Mechanisms of Multidrug Resistance in Cancer (original) (raw)

• Lage H (2008) An overview of cancer multidrug resistance: a still unsolved problem. Cell Mol Life Sci 65:3145–3167
  Article CAS PubMed Google Scholar
• Mellor HR, Callaghan R (2008) Resistance to chemotherapy in cancer: a complex and integrated cellular response. Pharmacology 81:275–300
  Article CAS PubMed Google Scholar
• Mimeault M, Hauke R, Batra SK (2008) Recent advances on the molecular mechanisms involved in the drug resistance of cancer cells and novel targeting therapies. Clin Pharmacol Ther 83:673–691
  Article CAS PubMed Google Scholar
• Flaten GE, Dhanikula AB, Luthman K, Brandl M (2006) Drug permeability across a phospholipid vesicle based barrier: a novel approach for studying passive diffusion. Eur J Pharm Sci 27:80–90
  Article CAS PubMed Google Scholar
• Dobson PD, Kell DB (2008) Carrier-mediated cellular uptake of pharmaceutical drugs: an exception or the rule? Nat Rev Drug Discov 7:205–220
  Article CAS PubMed Google Scholar
• Assaraf YG (2007) Molecular basis of antifolate resistance. Cancer Metastasis Rev 26:153–181
  Article CAS PubMed Google Scholar
• Hediger MA, Romero MF, Peng JB et al (2004) The ABCs of solute carriers: physiological, pathological and therapeutic implications of human membrane transport proteins. Pflugers Arch 447:465–468
  Article CAS PubMed Google Scholar
• Gray JH, Owen RP, Giacomini KM (2004) The concentrative nucleoside transporter family, SLC28. Pflugers Arch 447:728–734
  Article CAS PubMed Google Scholar
• Young JD, Yao SY, Sun L, Cass CE, Baldwin SA (2008) Human equilibrative nucleoside transporter (ENT) family of nucleoside and nucleobase transporter proteins. Xenobiotica 38:995–1021
  Article CAS PubMed Google Scholar
• Zhang J, Visser F, King KM et al (2007) The role of nucleoside transporters in cancer chemotherapy with nucleoside drugs. Cancer Metastasis Rev 26:85–110
  Article PubMed CAS Google Scholar
• Mackey JR, Mani RS, Selner M et al (1998) Functional nucleoside transporters are required for gemcitabine influx and manifestation of toxicity in cancer cell lines. Cancer Res 58:4349–4357
  CAS PubMed Google Scholar
• Farrell JJ, Elsaleh H, Garcia M et al (2009) Human equilibrative nucleoside transporter 1 levels predict response to gemcitabine in patients with pancreatic cancer. Gastroenterology 136: 187–195
  Article PubMed Google Scholar
• Smith NF, Acharya MR, Desai N, Figg WD, Sparreboom A (2005) Identification of OATP1B3 as a high-affinity hepatocellular transporter of paclitaxel. Cancer Biol Ther 4:815–818
  Article CAS PubMed Google Scholar
• Smith NF, Marsh S, Scott-Horton TJ et al (2007) Variants in the SLCO1B3 gene: interethnic distribution and association with paclitaxel pharmacokinetics. Clin Pharmacol Ther 81:76–82
  Article CAS PubMed Google Scholar
• Hall MD, Okabe M, Shen DW, Liang XJ, Gottesman MM (2008) The role of cellular accumulation in determining sensitivity to platinum-based chemotherapy. Annu Rev Pharmacol Toxicol 48:495–535
  Article CAS PubMed Google Scholar
• Wang DS, Jonker JW, Kato Y et al (2002) Involvement of organic cation transporter 1 in hepatic and intestinal distribution of metformin. J Pharmacol Exp Ther 302:510–515
  Article CAS PubMed Google Scholar
• Kimura N, Masuda S, Tanihara Y et al (2005) Metformin is a superior substrate for renal organic cation transporter OCT2 rather than hepatic OCT1. Drug Metab Pharmacokinet 20:379–386
  Article CAS PubMed Google Scholar
• Okabe M, Szakacs G, Reimers MA et al (2008) Profiling SLCO and SLC22 genes in the NCI-60 cancer cell lines to identify drug uptake transporters. Mol Cancer Ther 7:3081–3091
  Article CAS PubMed Google Scholar
• Scherf U, Ross DT, Waltham M et al (2000) A gene expression database for the molecular pharmacology of cancer. Nat Genet 24:236–244
  Article CAS PubMed Google Scholar
• Rabow AA, Shoemaker RH, Sausville EA, Covell DG (2002) Mining the National Cancer Institute’s tumor-screening database: identification of compounds with similar cellular activities. J Med Chem 45:818–840
  Article CAS PubMed Google Scholar
• Shi LM, Fan Y, Lee JK et al (2000) Mining and visualizing large anticancer drug discovery databases. J Chem Inf Comput Sci 40:367–379
  CAS PubMed Google Scholar
• Weinstein JN, Kohn KW, Grever MR et al (1992) Neural computing in cancer drug development: predicting mechanism of action. Science 258:447–451
  Article CAS PubMed Google Scholar
• Weinstein JN, Myers TG, O’Connor PM et al (1997) An information-intensive approach to the molecular pharmacology of cancer. Science 275:343–349
  Article CAS PubMed Google Scholar
• Gillet JP, Efferth T, Remacle J (2007) Chemotherapy-induced resistance by ATP-binding cassette transporter genes. Biochim Biophys Acta 1775:237–262
  CAS PubMed Google Scholar
• Szakacs G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM (2006) Targeting multidrug resistance in cancer. Nat Rev Drug Discov 5:219–234
  Article CAS PubMed Google Scholar
• Callaghan R, Crowley E, Potter S, Kerr ID (2008) P-glycoprotein: so many ways to turn it on. J Clin Pharmacol 48:365–378
  Article CAS PubMed Google Scholar
• Deeley RG, Westlake C, Cole SP (2006) Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol Rev 86:849–899
  Article CAS PubMed Google Scholar
• Polgar O, Robey RW, Bates SE (2008) ABCG2: structure, function and role in drug response. Expert Opin Drug Metab Toxicol 4:1–15
  Article CAS PubMed Google Scholar
• Awasthi S, Singhal SS, Awasthi YC et al (2008) RLIP76 and Cancer. Clin Cancer Res 14:4372–4377
  Article CAS PubMed Google Scholar
• Kuo MT, Chen HH, Song IS, Savaraj N, Ishikawa T (2007) The roles of copper transporters in cisplatin resistance. Cancer Metastasis Rev 26:71–83
  Article CAS PubMed Google Scholar
• Drake KJ, Singhal J, Yadav S et al (2007) RALBP1/RLIP76 mediates multidrug resistance. Int J Oncol 30:139–144
  CAS PubMed Google Scholar
• Singhal SS, Singhal J, Nair MP et al (2007) Doxorubicin transport by RALBP1 and ABCG2 in lung and breast cancer. Int J Oncol 30:717–725
  CAS PubMed Google Scholar
• Gouaze-Andersson V, Cabot MC (2006) Glycosphingolipids and drug resistance. Biochim Biophys Acta 1758:2096–2103
  Article CAS PubMed Google Scholar
• Hendrich AB, Michalak K (2003) Lipids as a target for drugs modulating multidrug resistance of cancer cells. Curr Drug Targets 4:23–30
  Article CAS PubMed Google Scholar
• Thevissen K, Francois IE, Winderickx J, Pannecouque C, Cammue BP (2006) Ceramide involvement in apoptosis and apoptotic diseases. Mini Rev Med Chem 6:699–709
  Article CAS PubMed Google Scholar
• Gouaze-Andersson V, Yu JY, Kreitenberg AJ et al (2007) Ceramide and glucosylceramide upregulate expression of the multidrug resistance gene MDR1 in cancer cells. Biochim Biophys Acta 1771:1407–1417
  CAS PubMed Google Scholar
• Liu YY, Yu JY, Yin D et al (2008) A role for ceramide in driving cancer cell resistance to doxorubicin. FASEB J 22:2541–2551
  Article CAS PubMed Google Scholar
• Shen DW, Akiyama S, Schoenlein P, Pastan I, Gottesman MM (1995) Characterisation of high-level cisplatin-resistant cell lines established from a human hepatoma cell line and human KB adenocarcinoma cells: cross-resistance and protein changes. Br J Cancer 71:676–683
  CAS PubMed Google Scholar
• Shen D, Pastan I, Gottesman MM (1998) Cross-resistance to methotrexate and metals in human cisplatin-resistant cell lines results from a pleiotropic defect in accumulation of these compounds associated with reduced plasma membrane binding proteins. Cancer Res 58:268–275
  CAS PubMed Google Scholar
• Shen DW, Goldenberg S, Pastan I, Gottesman MM (2000) Decreased accumulation of (14C)carboplatin in human cisplatin-resistant cells results from reduced energy-dependent uptake. J Cell Physiol 183:108–116
  Article CAS PubMed Google Scholar
• Shen DW, Su A, Liang XJ, Pai-Panandiker A, Gottesman MM (2004) Reduced expression of small GTPases and hypermethylation of the folate binding protein gene in cisplatin-resistant cells. Br J Cancer 91:270–276
  CAS PubMed Google Scholar
• Liang XJ, Shen DW, Garfield S, Gottesman MM (2003) Mislocalization of membrane proteins associated with multidrug resistance in cisplatin-resistant cancer cell lines. Cancer Res 63:5909–5916
  CAS PubMed Google Scholar
• Liang XJ, Mukherjee S, Shen DW, Maxfield FR, Gottesman MM (2006) Endocytic recycling compartments altered in cisplatin-resistant cancer cells. Cancer Res 66:2346–2353
  Article CAS PubMed Google Scholar
• Chauhan SS, Liang XJ, Su AW et al (2003) Reduced endocytosis and altered lysosome function in cisplatin-resistant cell lines. Br J Cancer 88:1327–1334
  Article CAS PubMed Google Scholar
• Liang XJ, Yin JJ, Zhou JW et al (2004) Changes in biophysical parameters of plasma membranes influence cisplatin resistance of sensitive and resistant epidermal carcinoma cells. Exp Cell Res 293:283–291
  Article CAS PubMed Google Scholar
• Brown CM, Reisfeld B, Mayeno AN (2008) Cytochromes P450: a structure-based summary of biotransformations using representative substrates. Drug Metab Rev 40:1–100
  Article CAS PubMed Google Scholar
• Oyama T, Kagawa N, Kunugita N et al (2004) Expression of cytochrome P450 in tumor tissues and its association with cancer development. Front Biosci 9:1967–1976
  Article CAS PubMed Google Scholar
• Purnapatre K, Khattar SK, Saini KS (2008) Cytochrome P450s in the development of target-based anticancer drugs. Cancer Lett 259:1–15
  Article CAS PubMed Google Scholar
• van Schaik RH (2008) CYP450 pharmacogenetics for personalizing cancer therapy. Drug Resist Updat 11:77–98
  Article PubMed CAS Google Scholar
• Xie HJ, Yasar U, Lundgren S et al (2003) Role of polymorphic human CYP2B6 in cyclophosphamide bioactivation. Pharma­cogenomics J 3:53–61
  Article CAS PubMed Google Scholar
• Xie H, Griskevicius L, Stahle L et al (2006) Pharmacogenetics of cyclophosphamide in patients with hematological malignancies. Eur J Pharm Sci 27:54–61
  Article CAS PubMed Google Scholar
• Rodriguez-Novoa S, Barreiro P, Rendon A et al (2005) Influence of 516G>T polymorphisms at the gene encoding the CYP450–2B6 isoenzyme on efavirenz plasma concentrations in HIV-infected subjects. Clin Infect Dis 40:1358–1361
  Article CAS PubMed Google Scholar
• Rotger M, Colombo S, Furrer H et al (2005) Influence of CYP2B6 polymorphism on plasma and intracellular concentrations and toxicity of efavirenz and nevirapine in HIV-infected patients. Pharmacogenet Genomics 15:1–5
  Article CAS PubMed Google Scholar
• Wang J, Sonnerborg A, Rane A et al (2006) Identification of a novel specific CYP2B6 allele in Africans causing impaired metabolism of the HIV drug efavirenz. Pharmacogenet Genomics 16:191–198
  Article PubMed CAS Google Scholar
• Huttunen KM, Mahonen N, Raunio H, Rautio J (2008) Cytochrome P450-activated prodrugs: targeted drug delivery. Curr Med Chem 15:2346–2365
  Article CAS PubMed Google Scholar
• Pal D, Mitra AK (2006) MDR- and CYP3A4-mediated drug-drug interactions. J Neuro­immune Pharmacol 1:323–339
  Article PubMed Google Scholar
• Ghezzi P, Di Simplicio P (2007) Glutathiony­lation pathways in drug response. Curr Opin Pharmacol 7:398–403
  Article CAS PubMed Google Scholar
• Iyanagi T (2007) Molecular mechanism of phase I and phase II drug-metabolizing enzymes: implications for detoxification. Int Rev Cytol 260:35–112
  Article CAS PubMed Google Scholar
• Hemmerich S, Verdugo D, Rath VL (2004) Strategies for drug discovery by targeting sulfation pathways. Drug Discov Today 9:967–975
  Article CAS PubMed Google Scholar
• Townsend DM, Findlay VL, Tew KD (2005) Glutathione S-transferases as regulators of kinase pathways and anticancer drug targets. Methods Enzymol 401:287–307
  Article CAS PubMed Google Scholar
• Sorich MJ, Smith PA, Miners JO, Mackenzie PI, McKinnon RA (2008) Recent advances in the in silico modelling of UDP glucuronosyltransferase substrates. Curr Drug Metab 9:60–69
  Article CAS PubMed Google Scholar
• Gamage N, Barnett A, Hempel N et al (2006) Human sulfotransferases and their role in chemical metabolism. Toxicol Sci 90:5–22
  Article CAS PubMed Google Scholar
• Butcher NJ, Tiang J, Minchin RF (2008) Regulation of arylamine N-acetyltransferases. Curr Drug Metab 9:498–504
  Article CAS PubMed Google Scholar
• Ekhart C, Rodenhuis S, Smits PH, Beijnen JH, Huitema AD (2009) An overview of the relations between polymorphisms in drug metabolising enzymes and drug transporters and survival after cancer drug treatment. Cancer Treat Rev 35:18–31
  Article CAS PubMed Google Scholar
• Safaei R, Larson BJ, Cheng TC et al (2005) Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells. Mol Cancer Ther 4:1595–1604
  Article CAS PubMed Google Scholar
• Liang XJ, Shen DW, Chen KG et al (2005) Trafficking and localization of platinum complexes in cisplatin-resistant cell lines monitored by fluorescence-labeled platinum. J Cell Physiol 202:635–641
  Article CAS PubMed Google Scholar
• Safaei R, Katano K, Larson BJ et al (2005) Intracellular localization and trafficking of fluorescein-labeled cisplatin in human ovarian carcinoma cells. Clin Cancer Res 11:756–767
  CAS PubMed Google Scholar
• Kalayda GV, Wagner CH, Buss I, Reedijk J, Jaehde U (2008) Altered localisation of the copper efflux transporters ATP7A and ATP7B associated with cisplatin resistance in human ovarian carcinoma cells. BMC Cancer 8:175
  Article PubMed CAS Google Scholar
• Chen KG, Valencia JC, Lai B et al (2006) Melanosomal sequestration of cytotoxic drugs contributes to the intractability of malignant melanomas. Proc Natl Acad Sci USA 103:9903–9907
  Article CAS PubMed Google Scholar
• Chen KG, Szakacs G, Annereau JP et al (2005) Principal expression of two mRNA isoforms (ABCB 5alpha and ABCB 5beta ) of the ATP-binding cassette transporter gene ABCB 5 in melanoma cells and melanocytes. Pigment Cell Res 18:102–112
  Article CAS PubMed Google Scholar
• Steinbach D, Gillet JP, Sauerbrey A et al (2006) ABCA3 as a possible cause of drug resistance in childhood acute myeloid leukemia. Clin Cancer Res 12:4357–4363
  Article CAS PubMed Google Scholar
• Chapuy B, Koch R, Radunski U et al (2008) Intracellular ABC transporter A3 confers multidrug resistance in leukemia cells by lysosomal drug sequestration. Leukemia 22:1576–1586
  Article CAS PubMed Google Scholar
• Cheong N, Madesh M, Gonzales LW et al (2006) Functional and trafficking defects in ATP binding cassette A3 mutants associated with respiratory distress syndrome. J Biol Chem 281:9791–9800
  Article CAS PubMed Google Scholar
• Theocharis SE, Margeli AP, Klijanienko JT, Kouraklis GP (2004) Metallothionein expression in human neoplasia. Histopathology 45:103–118
  Article CAS PubMed Google Scholar
• Thirumoorthy N, Manisenthil Kumar KT, Shyam Sundar A, Panayappan L, Chatterjee M (2007) Metallothionein: an overview. World J Gastroenterol 13:993–996
  CAS PubMed Google Scholar
• Harper JW, Elledge SJ (2007) The DNA damage response: ten years after. Mol Cell 28:739–745
  Article CAS PubMed Google Scholar
• Ashwell S, Zabludoff S (2008) DNA damage detection and repair pathways–recent advances with inhibitors of checkpoint kinases in cancer therapy. Clin Cancer Res 14:4032–4037
  Article CAS PubMed Google Scholar
• Martin LP, Hamilton TC, Schilder RJ (2008) Platinum resistance: the role of DNA repair pathways. Clin Cancer Res 14:1291–1295
  Article CAS PubMed Google Scholar
• Sarkaria JN, Kitange GJ, James CD et al (2008) Mechanisms of chemoresistance to alkylating agents in malignant glioma. Clin Cancer Res 14:2900–2908
  Article CAS PubMed Google Scholar
• Hakem R (2008) DNA-damage repair; the good, the bad, and the ugly. EMBO J 27:589–605
  Article CAS PubMed Google Scholar
• Helleday T, Petermann E, Lundin C, Hodgson B, Sharma RA (2008) DNA repair pathways as targets for cancer therapy. Nat Rev Cancer 8:193–204
  Article CAS PubMed Google Scholar
• Dabholkar M, Bostick-Bruton F, Weber C et al (1992) ERCC1 and ERCC2 expression in malignant tissues from ovarian cancer patients. J Natl Cancer Inst 84:1512–1517
  Article CAS PubMed Google Scholar
• Kang S, Ju W, Kim JW et al (2006) Association between excision repair cross-complementation group 1 polymorphism and clinical outcome of platinum-based chemotherapy in patients with epithelial ovarian cancer. Exp Mol Med 38:320–324
  CAS PubMed Google Scholar
• Olaussen KA, Dunant A, Fouret P et al (2006) DNA repair by ERCC1 in non-small-cell lung cancer and cisplatin-based adjuvant chemotherapy. N Engl J Med 355:983–991
  Article CAS PubMed Google Scholar
• Metzger R, Leichman CG, Danenberg KD et al (1998) ERCC1 mRNA levels complement thymidylate synthase mRNA levels in predicting response and survival for gastric cancer patients receiving combination cisplatin and fluorouracil chemotherapy. J Clin Oncol 16:309–316
  CAS PubMed Google Scholar
• Fink D, Nebel S, Norris PS et al (1998) Enrichment for DNA mismatch repair-deficient cells during treatment with cisplatin. Int J Cancer 77:741–746
  Article CAS PubMed Google Scholar
• Strathdee G, MacKean MJ, Illand M, Brown R (1999) A role for methylation of the hMLH1 promoter in loss of hMLH1 expression and drug resistance in ovarian cancer. Oncogene 18:2335–2341
  Article CAS PubMed Google Scholar
• Karran P, Marinus MG (1982) Mismatch correction at O6-methylguanine residues in E. coli DNA. Nature 296:868–869
  Article CAS PubMed Google Scholar
• Yoshioka K, Yoshioka Y, Hsieh P (2006) ATR kinase activation mediated by MutSalpha and MutLalpha in response to cytotoxic O6-methylguanine adducts. Mol Cell 22:501–510
  Article CAS PubMed Google Scholar
• Verbeek B, Southgate TD, Gilham DE, Margison GP (2008) O6-Methylguanine-DNA methyltransferase inactivation and chemotherapy. Br Med Bull 85:17–33
  Article CAS PubMed Google Scholar
• Okada H, Mak TW (2004) Pathways of apoptotic and non-apoptotic death in tumour cells. Nat Rev Cancer 4:592–603
  Article CAS PubMed Google Scholar
• Broker LE, Kruyt FA, Giaccone G (2005) Cell death independent of caspases: a review. Clin Cancer Res 11:3155–3162
  Article PubMed Google Scholar
• Falschlehner C, Emmerich CH, Gerlach B, Walczak H (2007) TRAIL signalling: decisions between life and death. Int J Biochem Cell Biol 39:1462–1475
  Article CAS PubMed Google Scholar
• Tait SW, Green DR (2008) Caspase-independent cell death: leaving the set without the final cut. Oncogene 27:6452–6461
  Article CAS PubMed Google Scholar
• Rodriguez-Nieto S, Zhivotovsky B (2006) Role of alterations in the apoptotic machinery in sensitivity of cancer cells to treatment. Curr Pharm Des 12:4411–4425
  Article CAS PubMed Google Scholar
• Viktorsson K, Lewensohn R, Zhivotovsky B (2005) Apoptotic pathways and therapy resistance in human malignancies. Adv Cancer Res 94:143–196
  Article CAS PubMed Google Scholar
• Sjostrom J, Blomqvist C, von Boguslawski K et al (2002) The predictive value of bcl-2, bax, bcl-xL, bag-1, fas, and fasL for chemotherapy response in advanced breast cancer. Clin Cancer Res 8:811–816
  CAS PubMed Google Scholar
• Malamou-Mitsi V, Gogas H, Dafni U et al (2006) Evaluation of the prognostic and predictive value of p53 and Bcl-2 in breast cancer patients participating in a randomized study with dose-dense sequential adjuvant chemotherapy. Ann Oncol 17:1504–1511
  Article CAS PubMed Google Scholar
• Krug LM, Miller VA, Filippa DA et al (2003) Bcl-2 and bax expression in advanced non-small cell lung cancer: lack of correlation with chemotherapy response or survival in patients treated with docetaxel plus vinorelbine. Lung Cancer 39:139–143
  Article PubMed Google Scholar
• Bonetti A, Zaninelli M, Leone R et al (1998) Bcl-2 but not p53 expression is associated with resistance to chemotherapy in advanced breast cancer. Clin Cancer Res 4:2331–2336
  CAS PubMed Google Scholar
• Buchholz TA, Davis DW, McConkey DJ et al (2003) Chemotherapy-induced apoptosis and Bcl-2 levels correlate with breast cancer response to chemotherapy. Cancer J 9:33–41
  Article CAS PubMed Google Scholar
• Kedersha NL, Rome LH (1986) Isolation and characterization of a novel ribonucleoprotein particle: large structures contain a single species of small RNA. J Cell Biol 103:699–709
  Article CAS PubMed Google Scholar
• Kedersha NL, Heuser JE, Chugani DC, Rome LH (1991) Vaults. III. Vault ribonucleoprotein particles open into flower-like structures with octagonal symmetry. J Cell Biol 112:225–235
  Article CAS PubMed Google Scholar
• Rome L, Kedersha N, Chugani D (1991) Unlocking vaults: organelles in search of a function. Trends Cell Biol 1:47–50
  Article CAS PubMed Google Scholar
• Kedersha NL, Miquel MC, Bittner D, Rome LH (1990) Vaults. II. Ribonucleoprotein structures are highly conserved among higher and lower eukaryotes. J Cell Biol 110:895–901
  Article CAS PubMed Google Scholar
• van Zon A, Mossink MH, Scheper RJ, Sonneveld P, Wiemer EA (2003) The vault complex. Cell Mol Life Sci 60:1828–1837
  Article PubMed CAS Google Scholar
• Izquierdo MA, Scheffer GL, Flens MJ et al (1996) Broad distribution of the multidrug resistance-related vault lung resistance protein in normal human tissues and tumors. Am J Pathol 148:877–887
  CAS PubMed Google Scholar
• Kickhoefer VA, Rajavel KS, Scheffer GL et al (1998) Vaults are up-regulated in multidrug-resistant cancer cell lines. J Biol Chem 273:8971–8974
  Article CAS PubMed Google Scholar
• Mossink MH, van Zon A, Scheper RJ, Sonneveld P, Wiemer EA (2003) Vaults: a ribonucleoprotein particle involved in drug resistance? Oncogene 22:7458–7467
  Article CAS PubMed Google Scholar
• Steiner E, Holzmann K, Elbling L, Micksche M, Berger W (2006) Cellular functions of vaults and their involvement in multidrug resistance. Curr Drug Targets 7:923–934
  Article CAS PubMed Google Scholar
• Berger W, Steiner E, Grusch M, Elbling L, Micksche M (2009) Vaults and the major vault protein: novel roles in signal pathway regulation and immunity. Cell Mol Life Sci 66:43–61
  Article CAS PubMed Google Scholar
• Scheper RJ, Broxterman HJ, Scheffer GL et al (1993) Overexpression of a M(r) 110,000 vesicular protein in non-P-glycoprotein-mediated multidrug resistance. Cancer Res 53:1475–1479
  CAS PubMed Google Scholar
• Kitazono M, Okumura H, Ikeda R et al (2001) Reversal of LRP-associated drug resistance in colon carcinoma SW-620 cells. Int J Cancer 91:126–131
  Article CAS PubMed Google Scholar
• Kitazono M, Sumizawa T, Takebayashi Y et al (1999) Multidrug resistance and the lung resistance-related protein in human colon carcinoma SW-620 cells. J Natl Cancer Inst 91:1647–1653
  Article CAS PubMed Google Scholar
• Laurencot CM, Scheffer GL, Scheper RJ, Shoemaker RH (1997) Increased LRP mRNA expression is associated with the MDR phenotype in intrinsically resistant human cancer cell lines. Int J Cancer 72:1021–1026
  Article CAS PubMed Google Scholar
• Scheffer GL, Wijngaard PL, Flens MJ et al (1995) The drug resistance-related protein LRP is the human major vault protein. Nat Med 1:578–582
  Article CAS PubMed Google Scholar
• Siva AC, Raval-Fernandes S, Stephen AG et al (2001) Up-regulation of vaults may be necessary but not sufficient for multidrug resistance. Int J Cancer 92:195–202
  Article CAS PubMed Google Scholar
• van Zon A, Mossink MH, Schoester M et al (2004) Efflux kinetics and intracellular distribution of daunorubicin are not affected by major vault protein/lung resistance-related protein (vault) expression. Cancer Res 64:4887–4892
  Article PubMed Google Scholar
• Mossink MH, van Zon A, Franzel-Luiten E et al (2002) Disruption of the murine major vault protein (MVP/LRP) gene does not induce hypersensitivity to cytostatics. Cancer Res 62:7298–7304
  CAS PubMed Google Scholar
• Mossink MH, de Groot J, van Zon A et al (2003) Unimpaired dendritic cell functions in MVP/LRP knockout mice. Immunology 110:58–65
  Article CAS PubMed Google Scholar
• Jin S, Scotto KW (1998) Transcriptional regulation of the MDR1 gene by histone acetyltransferase and deacetylase is mediated by NF-Y. Mol Cell Biol 18:4377–4384
  CAS PubMed Google Scholar
• Li H, Liu H, Wang Z et al (2008) The role of transcription factors Sp1 and YY1 in proximal promoter region in initiation of transcription of the mu opioid receptor gene in human lymphocytes. J Cell Biochem 104:237–250
  Article CAS PubMed Google Scholar
• Tlsty TD, Coussens LM (2006) Tumor stroma and regulation of cancer development. Annu Rev Pathol 1:119–150
  Article CAS PubMed Google Scholar
• Cosse JP, Michiels C (2008) Tumour hypoxia affects the responsiveness of cancer cells to chemotherapy and promotes cancer progression. Anticancer Agents Med Chem 8:790–797
  CAS PubMed Google Scholar
• Netti PA, Berk DA, Swartz MA, Grodzinsky AJ, Jain RK (2000) Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 60:2497–2503
  CAS PubMed Google Scholar
• Heldin CH, Rubin K, Pietras K, Ostman A (2004) High interstitial fluid pressure – an obstacle in cancer therapy. Nat Rev Cancer 4:806–813
  Article CAS PubMed Google Scholar
• Tredan O, Galmarini CM, Patel K, Tannock IF (2007) Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst 99:1441–1454
  Article CAS PubMed Google Scholar
• Magzoub M, Jin S, Verkman AS (2008) Enhanced macromolecule diffusion deep in tumors after enzymatic digestion of extracellular matrix collagen and its associated proteoglycan decorin. FASEB J 22:276–284
  Article CAS PubMed Google Scholar
• Padera TP, Stoll BR, Tooredman JB et al (2004) Pathology: cancer cells compress intratumour vessels. Nature 427:695
  Article CAS PubMed Google Scholar
• Jain RK (1988) Determinants of tumor blood flow: a review. Cancer Res 48:2641–2658
  CAS PubMed Google Scholar
• Netti PA, Hamberg LM, Babich JW et al (1999) Enhancement of fluid filtration across tumor vessels: implication for delivery of macromolecules. Proc Natl Acad Sci USA 96:3137–3142
  Article CAS PubMed Google Scholar
• Leu AJ, Berk DA, Lymboussaki A, Alitalo K, Jain RK (2000) Absence of functional lymphatics within a murine sarcoma: a molecular and functional evaluation. Cancer Res 60:4324–4327
  CAS PubMed Google Scholar
• Salnikov AV, Iversen VV, Koisti M et al (2003) Lowering of tumor interstitial fluid pressure specifically augments efficacy of chemotherapy. FASEB J 17:1756–1758
  CAS PubMed Google Scholar
• Roos A (1978) Weak acids, weak bases and intracellular pH. Respir Physiol 33:27–30
  Article CAS PubMed Google Scholar
• Gerweck LE, Vijayappa S, Kozin S (2006) Tumor pH controls the in vivo efficacy of weak acid and base chemotherapeutics. Mol Cancer Ther 5:1275–1279
  Article CAS PubMed Google Scholar
• Boyer MJ (1997) Bioreductive agents: a clinical update. Oncol Res 9:391–395
  CAS PubMed Google Scholar
• Lluis JM, Morales A, Blasco C et al (2005) Critical role of mitochondrial glutathione in the survival of hepatocytes during hypoxia. J Biol Chem 280:3224–3232
  Article CAS PubMed Google Scholar
• Murphy BJ, Laderoute KR, Chin RJ, Sutherland RM (1994) Metallothionein IIA is up-regulated by hypoxia in human A431 squamous carcinoma cells. Cancer Res 54:5808–5810
  CAS PubMed Google Scholar
• Comerford KM, Wallace TJ, Karhausen J et al (2002) Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res 62:3387–3394
  CAS PubMed Google Scholar
• Liu L, Ning X, Sun L et al (2008) Hypoxia-inducible factor-1 alpha contributes to hypoxia-induced chemoresistance in gastric cancer. Cancer Sci 99:121–128
  CAS PubMed Google Scholar
• Han HK, Han CY, Cheon EP, Lee J, Kang KW (2007) Role of hypoxia-inducible factor-alpha in hepatitis-B-virus X protein-mediated MDR1 activation. Biochem Biophys Res Commun 357:567–573
  Article CAS PubMed Google Scholar
• Song X, Liu X, Chi W et al (2006) Hypoxia-induced resistance to cisplatin and doxorubicin in non-small cell lung cancer is inhibited by silencing of HIF-1alpha gene. Cancer Chemother Pharmacol 58:776–784
  Article CAS PubMed Google Scholar
• Krishnamurthy P, Ross DD, Nakanishi T et al (2004) The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J Biol Chem 279:24218–24225
  Article CAS PubMed Google Scholar
• Alkatout I, Kabelitz D, Kalthoff H, Tiwari S (2008) Prowling wolves in sheep’s clothing: the search for tumor stem cells. Biol Chem 389:799–811
  Article CAS PubMed Google Scholar
• Trumpp A, Wiestler OD (2008) Mechanisms of Disease: cancer stem cells–targeting the evil twin. Nat Clin Pract Oncol 5:337–347
  CAS PubMed Google Scholar
• Kim M, Turnquist H, Jackson J et al (2002) The multidrug resistance transporter ABCG2 (breast cancer resistance protein 1) effluxes Hoechst 33342 and is overexpressed in hematopoietic stem cells. Clin Cancer Res 8:22–28
  CAS PubMed Google Scholar
• Zhou S, Schuetz JD, Bunting KD et al (2001) The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 7:1028–1034
  Article CAS PubMed Google Scholar
• Bunting KD (2002) ABC transporters as phenotypic markers and functional regulators of stem cells. Stem Cells 20:11–20
  Article CAS PubMed Google Scholar
• Hirschmann-Jax C, Foster AE, Wulf GG et al (2004) A distinct “side population” of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA 101:14228–14233
  Article CAS PubMed Google Scholar
• Schatton T, Murphy GF, Frank NY et al (2008) Identification of cells initiating human melanomas. Nature 451:345–349
  Article CAS PubMed Google Scholar
• Frank NY, Margaryan A, Huang Y et al (2005) ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res 65:4320–4333
  Article CAS PubMed Google Scholar
• Frank NY, Pendse SS, Lapchak PH et al (2003) Regulation of progenitor cell fusion by ABCB5 P-glycoprotein, a novel human ATP-binding cassette transporter. J Biol Chem 278:47156–47165
  Article CAS PubMed Google Scholar
• Fromm MF (2004) Importance of P-glyco­protein at blood-tissue barriers. Trends Pharmacol Sci 25:423–429
  Article CAS PubMed Google Scholar
• Borst P, Elferink RO (2002) Mammalian ABC transporters in health and disease. Annu Rev Biochem 71:537–592
  Article CAS PubMed Google Scholar
• Trowsdale J, Hanson I, Mockridge I et al (1990) Sequences encoded in the class II region of the MHC related to the ‘ABC’ superfamily of transporters. Nature 348:741–744
  Article CAS PubMed Google Scholar
• Abele R, Tampe R (2004) The ABCs of immunology: structure and function of TAP, the transporter associated with antigen processing. Physiology (Bethesda) 19:216–224
  CAS Google Scholar
• Takahashi K, Kimura Y, Nagata K et al (2005) ABC proteins: key molecules for lipid homeostasis. Med Mol Morphol 38:2–12
  Article CAS PubMed 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
  Article CAS PubMed Google Scholar
• Ueda K, Cardarelli C, Gottesman MM, Pastan I (1987) Expression of a full-length cDNA for the human “_MDR1_” gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc Natl Acad Sci USA 84:3004–3008
  Article CAS PubMed Google Scholar
• Ueda K, Clark DP, Chen CJ et al (1987) The human multidrug resistance (mdr1) gene. cDNA cloning and transcription initiation. J Biol Chem 262:505–508
  CAS PubMed Google Scholar
• Cole SP, Bhardwaj G, Gerlach JH et al (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258:1650–1654
  Article CAS PubMed Google Scholar
• Doyle LA, Yang W, Abruzzo LV et al (1998) A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci USA 95:15665–15670
  Article CAS PubMed Google Scholar
• Ambudkar SV, Kim IW, Sauna ZE (2006) The power of the pump: mechanisms of action of P-glycoprotein (ABCB1). Eur J Pharm Sci 27:392–400
  Article CAS PubMed Google Scholar
• Cascorbi I (2006) Role of pharmacogenetics of ATP-binding cassette transporters in the pharmacokinetics of drugs. Pharmacol Ther 112:457–473
  Article CAS PubMed Google Scholar
• Choudhuri S, Klaassen CD (2006) Structure, function, expression, genomic organization, and single nucleotide polymorphisms of human ABCB1 (MDR1), ABCC (MRP), and ABCG2 (BCRP) efflux transporters. Int J Toxicol 25:231–259
  Article CAS PubMed Google Scholar
• Ieiri I, Takane H, Otsubo K (2004) The MDR1 (ABCB1) gene polymorphism and its clinical implications. Clin Pharmacokinet 43:553–576
  Article CAS PubMed Google Scholar
• Kimchi-Sarfaty C, Oh JM, Kim IW et al (2007) A “silent” polymorphism in the MDR1 gene changes substrate specificity. Science 315:525–528
  Article CAS PubMed Google Scholar
• Fung KL, Gottesman MM (2009) A synonymous polymorphism in a common MDR1 (ABCB1) haplotype shapes protein function. Biochim Biophys Acta 1794:860–871
  CAS PubMed Google Scholar
• Kohno K, Sato S, Takano H, Matsuo K, Kuwano M (1989) The direct activation of human multidrug resistance gene (MDR1) by anticancer agents. Biochem Biophys Res Commun 165:1415–1421
  Article CAS PubMed Google Scholar
• Chaudhary PM, Roninson IB (1993) Induction of multidrug resistance in human cells by transient exposure to different chemotherapeutic drugs. J Natl Cancer Inst 85:632–639
  Article CAS PubMed Google Scholar
• Robey RW, Polgar O, Deeken J, To KW, Bates SE (2007) ABCG2: determining its relevance in clinical drug resistance. Cancer Metastasis Rev 26:39–57
  Article CAS PubMed Google Scholar
• Hirose M, Hosoi E, Hamano S, Jalili A (2003) Multidrug resistance in hematological malignancy. J Med Invest 50:126–135
  PubMed Google Scholar
• Ross DD (2000) Novel mechanisms of drug resistance in leukemia. Leukemia 14:467–473
  Article CAS PubMed Google Scholar
• van den Heuvel-Eibrink MM, Sonneveld P, Pieters R (2000) The prognostic significance of membrane transport-associated multidrug resistance (MDR) proteins in leukemia. Int J Clin Pharmacol Ther 38:94–110
  PubMed Google Scholar
• Marie JP, Legrand O (1999) MDR1/P-GP expression as a prognostic factor in acute leukemias. Adv Exp Med Biol 457:1–9
  CAS PubMed Google Scholar
• Wuchter C, Leonid K, Ruppert V et al (2000) Clinical significance of P-glycoprotein expression and function for response to induction chemotherapy, relapse rate and overall survival in acute leukemia. Haematologica 85:711–721
  CAS PubMed Google Scholar
• Tafuri A, Gregorj C, Petrucci MT et al (2002) MDR1 protein expression is an independent predictor of complete remission in newly diagnosed adult acute lymphoblastic leukemia. Blood 100:974–981
  Article CAS PubMed Google Scholar
• Wattel E, Lepelley P, Merlat A et al (1995) Expression of the multidrug resistance P glycoprotein in newly diagnosed adult acute lymphoblastic leukemia: absence of correlation with response to treatment. Leukemia 9:1870–1874
  CAS PubMed 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
  Article CAS PubMed Google Scholar
• Leonessa F, Clarke R (2003) ATP binding cassette transporters and drug resistance in breast cancer. Endocr Relat Cancer 10:43–73
  Article CAS PubMed Google Scholar
• Efferth T, Gillet JP, Sauerbrey A et al (2006) Expression profiling of ATP-binding cassette transporters in childhood T-cell acute lymphoblastic leukemia. Mol Cancer Ther 5:1986–1994
  Article CAS PubMed Google Scholar
• Gillet JP, Schneider J, Bertholet V et al (2006) Microarray Expression Profiling of ABC Transporters in Human Breast Cancer. Cancer Genom Proteom 3:97–106
  CAS Google Scholar
• Gillet JP, Efferth T, Steinbach D et al (2004) Microarray-based detection of multidrug resistance in human tumor cells by expression profiling of ATP-binding cassette transporter genes. Cancer Res 64:8987–8993
  Article CAS PubMed Google Scholar
• Szakacs G, Annereau JP, Lababidi S et al (2004) Predicting drug sensitivity and resistance: profiling ABC transporter genes in cancer cells. Cancer Cell 6:129–137
  Article CAS PubMed Google Scholar
• Rhodes DR, Chinnaiyan AM (2005) Integrative analysis of the cancer transcriptome. Nat Genet 37(Suppl):S31–S37
  Article CAS PubMed Google Scholar
• Rhodes DR, Kalyana-Sundaram S, Mahavisno V et al (2007) Oncomine 3.0: genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles. Neoplasia 9:166–180
  Article CAS PubMed Google Scholar
• Rhodes DR, Kalyana-Sundaram S, Tomlins SA et al (2007) Molecular concepts analysis links tumors, pathways, mechanisms, and drugs. Neoplasia 9:443–454
  Article CAS PubMed Google Scholar
• Rhodes DR, Yu J, Shanker K et al (2004) ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 6:1–6
  CAS PubMed Google Scholar
• Annereau JP, Szakacs G, Tucker CJ et al (2004) Analysis of ATP-binding cassette transporter expression in drug-selected cell lines by a microarray dedicated to multidrug resistance. Mol Pharmacol 66:1397–1405
  Article CAS PubMed Google Scholar
• Orina JN, Calcagno AM, Wu C-P, et al (2009) Evaluation of current methods to analyze the expression profiles of ABC transporters yields an improved drug-discovery database. Mol Cancer Ther 8:2057–2066
  Article CAS PubMed Google Scholar
• Filipits M, Stranzl T, Pohl G et al (2000) Drug resistance factors in acute myeloid leukemia: a comparative analysis. Leukemia 14:68–76
  Article CAS PubMed Google Scholar
• Hart SM, Ganeshaguru K, Scheper RJ et al (1997) Expression of the human major vault protein LRP in acute myeloid leukemia. Exp Hematol 25:1227–1232
  CAS PubMed Google Scholar
• List AF, Spier CS, Grogan TM et al (1996) Overexpression of the major vault transporter protein lung-resistance protein predicts treatment outcome in acute myeloid leukemia. Blood 87:2464–2469
  CAS PubMed Google Scholar
• Xu D, Arestrom I, Virtala R et al (1999) High levels of lung resistance related protein mRNA in leukaemic cells from patients with acute myelogenous leukaemia are associated with inferior response to chemotherapy and prior treatment with mitoxantrone. Br J Haematol 106:627–633
  Article CAS PubMed Google Scholar
• Legrand O, Simonin G, Beauchamp-Nicoud A, Zittoun R, Marie JP (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
  CAS PubMed 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
  CAS PubMed Google Scholar
• Schaich M, Soucek S, Thiede C, Ehninger G, Illmer T (2005) MDR1 and MRP1 gene expression are independent predictors for treatment outcome in adult acute myeloid leukaemia. Br J Haematol 128:324–332
  Article CAS PubMed Google Scholar
• Sunnaram BL, Gandemer V, Sebillot M et al (2003) LRP overexpression in monocytic lineage. Leuk Res 27:755–759
  Article CAS PubMed Google Scholar
• van den Heuvel-Eibrink MM, Wiemer EA, Prins A et al (2002) Increased expression of the breast cancer resistance protein (BCRP) in relapsed or refractory acute myeloid leukemia (AML). Leukemia 16:833–839
  Article PubMed CAS Google Scholar
• Borg AG, Burgess R, Green LM, Scheper RJ, Yin JA (1998) Overexpression of lung-resistance protein and increased P-glycoprotein function in acute myeloid leukaemia cells predict a poor response to chemotherapy and reduced patient survival. Br J Haematol 103:1083–1091
  Article CAS PubMed Google Scholar
• Filipits M, Pohl G, Stranzl T et al (1998) Expression of the lung resistance protein predicts poor outcome in de novo acute myeloid leukemia. Blood 91:1508–1513
  CAS PubMed Google Scholar
• Pirker R, Pohl G, Stranzl T et al (1999) The lung resistance protein (LRP) predicts poor outcome in acute myeloid leukemia. Adv Exp Med Biol 457:133–139
  CAS PubMed Google Scholar
• Oh EJ, Kahng J, Kim Y et al (2003) Expression of functional markers in acute lymphoblastic leukemia. Leuk Res 27:903–908
  Article CAS PubMed Google Scholar
• Valera ET, Scrideli CA, Queiroz RG, Mori BM, Tone LG (2004) Multiple drug resistance protein (MDR-1), multidrug resistance-related protein (MRP) and lung resistance protein (LRP) gene expression in childhood acute lymphoblastic leukemia. Sao Paulo Med J 122:166–171
  Article PubMed Google Scholar
• Volm M, Stammler G, Zintl F, Koomagi R, Sauerbrey A (1997) Expression of lung resistance-related protein (LRP) in initial and relapsed childhood acute lymphoblastic leukemia. Anticancer Drugs 8:662–665
  Article CAS PubMed Google Scholar
• Ohno N, Tani A, Uozumi K et al (2001) Expression of functional lung resistance–related protein predicts poor outcome in adult T-cell leukemia. Blood 98:1160–1165
  Article CAS PubMed Google Scholar
• Filipits M, Drach J, Pohl G et al (1999) Expression of the lung resistance protein predicts poor outcome in patients with multiple myeloma. Clin Cancer Res 5:2426–2430
  CAS PubMed Google Scholar
• Raaijmakers HG, Izquierdo MA, Lokhorst HM et al (1998) Lung-resistance-related protein expression is a negative predictive factor for response to conventional low but not to intensified dose alkylating chemotherapy in multiple myeloma. Blood 91:1029–1036
  CAS PubMed Google Scholar
• Rimsza LM, Campbell K, Dalton WS et al (1999) The major vault protein (MVP), a new multidrug resistance associated protein, is frequently expressed in multiple myeloma. Leuk Lymphoma 34:315–324
  CAS PubMed Google Scholar
• Brinkhuis M, Izquierdo MA, Baak JP et al (2002) Expression of multidrug resistance-associated markers, their relation to quantitative pathologic tumour characteristics and prognosis in advanced ovarian cancer. Anal Cell Pathol 24:17–23
  CAS PubMed Google Scholar
• Izquierdo MA, van der Zee AG, Vermorken JB et al (1995) Drug resistance-associated marker Lrp for prediction of response to chemotherapy and prognoses in advanced ovarian carcinoma. J Natl Cancer Inst 87: 1230–1237
  Article CAS PubMed Google Scholar
• Mayr D, Pannekamp U, Baretton GB et al (2000) Immunohistochemical analysis of drug resistance-associated proteins in ovarian carcinomas. Pathol Res Pract 196:469–475
  CAS PubMed Google Scholar
• Arts HJ, Katsaros D, de Vries EG et al (1999) Drug resistance-associated markers P-glycoprotein, multidrug resistance-associated protein 1, multidrug resistance-associated protein 2, and lung resistance protein as prognostic factors in ovarian carcinoma. Clin Cancer Res 5:2798–2805
  CAS PubMed Google Scholar
• Burger H, Foekens JA, Look MP et al (2003) RNA expression of breast cancer resistance protein, lung resistance-related protein, multidrug resistance-associated proteins 1 and 2, and multidrug resistance gene 1 in breast cancer: correlation with chemotherapeutic response. Clin Cancer Res 9:827–836
  CAS PubMed Google Scholar
• Linn SC, Pinedo HM, van Ark-Otte J et al (1997) Expression of drug resistance proteins in breast cancer, in relation to chemotherapy. Int J Cancer 71:787–795
  Article CAS PubMed Google Scholar
• Schneider J, Lucas R, Sanchez J et al (2000) Modulation of molecular marker expression by induction chemotherapy in locally advanced breast cancer: correlation with the response to therapy and the expression of MDR1 and LRP. Anticancer Res 20:4373–4377
  CAS PubMed Google Scholar
• Kanzaki A, Toi M, Nakayama K et al (2001) Expression of multidrug resistance-related transporters in human breast carcinoma. Jpn J Cancer Res 92:452–458
  CAS PubMed Google Scholar
• Pohl G, Filipits M, Suchomel RW et al (1999) Expression of the lung resistance protein (LRP) in primary breast cancer. Anticancer Res 19:5051–5055
  CAS PubMed Google Scholar
• Volm M, Mattern J, Koomagi R (1997) Expression of lung resistance-related protein (LRP) in non-small cell lung carcinomas of smokers and non-smokers and its predictive value for doxorubicin resistance. Anticancer Drugs 8:931–936
  Article CAS PubMed Google Scholar
• Volm M, Rittgen W (2000) Cellular predictive factors for the drug response of lung cancer. Anticancer Res 20:3449–3458
  CAS PubMed Google Scholar
• Chiou JF, Liang JA, Hsu WH et al (2003) Comparing the relationship of Taxol-based chemotherapy response with P-glycoprotein and lung resistance-related protein expression in non-small cell lung cancer. Lung 181:267–273
  Article CAS PubMed Google Scholar
• Dingemans AM, van Ark-Otte J, van der Valk P et al (1996) Expression of the human major vault protein LRP in human lung cancer samples and normal lung tissues. Ann Oncol 7:625–630
  CAS PubMed 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
  Article CAS PubMed 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
  Article CAS PubMed Google Scholar
• Uozaki H, Horiuchi H, Ishida T et al (1997) Overexpression of resistance-related proteins (metallothioneins, glutathione-S-transferase pi, heat shock protein 27, and lung resistance-related protein) in osteosarcoma. Relationship with poor prognosis. Cancer 79:2336–2344
  Article CAS PubMed Google Scholar
• Gaumann A, Tews DS, Mentzel T et al (2003) Expression of drug resistance related proteins in sarcomas of the pulmonary artery and poorly differentiated leiomyosarcomas of other origin. Virchows Arch 442:529–537
  CAS PubMed Google Scholar
• Plaat BE, Hollema H, Molenaar WM et al (2000) Soft tissue leiomyosarcomas and malignant gastrointestinal stromal tumors: differences in clinical outcome and expression of multidrug resistance proteins. J Clin Oncol 18:3211–3220
  CAS PubMed Google Scholar
• Zurita AJ, Diestra JE, Condom E et al (2003) Lung resistance-related protein as a predictor of clinical outcome in advanced testicular germ-cell tumours. Br J Cancer 88:879–886
  Article CAS PubMed Google Scholar
• Mandoky L, Geczi L, Doleschall Z et al (2004) Expression and prognostic value of the lung resistance-related protein (LRP) in germ cell testicular tumors. Anticancer Res 24:1097–1104
  CAS PubMed Google Scholar
• Boonstra R, Timmer-Bosscha H, van Echten-Arends J et al (2004) Mitoxantrone resistance in a small cell lung cancer cell line is associated with ABCA2 upregulation. Br J Cancer 90:2411–2417
  CAS PubMed Google Scholar
• Vulevic B, Chen Z, Boyd JT et al (2001) Cloning and characterization of human adenosine 5′-triphosphate-binding cassette, sub-family A, transporter 2 (ABCA2). Cancer Res 61:3339–3347
  CAS PubMed Google Scholar
• Takara K, Sakaeda T, Okumura K (2006) An update on overcoming MDR1-mediated multidrug resistance in cancer chemotherapy. Curr Pharm Des 12:273–286
  Article CAS PubMed Google Scholar
• Calcagno AM, Kim IW, Wu CP, Shukla S, Ambudkar SV (2007) ABC drug transporters as molecular targets for the prevention of multidrug resistance and drug-drug interactions. Curr Drug Deliv 4:324–333
  Article CAS PubMed Google Scholar
• Smith AJ, van Helvoort A, van Meer G et al (2000) MDR3 P-glycoprotein, a phosphatidylcholine translocase, transports several cytotoxic drugs and directly interacts with drugs as judged by interference with nucleotide trapping. J Biol Chem 275:23530–23539
  Article CAS PubMed Google Scholar
• Huang Y, Anderle P, Bussey KJ et al (2004) Membrane transporters and channels: role of the transportome in cancer chemosensitivity and chemoresistance. Cancer Res 64:4294–4301
  Article CAS PubMed Google Scholar
• Childs S, Yeh RL, Hui D, Ling V (1998) Taxol resistance mediated by transfection of the liver-specific sister gene of P-glycoprotein. Cancer Res 58:4160–4167
  CAS PubMed Google Scholar
• Deeley RG, Cole SP (2006) Substrate recognition and transport by multidrug resistance protein 1 (ABCC1). FEBS Lett 580:1103–1111
  Article CAS PubMed Google Scholar
• Guminski AD, Balleine RL, Chiew YE et al (2006) MRP2 (ABCC2) and cisplatin sensitivity in hepatocytes and human ovarian carcinoma. Gynecol Oncol 100:239–246
  Article CAS PubMed Google Scholar
• Huisman MT, Chhatta AA, van Tellingen O, Beijnen JH, Schinkel AH (2005) MRP2 (ABCC2) transports taxanes and confers paclitaxel resistance and both processes are stimulated by probenecid. Int J Cancer 116:824–829
  Article CAS PubMed Google Scholar
• Jedlitschky G, Hoffmann U, Kroemer HK (2006) Structure and function of the MRP2 (ABCC2) protein and its role in drug disposition. Expert Opin Drug Metab Toxicol 2:351–366
  Article CAS PubMed Google Scholar
• Materna V, Stege A, Surowiak P, Priebsch A, Lage H (2006) RNA interference-triggered reversal of ABCC2-dependent cisplatin resistance in human cancer cells. Biochem Biophys Res Commun 348:153–157
  Article CAS PubMed Google Scholar
• Zelcer N, Saeki T, Reid G, Beijnen JH, Borst P (2001) Characterization of drug transport by the human multidrug resistance protein 3 (ABCC3). J Biol Chem 276:46400–46407
  Article CAS PubMed Google Scholar
• Zeng H, Chen ZS, Belinsky MG, Rea PA, Kruh GD (2001) Transport of methotrexate (MTX) and folates by multidrug resistance protein (MRP) 3 and MRP1: effect of polyglutamylation on MTX transport. Cancer Res 61:7225–7232
  CAS PubMed Google Scholar
• Chen ZS, Lee K, Kruh GD (2001) Transport of cyclic nucleotides and estradiol 17-beta-d-glucuronide by multidrug resistance protein 4. Resistance to 6-mercaptopurine and 6-thioguanine. J Biol Chem 276:33747–33754
  Article CAS PubMed Google Scholar
• Ritter CA, Jedlitschky G, Meyer zu Schwabedissen H et al (2005) Cellular export of drugs and signaling molecules by the ATP-binding cassette transporters MRP4 (ABCC4) and MRP5 (ABCC5). Drug Metab Rev 37:253–278
  Article CAS PubMed Google Scholar
• Tian Q, Zhang J, Chan SY et al (2006) Topotecan is a substrate for multidrug resistance associated protein 4. Curr Drug Metab 7:105–118
  Article CAS PubMed Google Scholar
• Tian Q, Zhang J, Tan TM et al (2005) Human multidrug resistance associated protein 4 confers resistance to camptothecins. Pharm Res 22:1837–1853
  Article CAS PubMed Google Scholar
• Pratt S, Shepard RL, Kandasamy RA et al (2005) The multidrug resistance protein 5 (ABCC5) confers resistance to 5-fluorouracil and transports its monophosphorylated metabolites. Mol Cancer Ther 4:855–863
  Article CAS PubMed Google Scholar
• Belinsky MG, Chen ZS, Shchaveleva I, Zeng H, Kruh GD (2002) Characterization of the drug resistance and transport properties of multidrug resistance protein 6 (MRP6, ABCC6). Cancer Res 62:6172–6177
  CAS PubMed Google Scholar
• Naramoto H, Uematsu T, Uchihashi T et al (2007) Multidrug resistance-associated protein 7 expression is involved in cross-resistance to docetaxel in salivary gland adenocarcinoma cell lines. Int J Oncol 30:393–401
  CAS PubMed Google Scholar
• Hopper-Borge E, Chen ZS, Shchaveleva I, Belinsky MG, Kruh GD (2004) Analysis of the drug resistance profile of multidrug resistance protein 7 (ABCC10): resistance to docetaxel. Cancer Res 64:4927–4930
  Article CAS PubMed Google Scholar
• Chen ZS, Guo Y, Belinsky MG, Kotova E, Kruh GD (2005) Transport of bile acids, sulfated steroids, estradiol 17-beta-d-glucuronide, and leukotriene C4 by human multidrug resistance protein 8 (ABCC11). Mol Pharmacol 67:545–557
  Article CAS PubMed Google Scholar
• Guo Y, Kotova E, Chen ZS et al (2003) MRP8, ATP-binding cassette C11 (ABCC11), is a cyclic nucleotide efflux pump and a resistance factor for fluoropyrimidines 2′, 3′-dideoxycytidine and 9′-(2′-phosphonylmethoxyethyl)adenine. J Biol Chem 278:29509–29514
  Article CAS PubMed Google Scholar