Interaction of immunosuppressive drugs with human organic anion transporter (OAT) 1 and OAT3, and multidrug resistance-associated protein (MRP) 2 and MRP4

Translational Research

Volumn 162, Issue 6, 2013, Pages 398-409

  El Sheikh, Azza A K ^a   Greupink, Rick ^b   Wortelboer, Heleen M ^c   Van Den Heuvel, Jeroen J M W ^b   Schreurs, Marieke ^b   Koenderink, Jan B ^b   Masereeuw, Rosalinde ^b   Russel, Frans G M ^b  

^a Minia University   (Egypt)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c TNO   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AZATHIOPRINE; CYCLOPHOSPHAMIDE; CYCLOSPORIN; CYCLOSPORIN A; CYTARABINE; DEXAMETHASONE; HYDROCORTISONE; IMMUNOSUPPRESSIVE AGENT; MERCAPTOPURINE; MITOXANTRONE; MULTIDRUG RESISTANCE PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 4; MYCOPHENOLIC ACID; ORGANIC ANION TRANSPORTER 1; ORGANIC ANION TRANSPORTER 3; TACROLIMUS; VINBLASTINE; VINCRISTINE;

ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG PROTEIN BINDING; DRUG TRANSPORT; HUMAN; HUMAN CELL; MEMBRANE VESICLE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION;

EID: 84887992470     PISSN: 19315244     EISSN: 18781810     Source Type: Journal    
DOI: 10.1016/j.trsl.2013.08.003     Document Type: Article

References (59)

1. D. Cattaneo, S. Baldelli, and N. Perico Pharmacogenetics of immunosuppressants: progress, pitfalls and promises Am J Transplant 8 2008 1374 1383
2. U. Christians, T. Strom, and Y.L. Zhang Active drug transport of immunosuppressants: new insights for pharmacokinetics and pharmacodynamics Ther Drug Monit 28 2006 39 44
3. M. Mourad, P. Wallemacq, and M. De Meyer Biotransformation enzymes and drug transporters pharmacogenetics in relation to immunosuppressive drugs: impact on pharmacokinetics and clinical outcome Transplantation 85 2008 S19 S24
4. A.A. El-Sheikh, R. Masereeuw, and F.G. Russel Mechanisms of renal anionic drug transport Eur J Pharmacol 585 2008 245 255
5. S.H. Cha, T. Sekine, and J.I. Fukushima Identification and characterization of human organic anion transporter 3 expressing predominantly in the kidney Mol Pharmacol 59 2001 1277 1286
6. T.P. Schaub, J. Kartenbeck, and J. Konig Expression of the conjugate export pump encoded by the mrp2 gene in the apical membrane of kidney proximal tubules J Am Soc Nephrol 8 1997 1213 1221
7. R.A. Van Aubel, P.H. Smeets, J.G. Peters, R.J. Bindels, and F.G. Russel The MRP4/ABCC4 gene encodes a novel apical organic anion transporter in human kidney proximal tubules: putative efflux pump for urinary cAMP and cGMP J Am Soc Nephrol 13 2002 595 603
8. S.K. Nigam, K.T. Bush, and V. Bhatnagar Drug and toxicant handling by the OAT organic anion transporters in the kidney and other tissues Nat Clin Pract Nephrol 3 2007 443 448
9. T.M. Bosch, I. Meijerman, J.H. Beijnen, and J.H. Schellens Genetic polymorphisms of drug-metabolising enzymes and drug transporters in the chemotherapeutic treatment of cancer Clin Pharmacokinet 45 2006 253 285
10. A. Ponte-Sucre Availability and applications of ATP-binding cassette (ABC) transporter blockers Appl Microbiol Biotechnol 76 2007 279 286
11. J. Wolf, T. Stranzl, and M. Filipits Expression of resistance markers to methotrexate predicts clinical improvement in patients with rheumatoid arthritis Ann Rheum Dis 64 2005 564 568
12. H. Burger, J.A. Foekens, and M.P. Look RNA expression of breast cancer resistance protein, lung resistance-related protein, multidrug resistance-associated proteins 1 and 2, and multidrug resistance gene 1 in breast cancer: correlation with chemotherapeutic response Clin Cancer Res 9 2003 827 836
13. M.D. Norris, J. Smith, and K. Tanabe Expression of multidrug transporter MRP4/ABCC4 is a marker of poor prognosis in neuroblastoma and confers resistance to irinotecan in vitro Mol Cancer Ther 4 2005 547 553
14. A.A. El-Sheikh, J.J. van den Heuvel, J.B. Koenderink, and F.G. Russel Interaction of nonsteroidal anti-inflammatory drugs with multidrug resistance protein (MRP) 2/ABCC2- and MRP4/ABCC4-mediated methotrexate transport J Pharmacol Exp Ther 320 2007 229 235
15. R.E. Bullingham, A.J. Nicholls, and B.R. Kamm Clinical pharmacokinetics of mycophenolate mofetil Clin Pharmacokinet 34 1998 429 455
16. M. Takeda, S. Khamdang, and S. Narikawa Characterization of methotrexate transport and its drug interactions with human organic anion transporters J Pharmacol Exp Ther 302 2002 666 671
17. M. Masuda, Y. I'izuka, and M. Yamazaki Methotrexate is excreted into the bile by canalicular multispecific organic anion transporter in rats Cancer Res 57 1997 3506 3510
18. Z.S. Chen, K. Lee, and S. Walther Analysis of methotrexate and folate transport by multidrug resistance protein 4 (ABCC4): MRP4 is a component of the methotrexate efflux system Cancer Res 62 2002 3144 3150
19. C.E. Staatz, and S.E. Tett Clinical pharmacokinetics and pharmacodynamics of mycophenolate in solid organ transplant recipients Clin Pharmacokinet 46 2007 13 58
20. N.A. Wolff, B.C. Burckhardt, G. Burckhardt, M. Oellerich, and V.W. Armstrong Mycophenolic acid (MPA) and its glucuronide metabolites interact with transport systems responsible for excretion of organic anions in the basolateral membrane of the human kidney Nephrol Dial Transplant 22 2007 2497 2503
21. Y. Takekuma, H. Kakiuchi, and K. Yamazaki Difference between pharmacokinetics of mycophenolic acid (MPA) in rats and that in humans is caused by different affinities of MRP2 to a glucuronized form J Pharm Pharm Sci 10 2007 71 85
22. D.A. Hesselink, R.M. van Hest, and R.A. Mathot Cyclosporine interacts with mycophenolic acid by inhibiting the multidrug resistance-associated protein 2 Am J Transplant 5 2005 987 994
23. M. Kobayashi, H. Saitoh, M. Kobayashi, K. Tadano, Y. Takahashi, and T. Hirano Cyclosporin A, but not tacrolimus, inhibits the biliary excretion of mycophenolic acid glucuronide possibly mediated by multidrug resistance-associated protein 2 in rats J Pharmacol Exp Ther 309 2004 1029 1035
24. I.S. Westley, L.R. Brogan, R.G. Morris, A.M. Evans, and B.C. Sallustio Role of Mrp2 in the hepatic disposition of mycophenolic acid and its glucuronide metabolites: effect of cyclosporine Drug Metab Dispos 34 2006 261 266
25. N. Lloberas, J. Torras, and J.M. Cruzado Influence of MRP2 on MPA pharmacokinetics in renal transplant recipients-results of the Pharmacogenomic Substudy within the Symphony Study Nephrol Dial Transplant 26 2011 3784 3793
26. T. Fukuda, H.I. Brunner, A.C. Sagcal-Gironella, and A.A. Vinks Nonsteroidal anti-inflammatory drugs may reduce enterohepatic recirculation of mycophenolic acid in patients with childhood-onset systemic lupus erythematosus Ther Drug Monit 33 2011 658 662
27. N.W. Brown, M.M. Aw, G. Mieli-Vergani, A. Dhawan, and J.M. Tredger Mycophenolic acid and mycophenolic acid glucuronide pharmacokinetics in pediatric liver transplant recipients: effect of cyclosporine and tacrolimus comedication Ther Drug Monit 24 2002 598 606
28. H. Hohage, M. Zeh, M. Heck, U.W. Gerhardt, U. Welling, and B.M. Suwelack Differential effects of cyclosporine and tacrolimus on mycophenolate pharmacokinetics in patients with impaired kidney function Transplant Proc 37 2005 1748 1750
29. H. Kagaya, M. Miura, and S. Satoh No pharmacokinetic interactions between mycophenolic acid and tacrolimus in renal transplant recipients J Clin Pharm Ther 33 2008 193 201
30. Z.S. Chen, K. Lee, and G.D. Kruh Transport of cyclic nucleotides and estradiol 17-beta-D-glucuronide by multidrug resistance protein 4: resistance to 6-mercaptopurine and 6-thioguanine J Biol Chem 276 2001 33747 33754
31. P.R. Wielinga, G. Reid, and E.E. Challa Thiopurine metabolism and identification of the thiopurine metabolites transported by MRP4 and MRP5 overexpressed in human embryonic kidney cells Mol Pharmacol 62 2002 1321 1331
32. S. Ohtsuki, H. Asaba, and H. Takanaga Role of blood-brain barrier organic anion transporter 3 (OAT3) in the efflux of indoxyl sulfate, a uremic toxin: its involvement in neurotransmitter metabolite clearance from the brain J Neurochem 83 2002 57 66
33. K. Hosoya, A. Makihara, and Y. Tsujikawa Roles of inner blood-retinal barrier organic anion transporter 3 in the vitreous/retina-to-blood efflux transport of p-aminohippuric acid, benzylpenicillin, and 6-mercaptopurine J Pharmacol Exp Ther 329 2009 87 93
34. S. Mori, S. Ohtsuki, H. Takanaga, T. Kikkawa, Y.S. Kang, and T. Terasaki Organic anion transporter 3 is involved in the brain-to-blood efflux transport of thiopurine nucleobase analogs J Neurochem 90 2004 931 941
35. Y. Kobayashi, N. Ohshiro, A. Tsuchiya, N. Kohyama, M. Ohbayashi, and T. Yamamoto Renal transport of organic compounds mediated by mouse organic anion transporter 3 (mOat3): further substrate specificity of mOat3 Drug Metab Dispos 32 2004 479 483
36. R.A. Van Aubel, J.B. Koenderink, J.G. Peters, C.H. Van Os, and F.G. Russel Mechanisms and interaction of vinblastine and reduced glutathione transport in membrane vesicles by the rabbit multidrug resistance protein Mrp2 expressed in insect cells Mol Pharmacol 56 1999 714 719
37. C. Zimmermann, W.K. van de, S.E. van de, E. Wagenaar, C. Vens, and A.H. Schinkel Species-dependent transport and modulation properties of human and mouse multidrug resistance protein 2 (MRP2/Mrp2, ABCC2/Abcc2) Drug Metab Dispos 36 2008 631 640
38. Y. Cui, J. Konig, J.K. Buchholz, H. Spring, I. Leier, and D. Keppler Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells Mol Pharmacol 55 1999 929 937
39. J.J. van Zanden, M.A. de, and H.M. Wortelboer Reversal of in vitro cellular MRP1 and MRP2 mediated vincristine resistance by the flavonoid myricetin Biochem Pharmacol 69 2005 1657 1665
40. R.S. Huang, D.J. Murry, and D.R. Foster Role of xenobiotic efflux transporters in resistance to vincristine Biomed Pharmacother 62 2008 59 64
41. R.E. Ferguson, S.M. Jackson, and A.J. Stanley Intrinsic chemotherapy resistance to the tubulin-binding antimitotic agents in renal cell carcinoma Int J Cancer 115 2005 155 163
42. D. Steinbach, J. Friedrich, and K. Dawczynski Are MTT assays the right tool to analyze drug resistance caused by ABC-transporters in patient samples? Leuk Lymphoma 46 2005 1357 1363
43. T. Fojo, and H.M. Coley The role of efflux pumps in drug-resistant metastatic breast cancer: new insights and treatment strategies Clin Breast Cancer 7 2007 749 756
44. J. Zhang, Q. Tian, and C.S. Yung Metabolism and transport of oxazaphosphorines and the clinical implications Drug Metab Rev 37 2005 611 703
45. Q. Tian, J. Zhang, and T.M. Tan Human multidrug resistance associated protein 4 confers resistance to camptothecins Pharm Res 22 2005 1837 1853
46. J. Zhang, K.Y. Ng, and P.C. Ho Interaction of oxazaphosphorines with multidrug resistance-associated protein 4 (MRP4) AAPS J 12 2010 300 308
47. E. Beery, P. Middel, and A. Bahn Molecular evidence of organic ion transporters in the rat adrenal cortex with adrenocorticotropin-regulated zonal expression Endocrinology 144 2003 4519 4526
48. A.R. Asif, J. Steffgen, and M. Metten Presence of organic anion transporters 3 (OAT3) and 4 (OAT4) in human adrenocortical cells Pflugers Arch 450 2005 88 95
49. A. Bahn, A. Hauss, and D. Appenroth RT-PCR-based evidence for the in vivo stimulation of renal tubular p-aminohippurate (PAH) transport by triiodothyronine (T3) or dexamethasone (DEXA) in kidney tissue of immature and adult rats Exp Toxicol Pathol 54 2003 367 373
50. C. Suzuki, N. Sano, and H. Takikawa Effect of dexamethasone on biliary excretion of bile acids and organic anions in rats Hepatol Res 25 2003 48 54
51. A. Courtois, L. Payen, A. Guillouzo, and O. Fardel Up-regulation of multidrug resistance-associated protein 2 (MRP2) expression in rat hepatocytes by dexamethasone FEBS Lett 459 1999 381 385
52. R.Z. Turncliff, P.J. Meier, and K.L. Brouwer Effect of dexamethasone treatment on the expression and function of transport proteins in sandwich-cultured rat hepatocytes Drug Metab Dispos 32 2004 834 839
53. B. Prevoo, D.S. Miller, and F.M. van de Water Rapid, nongenomic stimulation of multidrug resistance protein 2 (Mrp2) activity by glucocorticoids in renal proximal tubule J Pharmacol Exp Ther 338 2011 362 371
54. N. Zelcer, M.T. Huisman, and G. Reid Evidence for two interacting ligand binding sites in human multidrug resistance protein 2 (ATP binding cassette C2) J Biol Chem 278 2003 23538 23544
55. R.A. Van Aubel, P.H. Smeets, J.J. van den Heuvel, and F.G. Russel Human organic anion transporter MRP4 (ABCC4) is an efflux pump for the purine end metabolite urate with multiple allosteric substrate binding sites Am J Physiol Renal Physiol 288 2005 F327 F333
56. C. Sauvant, H. Holzinger, and M. Gekle Modulation of the basolateral and apical step of transepithelial organic anion secretion in proximal tubular opossum kidney cells: acute effects of epidermal growth factor and mitogen-activated protein kinase J Biol Chem 276 2001 14695 14703
57. I.E. Smith, and T.J. Powles MMM (mitomycin/mitoxantrone/methotrexate): an effective new regimen in the treatment of metastatic breast cancer Oncology 50 1993 9 15
58. A. Montes, T.J. Powles, M.E. O'Brien, S.E. Ashley, J. Luckit, and J. Treleaven A toxic interaction between mitomycin C and tamoxifen causing the haemolytic uraemic syndrome Eur J Cancer 29A 1993 1854 1857
59. L. Panasci, G. Shenouda, L. Begin, M. Pollak, A. Reinke, and R. Margolese Mitomycin C and mitoxantrone chemotherapy for advanced breast cancer: efficacy with minimal gastrointestinal toxicity and alopecia Cancer Chemother Pharmacol 26 1990 457 460