Kidney transplantation down-regulates expression of organic cation transporters, which translocate β-blockers and fluoroquinolones

Molecular Pharmaceutics

Volumn 10, Issue 6, 2013, Pages 2370-2380

  Ciarimboli, Giuliano ^a   Schröter, Rita ^a   Neugebauer, Ute ^a   Vollenbröker, Beate ^a   Gabriëls, Gert ^a   Brzica, Hrvoje ^a,b   Sabolić, Ivan ^a,b   Pietig, Gesine ^a   Pavenstädt, Hermann ^a   Schlatter, Eberhard ^a   Edemir, Bayram ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b INSTITUTE FOR MEDICAL RESEARCH AND OCCUPATIONAL HEALTH   (Croatia)

Author keywords

acute rejection; drugs; kidney transplantation; organic cation transporters

Indexed keywords

ATENOLOL; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CYCLOSPORIN A; NORFLOXACIN; OFLOXACIN; ORGANIC CATION TRANSPORTER 1; ORGANIC CATION TRANSPORTER 2; PINDOLOL; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; DOWN REGULATION; DRUG TRANSPORT; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY ALLOGRAFT; KIDNEY GRAFT REJECTION; KIDNEY TRANSPLANTATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION;

ADRENERGIC BETA-ANTAGONISTS; ANIMALS; BLOTTING, WESTERN; CELL LINE; CYCLOSPORINE; FLUOROQUINOLONES; HUMANS; IMMUNOHISTOCHEMISTRY; KIDNEY TRANSPLANTATION; KIDNEY TUBULES, PROXIMAL; MALE; ORGANIC CATION TRANSPORT PROTEINS; ORGANIC CATION TRANSPORTER 1; RATS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84878623788     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp4000234     Document Type: Article

References (57)

1. Chatzikyrkou, C.; Menne, J.; Gwinner, W.; Schmidt, B. M.; Lehner, F.; Blume, C.; Schwarz, A.; Haller, H.; Schiffer, M. Pathogenesis and management of hypertension after kidney transplantation J. Hypertens. 2011, 29, 2283-2294
2. Manitpisitkul, W.; McCann, E.; Lee, S.; Weir, M. R. Drug interactions in transplant patients: what everyone should know Curr. Opin. Nephrol. Hypertens. 2009, 18, 404-411
3. Naud, J.; Nolin, T. D.; Leblond, F. A.; Pichette, V. Current understanding of drug disposition in kidney disease J. Clin. Pharmacol. 2012, 52, 10S-22S
4. Neuhoff, S.; Ungell, A. L.; Zamora, I.; Artursson, P. pH-dependent bidirectional transport of weakly basic drugs across Caco-2 monolayers: implications for drug-drug interactions Pharm. Res. 2003, 20, 1141-1148
5. Ciarimboli, G. Organic cation transporters Xenobiotica 2008, 38, 936-971
6. Alnouti, Y.; Petrick, J. S.; Klaassen, C. D. Tissue distribution and ontogeny of organic cation transporters in mice Drug Metab. Dispos. 2006, 34, 477-482
7. Holle, S. K.; Ciarimboli, G.; Edemir, B.; Neugebauer, U.; Pavenstadt, H.; Schlatter, E. Properties and regulation of organic cation transport in freshly isolated mouse proximal tubules analyzed with a fluorescence reader-based method Pflugers Arch. 2011, 462, 359-369
8. Gründemann, D.; Gorboulev, V.; Gambaryan, S.; Veyhl, M.; Koepsell, H. Drug excretion mediated by a new prototype of polyspecific transporter Nature 1994, 372, 549-552
9. Karbach, U.; Kricke, J.; Meyer-Wentrup, F.; Gorboulev, V.; Volk, C.; Loffing-Cueni, D.; Kaissling, B.; Bachmann, S.; Koepsell, H. Localization of organic cation transporters OCT1 and OCT2 in rat kidney Am. J. Physiol.: Renal Physiol. 2000, 279, F679-F687
10. Gorboulev, V.; Ulzheimer, J. C.; Akhoundova, A.; Ulzheimer-Teuber, I.; Karbach, U.; Quester, S.; Baumann, C.; Lang, F.; Busch, A. E.; Koepsell, H. Cloning and characterization of two human polyspecific organic cation transporters DNA Cell Biol. 1997, 16, 871-881
11. Motohashi, H.; Sakurai, Y.; Saito, H.; Masuda, S.; Urakami, Y.; Goto, M.; Fukatsu, A.; Ogawa, O.; Inui, K. K. Gene expression levels and immunolocalization of organic ion transporters in the human kidney J. Am. Soc. Nephrol. 2002, 13, 866-874
12. Velic, A.; Hirsch, J. R.; Bartel, J.; Thomas, R.; Schroter, R.; Stegemann, H.; Edemir, B.; August, C.; Schlatter, E.; Gabriels, G. Renal transplantation modulates expression and function of receptors and transporters of rat proximal tubules J. Am. Soc. Nephrol. 2004, 15, 967-977
13. Gabriels, G.; August, C.; Grisk, O.; Steinmetz, M.; Kosch, M.; Rahn, K. H.; Schlatter, E. Impact of renal transplantation on small vessel reactivity Transplantation 2003, 75, 689-697
14. Livak, K. J.; Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 2001, 25, 402-408
15. Brzica, H.; Breljak, D.; Vrhovac, I.; Sabolic, I. Role of microwave heating in antigen retrieval in cryosections of formalin-fixed tissues. In Microwave Heating; Chandra, U., Ed.; InTech, Open Access Publisher: New York, 2011; pp 41-62.
16. Busch, A. E.; Quester, S.; Ulzheimer, J. C.; Waldegger, S.; Gorboulev, V.; Arndt, P.; Lang, F.; Koepsell, H. Electrogenic properties and substrate specificity of the polyspecific rat cation transporter rOCT1 J. Biol. Chem. 1996, 271, 32599-32604
17. Busch, A. E.; Quester, S.; Ulzheimer, J. C.; Gorboulev, V.; Akhoundova, A.; Waldegger, S.; Lang, F.; Koepsell, H. Monoamine neurotransmitter transport mediated by the polyspecific cation transporter rOCT1 FEBS Lett. 1996, 395, 153-156
18. Arndt, P.; Volk, C.; Gorboulev, V.; Budiman, T.; Popp, C.; Ulzheimer-Teuber, I.; Akhoundova, A.; Koppatz, S.; Bamberg, E.; Nagel, G.; Koepsell, H. Interaction of cations, anions, and weak base quinine with rat renal cation transporter rOCT2 compared with rOCT1 Am. J. Physiol.: Renal Physiol. 2001, 281, F454-F468
19. Wilde, S.; Schlatter, E.; Koepsell, H.; Edemir, B.; Reuter, S.; Pavenstadt, H.; Neugebauer, U.; Schroter, R.; Brast, S.; Ciarimboli, G. Calmodulin-associated post-translational regulation of rat organic cation transporter 2 in the kidney is gender dependent Cell. Mol. Life Sci. 2009, 66, 1729-1740
20. Lee, W. K.; Reichold, M.; Edemir, B.; Ciarimboli, G.; Warth, R.; Koepsell, H.; Thévenod, F. The organic cation transporters OCT1, 2, and 3 mediate high affinity transport of the mutagenic vital dye ethidium in the kidney proximal tubule Am. J. Physiol.: Renal Physiol. 2009, 296, F1504-F1513
21. Pietig, G.; Mehrens, T.; Hirsch, J. R.; Cetinkaya, I.; Piechota, H.; Schlatter, E. Properties and regulation of organic cation transport in freshly isolated human proximal tubules J. Biol. Chem. 2001, 276, 33741-33746
22. Mehrens, T.; Lelleck, S.; Cetinkaya, I.; Knollmann, M.; Hohage, H.; Gorboulev, V.; Boknik, P.; Koepsell, H.; Schlatter, E. The affinity of the organic cation transporter rOCT1 is increased by protein kinase C-dependent phosphorylation J. Am. Soc. Nephrol. 2000, 11, 1216-1224
23. Ciarimboli, G.; Struwe, K.; Arndt, P.; Gorboulev, V.; Koepsell, H.; Schlatter, E.; Hirsch, J. R. Regulation of the human organic cation transporter hOCT1 J. Cell. Physiol. 2004, 201, 420-428
24. Biermann, J.; Lang, D.; Gorboulev, V.; Koepsell, H.; Sindic, A.; Schroter, R.; Zvirbliene, A.; Pavenstadt, H.; Schlatter, E.; Ciarimboli, G. Characterization of regulatory mechanisms and states of human organic cation transporter 2 Am. J. Physiol.: Cell. Physiol. 2006, 290, C1521-C1531
25. + and water channels in the collecting duct Am. J. Transplant. 2005, 5, 1276-1285
26. Edemir, B.; Reuter, S.; Borgulya, R.; Schroter, R.; Neugebauer, U.; Gabriels, G.; Schlatter, E. Acute rejection modulates gene expression in the collecting duct J. Am. Soc. Nephrol. 2008, 19, 538-546
27. Ciarimboli, G.; Schlatter, E. Regulation of organic cation transport Pflugers Arch. 2005, 449, 423-441
28. Sun, H.; Frassetto, L.; Benet, L. Z. Effects of renal failure on drug transport and metabolism Pharmacol. Ther. 2006, 109, 1-11
29. Ji, L.; Masuda, S.; Saito, H.; Inui, K. Down-regulation of rat organic cation transporter rOCT2 by 5/6 nephrectomy Kidney Int. 2002, 62, 514-524
30. Thomas, M. C.; Tikellis, C.; Burns, W. C.; Thallas, V.; Forbes, J. M.; Cao, Z.; Osicka, T. M.; Russo, L. M.; Jerums, G.; Ghabrial, H.; Cooper, M. E.; Kantharidis, P. Reduced tubular cation transport in diabetes: prevented by ACE inhibition Kidney Int. 2003, 63, 2152-2161
31. Heemskerk, S.; Wouterse, A. C.; Russel, F. G.; Masereeuw, R. Nitric oxide down-regulates the expression of organic cation transporters (OCT) 1 and 2 in rat kidney during endotoxemia Eur. J. Pharmacol. 2008, 584, 390-397
32. Schneider, R.; Meusel, M.; Betz, B.; Kersten, M.; Moller-Ehrlich, K.; Wanner, C.; Koepsell, H.; Sauvant, C. Nitric oxide-induced regulation of renal organic cation transport after renal ischemia-reperfusion injury Am. J. Physiol.: Renal Physiol. 2011, 301, F997-F1004
33. Wang, J. J.; Hendrich, K. S.; Jackson, E. K.; Ildstad, S. T.; Williams, D. S.; Ho, C. Perfusion quantitation in transplanted rat kidney by MRI with arterial spin labeling Kidney Int. 1998, 53, 1783-1791
34. Flechner, S. M.; Kurian, S. M.; Head, S. R.; Sharp, S. M.; Whisenant, T. C.; Zhang, J.; Chismar, J. D.; Horvath, S.; Mondala, T.; Gilmartin, T.; Cook, D. J.; Kay, S. A.; Walker, J. R.; Salomon, D. R. Kidney transplant rejection and tissue injury by gene profiling of biopsies and peripheral blood lymphocytes Am. J. Transplant. 2004, 4, 1475-1489
35. Baigent, C.; Burbury, K.; Wheeler, D. Premature cardiovascular disease in chronic renal failure Lancet 2000, 356, 147-152
36. Luke, R. G. Hypertension in renal transplant recipients Kidney Int. 1987, 31, 1024-1037
37. Opelz, G.; Wujciak, T.; Ritz, E. Association of chronic kidney graft failure with recipient blood pressure. Collaborative Transplant Study Kidney Int. 1998, 53, 217-222
38. Kasiske, B. L.; Chakkera, H. A.; Roel, J. Explained and unexplained ischemic heart disease risk after renal transplantation J. Am. Soc. Nephrol. 2000, 11, 1735-1743
39. Sarro, E.; Jacobs-Cacha, C.; Itarte, E.; Meseguer, A. A pharmacologically-based array to identify targets of cyclosporine A-induced toxicity in cultured renal proximal tubule cells Toxicol. Appl. Pharmacol. 2012, 258, 275-287
40. Colombani, P. M.; Robb, A.; Hess, A. D. Cyclosporin A binding to calmodulin: a possible site of action on T lymphocytes Science 1985, 228, 337-339
41. Ciarimboli, G.; Koepsell, H.; Iordanova, M.; Gorboulev, V.; Dürner, B.; Lang, D.; Edemir, B.; Schröter, R.; van Le, T.; Schlatter, E. Individual PKC-phosphorylation sites in organic cation transporter 1 determine substrate selectivity and transport regulation J. Am. Soc. Nephrol. 2005, 16, 1562-1570
42. Wojcicki, J.; Jaroszynska, M.; Drozdzik, M.; Pawlik, A.; Gawronska-Szklarz, B.; Sterna, R. Comparative pharmacokinetics and pharmacodynamics of propranolol and atenolol in normolipaemic and hyperlipidaemic obese subjects Biopharm. Drug Dispos. 2003, 24, 211-218
43. Jennings, G. L.; Bobik, A.; Fagan, E. T.; Korner, P. I. Pindolol pharmacokinetics in relation to time course of inhibition of exercise tachycardia Br. J. Clin. Pharmacol. 1979, 7, 245-256
44. Marier, J. F.; Ducharme, M. P.; DiMarco, M.; Di, S. M.; Morelli, G.; Tippabhotla, S. K.; Badri, N.; Rampal, A.; Monif, T. Two open-label, randomized, crossover studies assessing the bioequivalence of ofloxacin administered as immediate-and extended-release formulations in healthy subjects Clin. Ther. 2006, 28, 2070-2080
45. Al-Rashood, K.; Al-Khamis, K.; El-Sayed, Y.; Al-Bella, S.; Al-Yamani, M.; Alam, S.; Dham, R. Bioequivalence evaluation of norfloxacin 400 mg tablets (Uroxin and Noroxin) in healthy human volunteers Biopharm. Drug Dispos. 2000, 21, 175-179
46. Flouvat, B.; Decourt, S.; Aubert, P.; Potaux, L.; Domart, M.; Goupil, A.; Baglin, A. Pharmacokinetics of atenolol in patients with terminal renal failure and influence of haemodialysis Br. J. Clin. Pharmacol. 1980, 9, 379-385
47. Kirch, W.; Kohler, H.; Mutschler, E.; Schafer, M. Pharmacokinetics of atenolol in relation to renal function Eur. J. Clin. Pharmacol. 1981, 19, 65-71
48. Ohnhaus, E. E.; Heidemann, H.; Meier, J.; Maurer, G. Metabolism of pindolol in patients with renal failure Eur. J. Clin. Pharmacol. 1982, 22, 423-428
49. White, L. O.; MacGowan, A. P.; Mackay, I. G.; Reeves, D. S. The pharmacokinetics of ofloxacin, desmethyl ofloxacin and ofloxacin N -oxide in haemodialysis patients with end-stage renal failure J. Antimicrob. Chemother. 1988, 22 (Suppl C) 65-72
50. Bachmakov, I.; Glaeser, H.; Endress, B.; Morl, F.; Konig, J.; Fromm, M. F. Interaction of beta-blockers with the renal uptake transporter OCT2 Diabetes, Obes. Metab. 2009, 11, 1080-1083
51. Kaewmokul, S.; Chatsudthipong, V.; Evans, K. K.; Dantzler, W. H.; Wright, S. H. Functional mapping of rbOCT1 and rbOCT2 activity in the S2 segment of rabbit proximal tubule Am. J. Physiol.: Renal Physiol. 2003, 285, F1149-F1159
52. Foote, E. F.; Halstenson, C. E. Effects of probenecid and cimetidine on renal disposition of ofloxacin in rats Antimicrob. Agents Chemother. 1998, 42, 456-458
53. Okuda, M.; Urakami, Y.; Saito, H. I. K. Molecular mechanisms of organic cation transport in OCT2-expressing Xenopus oocytes Biochim. Biophys. Acta 1999, 1417, 224-231
54. Yano, I.; Ito, T.; Takano, M.; Inui, K. Evaluation of renal tubular secretion and reabsorption of levofloxacin in rats Pharm. Res. 1997, 14, 508-511
55. Ott, R. J.; Hui, A. C.; Wong, F. M.; Hsyu, P. H.; Giacomini, K. M. Interactions of quinidine and quinine and (+)- and (-)-pindolol with the organic cation/proton antiporter in renal brush border membrane vesicles Biochem. Pharmacol. 1991, 41, 142-145
56. Matsuo, Y.; Yano, I.; Ito, T.; Hashimoto, Y.; Inui, K. Transport of quinolone antibacterial drugs in a kidney epithelial cell line, LLC-PK1 J. Pharmacol. Exp. Ther. 1998, 287, 672-678
57. Ohta, K. Y.; Imamura, Y.; Okudaira, N.; Atsumi, R.; Inoue, K.; Yuasa, H. Functional characterization of multidrug and toxin extrusion protein 1 as a facilitative transporter for fluoroquinolones J. Pharmacol. Exp. Ther. 2009, 328, 628-634