MRP1 and its role in anticancer drug resistance

References

• Akan I, Akan S, Akca H, et al. (2005). Multidrug resistance-associated protein 1 (MRP1) mediated vincristine resistance: Effects of N-acetylcysteine and Buthionine sulfoximine. Cancer Cell Int 5:22
   PubMed Web of Science ®Google Scholar
• Alisi A, Cho WC, Locatelli F, Fruci D. (2013). Multidrug resistance and cancer stem cells in neuroblastoma and hepatoblastoma. Int J Mol Sci 14:24706–24725
   PubMed Web of Science ®Google Scholar
• Almquist KC, Loe DW, Hipfner DR, et al. (1995). Characterization of the M(r) 190,000 multidrug resistance protein (MRP) in drug-selected and transfected human tumor cell. Cancer Res 55:102–110
   PubMed Web of Science ®Google Scholar
• Ambudkar SV, Dey S, Hrycyna CA, et al. (1999). Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu Rev Pharmacol Toxicol 39:361–398
   PubMed Web of Science ®Google Scholar
• Amram S, Ganoth A, Tichon O, et al. (2014). Structural characterization of the drug translocation path of MRP1/ABCC1. Isr J Chem 54:1382–1393
   Web of Science ®Google Scholar
• Armstrong JS, Jones DP. (2002). Glutathione depletion enforces the mitochondrial permeability transition and causes cell death in Bcl-2 overexpressing HL60 cells. FASEB J 16:1263–1265
   PubMed Web of Science ®Google Scholar
• Arroyo JD, Chevillet JR, Kroh EM, et al. (2011). Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A 108:5003–5008
   PubMed Web of Science ®Google Scholar
• Atalay C, Deliloglu Gurhan I, Irkkan C, Gunduz U. (2006). Multidrug resistance in locally advanced breast cancer. Tumour Biol 27:309–318
   PubMed Web of Science ®Google Scholar
• Bagnoli M, Beretta GL, Gatti L, et al. (2013). Clinicopathological impact of ABCC1/MRP1 and ABCC4/MRP4 in epithelial ovarian carcinoma. Biomed Res Int 2013: Article ID 143202
   PubMed Web of Science ®Google Scholar
• Bakos E, Evers R, Sinkó E, et al. (2000). Interactions of the human multidrug resistance proteins MRP1 and MRP2 with organic anions. Mol Pharmacol 57:760–768
   PubMed Web of Science ®Google Scholar
• Bakos E, Evers R, Szakács G, et al. (1998). Functional multidrug resistance protein (MRP1) lacking the N-terminal transmembrane domain. J Biol Chem 273:32167–32175
   PubMed Web of Science ®Google Scholar
• Bakos E, Homolya L. (2007). Portrait of multifaceted transporter, the multidrug resistance-associated protein 1 (MRP1/ABCC1). Pflugers Arch 453:621–641
   PubMed Web of Science ®Google Scholar
• Bao GS, Wang WA, Wang TZ, et al. (2011). Overexpression of human MRP1 in neurons causes resistance to antiepileptic drugs in Drosophila seizure mutants. J Neurogenet 25:201–206
   PubMed Web of Science ®Google Scholar
• Bebawy M, Combes V, Lee E, et al. (2009). Membrane microparticles mediate transfer of P-glycoprotein to drug sensitive cancer cells. Leukemia 23:1643–1649
   PubMed Web of Science ®Google Scholar
• Bebawy M, Roseblade A, Luk F, et al. (2013). Cell-derived microparticles: New targets in the therapeutic management of disease. J Pharm Pharm Sci 16:238–253
   PubMed Web of Science ®Google Scholar
• Berger W, Setinek U, Hollaus P, et al. (2005). Multidrug resistance markers P-glycoprotein, multidrug resistance protein 1, and lung resistance protein in non-small cell lung cancer: Prognostic implications. J Cancer Res Clin Oncol 131:355–363
   PubMed Web of Science ®Google Scholar
• Bordow SB, Haber M, Madafiglio J, et al. (1994). Expression of the multidrug resistance-associated protein (MRP) gene correlates with amplification and overexpression of the N-myc oncogene in childhood neuroblastoma. Cancer Res 54:5036–5040
   PubMed Web of Science ®Google Scholar
• Borst P, Evers R, Kool M, Wijnholds J. (2000). A family of drug transporters: The multidrug resistance-associated proteins. J Natl Cancer Inst 92:1295–1302
   PubMed Web of Science ®Google Scholar
• Boumendjel A, Baubichon-Cortay H, Trompier D, et al. (2005). Anticancer multidrug resistance mediated by MRP1: Recent advances in the discovery of reversal agents. Med Res Rev 25:453–472
   PubMed Web of Science ®Google Scholar
• Brandmann M, Tulpule K, Schmidt MM, Dringen R. (2012). The antiretroviral protease inhibitors indinavir and nelfinavir stimulate Mrp1-mediated GSH export from cultured brain astrocytes. J Neurochem 120:78–92
   PubMed Web of Science ®Google Scholar
• Brase JC, Johannes M, Schlomm T, et al. (2011). Circulating miRNAs are correlated with tumor progression in prostate cancer. Int J Cancer 128:608–616
   PubMed Web of Science ®Google Scholar
• Brock I, Hipfner DR, Nielsen BS, et al. (1995). Sequential coexpression of the multidrug resistance genes MRP and mdr1 and their products in VP-16 (etoposide)-selected H69 small cell lung cancer cells. Cancer Res 55:459–462
   PubMed Web of Science ®Google Scholar
• Buda G, Ricci D, Huang CC, et al. (2010). Polymorphisms in the multiple drug resistance protein 1 and in P-glycoprotein 1 are associated with time to event outcomes in patients with advanced multiple myeloma treated with bortezomib and pegylated liposomal doxorubicin. Ann Hematol 89:1133–1140
   PubMed Web of Science ®Google Scholar
• Callaghan R, Luk F, Bebawy M. (2014). Inhibition of the multidrug resistance P-glycoprotein: Time for a change of strategy? Drug Metab Dispos 42:623–631
   PubMed Web of Science ®Google Scholar
• Campos L, Guyotat D, Archimbaud E, et al. (1992). Clinical significance of multidrug resistance P-glycoprotein expression on acute nonlymphoblastic leukemia cells at diagnosis. Blood 79:473–476
   PubMed Web of Science ®Google Scholar
• Chan JA, Krichevsky AM, Kosik KS. (2005). MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65:6029–6033
   PubMed Web of Science ®Google Scholar
• Chaptal V, Magnard S, Gueguen-Chaignon V, et al. (2014). Nucleotide-free crystal structure of nucleotide-binding domain 1 from human ABCC1 supports a ‘general-base catalysis’ mechanism for ATP hydrolysis. Biochem Pharmacol 3:1000150
   Google Scholar
• Chen X, Ba Y Ma, Cai L, et al. (2008). Characterization of microRNAs in serum: A novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 18:997–1006
   PubMed Web of Science ®Google Scholar
• Chen X, Liang H, Zhang J, et al. (2012). Secreted microRNAs: A new form of intercellular communication. Trends Cell Biol 22:125–132
   PubMed Web of Science ®Google Scholar
• Chen YH, Wang CC, Xiao X, et al. (2013). Multidrug resistance-associated protein 1 decreases the concentrations of antiepileptic drugs in cortical extracellular fluid in amygdale kindling rats. Acta Pharmacol Sin 34:473–479
   PubMed Web of Science ®Google Scholar
• Cheng HH, Mitchell PS, Kroh EM, et al. (2013). Circulating microRNA profiling identifies a subset of metastatic prostate cancer patients with evidence of cancer-associated hypoxia. PLoS One 8:e69239
   PubMed Web of Science ®Google Scholar
• Cho S, Lu M, He X, et al. (2011). Notch1 regulates the expression of the multidrug resistance gene ABCC1/MRP1 in cultured cancer cells. Proc Natl Acad Sci U S A 108:20778–20783
   PubMed Web of Science ®Google Scholar
• Citti A, Boldrini R, Inserra A, et al (2012). Expression of multidrug resistance-associated proteins in paediatric soft tissue sarcomas before and after chemotherapy. Int J Oncol 41:117–124
   PubMed Web of Science ®Google Scholar
• Cole S. (1986). Rapid chemosensitivity testing of human lung tumor cells using the MTT assay. Cancer Chemother Pharmacol 17:259–263
   PubMed Web of Science ®Google Scholar
• Cole S, Bhardwaj G, Gerlach J, et al. (1992). Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258:1650–1654
   PubMed Web of Science ®Google Scholar
• Cole S, Downes HF, Mirski SE, Clements DJ. (1990). Alterations in glutathione and glutathione-related enzymes in a multidrug-resistant small cell lung cancer cell line. Mol Pharmacol 37:192–197
   PubMed Web of Science ®Google Scholar
• Cole SP. (2014). Targeting multidrug resistance protein 1 (MRP1, ABCC1): Past, present, and future. Annu Rev Pharmacol Toxicol 54:95–117
   PubMed Web of Science ®Google Scholar
• Cole SP, Deeley RG. (1998). Multidrug resistance mediated by the ATP-binding cassette transporter protein MRP. Bioessays 20:931–940
   PubMed Web of Science ®Google Scholar
• Cornwell MM, Tsuruo T, Gottesman M, Pastan I. (1987). ATP-binding properties of P glycoprotein from multidrug-resistant KB cells. FASEB J 1:51–54
   PubMed Web of Science ®Google Scholar
• Dantzig AH, Shepard RL, Pratt SE, et al. (2004). Evaluation of the binding of the tricyclic isoxazole photoaffinity label LY475776 to multidrug resistance associated protein 1 (MRP1) orthologs and several ATP-binding cassette (ABC) drug transporters. Biochem Pharmacol 67:1111–1121
   PubMed Web of Science ®Google Scholar
• DeGorter MK, Conseil G, Deeley RG, et al. (2008). Molecular modeling of the human multidrug resistance protein 1 (MRP1/ABCC1). Biochem Biophys Res Commun 365:29–34
   PubMed Web of Science ®Google Scholar
• Deshmukh LP, Rode SD, Wagh PV, et al. (2013). Oxidative stress and antioxidants in focus: A review. Inventi Impact: Mol Pharmacol 37:106–112
   Google Scholar
• Di Pietro A, Conseil G, Pérez-Victoria J, et al. (2002). Modulation by flavonoids of cell multidrug resistance mediated by P-glycoprotein and related ABC transporters. Cell Mol Life Sci 59:307–322
   PubMed Web of Science ®Google Scholar
• Diehl P, Fricke A, Sander L, et al. (2012). Microparticles: Major transport vehicles for distinct microRNAs in circulation. Cardiovasc Res 93:633–644
   PubMed Web of Science ®Google Scholar
• Diestra JE, Condom E, Del Muro XG, et al. (2003). Expression of multidrug resistance proteins P-glycoprotein, multidrug resistance protein 1, breast cancer resistance protein and lung resistance related protein in locally advanced bladder cancer treated with neoadjuvant chemotherapy: Biological and clinical implications. J Urol 170:1383–1387
   PubMed Web of Science ®Google Scholar
• Dinger ME, Mercer TR, Mattick JS. (2008). RNAs as extracellular signaling molecules. J Mol Endocrinol 40:151–159
   PubMed Web of Science ®Google Scholar
• Distler JHW, Huber LC, Gay S, et al. (2006). Microparticles as mediators of cellular cross-talk in inflammatory disease. Autoimmunity 39:683–690
   PubMed Web of Science ®Google Scholar
• Domingo-Fernandez R, Watters K, Piskareva O, et al. (2013). The role of genetic and epigenetic alterations in neuroblastoma disease pathogenesis. Pediatr Surg Int 29:101–119
   PubMed Web of Science ®Google Scholar
• Dransfeld C, Schmiedgen M, Kramer M, et al. (2013). Multidrug-related protein 1 (MRP1) polymorphisms rs129081, rs212090, and rs212091 predict survival in acute myeloid leukemia. Blood 122:2580
   Google Scholar
• Dryver ET, Jernström H, Tompkins K, et al. (2003). Follow-up of patients with Hodgkin’s disease following curative treatment: The routine CT scan is of little value. Br J Cancer 89:482–486
   PubMed Web of Science ®Google Scholar
• Faggad A, Darb-Esfahani S, Wirtz R, et al. (2009). Expression of multidrug resistance-associated protein 1 in invasive ovarian carcinoma: Implication for prognosis. Histopathology 54:657–666
   PubMed Web of Science ®Google Scholar
• Falasca M, Linton KJ. (2012). Investigational ABC transporter inhibitors. Expert Opin Investig Drugs 21:657–666
   PubMed Web of Science ®Google Scholar
• Farber LR, Prosnitz LR, Cadman EC, et al. (1980). Curative potential of combined modality therapy for advanced Hodgkin’s disease. Cancer 46:1509–1517
   PubMed Web of Science ®Google Scholar
• Filipits M, Pohl G, Rudas M, et al. (2005). Clinical role of multidrug resistance protein 1 expression in chemotherapy resistance in early-stage breast cancer: The Austrian Breast and Colorectal Cancer Study Group. J Clin Oncol 23:1161–1168
   PubMed Web of Science ®Google Scholar
• Frei E. (1985). Curative cancer chemotherapy. Cancer Res 45:6523–6537
   PubMed Web of Science ®Google Scholar
• Gekeler V, Ise W, Sanders KH, et al. (1995). The leukotriene LTD4 receptor antagonist Mk571 specifically modulates MRP associated multidrug resistance. Biochem Biophys Res Commun 208:345–352
   PubMed Web of Science ®Google Scholar
• Gennuso F, Fernetti C, Tirolo C, et al. (2004). Bilirubin protects astrocytes from its own toxicity by inducing up-regulation and translocation of multidrug resistance-associated protein 1 (Mrp1). Proc Natl Acad Sci U S A 101:2470–2475
   PubMed Web of Science ®Google Scholar
• Germann UA, Ford PJ, Shlyakhter D, et al. (1997). Chemosensitization and drug accumulation effects of VX-710, verapamil, cyclosporin A, MS-209 and GF120918 in multidrug resistant HL60/ADR cells expressing the multidrug resistance-associated protein MRP. Anticancer Drugs 8:141–155
   PubMed Web of Science ®Google Scholar
• Gonda D, Goyal A, Akers J, et al. (2014). Glioblastoma microvesicles transport RNA and proteins, promoting tumor growth. In: Hayat MA, ed. Tumors of the central nervous system. Netherlands: Springer. 101–112
   Google Scholar
• Gong J, Jaiswal R, Mathys JM, et al. (2012). Microparticles and their emerging role in cancer multidrug resistance. Cancer Treat Rev 38:226–234
   PubMed Web of Science ®Google Scholar
• Gong J, Luk F, Jaiswal R, et al. (2013). Microparticle drug sequestration provides a parallel pathway in the acquisition of cancer drug resistance. Eur J Pharmacol 721:116–125
   PubMed Web of Science ®Google Scholar
• Gurbuxani S, Singh Arya L, Raina V, et al. (2001). Significance of MDR1, MRP1, GSTpi and GSTmu mRNA expression in acute lymphoblastic leukemia in Indian patients. Cancer Lett 167:73–83
   PubMed Web of Science ®Google Scholar
• Haber M, Bordow SB, Gilbert J, et al. (1999). Altered expression of the MYCN oncogene modulates MRP gene expression and response to cytotoxic drugs in neuroblastoma cells. Oncogene 18:2777–2782
   PubMed Web of Science ®Google Scholar
• Haber M, Smith J, Bordow SB, et al. (2006). Association of high-level MRP1 expression with poor clinical outcome in a large prospective study of primary neuroblastoma. J Clin Oncol 24:1546–1553
   PubMed Web of Science ®Google Scholar
• Hollenstein K, Dawson RJ, Locher KP. (2007). Structure and mechanism of ABC transporter proteins. Curr Opin Struct Biol 17:412–418
   PubMed Web of Science ®Google Scholar
• Hooijberg JH, Broxterman HJ, Scheffer GL, et al. (1999). Potent interaction of flavopiridol with MRP1. Br J Cancer 81:269–276
   PubMed Web of Science ®Google Scholar
• Huang CL, Kohno N, Ogawa E, et al. (1998). Correlation of Reduction in MRP-1/CD9 and KAI1/CD82 expression with recurrences in breast cancer patients. Am J Pathol 153:973–983
   PubMed Web of Science ®Google Scholar
• Huang TH, Bebawy M, Tran VH, Roufogalis BD. (2007). Specific reversal of multidrug resistance to colchicine in CEM/VLB(100) cells by Gynostemma pentaphyllum extract. Phytomedicine 14:830–839
   PubMed Web of Science ®Google Scholar
• Jaiswal R, Gong J, Sambasivam S, et al. (2012a). Microparticle-associated nucleic acids mediate trait dominance in cancer. FASEB J 26:420–429
   PubMed Web of Science ®Google Scholar
• Jaiswal R, Luk F, Dalla PV, et al. (2013). Breast cancer-derived microparticles display tissue selectivity in the transfer of resistance proteins to cells. PLoS One 8:e61515
   PubMed Web of Science ®Google Scholar
• Jaiswal R, Luk F, Gong J, et al. (2012b). Microparticle conferred microRNA profiles – implications in the transfer and dominance of cancer traits. Mol Cancer 11:37
   PubMed Web of Science ®Google Scholar
• Jedlitschky G, Leier I, Buchholz U, et al. (1996). Transport of glutathione, glucuronate, and sulfate conjugates by the MRP gene-encoded conjugate export pump. Cancer Res 56:988–994
   PubMed Web of Science ®Google Scholar
• Juliano RL, Ling V. (1976). A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta 455:152–162
   PubMed Web of Science ®Google Scholar
• Jungsuwadee P, Zhao T, Stolarczyk EI, et al. (2012). The G671V variant of MRP1/ABCC1 links doxorubicin-induced acute cardiac toxicity to disposition of the glutathione conjugate of 4-hydroxy-2-trans-nonenal. Pharmacogenet Genomics 22:273
   PubMed Web of Science ®Google Scholar
• Kachadourian R, Day BJ. (2006). Flavonoid-induced glutathione depletion: Potential implications for cancer treatment. Free Radic Biol Med 41:65–76
   PubMed Web of Science ®Google Scholar
• Kanigur G, Gurel C, Saitoglu M, et al. (2010). The role of multidrug resistance protein (MRP-1) in platelet activation with allergic asthma. Haematologica 95:752
   PubMed Web of Science ®Google Scholar
• Kerb R, Hoffmeyer S, Brinkmann U. (2001). ABC drug transporters: Hereditary polymorphisms and pharmacological impact in MDR1, MRP1 and MRP2. Pharmacogenomics 2:51–64
   PubMed Web of Science ®Google Scholar
• Kim B, Fatayer H, Hanby AM, et al. (2013). Neoadjuvant chemotherapy induces expression levels of breast cancer resistance protein that predict disease-free survival in breast cancer. PLoS One 8:e62766
   PubMedGoogle Scholar
• Komdeur R, Plaat BE, van der Graaf WTA, et al. (2003). Expression of multidrug resistance proteins, P-gp, MRP1 and LRP, in soft tissue sarcomas analysed according to their histological type and grade. Eur J Cancer 39:909–916
   PubMed Web of Science ®Google Scholar
• Kosaka N, Iguchi H, Ochiya T. (2010). Circulating microRNA in body fluid: A new potential biomarker for cancer diagnosis and prognosis. Cancer Sci 101:2087–2092
   PubMed Web of Science ®Google Scholar
• Krause MS, Oliveira LP, Silveira EMS, et al. (2007). MRP1/GS-X pump ATPase expression: Is this the explanation for the cytoprotection of the heart against oxidative stress-induced redox imbalance in comparison to skeletal muscle cells? Cell Biochem Funct 25:23–32
   PubMed Web of Science ®Google Scholar
• Krishnamachary N, Ma L, Zheng L, et al. (1993). Analysis of MRP gene expression and function in HL60 cells isolated for resistance to adriamycin. Oncol Res 6:119–127
   Web of Science ®Google Scholar
• Kuss BJ, Corbo M, Lau WM, et al. (2002). In vitro and in vivo downregulation of MRP1 by antisense oligonucleotides: A potential role in neuroblastoma therapy. Int J Cancer 98:128–133
   PubMed Web of Science ®Google Scholar
• Kuwazuru Y, Yoshimura A, Hanada S, et al. (1990). Expression of the multidrug transporter, P-glycoprotein, in acute leukemia cells and correlation to clinical drug resistance. Cancer 66:868–873
   PubMed Web of Science ®Google Scholar
• Laffont B, Corduan A, Plé H, et al. (2013). Activated platelets can deliver mRNA regulatory Ago2 microRNA complexes to endothelial cells via microparticles. Blood. 122:253–261
   Google Scholar
• Larkin A, O’Driscoll L, Kennedy S, et al. (2004). Investigation of MRP-1 protein and MDR-1 P-glycoprotein expression in invasive breast cancer: A prognostic study. Int J Cancer 112:286–294
   PubMed Web of Science ®Google Scholar
• Laupeze B, Amiot L, Drenou B, et al. (2002). High multidrug resistance protein activity in acute myeloid leukaemias is associated with poor response to chemotherapy and reduced patient survival. Br J Haematol 116:834–838
   PubMed Web of Science ®Google Scholar
• Lee SH, Lee MS, Lee JH, et al. (2010). MRP1 polymorphisms associated with citalopram response in patients with major depression. J Clin Psychopharmacol 30:116–125
   PubMed Web of Science ®Google Scholar
• Lee YJ, Kusuhara H, Sugiyama Y. (2004). Do multidrug resistance-associated protein-1 and -2 play any role in the elimination of estradiol-17beta-glucuronide and 2,4-dinitrophenyl-S-glutathione across the blood-cerebrospinal fluid barrier? J Pharm Sci 93:99–107
   PubMed Web of Science ®Google Scholar
• Legrand O, Simonin G, Beauchamp-Nicoud A, et al. (1999). Simultaneous activity of MRP1 and Pgp is correlated with in vitro resistance to daunorubicin and with in vivo resistance in adult acute myeloid leukemia. Blood 94:1046–1056
   PubMed Web of Science ®Google Scholar
• Leith CP, Kopecky KJ, Chen IM, et al. (1999). Frequency and clinical significance of the expression of the multidrug resistance proteins MDR1/P-glycoprotein, MRP1, and LRP in acute myeloid leukemia. A Southwest Oncology Group Study. Blood 94:1086–1099
   PubMed Web of Science ®Google Scholar
• Leslie EM, Deeley RG, Cole SPC. (2001a). Toxicological relevance of the multidrug resistance protein 1, MRP1 (ABCC1) and related transporters. Toxicology 167:3–23
   PubMed Web of Science ®Google Scholar
• Leslie EM, Deeley RG, Cole SPC. (2003). Bioflavonoid stimulation of glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). Drug Metab Dispos 31:11–15
   PubMed Web of Science ®Google Scholar
• Leslie EM, Deeley RG, Cole SPC. (2005). Multidrug resistance proteins: Role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 204:216–237
   PubMed Web of Science ®Google Scholar
• Leslie EM, Mao Q, Oleschuk CJ, et al. (2001b). Modulation of multidrug resistance protein 1 (MRP1/ABCC1) transport and ATPase activities by interaction with dietary flavonoids. Mol Pharmacol 59:1171–1180
   PubMed Web of Science ®Google Scholar
• Li CC, Eaton SA, Young PE, et al. (2013). Glioma microvesicles carry selectively packaged coding and non-coding RNAs which alter gene expression in recipient cells. RNA Biol 10:1333
   PubMed Web of Science ®Google Scholar
• Li J, Li ZN, Yu LC, et al. (2010). Association of expression of MRP1, BCRP, LRP and ERCC1 with outcome of patients with locally advanced non-small cell lung cancer who received neoadjuvant chemotherapy. Lung Cancer 69:116–122
   PubMed Web of Science ®Google Scholar
• Li Y, Paxton JW. (2012). The effects of flavonoids on the ABC transporters: Consequences for the pharmacokinetics of substrate drugs. Expert Opin Drug Metab Toxicol 9:267–285
   Web of Science ®Google Scholar
• Liang Z, Wu H, Xia J, et al. (2010). Involvement of miR-326 in chemotherapy resistance of breast cancer through modulating expression of multidrug resistance-associated protein 1. Biochem Pharmacol 79:817–824
   PubMed Web of Science ®Google Scholar
• Liu C, Li Z, Bi L, et al. (2014). NOTCH1 signaling promotes chemoresistance via regulating ABCC1 expression in prostate cancer stem cells. Mol Cell Biochem 393:265–270
   PubMed Web of Science ®Google Scholar
• Liu YH, Di YM, Zhou ZW, et al. (2010). Multidrug resistance-associated proteins and implications in drug development. Clin Exp Pharmacol Physiol 37:115–120
   PubMed Web of Science ®Google Scholar
• Loe DW, Almquist KC, Deeley RG, Cole SPC. (1996). Multidrug resistance protein (MRP)-mediated transport of leukotriene c and chemotherapeutic agents in membrane vesicles: Demonstration of glutathione-dependent vincristine transport. J Biol Chem 271:9675–9682
   PubMed Web of Science ®Google Scholar
• Loe DW, Deeley RG, Cole SPC. (2000). Verapamil stimulates glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). J Pharmacol Exp Ther 293:530–538
   PubMed Web of Science ®Google Scholar
• Lu JF, Luk F, Gong J, et al. (2013). Microparticles mediate MRP1 intercellular transfer and the re-templating of intrinsic resistance pathways. Pharmacol Res 76:77–83
   PubMed Web of Science ®Google Scholar
• Lu M, Majumdar N, Jiang R, et al. (2012). Notch1 affects ABCC1-mediated drug efflux and drug sensitivity in MCF7 breast cancer cells. Cancer Res 72:772
   Google Scholar
• Lu QJ, Dong F, Zhang JH, et al. (2004). Expression of multidrug resistance-related markers in primary neuroblastoma. Chin Med J (Engl) 117:1358–1363
   PubMedGoogle Scholar
• Ma J, Cai W, Zhang Y, et al. (2013). Innate immune cell-derived microparticles facilitate hepatocarcinoma metastasis by transferring integrin alpha(M)beta(2) to tumor cells. J Immunol 191:3453–3461
   PubMed Web of Science ®Google Scholar
• Mahjoubi F, Akbari S. (2012). Multidrug resistance-associated protein 1 predicts relapse in Iranian childhood acute lymphoblastic leukemia. Asian Pac J Cancer Prev 13:2285–2289
   PubMed Web of Science ®Google Scholar
• Manciu L, Chang XB, Buyse F, et al. (2003). Intermediate structural states involved in MRP1-mediated drug transport role of glutathione. J Biol Chem 278:3347–3356
   PubMed Web of Science ®Google Scholar
• Manohar CF, Bray JA, Salwen HR, et al. (2004). MYCN-mediated regulation of the MRP1 promoter in human neuroblastoma. Oncogene 23:753–762
   PubMed Web of Science ®Google Scholar
• Martin-Broto J, Gutierrez AM, Ramos RF, et al. (2014). MRP1 overexpression determines poor prognosis in prospectively treated patients with localized high-risk soft tissue sarcoma of limbs and trunk wall: An ISG/GEIS study. Mol Cancer Ther 13:249–259
   PubMed Web of Science ®Google Scholar
• Matsson P, Pedersen J, Norinder U, et al. (2009). Identification of novel specific and general inhibitors of the three major human ATP-binding cassette transporters P-gp, BCRP and MRP2 among registered drugs. Pharm Res 26:1816–1831
   PubMed Web of Science ®Google Scholar
• Mause SF, Weber C. (2010). Microparticles: Protagonists of a novel communication network for intercellular information exchange. Circ Res 107:1047–1057
   PubMed Web of Science ®Google Scholar
• Mimmack M, Gallagher MP, Pearce SR, et al. (1989). Energy coupling to periplasmic binding protein-dependent transport systems: Stoichiometry of ATP hydrolysis during transport in vivo. Proc Natl Acad Sci 86:8257–8261
   PubMed Web of Science ®Google Scholar
• Mirski SEL, Gerlach JH, Cole SPC. (1987). Multidrug resistance in a human small cell lung cancer cell line selected in adriamycin. Cancer Res 47:2594–2598
   PubMed Web of Science ®Google Scholar
• Morel O, Morel N, Freyssinet JM, Toti F. (2008). Platelet microparticles and vascular cells interactions: A checkpoint between the haemostatic and thrombotic responses. Platelets 19:9–23
   PubMed Web of Science ®Google Scholar
• Morris ME, Zhang S. (2006). Flavonoid-drug interactions: Effects of flavonoids on ABC transporters. Life Sci 78:2116–2130
   PubMed Web of Science ®Google Scholar
• Mueller CFH, Afzal S, Becher UM, et al. (2010). Role of the multidrug resistance protein-1 (MRP1) for endothelial progenitor cell function and survival. J Mol Cell Cardiol 49:482–489
   PubMed Web of Science ®Google Scholar
• Munoz M, Henderson M, Haber M, Norris M. (2007). Role of the MRP1/ABCC1 multidrug transporter protein in cancer. IUBMB Life 59:752–757
   PubMed Web of Science ®Google Scholar
• Nguyen H, Zhang S, Morris ME. (2003). Effect of flavonoids on MRP1-mediated transport in Panc-1 cells. J Pharm Sci 92:250–257
   PubMed Web of Science ®Google Scholar
• Nies AT, Jedlitschky G, König J, et al. (2004). Expression and immunolocalization of the multidrug resistance proteins, MRP1-MRP6 (ABCC1-ABCC6), in human brain. Neuroscience 129:349–360
   PubMed Web of Science ®Google Scholar
• Nooter K, Riviere Dela, Look GB, et al. (1997). The prognostic significance of expression of the multidrug resistance-associated protein (MRP) in primary breast cancer. Br J Cancer 76:486
   PubMed Web of Science ®Google Scholar
• Norman BH, Gruber JM, Hollinshead SP, et al. (2002). Tricyclic isoxazoles are novel inhibitors of the multidrug resistance protein (MRP1). Bioorg Med Chem Lett 12:883–886
   PubMed Web of Science ®Google Scholar
• Norman BH, Lander PA, Gruber JM, et al. (2005). Cyclohexyl-linked tricyclic isoxazoles are potent and selective modulators of the multidrug resistance protein (MRP1). Bioorg Med Chem Lett 15:5526–5530
   PubMed Web of Science ®Google Scholar
• Oda Y, Schneider-Stock R, Ryś J, et al. (1996). Expression of multidrug-resistance-associated protein gene in human soft-tissue sarcomas. J Cancer Res Clin Oncol 122:161–165
   PubMed Web of Science ®Google Scholar
• Ota E, Abe Y, Oshika Y, et al. (1995). Expression of the multidrug resistance-associated protein (MRP) gene in non-small-cell lung cancer. Br J Cancer 72:550
   PubMed Web of Science ®Google Scholar
• Pajeva IK, Globisch C, Wiese M. (2009). Combined pharmacophore modeling, docking, and 3D QSAR studies of ABCB1 and ABCC1 transporter inhibitors. ChemMedChem 4:1883–1896
   PubMed Web of Science ®Google Scholar
• Patrick AE, Thomas PJ. (2012). Development of CFTR structure. Front Pharmacol 3:162
   PubMed Web of Science ®Google Scholar
• Plasschaert SL, de Bont ES, Boezen M, et al. (2005). Expression of multidrug resistance-associated proteins predicts prognosis in childhood and adult acute lymphoblastic leukemia. Clin Cancer Res 11:8661–8668
   PubMed Web of Science ®Google Scholar
• Pogribny IP, Filkowski JN, Tryndyak VP, et al. (2010). Alterations of microRNAs and their targets are associated with acquired resistance of MCF-7 breast cancer cells to cisplatin. Int J Cancer 127:1785–1794
   PubMed Web of Science ®Google Scholar
• Pokharel D, Padula MP, Lu F, Tacchi JL, et al. (2014). Proteome analysis of multidrug-resistant, breast cancer-derived microparticles. J Extracell Vesicles 3:24384
   Google Scholar
• Rajagopal A, Simon SM. (2003). Subcellular localization and activity of multidrug resistance proteins. Mol Biol Cell 14:3389–3399
   PubMed Web of Science ®Google Scholar
• Rees DC, Johnson E, Lewinson O. (2009). ABC transporters: The power to change. Nat Rev Mol Cell Biol 10:218–227
   PubMed Web of Science ®Google Scholar
• Romermann K, Wanek T, Bankstahl M, et al. (2013). (R)-[(11)C]verapamil is selectively transported by murine and human P-glycoprotein at the blood-brain barrier, and not by MRP1 and BCRP. Nucl Med Biol 40:873–878
   PubMed Web of Science ®Google Scholar
• Rothnie A, Callaghan R, Deeley RG, Cole SPC. (2006). Role of GSH in estrone sulfate binding and translocation by the multidrug resistance protein 1 (MRP1/ABCC1). J Biol Chem 281:13906–13914
   PubMed Web of Science ®Google Scholar
• Roundhill EA, Burchill SA. (2012). Detection and characterisation of multi-drug resistance protein 1 (MRP-1) in human mitochondria. Br J Cancer 106:1224–1233
   PubMed Web of Science ®Google Scholar
• Salerno M, Loechariyakul P, Saengkhae C, Garnier-Suillerot A. (2004). Relation between the ability of some compounds to modulate the MRP1-mediated efflux of glutathione and to inhibit the MRPl-mediated efflux of daunorubicin. Biochem Pharmacol 68:2159–2165
   PubMed Web of Science ®Google Scholar
• Saraswathy M, Gong S. (2013). Different strategies to overcome multidrug resistance in cancer. Biotechnol Adv 31:1397–1407
   PubMed Web of Science ®Google Scholar
• Schaich M, Soucek S, Thiede C, et al. (2005). MDR1 and MRP1 gene expression are independent predictors for treatment outcome in adult acute myeloid leukaemia. Br J Haematol 128:324–332
   PubMed Web of Science ®Google Scholar
• Schroeter EH, Kisslinger JA, Kopan R. (1998). Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393:382–386
   PubMed Web of Science ®Google Scholar
• Schulte JH, Lindner S, Bohrer A, et al. (2013). MYCN and ALKF1174L are sufficient to drive neuroblastoma development from neural crest progenitor cells. Oncogene 32:1059–1065
   PubMed Web of Science ®Google Scholar
• Sedlakova I, Laco J, Tosner J, et al. (2013). [Drug resistance proteins LRP, Pgp, MRP1, MRP3 and MRP5 in ovarian cancer patients]. Ceska Gynekol 78:545–553
   PubMedGoogle Scholar
• Seelig A, Blatter XL, Wohnsland F. (2000). Substrate recognition by P-glycoprotein and the multidrug resistance-associated protein MRP1: A comparison. Int J Clin Pharmacol Ther 38:111–121
   PubMed Web of Science ®Google Scholar
• Semsei AF, Erdelyi DJ, Ungvari I, et al. (2012). ABCC1 polymorphisms in anthracycline-induced cardiotoxicity in childhood acute lymphoblastic leukaemia. Cell Biol Int 36:79–86
   PubMed Web of Science ®Google Scholar
• Slovak ML, Ho JP, Bhardwaj G, et al. (1993). Localization of a novel multidrug resistance-associated gene in the HT1080/DR4 and H69AR human tumor cell lines. Cancer Res 53:3221–3225
   PubMed Web of Science ®Google Scholar
• Slovak ML, Hoeltge GA, Dalton WS, Trent JM. (1988). Pharmacological and biological evidence for differing mechanisms of doxorubicin resistance in two human tumor cell lines. Cancer Res 48:2793–2797
   PubMed Web of Science ®Google Scholar
• Smith PC, Karpowich N, Millen L, et al. (2002). ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol Cell 10:139–149
   PubMed Web of Science ®Google Scholar
• Spiegl-Kreinecker S, Buchroithner J, Elbling L, et al. (2002). Expression and functional activity of the ABC-transporter proteins P-glycoprotein and multidrug-resistance protein 1 in human brain tumor cells and astrocytes. J Neurooncol 57:27–36
   PubMed Web of Science ®Google Scholar
• Stride BD, Grant CE, Loe DW, et al. (1997). Pharmacological characterization of the murine and human orthologs of multidrug-resistance protein in transfected human embryonic kidney cells. Mol Pharmacol 52:344–353
   PubMed Web of Science ®Google Scholar
• Sullivan GF, Yang JM, Vassil A, et al. (2000). Regulation of expression of the multidrug resistance protein MRP1 by p53 in human prostate cancer cells. J Clin Invest 105:1261–1267
   PubMed Web of Science ®Google Scholar
• Sun J, He ZG, Cheng G, et al. (2004). Multidrug resistance P-glycoprotein: Crucial significance in drug disposition and interaction. Med Sci Monit 10:RA5
   PubMed Web of Science ®Google Scholar
• Tadepalle N, Koehler Y, Brandmann M, et al. (2014). Arsenite stimulates glutathione export and glycolytic flux in viable primary rat brain astrocytes. Neurochem Int 76:1–11
   PubMed Web of Science ®Google Scholar
• Taheri M, Mahjoubi F. (2013). MRP1 but not MDR1 is associated with response to neoadjuvant chemotherapy in breast cancer patients. Dis Markers 34:387–393
   PubMed Web of Science ®Google Scholar
• Tamaki A, Ierano C, Szakacs G, et al. (2011). The controversial role of ABC transporters in clinical oncology. Essays Biochem 50:209–232
   PubMed Web of Science ®Google Scholar
• Tang R, Faussat AM, Majdak P, et al. (2004). Valproic acid inhibits proliferation and induces apoptosis in acute myeloid leukemia cells expressing P-gp and MRP1. Leukemia 18:1246–1251
   PubMed Web of Science ®Google Scholar
• Tarling EJ, de Aguiar Vallim TQ, Edwards PA. (2013). Role of ABC transporters in lipid transport and human disease. Trends Endocrinol Metab 24:342–350
   PubMed Web of Science ®Google Scholar
• Teodori E, Dei S, Martelli C, et al. (2006). The functions and structure of ABC transporters: Implications for the design of new inhibitors of Pgp and MRP1 to control multidrug resistance (MDR). Curr Drug Targets 7:893–909
   PubMed Web of Science ®Google Scholar
• Tran VH, Marks D, Duke RK, et al. (2011). Modulation of P-glycoprotein-mediated anticancer drug accumulation, cytotoxicity, and ATPase activity by flavonoid interactions. Nutr Cancer 63:435–443
   PubMed Web of Science ®Google Scholar
• Turchinovich A, Weiz L, Burwinkel B. (2013). Isolation of circulating microRNA associated with RNA-binding protein. In: Kosaka N, ed. Circulating microRNAs. New York: Springer. 97–107
   Google Scholar
• Valadi H, Ekström K, Bossios A, et al. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654–659
   PubMed Web of Science ®Google Scholar
• van der Kolk D, de Vries E, Noordhoek L, et al. (2001). Activity and expression of the multidrug resistance proteins P-glycoprotein, MRP1, MRP2, MRP3 and MRP5 in de novo and relapsed acute myeloid leukemia. Leukemia 15:1544–1553
   PubMed Web of Science ®Google Scholar
• van der Kolk DM, Vellenga E, Scheffer GL, et al. (2002). Expression and activity of breast cancer resistance protein (BCRP) in de novo and relapsed acute myeloid leukemia. Blood 99:3763–3770
   PubMed Web of Science ®Google Scholar
• Versantvoort C, Schuurhuis G, Pinedo H, et al. (1993). Genistein modulates the decreased drug accumulation in non-P-glycoprotein mediated multidrug resistant tumour cells. Br J Cancer 68:939–946
   PubMed Web of Science ®Google Scholar
• Villar VH, Vögler O, Barceló F, et al. (2013). Oleanolic and maslinic acid sensitize soft tissue sarcoma cells to doxorubicin by inhibiting the multidrug resistance protein MRP-1, but not P-glycoprotein. J Nutr Biochem 25:429–438
   PubMed Web of Science ®Google Scholar
• Volinia S, Calin GA, Liu CG, et al. (2006). A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 103:2257–2261
   PubMed Web of Science ®Google Scholar
• Vulsteke C, Lambrechts D, Dieudonné A, et al. (2013). Genetic variability in the multidrug resistance associated protein-1 (ABCC1/MRP1) predicts hematological toxicity in breast cancer patients receiving (neo-)adjuvant chemotherapy with 5-fluorouracil, epirubicin and cyclophosphamide (FEC). Ann Oncol 24:1513–1525
   PubMed Web of Science ®Google Scholar
• Wang S, Ryder H, Pretswell I, et al. (2002). Studies on quinazolinones as dual inhibitors of Pgp and MRP1 in multidrug resistance. Bioorg Med Chem Lett 12:571–574
   PubMed Web of Science ®Google Scholar
• Weng AP, Ferrando AA, Lee W, et al. (2004). Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306:269–271
   PubMed Web of Science ®Google Scholar
• Westlake CJ, Cole SPC, Deeley RG. (2005). Role of the NH2-terminal membrane spanning domain of multidrug resistance protein 1/ABCC1 in protein processing and trafficking. Mol Biol Cell 16:2483–2492
   PubMed Web of Science ®Google Scholar
• Westlake CJ, Payen L, Gao M, et al. (2004). Identification and characterization of functionally important elements in the multidrug resistance protein 1 COOH-terminal region. J Biol Chem 279:53571–53583
   PubMed Web of Science ®Google Scholar
• Wijnholds J, Evers R, van Leusden MR, et al. (1997). Increased sensitivity to anticancer drugs and decreased inflammatory response in mice lacking the multidrug resistance-associated protein. Nat Med 3:1275–1279
   PubMed Web of Science ®Google Scholar
• Williams Z, Ben-Dov IZ, Elias R, et al. (2013). Comprehensive profiling of circulating microRNA via small RNA sequencing of cDNA libraries reveals biomarker potential and limitations. Proc Natl Acad Sci U S A 110:4255–4260
   PubMed Web of Science ®Google Scholar
• Winter SS, Ricci J, Luo L, et al. (2013). ATP Binding Cassette C1 (ABCC1/MRP1)-mediated drug efflux contributes to disease progression in T-lineage acute lymphoblastic leukemia. Health 5:41–50
   PubMedGoogle Scholar
• Yoh K, Ishii G, Yokose T, et al. (2004). Breast cancer resistance protein impacts clinical outcome in platinum-based chemotherapy for advanced non-small cell lung cancer. Clin Cancer Res 10:1691–1697
   PubMed Web of Science ®Google Scholar
• Zhang B, Liu M, Tang HK, et al. (2012). The expression and significance of MRP1, LRP, TOPOIIβ, and BCL2 in tongue squamous cell carcinoma. J Oral Pathol Med 41:141–148
   PubMed Web of Science ®Google Scholar
• Zhang JT. (2000). Determinant of the extracellular location of the N-terminus of human multidrug-resistance-associated protein. Biochem J 348:597–606
   PubMed Web of Science ®Google Scholar