Regulatory pathways for ATP-binding cassette transport proteins in kidney proximal tubules

AAPS Journal

Volumn 14, Issue 4, 2012, Pages 883-894

  Masereeuw, Rosalinde ^a   Russel, Frans G M ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Breast cancer resistance protein; Kidney disease; Multidrug resistance protein; P glycoprotein; Transport regulation

Indexed keywords

ABC TRANSPORTER; ALLYL SULFIDE; AMINOGLYCOSIDE ANTIBIOTIC AGENT; AROMATIC HYDROCARBON RECEPTOR; BREAST CANCER RESISTANCE PROTEIN; CISPLATIN; CLOTRIMAZOLE; CONTRAST MEDIUM; CORTISONE; CYCLOSPORIN A; DEXAMETHASONE; DOXORUBICIN; ENDOTHELIN 1; GENTAMICIN; HYDROCORTISONE; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN 4; MULTIDRUG RESISTANCE PROTEIN 5; MULTIDRUG RESISTANCE PROTEIN 6; NIFEDIPINE; PHENOBARBITAL; RIFAMPICIN; SPIRONOLACTONE; STEROID HORMONE; TRIAMCINOLONE ACETONIDE; UNINDEXED DRUG; VITAMIN K GROUP;

ACUTE KIDNEY FAILURE; CHRONIC KIDNEY FAILURE; DRUG DISPOSITION; DRUG EFFECT; DRUG EXCRETION; HORMONAL REGULATION; HUMAN; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE DAMAGE; NEPHROTOXICITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; TISSUE DISTRIBUTION; TISSUE REGENERATION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; HUMANS; KIDNEY TUBULES, PROXIMAL; PHARMACEUTICAL PREPARATIONS; SIGNAL TRANSDUCTION;

EID: 84869119273     PISSN: 15507416     EISSN: None     Source Type: Journal    
DOI: 10.1208/s12248-012-9404-z     Document Type: Review

References (100)

1. Giacomini KM, Huang SM, Tweedie DJ, Benet LZ, Brouwer KL, Chu X, et al. Membrane transporters in drug development. Nat Rev Drug Discov. 2010;9:215-36.
2. Masereeuw R, Russel FG. Therapeutic implications of renal anionic drug transporters. Pharmacol Ther. 2010;126:200-16.
3. Wu W, Dnyanmote AV, Nigam SK. Remote communication through solute carriers and ATP binding cassette drug transporter pathways: an update on the remote sensing and signaling hypothesis. Mol Pharmacol. 2011;79:795-805.
4. Moitra K, Dean M. Evolution of ABC transporters by gene duplication and their role in human disease. Biol Chem. 2011;392:29-37.
5. Schinkel AH, Mayer U, Wagenaar E, Mol CA, van Deemter L, Smit JJ, et al. Normal viability and altered pharmacokinetics in mice lacking mdr1-Type (drug-Transporting) P-glycoproteins. Proc Natl Acad Sci USA. 1997;94:4028-33.
6. Vlaming ML, van Esch A, Pala Z, Wagenaar E, van de Wetering K, van Tellingen O, et al. Abcc2 (Mrp2), Abcc3 (Mrp3), and Abcg2 (Bcrp1) are the main determinants for rapid elimination of methotrexate and its toxic metabolite 7-hydroxymethotrexate in vivo. Mol Cancer Ther. 2009;8:3350-9.
7. Chen ZS, Tiwari AK. Multidrug resistance proteins (MRPs/ABCCs) in cancer chemotherapy and genetic diseases. FEBS J. 2011;278:3226-45.
8. Russel FG, Koenderink JB, Masereeuw R. Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules. Trends Pharmacol Sci. 2008;29:200-7.
9. Thiebaut F, Tsuro 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;84:7735-8.
10. Aller SG, Yu J, Ward A, Weng Y, Chittaboina S, Zhuo R, et al. Structure of P-glycoprotein reveals a molecular basis for polyspecific drug binding. Science. 2009;323:1718-22.
11. Cascorbi I. P-glycoprotein: tissue distribution, substrates, and functional consequences of genetic variations. In: Fromm MF, Kim RB, editors. Drug transporters. Berlin: Springer; 2011. p. 261-83.
12. Huls M, Russel FG, Masereeuw R. The role of ATP binding cassette transporters in tissue defense and organ regeneration. J Pharmacol Exp Ther. 2009;328:3-9.
13. Resta-Lenert S, Smitham J, Barrett KE. Epithelial dysfunction associated with the development of colitis in conventionally housed mdr1a-/-mice. Am J Physiol Gastrointest Liver Physiol. 2005;289:G153-62.
14. Juyal G, Midha V, Amre D, Sood A, Seidman E, Thelma BK. Associations between common variants in the MDR1 (ABCB1) gene and ulcerative colitis among North Indians. Pharmacogenet Genomics. 2009;19:77-85.
15. 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;16:1501-11.
16. NaesensM, Lerut E, de Jonge H, Van Damme B, Vanrenterghem Y, Kuypers DR. Donor age and renal P-glycoprotein expression associatewith chronic histological damage in renal allografts. JAm Soc Nephrol. 2009;20:2468-80.
17. Choi HJ, Cho HY, Ro H, Lee SH, Han KH, Lee H, et al. Polymorphisms of the MDR1 and MIF genes in children with nephrotic syndrome. Pediatr Nephrol. 2011;26:1981-8.
18. Huls M, Kramers C, Levtchenko EN, Wilmer MJ, Dijkman HB, Kluijtmans LA, et al. P-glycoprotein-deficient mice have proximal tubule dysfunction but are protected against ischemic renal injury. Kidney Int. 2007;72:1233-41.
19. Wilmer MJ, Schoeber JP, van den Heuvel LP, Levtchenko EN. Cystinosis: practical tools for diagnosis and treatment. Pediatr Nephrol. 2011;26:205-15.
20. Peeters K, Wilmer MJ, Schoeber JP, Reijnders D, van den Heuvel LP, Masereeuw R, et al. Role of P-glycoprotein expression and function in cystinotic renal proximal tubular cells. Pharmaceutics. 2012;3:782-92.
21. van de Water FM, Masereeuw R, Russel FGM. Function and regulation of multidrug resistance proteins in the renal elimination of organic anions. Drug Metab Rev. 2005;37:457-85.
22. Wijnholds J, SchefferGL, van der ValkM, van der Valk P, Beijnen JH, Scheper RJ, et al. Multidrug resistance protein 1 protects the oropharyngeal mucosal layer and the testicular tubules against drug-induced damage. J Exp Med. 1998;188:797-808.
23. Masereeuw R, Notenboom S, Smeets PH, Wouterse AC, Russel FG. Impaired renal secretion of substrates for the multidrug resistance protein 2 in mutant transport-deficient (TR-) rats. J Am Soc Nephrol. 2003;14:2741-9.
24. Van Aubel RA, Smeets PH, Peters JG, Bindels RJ, Russel FG. 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. 2002;13:595-603.
25. Smeets PH, Van Aubel RA, Wouterse AC, van den Heuvel JJ, Russel FG. Contribution of multidrug resistance protein 2 (MRP2/ABCC2) to the renal excretion of p-Aminohippurate (PAH) and identification of MRP4 (ABCC4) as a novel PAH transporter. J Am Soc Nephrol. 2004;15:2828-35.
26. Kiser JJ, Aquilante CL, Anderson PL, King TM, Carten ML, Fletcher CV. Clinical and genetic determinants of intracellular tenofovir diphosphate concentrations in HIV-infected patients. J Acquir Immune Defic Syndr. 2008;47:298-303.
27. 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;19:276-88.
28. Borst P, van de Wetering K, Schlingemann R. Does the absence of ABCC6 (multidrug resistance protein 6) in patients with pseudoxanthoma elasticum prevent the liver from providing sufficient vitamin K to the periphery? Cell Cycle. 2008;7:1575-9.
29. Fulop K, Jiang Q, Wetering KV, Pomozi V, Szabo PT, Aranyi T, et al. ABCC6 does not transport vitamin K3-glutathione conjugate from the liver: relevance to pathomechanisms of pseudoxanthoma elasticum. Biochem Biophys Res Commun. 2011;415:468-71.
30. Pushpakom SP, Liptrott NJ, Rodriguez-Novoa S, Labarga P, Soriano V, Albalater M, et al. Genetic variants of ABCC10, a novel tenofovir transporter, are associated with kidney tubular dysfunction. J Infect Dis. 2011;204:145-53.
31. Huls M, Brown CD, Windass AS, Sayer R, van den Heuvel JJ, Heemskerk S, et al. The breast cancer resistance protein transporter ABCG2 is expressed in the human kidney proximal tubule apical membrane. Kidney Int. 2008;73:220-5.
32. Huls M, van den Heuvel JJ, Dijkman HB, Russel FG, Masereeuw R. ABC transporter expression profiling after ischemic reperfusion injury in mouse kidney. Kidney Int. 2006;69:2186-93.
33. Storch CH, Ehehalt R, Haefeli WE, Weiss J. Localization of the human breast cancer resistance protein (BCRP/ABCG2) in lipid rafts/caveolae and modulation of its activity by cholesterol in vitro. J Pharmacol Exp Ther. 2007;323:257-64.
34. Jonker JW, Buitelaar M, Wagenaar E, van der Valk MA, Scheffer GL, Scheper RJ, et al. The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria. Proc Natl Acad Sci USA. 2002;99:15649-54.
35. Dankers AC, Sweep FC, Pertijs JC, Verweij V, van den Heuvel JJ, Koenderink JB, et al. Localization of breast cancer resistance protein (BCRP) in endocrine organs and inhibition of its transport activity by steroid hormones. Cell Tissue Res. 2012;349:551-63.
36. Woodward OM, Kottgen A, Coresh J, Boerwinkle E, Guggino WB, Kottgen M. Identification of a urate transporter, ABCG2, with a common functional polymorphism causing gout. Proc Natl Acad Sci USA. 2009;106:10338-42.
37. Van Aubel RA, Smeets PH, van den Heuvel JJ, Russel FG. 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. 2005;288:F327-33.
38. Jeong H, Herskowitz I, Kroetz DL, Rine J. Function-Altering SNPs in the human multidrug transporter gene ABCB1 identified using a Saccharomyces-based assay. PLoS Genet. 2007;3:e39.
39. Lu H, Klaassen C. Gender differences in mRNA expression of ATP-binding cassette efflux and bile acid transporters in kidney, liver, and intestine of 5/6 nephrectomized rats. Drug Metab Dispos. 2008;36:16-23.
40. Suzuki T, Zhao YL, Nadai M, Naruhashi K, Shimizu A, Takagi K, et al. Gender-related differences in expression and function of hepatic P-glycoprotein and multidrug resistance-Associated protein (MRP2) in rats. Life Sci. 2006;79:455-61.
41. Maher JM, Cheng X, Tanaka Y, Scheffer GL, Klaassen CD. Hormonal regulation of renal multidrug resistance-Associated proteins 3 and 4 (MRP3 and MRP4) in mice. Biochem Pharmacol. 2006;71:1470-8.
42. Chen C, Klaassen CD. Rat multidrug resistance protein 4 (MRP4, Abcc4): molecular cloning, organ distribution, postnatal renal expression, and chemical inducibility. Biochem Biophys Res Commun. 2004;317:46-53.
43. Ho LL, Kench JG, Handelsman DJ, Scheffer GL, Stricker PD, Grygiel JG, et al. Androgen regulation of multidrug resistanceassociated protein 4 (MRP4/ABCC4) in prostate cancer. Prostate. 2008;68:1421-9.
44. Merino G, van Herwaarden AE, Wagenaar E, Jonker JW, Schinkel AH. Sex-dependent expression and activity of the ATP-binding cassette transporter breast cancer resistance protein (BCRP/ABCG2) in liver. Mol Pharmacol. 2005;67:1765-71.
45. Wang H, Zhou L, Gupta A, Vethanayagam RR, Zhang Y, Unadkat JD, et al. Regulation of BCRP/ABCG2 expression by progesterone and 17beta-estradiol in human placental BeWo cells. Am J Physiol Endocrinol Metab. 2006;290:E798-807.
46. Prevoo B, Miller DS, van de Water FM, Wever KE, Russel FG, Flik G, et al. Rapid, nongenomic stimulation of multidrug resistance protein 2 (Mrp2) activity by glucocorticoids in renal proximal tubule. J Pharmacol Exp Ther. 2011;338:362-71.
47. Kumar S, Allen DA, Kieswich JE, Patel NS, Harwood S, Mazzon E, et al. Dexamethasone ameliorates renal ischemiareperfusion injury. J Am Soc Nephrol. 2009;20:2412-25.
48. Lai AZ, Abella JV, Park M. Crosstalk in Met receptor oncogenesis. Trends Cell Biol. 2009;19:542-51.
49. Gafter-Gvili A, Ram R, Gafter U, Shpilberg O, Raanani P. Renal failure associated with tyrosine kinase inhibitors-case report and review of the literature. Leuk Res. 2010;34:123-7.
50. Notenboom S, Miller DS, Smits P, Russel FG, Masereeuw R. Involvement of guanylyl cyclase and cGMP in the regulation of Mrp2-mediated transport in the proximal tubule. Am J Physiol Renal Physiol. 2004;287:F33-8.
51. Heemskerk S, van Koppen A, van den Broek L, Poelen GJ, Wouterse AC, Dijkman HB, et al. Nitric oxide differentially regulates renal ATP-binding cassette transporters during endotoxemia. Pflugers Arch. 2007;454:321-34.
52. Tanaka Y, Slitt AL, Leazer TM, Maher JM, Klaassen CD. Tissue distribution and hormonal regulation of the breast cancer resistance protein (BCRP/Abcg2) in rats and mice. Biochem Biophys Res Commun. 2005;326:181-7.
53. Imai Y, Ishikawa E, Asada S, Sugimoto Y. Estrogen-mediated post transcriptional down-regulation of breast cancer resistance protein/ABCG2. Cancer Res. 2005;65:596-604.
54. Demeule M, Jodoin J, Beaulieu E, Brossard M, Beliveau R. Dexamethasone modulation of multidrug transporters in normal tissues. FEBS Lett. 1999;442:208-14.
55. Aleksunes LM, Augustine LM, Scheffer GL, Cherrington NJ, Manautou JE. Renal xenobiotic transporters are differentially expressed in mice following cisplatin treatment. Toxicology. 2008;250:82-8.
56. Masereeuw R, Terlouw SA, van Aubel RAMH, Russel FGM, Miller DS. Endothelin B receptor-mediated regulation of ATPdriven drug secretion in renal proximal tubule. Mol Pharmacol. 2000;57:59-67.
57. Takada T, Suzuki H, Gotoh Y, Sugiyama Y. Regulation of the cell surface expression of human BCRP/ABCG2 by the phosphorylation state of Akt in polarized cells. Drug Metab Dispos. 2005;33:905-9.
58. Wever KE, Masereeuw R, Miller DS, Hang XM, Flik G. Endothelin and calciotropic hormones share regulatory pathways in multidrug resistance protein 2-mediated transport. Am J Physiol Renal Physiol. 2007;292:F38-46.
59. Magnarin M, Morelli M, Rosati A, Bartoli F, Candussio L, Giraldi T, et al. Induction of proteins involved in multidrug resistance (P-glycoprotein, MRP1, MRP2, LRP) and of CYP 3A4 by rifampicin in LLC-PK1 cells. Eur J Pharmacol. 2004;483:19-28.
60. Wagner M, Halilbasic E, Marschall HU, Zollner G, Fickert P, Langner C, et al. CAR and PXR agonists stimulate hepatic bile acid and bilirubin detoxification and elimination pathways in mice. Hepatology. 2005;42:420-30.
61. Heemskerk S, Peters JG, Louisse J, Sagar S, Russel FG, Masereeuw R. Regulation of P-glycoprotein in renal proximal tubule epithelial cells by LPS and TNF-Alpha. J Biomed Biotechnol. 2010;2010:525180.
62. Thévenod F, Friedmann JM, Katsen AD, Hauser IA. Upregulation of multidrug resistance P-glycoprotein via nuclear factor-kappaB activation protects kidney proximal tubule cells from cadmium-And reactive oxygen species-induced apoptosis. J Biol Chem. 2000;275:1887-96.
63. Notenboom S, Kuik LH, Peters B, Russel FGM, Masereeuw R. Up-regulation of the mulddrug resistance transporter 2 (MRP2) in renal proximal tubule cells by gentamicin. N Schmied Arch Pharmacol. 2005;371:R8.
64. Aleksunes LM, Goedken MJ, Rockwell CE, Thomale J, Manautou JE, Klaassen CD. Transcriptional regulation of renal cytoprotective genes by Nrf2 and its potential use as a therapeutic target to mitigate cisplatin-induced nephrotoxicity. J Pharmacol Exp Ther. 2010;335:2-12.
65. Laouari D, Yang R, Veau C, Blanke I, Friedlander G. Two apical multidrug transporters, P-gp and MRP2, are differently altered in chronic renal failure. Am J Physiol. 2001;280:F636-45.
66. Pei QL, Kobayashi Y, Tanaka Y, Taguchi Y, Higuchi K, Kaito M, et al. Increased expression of multidrug resistance-Associated protein 1 (MRP1) in hepatocyte basolateral membrane and renal tubular epithelia after bile duct ligation in rats. Hepatol Res. 2002;22:58-64.
67. Tanaka Y, Kobayashi Y, Gabazza EC, Higuchi K, Kamisako T, Kuroda M, et al. Increased renal expression of bilirubin glucuronide transporters in a rat model of obstructive jaundice. Am J Physiol Gastrointest Liver Physiol. 2002;282:G656-62.
68. Denk GU, Soroka CJ, Takeyama Y, Chen WS, Schuetz JD, Boyer JL. Multidrug resistance-Associated protein 4 is upregulated in liver but down-regulated in kidney in obstructive cholestasis in the rat. J Hepatol. 2004;40:585-91.
69. Wagner M, Fickert P, Zollner G, Fuchsbichler A, Silbert D, Tsybrovskyy O, et al. Role of farnesoid X receptor in determining hepatic ABC transporter expression and liver injury in bile ductligated mice. Gastroenterology. 2003;125:825-38.
70. Zollner G, Fickert P, Fuchsbichler A, Silbert D, Wagner M, Arbeiter S, et al. Role of nuclear bile acid receptor, FXR, in adaptive ABC transporter regulation by cholic and ursodeoxycholic acid in mouse liver, kidney and intestine. J Hepatol. 2003;39:480-8.
71. Terlouw SA, Masereeuw R, Russel FG. Modulatory effects of hormones, drugs, and toxic events on renal organic anion transport. Biochem Pharmacol. 2003;65:1393-405.
72. Notenboom S, Wouterse AC, Peters B, Kuik LH, Heemskerk S, Russel FG, et al. Increased apical insertion of the multidrug resistance protein 2 (MRP2/ABCC2) in renal proximal tubules following gentamicin exposure. J Pharmacol Exp Ther. 2006;318:1194-202.
73. Wang H, Wu X, Hudkins K, Mikheev A, Zhang H, Gupta A, et al. Expression of the breast cancer resistance protein (Bcrp1/Abcg2) in tissues from pregnant mice: effects of pregnancy and correlations with nuclear receptors. Am J Physiol Endocrinol Metab. 2006;291:E1295-304.
74. Xu S, Weerachayaphorn J, Cai SY, Soroka CJ, Boyer JL. Aryl hydrocarbon receptor and NF-E2-related factor 2 are key regulators of human MRP4 expression. Am J Physiol Gastrointest Liver Physiol. 2010;299:G126-35.
75. Beischlag TV, Luis MJ, Hollingshead BD, Perdew GH. The aryl hydrocarbon receptor complex and the control of gene expression. Crit Rev Eukaryot Gene Expr. 2008;18:207-50.
76. Mahringer A, Seymour A, Miller DS, Fricker G. Aryl hydrocarbon receptor-dependent regulation of the ABC transporters in kidney tubules from killifish (Fundulus heteroclitus). MDIBL Bulletin. 2009;48:102.
77. Flaveny CA, Murray IA, Perdew GH. Differential gene regulation by the human and mouse aryl hydrocarbon receptor. Toxicol Sci. 2010;114:217-25.
78. Tan KP, Wang B, Yang M, Boutros PC, Macaulay J, Xu H, et al. Aryl hydrocarbon receptor is a transcriptional activator of the human breast cancer resistance protein (BCRP/ABCG2). Mol Pharmacol. 2010;78:175-85.
79. Ma Q, Kinneer K, Bi Y, Chan JY, Kan YW. Induction of murine NAD(P)H:quinone oxidoreductase by 2,3,7,8-Tetrachlorodibenzo-p-dioxin requires the CNC (cap 'n' collar) basic leucine zipper transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2): cross-interaction between AhR (aryl hydrocarbon receptor) and Nrf2 signal transduction. Biochem J. 2004;377:205-13.
80. Hartmann G, Cheung AK, Piquette-Miller M. Inflammatory cytokines, but not bile acids, regulate expression of murine hepatic anion transporters in endotoxemia. J Pharmacol Exp Ther. 2002;303:273-81.
81. Liang M, Knox FG. Production and functional roles of nitric oxide in the proximal tubule. Am J Physiol. 2000;278: R1117-24.
82. Heemskerk S, Pickkers P, Bouw MPWJ, Draisma A, van der Hoeven JG, Peters WHM, et al. Upregulation of renal inducible nitric oxide synthase during human endotoxemia and sepsis is associated with proximal tubule injury. Clin J Am Soc Nephrol. 2006;1:853-62.
83. Tanaka Y, Chen C, Maher JM, Klaassen CD. Ischemiareperfusion of rat livers decreases liver and increases kidney multidrug resistance associated protein 2 (Mrp2). Toxicol Sci. 2008;101:171-8.
84. Vanholder R, Baurmeister U, Brunet P, Cohen G, Glorieux G, Jankowski J. A bench to bedside view of uremic toxins. J Am Soc Nephrol. 2008;19:863-70.
85. Lee CT, Kuo CC, Chen YM, Hsu CY, Lee WC, Tsai YC, et al. Factors associated with blood concentrations of indoxyl sulfate and p-cresol in patients undergoing peritoneal dialysis. Perit Dial Int. 2010;30:456-63.
86. Van Aubel RA, Smeets PH, van den Heuvel JJ, Russel FG. 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. 2005;288:F327-33.
87. Mutsaers HA, van den Heuvel LP, Ringens LH, Dankers AC, Russel FG, Wetzels JF, et al. Uremic toxins inhibit transport by breast cancer resistance protein andmultidrug resistance protein 4 at clinically relevant concentrations. PLoS One. 2011;6:e18438.
88. Huls M, Schoeber JP, Verfaillie CM, Luttun A, Ulloa-Montoya F, Menke AL, et al. Deficiency of either P-glycoprotein or breast cancer resistance protein protect against acute kidney injury. Cell Transplant. 2010;19:1195-208.
89. Zhang Z, Wu JY, Hait WN, Yang JM. Regulation of the stability of P-glycoprotein by ubiquitination. Mol Pharmacol. 2004;66:395-403.
90. Wakabayashi-Nakao K, Tamura A, Furukawa T, Nakagawa H, Ishikawa T. Quality control of human ABCG2 protein in the endoplasmic reticulum: ubiquitination and proteasomal degradation. Adv Drug Deliv Rev. 2009;61:66-72.
91. Hayashi H, Naoi S, Nakagawa T, Nishikawa T, Fukuda H, Imajoh-Ohmi S, et al. Sorting Nexin 27 interacts with multidrug resistance-Associated protein 4 (MRP4) and mediates internalization of MRP4. J Biol Chem. 2012;287:15054-65.
92. Hayashi H, Mizuno T, Horikawa R, Nagasaka H, Yabuki T, Takikawa H, et al. 4-phenylbutyrate modulates ubiquitination of hepatocanalicular MRP2 and reduces serum total bilirubin concentration. J Hepatol. 2012;56:1136-44.
93. Klaassen CD, Lu H, Cui JY. Epigenetic regulation of drug processing genes. Toxicol Mech Methods. 2011;21:312-24.
94. Koturbash I, Beland FA, Pogribny IP. Role of microRNAs in the regulation of drug metabolizing and transporting genes and the response to environmental toxicants. Expert Opin Drug Metab Toxicol. 2012;8:597-606.
95. Ho J, Kreidberg JA. The long and short of microRNAs in the kidney. J Am Soc Nephrol. 2012;23:400-4.
96. Haenisch S, Laechelt S, BruckmuellerH,Werk A, NoackA, Bruhn O, et al. Down-regulation of ATP-binding cassette C2 protein expression inHepG2 cells after rifampicin treatment ismediated by microRNA-379. Mol Pharmacol. 2011;80:314-20.
97. Turrini E, Haenisch S, Laechelt S, Diewock T, Bruhn O, Cascorbi I. MicroRNA profiling in K-562 cells under imatinib treatment: influence of miR-212 and miR-328 on ABCG2 expression. Pharmacogenet Genomics. 2012;22:198-205.
98. Chandrasekaran K, Karolina DS, Sepramaniam S, Armugam A, Wintour EM, Bertram JF, et al. Role of microRNAs in kidney homeostasis and disease. Kidney Int. 2012;81:617-27.
99. Lorenzen JM, Thum T. Circulating and urinary microRNAs in kidney disease. Clin J Am Soc Nephrol. 2012;(in press)
100. Krutzfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature. 2005;438:685-9.