Regulation of the expression of renal drug transporters in KEAP1-knockdown human tubular cells

Toxicology in Vitro

Volumn 29, Issue 5, 2015, Pages 884-892

  Jeong, Hyuk Sang ^a   Ryoo, In geun ^a   Kwak, Mi Kyoung ^a  

^a The Catholic University of Korea   (South Korea)

Author keywords

ABC transporters; KEAP1; NRF2; Proximal tubule epithelial cells; SLC transporters; Sulforaphane

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; CISPLATIN; DOXORUBICIN; FLUORESCENT DYE; HOE 33342; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN 1; SULFORAPHANE; TRANSCRIPTION FACTOR NRF2; ABC TRANSPORTER; BENZIMIDAZOLE DERIVATIVE; ISOTHIOCYANIC ACID DERIVATIVE; KEAP1 PROTEIN, HUMAN; NFE2L2 PROTEIN, HUMAN; PROPIONIC ACID DERIVATIVE; QUINOLINE DERIVATIVE; SIGNAL PEPTIDE; SULFORAFAN; VERLUKAST;

ARTICLE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; INCUBATION TIME; KIDNEY TUBULE CELL; KIDNEY TUBULE EPITHELIUM; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN STABILITY; WESTERN BLOTTING; CELL LINE; GENE SILENCING; GENETICS; METABOLISM;

ATP-BINDING CASSETTE TRANSPORTERS; BENZIMIDAZOLES; CELL LINE; CISPLATIN; DOXORUBICIN; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; ISOTHIOCYANATES; NF-E2-RELATED FACTOR 2; PROPIONATES; QUINOLINES;

EID: 84927610137     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2015.03.013     Document Type: Article

References (43)

1. Adachi T., Nakagawa H., Chung I., Hagiya Y., Hoshijima K., Noguchi N., Kuo M.T., Ishikawa T. Nrf2-dependent and -independent induction of ABC transporters ABCC1, ABCC2, and ABCG2 in HepG2 cells under oxidative stress. J. Exp. Ther. Oncol. 2007, 6:335-348.
2. Canet M.J., Merrell M.D., Harder B.G., Maher J.M., Wu T., Lickteig A.J., Jackson J.P., Zhang D.D., Yamamoto M., Cherrington N.J. Identification of a functional antioxidant response element within the eighth intron of the human ABCC3 gene. Drug. Metab. Dispos. 2014.
3. Cho H.Y., Kleeberger S.R. Nrf2 protects against airway disorders. Toxicol. Appl. Pharmacol. 2010, 244:43-56.
4. Choi B.H., Ryoo I.G., Kang H.C., Kwak M.K. The sensitivity of cancer cells to pheophorbide a-based photodynamic therapy is enhanced by Nrf2 silencing. PLoS ONE 2014, 9:e107158.
5. Durmus S., Naik J., Buil L., Wagenaar E., van Tellingen O., Schinkel A.H. In vivo disposition of doxorubicin is affected by mouse Oatp1a/1b and human OATP1A/1B transporters. Int. J. Cancer 2014, 135:1700-1710.
6. Hayashi A., Suzuki H., Itoh K., Yamamoto M., Sugiyama Y. Transcription factor Nrf2 is required for the constitutive and inducible expression of multidrug resistance-associated protein 1 in mouse embryo fibroblasts. Biochem. Biophys. Res. Commun. 2003, 310:824-829.
7. Hayes J.D., McMahon M. NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer. Trends Biochem. Sci. 2009, 34:176-188.
8. Hayes J.D., McMahon M., Chowdhry S., Dinkova-Kostova A.T. Cancer chemoprevention mechanisms mediated through the Keap1-Nrf2 pathway. Antioxid. Redox Signal. 2010, 13:1713-1748.
9. Hosoyamada M., Sekine T., Kanai Y., Endou H. Molecular cloning and functional expression of a multispecific organic anion transporter from human kidney. Am. J. Physiol. 1999, 276:F122-F128.
10. Huls M., Brown C.D., Windass A.S., Sayer R., van den Heuvel J.J., Heemskerk S., Russel F.G., Masereeuw R. The breast cancer resistance protein transporter ABCG2 is expressed in the human kidney proximal tubule apical membrane. Kidney Int. 2008, 73:220-225.
11. Inui K.I., Masuda S., Saito H. Cellular and molecular aspects of drug transport in the kidney. Kidney Int. 2000, 58:944-958.
12. Itoh K., Mimura J., Yamamoto M. Discovery of the negative regulator of Nrf2, Keap1: a historical overview. Antioxid. Redox Signal. 2010, 13:1665-1678.
13. 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.
14. Keppler D. Multidrug resistance proteins (MRPs, ABCCs): importance for pathophysiology and drug therapy. Handb. Exp. Pharmacol. 2011, 299-323.
15. Klaassen C.D., Reisman S.A. Nrf2 the rescue: effects of the antioxidative/electrophilic response on the liver. Toxicol. Appl. Pharmacol. 2010, 244:57-65.
16. Kwak M.K., Kensler T.W. Targeting NRF2 signaling for cancer chemoprevention. Toxicol. Appl. Pharmacol. 2010, 244:66-76.
17. Lalande M.E., Ling V., Miller R.G. Hoechst 33342 dye uptake as a probe of membrane permeability changes in mammalian cells. Proc. Natl. Acad. Sci. USA 1981, 78:363-367.
18. Lee W., Kim R.B. Transporters and renal drug elimination. Annu. Rev. Pharmacol. Toxicol. 2004, 44:137-166.
19. Magnarin M., Morelli M., Rosati A., Bartoli F., Candussio L., Giraldi T., Decorti G. 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.
20. Maher J.M., Cheng X., Slitt A.L., Dieter M.Z., Klaassen C.D. Induction of the multidrug resistance-associated protein family of transporters by chemical activators of receptor-mediated pathways in mouse liver. Drug Metab. Dispos. 2005, 33:956-962.
21. Marquez B., Van Bambeke F. ABC multidrug transporters: target for modulation of drug pharmacokinetics and drug-drug interactions. Curr. Drug Targets 2011, 12:600-620.
22. Masereeuw R., Russel F.G. Mechanisms and clinical implications of renal drug excretion. Drug Metab. Rev. 2001, 33:299-351.
23. Masereeuw R., Russel F.G. Regulatory pathways for ATP-binding cassette transport proteins in kidney proximal tubules. AAPS J. 2012, 14:883-894.
24. Masereeuw R., Mutsaers H.A., Toyohara T., Abe T., Jhawar S., Sweet D.H., Lowenstein J. The kidney and uremic toxin removal: glomerulus or tubule?. Semin. Nephrol. 2014, 34:191-208.
25. Masuda S., Terada T., Yonezawa A., Tanihara Y., Kishimoto K., Katsura T., Ogawa O., Inui K. Identification and functional characterization of a new human kidney-specific H+/organic cation antiporter, kidney-specific multidrug and toxin extrusion 2. J. Am. Soc. Nephrol. 2006, 17:2127-2135.
26. Mease K., Sane R., Podila L., Taub M.E. Differential selectivity of efflux transporter inhibitors in Caco-2 and MDCK-MDR1 monolayers: a strategy to assess the interaction of a new chemical entity with P-gp, BCRP, and MRP2. J. Pharm. Sci. 2012, 101:1888-1897.
27. Morrissey K.M., Stocker S.L., Wittwer M.B., Xu L., Giacomini K.M. Renal transporters in drug development. Annu. Rev. Pharmacol. Toxicol. 2013, 53:503-529.
28. Motohashi H., Inui K. Organic cation transporter OCTs (SLC22) and MATEs (SLC47) in the human kidney. Aaps j 2013, 15:581-588.
29. Okabe M., Unno M., Harigae H., Kaku M., Okitsu Y., Sasaki T., Mizoi T., Shiiba K., Takanaga H., Terasaki T., Matsuno S., Sasaki I., Ito S., Abe T. Characterization of the organic cation transporter SLC22A16: a doxorubicin importer. Biochem. Biophys. Res. Commun. 2005, 333:754-762.
30. Otsuka M., Matsumoto T., Morimoto R., Arioka S., Omote H., Moriyama Y. A human transporter protein that mediates the final excretion step for toxic organic cations. Proc. Natl. Acad. Sci. USA 2005, 102:17923-17928.
31. Race J.E., Grassl S.M., Williams W.J., Holtzman E.J. Molecular cloning and characterization of two novel human renal organic anion transporters (hOAT1 and hOAT3). Biochem. Biophys. Res. Commun. 1999, 255:508-514.
32. Ryoo I.G., Ha H., Kwak M.K. Inhibitory role of the KEAP1-NRF2 pathway in TGFbeta1-stimulated renal epithelial transition to fibroblastic cells: a modulatory effect on SMAD signaling. PLoS ONE 2014, 9:e93265.
33. Schaub T.P., Kartenbeck J., Konig J., Spring H., Dorsam J., Staehler G., Storkel S., Thon W.F., Keppler D. 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.
34. Singh A., Wu H., Zhang P., Happel C., Ma J., Biswal S. Expression of ABCG2 (BCRP) is regulated by Nrf2 in cancer cells that confers side population and chemoresistance phenotype. Mol. Cancer Ther. 2010, 9:2365-2376.
35. Suzuki T., Motohashi H., Yamamoto M. Toward clinical application of the Keap1-Nrf2 pathway. Trends Pharmacol. Sci. 2013, 34:340-346.
36. van Aubel R.A., Smeets P.H., Peters J.G., Bindels R.J., Russel F.G. 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.
37. Villeneuve N.F., Lau A., Zhang D.D. Regulation of the Nrf2-Keap1 antioxidant response by the ubiquitin proteasome system: an insight into cullin-ring ubiquitin ligases. Antioxid. Redox Signal. 2010, 13:1699-1712.
38. Vollrath V., Wielandt A.M., Iruretagoyena M., Chianale J. Role of Nrf2 in the regulation of the Mrp2 (ABCC2) gene. Biochem. J. 2006, 395:599-609.
39. Wagner M., Halilbasic E., Marschall H.U., Zollner G., Fickert P., Langner C., Zatloukal K., Denk H., Trauner M. CAR and PXR agonists stimulate hepatic bile acid and bilirubin detoxification and elimination pathways in mice. Hepatology 2005, 42:420-430.
40. Wang H., Wu X., Hudkins K., Mikheev A., Zhang H., Gupta A., Unadkat J.D., Mao Q. 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-E1304.
41. Wang X., Campos C.R., Peart J.C., Smith L.K., Boni J.L., Cannon R.E., Miller D.S. Nrf2 upregulates ATP binding cassette transporter expression and activity at the blood-brain and blood-spinal cord barriers. J. Neurosci. 2014, 34:8585-8593.
42. Xu S., Weerachayaphorn J., Cai S.Y., Soroka C.J., Boyer J.L. 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-G135.
43. Yacovino L.L., Aleksunes L.M. Endocrine and metabolic regulation of renal drug transporters. J. Biochem. Mol. Toxicol. 2012, 26:407-421.