Transgenic expression of the human MRP2 transporter reduces cisplatin accumulation and nephrotoxicity in Mrp2-Null mice

American Journal of Pathology

Volumn 184, Issue 5, 2014, Pages 1299-1308

  Wen, Xia ^a   Buckley, Brian ^b   McCandlish, Elizabeth ^b   Goedken, Michael J ^a   Syed, Samira ^a   Pelis, Ryan ^c   Manautou, José E ^d   Aleksunes, Lauren M ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c DALHOUSIE UNIVERSITY   (Canada)

^d UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALANINE AMINOTRANSFERASE; BREAST CANCER RESISTANCE PROTEIN; CISPLATIN; CREATININE; DNA; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE TRANSFERASE; HEME OXYGENASE 1; KIDNEY INJURY MOLECULE 1; METALLOTHIONEIN I; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 4; MULTIDRUG RESISTANCE PROTEIN 1; ORGANIC CATION TRANSPORTER 1; ORGANIC CATION TRANSPORTER 2; ORGANIC CATION TRANSPORTER 3; PLATINUM; RECOMBINANT PROTEIN; UREA; BIOLOGICAL MARKER; GLUTATHIONE; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE-ASSOCIATED PROTEIN 2; PROTEIN BINDING;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; CREATININE BLOOD LEVEL; CYTOSOLIC FRACTION; HUMAN; KIDNEY; KIDNEY INJURY; KIDNEY PROXIMAL TUBULE; LIVER; LIVER INJURY; MALE; MEMBRANE VESICLE; MOUSE; NEPHROTOXICITY; NONHUMAN; PLASMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; TOXICITY TESTING; UREA NITROGEN BLOOD LEVEL; WILD TYPE; ANIMAL; BIOLOGICAL MODEL; DEFICIENCY; DRUG EFFECTS; METABOLISM; PATHOLOGY; SF9 CELL LINE; TRANSGENIC MOUSE; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL MARKERS; BIOLOGICAL TRANSPORT; CISPLATIN; GLUTATHIONE; HUMANS; KIDNEY; LIVER; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PLATINUM; PROTEIN BINDING; SF9 CELLS;

EID: 84899538875     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2014.01.025     Document Type: Article

References (43)

1. S.S. Shord, D.M. Thompson, G.A. Krempl, and M.H. Hanigan Effect of concurrent medications on cisplatin-induced nephrotoxicity in patients with head and neck cancer Anticancer Drugs 17 2006 207 215
2. G. Ciarimboli, T. Ludwig, D. Lang, H. Pavenstadt, H. Koepsell, H.J. Piechota, J. Haier, U. Jaehde, J. Zisowsky, and E. Schlatter Cisplatin nephrotoxicity is critically mediated via the human organic cation transporter 2 Am J Pathol 167 2005 1477 1484
3. G. Ciarimboli, D. Deuster, A. Knief, M. Sperling, M. Holtkamp, B. Edemir, H. Pavenstadt, C. Lanvers-Kaminsky, A. am Zehnhoff-Dinnesen, A.H. Schinkel, H. Koepsell, H. Jurgens, and E. Schlatter Organic cation transporter 2 mediates cisplatin-induced oto- and nephrotoxicity and is a target for protective interventions Am J Pathol 176 2010 1169 1180
4. H. Burger, A. Zoumaro-Djayoon, A.W. Boersma, J. Helleman, E.M. Berns, R.H. Mathijssen, W.J. Loos, and E.A. Wiemer Differential transport of platinum compounds by the human organic cation transporter hOCT2 (hSLC22A2) Br J Pharmacol 159 2010 898 908
5. K.K. Filipski, W.J. Loos, J. Verweij, and A. Sparreboom Interaction of cisplatin with the human organic cation transporter 2 Clin Cancer Res 14 2008 3875 3880
6. K.K. Filipski, R.H. Mathijssen, T.S. Mikkelsen, A.H. Schinkel, and A. Sparreboom Contribution of organic cation transporter 2 (OCT2) to cisplatin-induced nephrotoxicity Clin Pharmacol Ther 86 2009 396 402
7. K. Iwata, K. Aizawa, S. Kamitsu, S. Jingami, E. Fukunaga, M. Yoshida, M. Yoshimura, A. Hamada, and H. Saito Effects of genetic variants in SLC22A2 organic cation transporter 2 and SLC47A1 multidrug and toxin extrusion 1 transporter on cisplatin-induced adverse events Clin Exp Nephrol 16 2012 843 851
8. N. Pabla, R.F. Murphy, K. Liu, and Z. Dong The copper transporter Ctr1 contributes to cisplatin uptake by renal tubular cells during cisplatin nephrotoxicity Am J Physiol Renal Physiol 296 2009 F505 F511
9. C.A. Larson, B.G. Blair, R. Safaei, and S.B. Howell The role of the mammalian copper transporter 1 in the cellular accumulation of platinum-based drugs Mol Pharmacol 75 2009 324 330
10. H.H. Chen, and M.T. Kuo Role of glutathione in the regulation of cisplatin resistance in cancer chemotherapy Met Based Drugs 2010 2010 1 7
11. X. Lin, T. Okuda, A. Holzer, and S.B. Howell The copper transporter CTR1 regulates cisplatin uptake in Saccharomyces cerevisiae Mol Pharmacol 62 2002 1154 1159
12. S. Ishida, J. Lee, D.J. Thiele, and I. Herskowitz Uptake of the anticancer drug cisplatin mediated by the copper transporter Ctr1 in yeast and mammals Proc Natl Acad Sci U S A 99 2002 14298 14302
13. K.D. Ivy, and J.H. Kaplan A re-evaluation of the role of hCTR1, the human high-affinity copper transporter, in platinum-drug entry into human cells Mol Pharmacol 83 2013 1237 1246
14. T. Nakamura, A. Yonezawa, S. Hashimoto, T. Katsura, and K. Inui Disruption of multidrug and toxin extrusion MATE1 potentiates cisplatin-induced nephrotoxicity Biochem Pharmacol 80 2010 1762 1767
15. T. Ishikawa, and F. Ali-Osman Glutathione-associated cis- diamminedichloroplatinum(II) metabolism and ATP-dependent efflux from leukemia cells: molecular characterization of glutathione-platinum complex and its biological significance J Biol Chem 268 1993 20116 20125
16. D.M. Townsend, J.A. Marto, M. Deng, T.J. Macdonald, and M.H. Hanigan High pressure liquid chromatography and mass spectrometry characterization of the nephrotoxic biotransformation products of Cisplatin Drug Metab Dispos 31 2003 705 713
17. 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
18. T. Kawabe, Z.S. Chen, M. Wada, T. Uchiumi, M. Ono, S. Akiyama, and M. Kuwano Enhanced transport of anticancer agents and leukotriene C4 by the human canalicular multispecific organic anion transporter (cMOAT/MRP2) FEBS Lett 456 1999 327 331
19. A.D. Guminski, R.L. Balleine, Y.E. Chiew, L.R. Webster, M. Tapner, G.C. Farrell, P.R. Harnett, and A. Defazio MRP2 (ABCC2) and cisplatin sensitivity in hepatocytes and human ovarian carcinoma Gynecol Oncol 100 2006 239 246
20. J.E. Manautou, V.M. Silva, G.E. Hennig, and H.E. Whiteley Repeated dosing with the peroxisome proliferator clofibrate decreases the toxicity of model hepatotoxic agents in male mice Toxicology 127 1998 1 10
21. D.P. Hartley, and C.D. Klaassen Detection of chemical-induced differential expression of rat hepatic cytochrome P450 mRNA transcripts using branched DNA signal amplification technology Drug Metab Dispos 28 2000 608 616
22. R. Xie, W. Johnson, L. Rodriguez, M. Gounder, G.S. Hall, and B. Buckley A study of the interactions between carboplatin and blood plasma proteins using size exclusion chromatography coupled to inductively coupled plasma mass spectrometry Anal Bioanal Chem 387 2007 2815 2822
23. L.M. Aleksunes, A.L. Slitt, J.M. Maher, L.M. Augustine, M.J. Goedken, J.Y. Chan, N.J. Cherrington, C.D. Klaassen, and J.E. Manautou Induction of Mrp3 and Mrp4 transporters during acetaminophen hepatotoxicity is dependent on Nrf2 Toxicol Appl Pharmacol 226 2008 74 83
24. H. Kidron, G. Wissel, N. Manevski, M. Hakli, R.A. Ketola, M. Finel, M. Yliperttula, H. Xhaard, and A. Urtti Impact of probe compound in MRP2 vesicular transport assays Eur J Pharm Sci 46 2012 100 105
25. C. Lechner, V. Reichel, U. Moenning, A. Reichel, and G. Fricker Development of a fluorescence-based assay for drug interactions with human Multidrug Resistance Related Protein (MRP2; ABCC2) in MDCKII-MRP2 membrane vesicles Eur J Pharm Biopharm 75 2010 284 290
26. W.R. Schelman, T.A. Mohammed, A.M. Traynor, J.M. Kolesar, R.M. Marnocha, J. Eickhoff, M. Keppen, D.B. Alberti, G. Wilding, N. Takebe, and G. Liu A phase I study of AT-101 with cisplatin and etoposide in patients with advanced solid tumors with an expanded cohort in extensive-stage small cell lung cancer Invest New Drugs 32 2014 295 302
27. Y. Alnouti, J.S. Petrick, and C.D. Klaassen Tissue distribution and ontogeny of organic cation transporters in mice Drug Metab Dispos 34 2006 477 482
28. X.Y. Chu, J.R. Strauss, M.A. Mariano, J. Li, D.J. Newton, X. Cai, R.W. Wang, J. Yabut, D.P. Hartley, D.C. Evans, and R. Evers Characterization of mice lacking the multidrug resistance protein MRP2 (ABCC2) J Pharmacol Exp Ther 317 2006 579 589
29. M.L. Vlaming, K. Mohrmann, E. Wagenaar, D.R. de Waart, R.P. Elferink, J.S. Lagas, O. van Tellingen, L.D. Vainchtein, H. Rosing, J.H. Beijnen, J.H. Schellens, and A.H. Schinkel Carcinogen and anticancer drug transport by Mrp2 in vivo: studies using Mrp2 (Abcc2) knockout mice J Pharmacol Exp Ther 318 2006 319 327
30. N. Scheer, P. Balimane, M.D. Hayward, S. Buechel, G. Kauselmann, and C.R. Wolf Generation and characterization of a novel MRP2 humanized mouse line Drug Metab Dispos 40 2012 2212 2218
31. J.A. Sprowl, V. Gregorc, C. Lazzari, R.H. Mathijssen, W.J. Loos, and A. Sparreboom Associations between ABCC2 polymorphisms and cisplatin disposition and efficacy Clin Pharmacol Ther 91 2012 1022 1026
32. M. Yamasaki, T. Makino, T. Masuzawa, Y. Kurokawa, H. Miyata, S. Takiguchi, K. Nakajima, Y. Fujiwara, N. Matsuura, M. Mori, and Y. Doki Role of multidrug resistance protein 2 (MRP2) in chemoresistance and clinical outcome in oesophageal squamous cell carcinoma Br J Cancer 104 2011 707 713
33. P.V. Korita, T. Wakai, Y. Shirai, Y. Matsuda, J. Sakata, M. Takamura, M. Yano, A. Sanpei, Y. Aoyagi, K. Hatakeyama, and Y. Ajioka Multidrug resistance-associated protein 2 determines the efficacy of cisplatin in patients with hepatocellular carcinoma Oncol Rep 23 2010 965 972
34. D.M. Townsend, M. Deng, L. Zhang, M.G. Lapus, and M.H. Hanigan Metabolism of Cisplatin to a nephrotoxin in proximal tubule cells J Am Soc Nephrol 14 2003 1 10
35. D.M. Townsend, and M.H. Hanigan Inhibition of γ-glutamyl transpeptidase or cysteine S-conjugate β-lyase activity blocks the nephrotoxicity of cisplatin in mice J Pharmacol Exp Ther 300 2002 142 148
36. S. Jenderny, H. Lin, T. Garrett, K.D. Tew, and D.M. Townsend Protective effects of a glutathione disulfide mimetic (NOV-002) against cisplatin induced kidney toxicity Biomed Pharmacother 64 2010 73 76
37. K. Yamauchi, H. Sakurai, T. Kimura, P. Wiriyasermkul, S. Nagamori, Y. Kanai, and N. Kohno System L amino acid transporter inhibitor enhances anti-tumor activity of cisplatin in a head and neck squamous cell carcinoma cell line Cancer Lett 276 2009 95 101
38. H. Izzedine, J.S. Hulot, E. Villard, C. Goyenvalle, S. Dominguez, J. Ghosn, M.A. Valantin, P. Lechat, and A.G. Deray Association between ABCC2 gene haplotypes and tenofovir-induced proximal tubulopathy J Infect Dis 194 2006 1481 1491
39. F.A. de Jong, T.J. Scott-Horton, D.L. Kroetz, H.L. McLeod, L.E. Friberg, R.H. Mathijssen, J. Verweij, S. Marsh, and A. Sparreboom Irinotecan-induced diarrhea: functional significance of the polymorphic ABCC2 transporter protein Clin Pharmacol Ther 81 2007 42 49
40. L. Wojnowski, B. Kulle, M. Schirmer, G. Schluter, A. Schmidt, A. Rosenberger, S. Vonhof, H. Bickeboller, M.R. Toliat, E.K. Suk, M. Tzvetkov, A. Kruger, S. Seifert, M. Kloess, H. Hahn, M. Loeffler, P. Nurnberg, M. Pfreundschuh, L. Trumper, J. Brockmoller, and G. Hasenfuss NAD(P)H oxidase and multidrug resistance protein genetic polymorphisms are associated with doxorubicin-induced cardiotoxicity Circulation 112 2005 3754 3762
41. W.J. Kim, J.H. Lee, J. Yi, Y.J. Cho, K. Heo, S.H. Lee, S.W. Kim, M.K. Kim, K.H. Kim, B. In Lee, and M.G. Lee A nonsynonymous variation in MRP2/ABCC2 is associated with neurological adverse drug reactions of carbamazepine in patients with epilepsy Pharmacogenet Genomics 20 2010 249 256
42. N. Sun, X. Sun, B. Chen, H. Cheng, J. Feng, L. Cheng, and Z. Lu MRP2 and GSTP1 polymorphisms and chemotherapy response in advanced non-small cell lung cancer Cancer Chemother Pharmacol 65 2010 437 446
43. A.J. Lickteig, X. Cheng, L.M. Augustine, C.D. Klaassen, and N.J. Cherrington Tissue distribution, ontogeny and induction of the transporters Multidrug and toxin extrusion (MATE) 1 and MATE2 mRNA expression levels in mice Life Sci 83 2008 59 64