tsuji A, 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
22. Koenen A, Kock K, Keiser M, Siegmund W, Kroemer HK, Grube M (2012) Steroid hormones specifically modify the activity of organic anion transporting polypeptides 2852. Eur J Pharm Sci 47:774–780
23. Kramer W, Stengelin S, Baringhaus KH, Enhsen A, Heuer H, Becker W, Corsiero D, Girbig F, Noll R, Weyland C (1999) Substrate specificity of the ileal and the hepatic Na(+)/bile acid cotransporters of the rabbit. I. Transport studies with membrane vesicles and cell lines expressing the cloned transporters. J Lipid Res 40:1604–1617
24. Kullak-Ublick GA, Ismair MG, Stieger B, Landmann L, Huber R, Pizzagalli F, Fattinger K, Meier PJ, 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
25. Lang K, Wagner C, Haddad G, Burnekova O, Geibel J (2003) Intracellular pH activates membrane-bound Na(+)/H(+) exchanger and vacuolar H(+)-ATPase in human embryonic kidney (HEK) cells. Cell Physiol Biochem 13:257–262
26. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
27. Magee PJ, Rowland I (2012) Soy products in the management of breast cancer. Curr Opin Clin Nutr Metab Care 15:586–591
28. Meier PJ, Stieger B (2002) Bile salt transporters. Annu Rev Physiol 64:635–661
29. Mortensen A, Kulling SE, Schwartz H, Rowland I, Ruefer CE, Rimbach G, Cassidy A, Magee P, Millar J, Hall WL, Birkved FK, Sorensen IK, Sontag G (2009) Analytical and compositional aspects of isoflavones in food and their biological effects. Mol Nutr Food Res 53:S266–S309
30. Nishimura M, Naito S (2005) Tissue-specific mRNA expression profiles of human ATP-binding cassette and solute carrier transporter superfamilies. Drug Metab Pharmacokinet 20:452–477
31. Pasqualini JR, Chetrite GS (2005) Recent insight on the control of enzymes involved in estrogen formation and transformation in human breast cancer. J Steroid Biochem Mol Biol 93:221–236
32. Pizzagalli F, Varga Z, Huber RD, Folkers G, Meier PJ, St-Pierre MV (2003) Identification of steroid sulfate transport processes in the human mammary gland. J Clin Endocrinol Metab 88:3902–3912
33. Pugazhendhi D, Watson KA, Mills S, Botting N, Pope GS, Darbre PD (2008) Effect of sulphation on the oestrogen agonist activity of the phytoestrogens genistein and daidzein in MCF-7 human breast cancer cells. J Endocrinol 197:503–515
34. Reed MJ, Purohit A, Woo LW, Newman SP, Potter BV (2005) Steroid sulfatase: molecular biology, regulation, and inhibition. Endocr Rev 26:171–202
35. Ritchie MR, Cummings JH, Morton MS, Steel CM, Bolton-Smith C, Riches AC (2006) A newly constructed and validated isoflavone database for the assessment of total genistein and daidzein intake. Br J Nutr 95:204–213
36. Roth M, Obaidat A, 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
37. Rüfer CE, Bub A, Moseneder J, Winterhalter P, Sturtz M, Kulling SE (2008) Pharmacokinetics of the soybean isoflavone daidzein in its aglycone and glucoside form: a randomized, double-blind, crossover study. Am J Clin Nutr 87:1314–1323
38. Santner SJ, Feil PD, Santen RJ (1984) In situ estrogen production via the estrone sulfatase pathway in breast tumors: relative importance versus the aromatase pathway. J Clin Endocrinol Metab 59:29–33
39. Schroeder A, Eckhardt U, Stieger B, Tynes R, Schteingart CD, Hofmann AF, Meier PJ, Hagenbuch B (1998) Substrate specificity of the rat liver Na(+)-bile salt cotransporter in Xenopus laevis oocytes and in CHO cells. Am J Physiol 274:G370–G375
40. Schweigmann H, Sanchez-Guijo A, Ugele B, Hartmann K, Hartmann MF, Bergmann M, Pfarrer C, Doring B, Wudy SA, Petzinger E, Geyer J, Grosser G (2014) Transport of the placental estriol precursor 16alpha-hydroxy-dehydroepiandrosterone sulfate (16alpha-OH-DHEAS) by stably transfected OAT4-, SOAT-, and NTCP-HEK293 cells. J Steroid Biochem Mol Biol 143:259–265. doi:10.1016/j.jsbmb.2014.03.013
41. Selcer KW, Kabler H, Sarap J, Xiao Z, Li PK (2002) Inhibition of steryl sulfatase activity in LNCaP human prostate cancer cells. Steroids 67:821–826
42. Sfakianos J, Coward L, Kirk M, Barnes S (1997) Intestinal uptake and biliary excretion of the isoflavone genistein in rats. J Nutr 127:1260–1268
43. Shneider BL, Dawson PA, Christie DM, Hardikar W, Wong MH, Suchy FJ (1995) Cloning and molecular characterization of the ontogeny of a rat ileal sodium-dependent bile acid transporter. J Clin Investig 95:745–754
44. Soukup ST, Al-Maharik N, Botting N, Kulling SE (2014) Quantification of soy isoflavones and their conjugative metabolites in plasma and urine: an automated and validated UHPLC-MS/MS method for use in large-scale studies. Anal Bioanal Chem 406:6007–6020
45. St-Pierre MV, Hagenbuch B, Ugele B, Meier PJ, Stallmach T (2002) Characterization of an organic anion-transporting polypeptide (OATP-B) in human placenta. J Clin Endocrinol Metab 87:1856–1863
46. Tamai I, Nezu J, Uchino H, Sai Y, Oku A, Shimane M, 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
47. Trauner M, Boyer JL (2003) Bile salt transporters: molecular characterization, function, and regulation. Physiol Rev 83:633–671
48. Ugele B, Bahn A, Rex-Haffner M (2008) 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 111:1–6
49. Wietrzyk J, Mazurkiewicz M, Madej J, Dzimira S, Grynkiewicz G, Radzikowski C, Opolski A (2004) Genistein alone or combined with cyclophosphamide may stimulate 16/C transplantable mouse mammary cancer growth. Med Sci Monitor 10:BR414–BR419
50. Wong MH, Oelkers P, Dawson PA (1995) Identification of a mutation in the ileal sodium-dependent bile acid transporter gene that abolishes transport activity. J Biol Chem 270:27228–27234
51. Wong CC, Botting NP, Orfila C, Al-Maharik N, Williamson G (2011) Flavonoid conjugates interact with organic anion transporters (OATs) and attenuate cytotoxicity of adefovir mediated by organic anion transporter 1 (OAT1/SLC22A6). Biochem Pharmacol 81:942–949
52. Zamora-Ros R, Ferrari P, González C, Tjønneland A, Olsen A, Bredsdorff L, Overvad K, Touillaud M, Perquier F, Fagherazzi G, Lukanova A, Tikk K, Aleksandrova K, Boeing H, Trichopoulou A, Trichopoulos D, Dilis V, Masala G, Sieri S, Mattiello A, Tumino R, Ricceri F, Bueno-de-Mesquita HB, Peeters PM, Weiderpass E, Skeie G, Engeset D, Menéndez V, Travier N, Molina-Montes E, Amiano P, Chirlaque M-D, Barricarte A, Wallström P, Sonestedt E, Sund M, Landberg R, Khaw K-T, Wareham N, Travis R, Scalbert A, Ward H, Riboli E, Romieu I (2013) Dietary flavonoid and lignan intake and breast cancer risk according to menopause and hormone receptor status in the European Prospective Investigation into Cancer and Nutrition (EPIC) Study. Breast Cancer Res Treat 139:163–176
53. Zhang Y, Kang H, Li B, Zhang R (2012) Positive effects of soy isoflavone food on survival of breast cancer patients in China. Asian Pac J Cancer Prev 13:479–482