Kidney-specific deletion of multidrug resistance-related protein 2 does not aggravate acute cyclosporine A nephrotoxicity in rats

Pharmacogenetics and Genomics

Volumn 22, Issue 6, 2012, Pages 408-420

  Mähler, Nicole ^a   Freyer, Martin ^a   Kauschke, Rene ^a   Schlüter, Torsten ^a   Steinbach, Antje C ^a   Oswald, Stefan ^a   Miehe, Bärbel ^a   Krebs, Alexander ^a   Rettig, Rainer ^a   Grisk, Olaf ^a  

^a UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Cyclosporine; Kidney transplantation; Multidrug resistancerelated protein 2; Oxidative stress; PCR array

Indexed keywords

CASPASE 8; CXCL3 CHEMOKINE; CYCLIN D1; CYCLOSPORIN A; CYTOCHROME P450 4A1; CYTOCHROME P450 4A3; EPOXIDE HYDROLASE; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; HEME OXYGENASE 1; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 2; PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; GENE DELETION; GLOMERULUS FILTRATION RATE; KIDNEY; KIDNEY BLOOD FLOW; KIDNEY CORTEX; NEPHRECTOMY; NEPHROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WILD TYPE;

ANIMALS; BLOOD PRESSURE; CYCLOSPORINE; GENE DELETION; GENE EXPRESSION REGULATION; GLOMERULAR FILTRATION RATE; GLUTATHIONE DISULFIDE; HEMODYNAMICS; KIDNEY; KIDNEY CORTEX; KIDNEY DISEASES; MALE; ORGAN SPECIFICITY; P-GLYCOPROTEIN; P-GLYCOPROTEINS; POLYMERASE CHAIN REACTION; RATS; RNA, MESSENGER; SUPEROXIDES;

ANIMALIA; RATTUS;

EID: 84861179273     PISSN: 17446872     EISSN: 17446880     Source Type: Journal    
DOI: 10.1097/FPC.0b013e32834a9bfd     Document Type: Article

References (57)

1. Naesens M, Kuypers DR, Sarwal M. Calcineurin inhibitor nephrotoxicity. Clin J Am Soc Nephrol 2009; 4:481-508.
2. Diederich D, Skopec J, Diederich A, Dai FX. Cyclosporine produces endothelial dysfunction by increased production of superoxide. Hypertension 1994; 23:957-961. (Pubitemid 24180845)
3. McGrath LT, Treacy R, McClean E, Brown JH. Oxidative stress in cyclosporin and azathioprine treated renal transplant patients. Clin Chim Acta 1997; 264:1-12. (Pubitemid 27336988)
4. Zhong Z, Arteel GE, Connor HD, Yin M, Frankenberg MV, Stachlewitz RF, et al. Cyclosporin A increases hypoxia and free radical production in rat kidneys: prevention by dietary glycine. Am J Physiol 1998; 275:F595-F604.
5. Servais H, Ortiz A, Devuyst O, Denamur S, Tulkens PM, Mingeot-Leclercq MP. Renal cell apoptosis induced by nephrotoxic drugs: cellular and molecular mechanisms and potential approaches to modulation. Apoptosis 2008; 13:11-32.
6. Amudha G, Josephine A, Sudhahar V, Varalakshmi P. Protective effect of lipoic acid on oxidative and peroxidative damage in cyclosporine A-induced renal toxicity. Int Immunopharmacol 2007; 7:1442-1449. (Pubitemid 47302885)
7. Krotz F, Keller M, Derflinger S, Schmid H, Gloe T, Bassermann F, et al. Mycophenolate acid inhibits endothelial NAD(P)H oxidase activity and superoxide formation by a Rac1-dependent mechanism. Hypertension 2007; 49:201-208. (Pubitemid 46360361)
8. Djamali A, Vidyasagar A, Adulla M, Hullett D, Reese S. Nox-2 is a modulator of fibrogenesis in kidney allografts. Am J Transplant 2009; 9:74-82.
9. Klintmalm G, Sawe J, Ringden O, von Bahr C, Magnusson A. Cyclosporine plasma levels in renal transplant patients. Association with renal toxicity and allograft rejection. Transplantation 1985; 39:132-137. (Pubitemid 15158467)
10. Halloran PF, Helms LM, Kung L, Noujaim J. The temporal profile of calcineurin inhibition by cyclosporine in vivo. Transplantation 1999; 68:1356-1361.
11. Napoli KL, Wang ME, Stepkowski SM, Kahan BD. Relative tissue distributions of cyclosporine and sirolimus after concomitant peroral administration to the rat: evidence for pharmacokinetic interactions. Ther Drug Monit 1998; 20:123-133. (Pubitemid 28163193)
12. Podder H, Stepkowski SM, Napoli KL, Clark J, Verani RR, Chou TC, et al. Pharmacokinetic interactions augment toxicities of sirolimus/cyclosporine combinations. J Am Soc Nephrol 2001; 12:1059-1071. (Pubitemid 32378348)
13. Hesselink DA, van Hest RM, Mathot RA, Bonthuis F, Weimar W, de Bruin RW, et al. Cyclosporine interacts with mycophenolic acid by inhibiting the multidrug resistance-associated protein 2. Am J Transplant 2005; 5:987-994. (Pubitemid 40571246)
14. Kobayashi M, Saitoh H, Kobayashi M, Tadano K, Takahashi Y, Hirano T. Cyclosporin A, but not tacrolimus, inhibits the biliary excretion of mycophenolic acid glucuronide possibly mediated by multidrug resistanceassociated protein 2 in rats. J Pharmacol Exp Ther 2004; 309:1029-1035. (Pubitemid 38669688)
15. Anglicheau D, Pllet N, Rabant M, Marquet P, Cassinat B, Meria P, et al. Role of P-glycoprotein in cyclosporine cytotoxicity in the cyclosporine- sirolimus interaction. Kidney Int 2006; 70:1019-1025. (Pubitemid 44344071)
16. Thiebaut F, Tsuruo T, Hamada H, Gottesman MM, Pastan I,Willingham MC. Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues. Proc Natl Acad Sci USA 1987; 84:7735-7738.
17. Schaub TP, Kartenbeck J, Konig J, Spring H, Dorsam J, Staehler G, et al. Expression of the MRP2 gene-encoded conjugate export pump in human kidney proximal tubules and in renal cell carcinoma. J Am Soc Nephrol 1999; 10:1159-1169. (Pubitemid 29246980)
18. del Moral RG, Andujar M, Ramirez C, Gomez-Morales M, Masseroli M, Aguilar M, et al. Chronic cyclosporin A nephrotoxicity, P-glycoprotein overexpression, and relationships with intrarenal angiotensin II deposits. Am J Pathol 1997; 151:1705-1714. (Pubitemid 27527933)
19. Koziolek MJ, Riess R, Geiger H, Thevenod F, Hauser IA. Expression of multidrug resistance P-glycoprotein in kidney allografts from cyclosporine A-treated patients. Kidney Int 2001; 60:156-166. (Pubitemid 32587550)
20. Joy MS, Nickeleit V, Hogan SL, Thompson BD, Finn WF. Calcineurin inhibitor-induced nephrotoxicity and renal expression of P-glycoprotein. Pharmacotherapy 2005; 25:779-789. (Pubitemid 40727128)
21. Hauser IA, Schaeffeler E, Gauer S, Scheuermann EH, Wegner B, Gossmann J, et al. ABCB1 genotype of the donor but not of the recipient is a major risk factor for cyclosporine-related nephrotoxicity after renal transplantation. J Am Soc Nephrol 2005; 16:1501-1511. (Pubitemid 41716536)
22. Vitko S, Margreiter R, Weimar W, Dantal J, Kuypers D, Winkler M, et al. Three-year efficacy and safety results from a study of everolimus versus mycophenolate mofetil in de novo renal transplant patients. Am J Transplant 2005; 5:2521-2530.
23. Nies AT, Schwab M, Keppler D. Interplay of conjugating enzymes with OATP uptake transporters and ABCC/MRP efflux pumps in the elimination of drugs. Expert Opin Drug Metab Toxicol 2008; 4:545-568. (Pubitemid 351890738)
24. Van Aubel RA, Masereeuw R, Russel FG. Molecular pharmacology of renal organic anion transporters. Am J Physiol Renal Physiol 2000; 279: F216-F232.
25. Jedlitschky G, Hoffmann U, Kroemer HK. Structure and function of the MRP2 (ABCC2) protein and its role in drug disposition. Expert Opin Drug Metab Toxicol 2006; 2:351-366. (Pubitemid 46141403)
26. Grisk O, Steinbach AC, Ciecholewski S, Schluter T, Kloting I, Schmidt H, et al. Multidrug resistance-related protein 2 genotype of the donor affects kidney graft function. Pharmacogenet Genomics 2009; 19:276-288.
27. Kato R, Nishide M, Kozu C, Iwamoto A, Urashima K, Suzuki K, et al. Is cyclosporine A transport inhibited by pravastatin via multidrug resistant protein 2? Eur J Clin Pharmacol 2010; 66: 153-158.
28. Grisk O, Heukaufer M, Steinbach A, Gruska S, Rettig R. Analysis of arterial pressure regulating systems in renal post-transplantation hypertension. J Hypertens 2004; 22:199-207. (Pubitemid 38293548)
29. Schluter T, Rohsius R,Wanka H, Schmid C, Siepelmeyer A, Rettig R, et al. Amiloride lowers arterial pressure in cyp1a1ren-2 transgenic rats without affecting renal vascular function. J Hypertens 2010; 28:2267-2277.
30. Bobadilla NA, Tapia E, Jimenez F, Sanchez-Lozada LG, Santamaria J, Monjardin A, et al. Dexamethasone increases eNOS gene expression and prevents renal vasoconstriction induced by cyclosporin. Am J Physiol 1999; 277:F464-F471. (Pubitemid 29459659)
31. Cibulskyte D, Pedersen M, Hjelm-Poulsen J, Hansen HE, Madsen M, Mortensen J. The pharmacokinetics and acute renal effects of oral microemulsion ciclosporin A in normal pigs. Int Immunopharmacol 2006; 6:627-634.
32. Owens CW, Belcher RV. A colorimetric micro-method for the determination of glutathione. Biochem J 1965; 94:705-711.
33. Attar F, Keyhani E, Keyhani J. A comparative study of superoxide dismutase activity assays in Crocus sativus L. corms. Appl Biochem Micro 2006; 42:101-106.
34. Jansen PL, Peters WH, Lamers WH. Hereditary chronic conjugated hyperbilirubinemia in mutant rats caused by defective hepatic anion transport. Hepatology 1985; 5:573-579. (Pubitemid 15029725)
35. Paulusma CC, Bosma PJ, Zaman GJ, Bakker CT, Otter M, Scheffer GL, et al. Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science 1996; 271: 1126-1128. (Pubitemid 26075228)
36. Fricker G, Drewe J, Huwyler J, Gutmann H, Beglinger C. Relevance of p-glycoprotein for the enteral absorption of cyclosporin A: in vitro-in vivo correlation. Br J Pharmacol 1996; 118:1841-1847. (Pubitemid 26252682)
37. Jin M, Shimada T, Yokogawa K, Nomura M, Ishizaki J, Piao Y, et al. Sitedependent contributions of P-glycoprotein and CYP3A to cyclosporin A absorption, and effect of dexamethasone in small intestine of mice. Biochem Pharmacol 2006; 72:1042-1050. (Pubitemid 44374466)
38. Yeldandi AV, Rao MS, Reddy JK. Hydrogen peroxide generation in peroxisome proliferator-induced oncogenesis. Mutat Res 2000; 448:159-177. (Pubitemid 30139452)
39. Williams JM, Murphy S, Burke M, Roman RJ. 20-hydroxyeicosatetraeonic acid: a new target for the treatment of hypertension. J Cardiovasc Pharmacol 2010; 56:336-344.
40. Nakamura M, Imaoka S, Miura K, Tanaka E, Misawa S, Funae Y. Induction of cytochrome P450 isozymes in rat renal microsomes by cyclosporin A. Biochem Pharmacol 1994; 48:1743-1746. (Pubitemid 24339000)
41. Seki T, Ishimoto T, Sakurai T, Yasuda Y, Taniguchi K, Doi M, et al. Increased excretion of urinary 20-HETE in rats with cyclosporine-induced nephrotoxicity. J Pharmacol Sci 2005; 97:132-137. (Pubitemid 40313109)
42. Abraham NG, Cao J, Sacerdoti D, Li X, Drummond G. Heme oxygenase: the key to renal function regulation. Am J Physiol Renal Physiol 2009; 297:F1137-F1152.
43. Shin DH, Park HM, Jung KA, Choi HG, Kim JA, Kim DD, et al. The NRF2- heme oxygenase-1 system modulates cyclosporin A-induced epithelialmesenchymal transition and renal fibrosis. Free Radic Biol Med 2010; 48:1051-1063.
44. Rezzani R, Rodella L, Buffoli B, Goodman AA, Abraham NG, Lianos EA, et al. Change in renal heme oxygenase expression in cyclosporine A-induced injury. J Histochem Cytochem 2005; 53:105-112. (Pubitemid 40130125)
45. Botros FT, Laniado-Schwartzman M, Abraham NG. Regulation of cyclooxygenase- and cytochrome p450-derived eicosanoids by heme oxygenase in the rat kidney. Hypertension 2002; 39:639-644. (Pubitemid 34165198)
46. Chu FF, Doroshow JH, Esworthy RS. Expression, characterization, and tissue distribution of a new cellular selenium-dependent glutathione peroxidase, GSHPx-GI. J Biol Chem 1993; 268:2571-2576. (Pubitemid 23057880)
47. Habeos IG, Ziros PG, Chartoumpekis D, Psyrogiannis A, Kyriazopoulou V, Papavassiliou AG. Simvastatin activates Keap1/Nrf2 signaling in rat liver. J Mol Med 2008; 86:1279-1285.
48. Singh A, Rangasamy T, Thimmulappa RK, Lee H, Osburn WO, Brigelius- Flohe R, et al. Glutathione peroxidase 2, the major cigarette smoke-inducible isoform of GPX in lungs, is regulated by Nrf2. Am J Respir Cell Mol Biol 2006; 35:639-650. (Pubitemid 44901853)
49. de Haan JB, Stefanovic N, Nikolic-Paterson D, Scurr LL, Croft KD, Mori TA, et al. Kidney expression of glutathione peroxidase-1 is not protective against streptozotocin-induced diabetic nephropathy. Am J Physiol Renal Physiol 2005; 289:F544-F551. (Pubitemid 41208469)
50. Amudha G, Josephine A, Varalakshmi P. Role of lipoic acid in reducing the oxidative stress induced by cyclosporine A. Clin Chim Acta 2006; 372:134-139. (Pubitemid 44286771)
51. Reis F, Rocha-Pereira P, Teixeira de Lemos E, Parada B, Baptista S, Figueiredo A, et al. Oxidative stress in cyclosporine-induced hypertension: evidence of beneficial effects or tolerance development with nitrate therapy. Transplant Proc 2007; 39:2494-2500. (Pubitemid 47588361)
52. Taille C, El-Benna J, Lanone S, Dang MC, Ogier-Denis E, Aubier M, et al. Induction of heme oxygenase-1 inhibits NAD(P)H oxidase activity by downregulating cytochrome b558 expression via the reduction of heme availability. J Biol Chem 2004; 279:28681-28688. (Pubitemid 38900152)
53. Jette L, Beaulieu E, Leclerc JM, Beliveau R. Cyclosporin A treatment induces overexpression of P-glycoprotein in the kidney and other tissues. Am J Physiol 1996; 270:F756-F765.
54. Jackson NM, O'Connor RP, Humes HD. Interactions of cyclosporine with renal proximal tubule cells and cellular membranes. Transplantation 1988; 46:109-114.
55. Kusuhara H, Sugiyama Y. In vitro-in vivo extrapolation of transportermediated clearance in the liver and kidney. Drug Metab Pharmacokinet 2009; 24:37-52.
56. Vollrath V, Wielandt AM, Iruretagoyena M, Chianale J. Role of Nrf2 in the regulation of the Mrp2 (ABCC2) gene. Biochem J 2006; 395:599-609.
57. Jigorel E, Le Vee M, Boursier-Neyret C, Parmentier Y, Fardel O. Differential regulation of sinusoidal and canalicular hepatic drug transporter expression by xenobiotics activating drug-sensing receptors in primary human hepatocytes. Drug Metab Dispos 2006; 34:1756-1763. (Pubitemid 44427479)