ABC transporters in the development of multidrug resistance in cancer therapy

Current Pharmaceutical Design

Volumn 22, Issue 30, 2016, Pages 4705-4716

  Długosz, Angelika ^a   Janecka, Anna ^a  

^a MEDICAL UNIVERSITY OF LODZ   (Poland)

Author keywords

ABC transporters; Efflux pumps; Gene expression; Multidrug resistance

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER A; ABC TRANSPORTER B; ABC TRANSPORTER C; ABC TRANSPORTER E; ABC TRANSPORTER F; ABC TRANSPORTER G; ANTINEOPLASTIC AGENT; BIRICODAR; CYCLOSPORIN; ELACRIDAR; TARIQUIDAR; UNCLASSIFIED DRUG;

BRAIN CANCER; BREAST CANCER; CANCER CELL; CANCER THERAPY; ESOPHAGUS CANCER; GENETIC POLYMORPHISM; HEMATOLOGIC MALIGNANCY; HUMAN; LUNG CANCER; MULTIDRUG RESISTANCE; NASOPHARYNX CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; CHEMISTRY; DRUG EFFECTS; DRUG RESISTANCE; METABOLISM; NEOPLASM;

ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; HUMANS; NEOPLASMS;

EID: 84989266622     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612822666160302103646     Document Type: Review

References (208)

1. Cui H, Zhang AJ, Chen M, Liu JJ. ABC Transporter inhibitors in reversing multidrug resistance to chemotherapy. Curr Drug Targets 2015; 22: 1356-71.
2. Sharom FJ. ABC multidrug transporters: Structure, function and role in chemoresistance. Pharmacogenomics 2008; 9: 105-27.
3. Deeley RG, Westlake C, Cole SP. Transmembrane transport of endo-and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol Rev 2006; 86: 849-99.
4. Katayama K, Noguchi K, Sugimoto Y. Regulations of PGlycoprotein/ ABCB1/MDR1 in Human Cancer Cells. New J Sci 2014; 10.
5. Juliano RL, Ling V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta 1976; 455: 152-62.
6. Rees DC, Johnson E, Lewinson O. ABC transporters: the power to change. Nat Rev Mol Cell Biol 2009; 10: 218-27.
7. Tarling EJ, de Aguiar Vallim TQ, Edwards PA. Role of ABC transporters in lipid transport and human disease. Trends Endocrinol Metab 2013; 24 (7): 342-50.
8. ter Beek J, Guskov A, Slotboom DJ. Structural diversity of ABC transporters. J Gen Physiol 2014; 143 (4): 419-35.
9. Chang X. A molecular understanding of ATP-dependent solute transport by multidrug resistance-associated protein MRP1. Cancer Metastasis Rev 2007; 26: 15-37.
10. Honorat M, Falson P, Terreux R, Di Pietro A, Dumontet C, Payen L. Multidrug resistance ABC transporter structure predictions by homology modeling approaches. Curr Drug Metab 2011; 12: 268-77.
11. Dean M. ABC transporters, drug resistance, and cancer stem cells. J. Mammary Gland Biol. Neoplasia 2009; 14: 3-9.
12. Rosa L López-Marqués, Poulsen LR, et al. Structure and mechanism of ATP-dependent phospholipid transporters. Biochim Biophys Acta 2014; 10: 1016.
13. Tiwari AK, Sodani K, Dai CL, Ashby CR Jr., Chen ZS. Revisiting the ABCs of multidrug resistance in cancer chemotherapy. Curr Pharm Biotechnol 2011; 12: 570-94.
14. Vasiliou V, Vasiliou K, Nebert DW. Human ATP-binding cassette (ABC) transporter family. Hum Genom 2009; 3 (3): 281-90.
15. Holohan C, Van Schaeybroeck S, Longley DB, Johnston PG. Cancer drug resistance: an evolving paradigm.Nat Rev Cancer 2013; 13 (10): 714-26.
16. Yin JY, Huang Q, Yang Y, et al. Characterization and analyses of multidrug resistance-associated protein 1 (MRP1/ABCC1) polymorphisms in Chinese population. Pharmacogenet Genom 2009; 19 (3): 206-16.
17. Yin J, Zhang J. Multidrug resistance-associated protein 1 (MRP1/ABCC1) polymorphism: from discovery to clinical application. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2011; 36 (10): 927-38.
18. Marie JP, Zhou DC, Gurbuxani S, Legrand O, Zittoun R. MDR1/P-glycoprotein in haematological neoplasms. Eur J Cancer 1996; 32: 1034-8.
19. Nieth C, Lage H. Induction of the ABC-transporters Mdr1/P-gp (ABCC1), mrpl (ABCC1), and bcrp (ABCG2) during establishment of multidrug resistance following exposure to mitoxantrone. J Chemother 2005; 17 (2): 215-23.
20. Doyle LA, Yang WD, Abruzzo LV, et al. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci USA 1998; 95 (26): 15665-70.
21. Sarkadi B, Homolya L, Szakacs G, Varadi A. Human multidrug resistnace ABCB and ABCG transporters: participation in a chemoimmunity defense system. Physiol Rev 2006; 86: 1179-236.
22. Choi YH, Yu AM. ABC transporters in multidrug resistance and pharmacokinetics, and strategies for drug development. Curr Pharm Des 2014; 20 (5): 793-807.
23. Albrecht Ch, Viturro E. The ABCA subfamily-gene and protein structures, functions and associated heredity diseases. Pflugers Arch-Eur J Physiol 2007; 453: 581-9.
24. Ogawa Y, Tsuda H, Hai E, et al. Clinical Role Of ABCF2 Expression In Breast Cancer. Anticancer Res 2006; 26: 1809-14.
25. Wenzel JJ, Pichler A, Kaminski WE. ABC A-subclass proteins: gatekeepers of cellular phospho-and sphingolipid transport. Front Biosci 2007; 12: 3177-93.
26. Aye IL, Singh AT, Keelan JA. Transport of lipids by ABC proteins: interactions and implications for cellular toxicity, viability and function. Chem Biol Interact 2009; 180 (3): 327-39.
27. Arnould I, Schriml LM, Prades C, et al. Identifying and characterizing a five-gene cluster of ATP-binding cassette transporters mapping to human chromosome 17q24: a new subgroup within the ABCA subfamily. GeneScreen 2004; 1: 157-64.
28. Aberuyi N, Rahgozar S, Moafi A. The role of ATP-binding cassette transporter A2 in childhood acute lymphoblastic leukemia multidrug resistance. Iran J Ped Hematol Oncol 2014; 4 (3): 118-26.
29. Warren Davis. The ATP-binding Cassette Transporter-2 (ABCA2) regulates cholesterol homeostasis and low-density lipoprotein receptor metabolism in N2a neuroblastoma cells. Biochim Biophys Acta 2011; 1811 (12): 1152-64.
30. Davis W. The ATP-binding cassette transporter-2 (ABCA2) regulates cholesterol homeostasis and low-density lipoprotein receptor metabolism in N2a neuroblastoma cells. Biochim Biophys Acta 2011; 1811: 1152-64.
31. Fitzgerald ML, Xavier R, Haley KJ, et al. ABCA3 inactivation in mice causes respiratory failure, loss of pulmonary surfactant, and depletion of lung phosphatidylglycerol. J Lipid Res 2007; 48:, 621-10.
32. Besnard V, Wert SE, Stahlman MT, et al. Deletion of Scap in alveolar type II cells influences lung lipid homeostasis and identifies a compensatory role for pulmonary lipofibroblasts. J Biol Chem 2009; 284 (6): 4018-30.
33. Pohla A, Devauxb PF, Herrmanna A. Function of prokaryotic and eukaryotic ABC proteins in lipid transport. Biochim Biophys Acta 2005; 1733: 29-52.
34. Piehler AP, Özcürümez M, Kaminski WE. A-subclass ATPbinding cassette proteins in brain lipid homeostasis and neurodegeneration. Front Psychiatry 2012; 3 (17): 1-16.
35. Grandjean-Forestier F, Stenger Ch, Robert J, Verdier M, Ratinaud MH. The P-glyporotein 170: just a multidrug resistance protein or a proteam molecule? ABC transporeters and Multidrug Resistance. USA: John Wiley & Sons 2006; pp. 17-46.
36. Chinn LW, Kroetz DL. ABCB1 pharmacogenetics: Progress, pitfalls, and promise. Clin Pharmacol Ther 2007; 81: 265-9.
37. Keppler D. Cholestasis and the role of basolateral efflux pumps. Z Gastroenterol 2011; 49 (12): 1553-7.
38. Gottesman MM, Ling V. The molecular basis of multidrug resistance in cancer: The early years of P-glycoprotein research. FEBS Lett 2006; 580: 998-1009.
39. Hennessy M, Spiers JP. A primer on the mechanics of P-glycoprotein the multidrug transporter. Pharmacol Res 2007; 55: 1-15.
40. Higgins CF. Multiple molecular mechanisms for multidrug resistance transporters. Nature 2007; 446: 749-57.
41. Kimura Y, Morita SY, Matsuo M, Ueda K. Mechanism of multidrug recognition by MDR1/ABCB1. Cancer Sci 2007; 98: 1303-10.
42. Ansbro MR, Shukla S, Ambudkar SV, Yuspa SH, Li L. Screening compounds with a novel high-throughput ABCB1-mediated efflux assay identifies drugs with known therapeutic targets at risk for multidrug resistance interference. PLoS One 2013; 8 (4): e60334.
43. Szakács G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM. Targeting multidrug resistance in cancer. Nat Rev Drug Discov 2006; 5: 219-34.
44. Trauner M, Fickert P, Halilbasic E, et al. Lessons from the toxic bile concept for the pathogenesis and treatment of cholestatic liver diseases. Wien Med Wochenschr 2008; 158: 542-8.
45. Tachibana T, Kato M, Takano J, Sugiyama Y. Predicting drug-drug interactions involving the inhibition of intestinal CYP3A4 and Pglycoprotein. Curr Drug Metab 2010; 11: 762-77.
46. Gotthardt D, Runz H, Keitel V, et al. A mutation in the canalicular phospholipid transporter gene, ABCB4, is associated with cholestasis, ductopenia, and cirrhosis in adults. Hepatology 2008; 48 (4): 1157-66.
47. Smit JJ, Schinkel AH, Mol CA, et al. Tissue distribution of the human MDR3 P-glycoprotein. Lab Invest 1994; 71: 638-49.
48. Strouse JJ, Ivnitski-Steele I, Waller A, et al. Fluorescent substrates for flow cytometric evaluation of efflux inhibition in ABCB1, ABCC1, and ABCG2 transporters.Anal Biochem 2013; 437 (1): 77-87.
49. Borst P, de Wolf C, van de Wetering K. Multidrug resistanceassociated proteins 3, 4, and 5. Pflugers Arch 2007; 453: 661-73.
50. Borst P, Evers R, Kool M, Wijnholds J. The multidrug protein family. Biochim Biophys Acta 1999; 1461: 347-57.
51. Wang P, Zhang Z, Gao K, et al. Expression and clinical significance of ABCC10 in the patients with non-small cell lung cancer (in Chinese). Zhongguo Fei Ai Za Zhi 2009; 12: 875-8.
52. Van Aubel RA, Masereeuw R, Russel FG. Molecular pharmacology of renal organic anion transporters. Am J Physiol Renal Physiol 2000; 279 (Suppl. 2): 216-32.
53. Kool M, de Haas M, Scheffer GL, et al. Analysis of expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, homologues of the multidrug resistance-associated protein gene (MRP1), in human cancer cell lines. Cancer Res 1997; 57: 3537-47.
54. Kool M, van der Linden M, de Haas M, Baas F, Borst P. Expression of human MRP6, a homologue of the multidrug resistance protein gene MRP1, in tissues and cancer cells. Cancer Res 1999; 59: 175-82.
55. Cheepala SB, Bao J, Nachagari D, et al. Crucial Role for Phylogenetically Conserved Cytoplasmic Loop 3 in ABCC4 Protein Expression. J Biol Chem 2013; 288 (31): 22207-18.
56. Domanitskaya N, Wangari-Talbot J, Jacobs J, et al. Abcc10 status affects mammary tumour growth, metastasis, and docetaxel treatment response. Br J Cancer 2014; 111 (4): 696-707.
57. Yabuuchi H, Shimizu H, Takayanagi S, Ishikawa T. Multiple splicing variants of two new human ATP-binding cassette transporters, ABCC11 and ABCC12. Biochem Biophys Res Commun 2001; 288: 933-9.
58. Sodani K, Pate A, Kathawala RJ, Chen ZS. Multidrug resistance associated proteins in multidrug resistance. Chin J Cancer 2012; 31: 58-72.
59. Valente RCI, Capella LS, Nascimento CR, Braga F. ABCB1 (Pglycoprotein) but not ABCC1 (MRP1) is downregulated in peripheral blood mononuclear cells of spontaneously hypertensive rats. Pflugers Arch 2008; 456 (2): 359-68.
60. Boumendjel A, McLeer-Florin A, Champelovier P, et al. A novel chalcone derivative which acts as a microtubule depolymerising agent and an inhibitor of P-gp and BCRP in in-vitro and in-vivo glioblastoma models. BMC Cancer 2009; 9: 242.
61. Hill Ch, Jamieson D, Thomas HD, et al. Characterisation of the roles of ABCB1, ABCC1, ABCC2 and ABCG2 in the transport and pharmacokinetics of actinomycin D in vitro and in vivo. Biochem Pharmacol 2013; 85 (1): 29-37.
62. Leslie EM, Deeley RG, Cole SPC. Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 2005; 204: 216-37.
63. Russel FG, Koenderink JB, Masereeuw R. Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules. Trends Pharmacol Sci 2008; 29: 200-7.
64. Borst P, Zelcer N, van de Wetering K. MRP2 and 3 in health and disease. Cancer Lett 2006; 234: 51-61.
65. St Pierre MV, Serrano MA, Macias RI, et al. Expression of members of the multidrug resistance protein family in human term placenta. Am J Physiol Regul Integr Comp Physiol 2000; 279: 1495-503.
66. Hirrlinger J, Konig J, Dringen R. Expression of mRNAs of multidrug resistance proteins (MRPs) in cultured rat astrocytes oligodendrocytes, microglial cells and neurones. J Neurochem 2002; 82: 716-9.
67. Leggas M, Adachi M, Scheffer GL, et al. MRP4 confers resistance to topotecan and protects the brain from chemotherapy. Mol Cell Biol 2004; 24: 7612-21.
68. Le Saux O, Martin L, Aherrahrou Z, Leftheriotis G, Váradi A, Brampton NC. The molecular and physiological roles of ABCC6: more than meets the eye. Front Gene 2012; 3: 289.
69. Martin LJ, Lau E, Singh H, et al. ABCC6 Localizes to the Mitochondria-Associated Membrane. Circ Res 2012; 111: 516-20.
70. Blazquez-Medela AM, Guihard PJ, FAO J, et al. ABCC6 deficiency is associated with activation of BMP signaling in liver and kidney. FEBS Open Bio 2015; 5: 257-63.
71. Kuzaj P, Kuhn J, Dabisch-Ruthe M, et al. ABCC6-a new player in cellular cholesterol and lipoprotein metabolism? Lipids Health Dis 2014; 13: 118.
72. Masereeuw R, Russel FGM. Regulatory pathways for ATP-binding cassette transport proteins in kidney proximal tubules. AAPS J 2012; 14 (4): 883-94.
73. Kruh GD, Guo Y, Hopper-Borge E, et al. ABCC10, ABCC11, and ABCC12. Pflugers Arch 2007; 453: 675-84.
74. Ono N, van der Heijgen I, Scheffer GL, et al. Multidrug resistance-associated protein 9 (ABCC12) is present in mouse and boar sperm. Biochem. J 2007; 406: 31-40.
75. Shimizu H, Taniguchi H, Hippo Y, Hayashizaki Y, Aburatani H, Ishikawa T. Characterization of the mouse Abcc12 gene and its transcript encoding an ATP-binding cassette transporter, an orthologue of human ABCC12. Gene 2003; 310: 17-28.
76. Quintieri L, Fantin M, Vizler C. Identification of molecular determinants of tumor sensitivity and resistance to anticancer drugs. Adv Exp Med Biol 2007; 593: 95-104.
77. Huang B, Gao Y, Tian D, Zheng M. A small interfering ABCE1-targeting RNA inhibits the proliferation and invasiveness of small cell lung cancer. Int J Mol Med 2010; 25: 687-93.
78. Ren Y, Li YH, Tian DL. Role of the ABCE1 gene in human lung adenocarcinoma. Oncol Rep 2012; 27: 965-70.
79. Barthelme D, Scheele U, Dinkelaker S, Janoschka A, Macmillan F. Structural organization of essential iron-sulfur clusters in the evolutionarily highly conserved ATP-binding cassette protein ABCE1. J Biol Chem 2007; 282: 14598-607.
80. Karcher A, Schele A, Hopfner KP. X-ray structure of the complete ABC enzyme ABCE1 from Pyrococcus abyssi. J Biol Chem 2008; 283: 7962-71.
81. Langmann T, Mauerer R, Zahn A, et al. Real-time reverse transcription-PCR expression profiling of the complete human ATPbinding cassette transporter superfamily in various tissues. Clin Chem 2003; 49: 230-8.
82. Kerr ID. Sequence analysis of twin ATP binding cassette proteins involved in translational control, antibiotic resistance, and ribonuclease L inhibition. Biochem Biophys Res Com 2004; 315: 166-73.
83. Tsuda H, Ito YM, Ohashi Y, et al. Identification of overexpression and amplification of ABCF2 in clear cell ovarian adenocarcinomas by cDNA microarray analyses. Clin Cancer Res 2005; 11: 6880-8.
84. Yasui K, Mihara S, Zhao C, et al. Alteration in copy numbers of genes as a mechanism for acquired drug resistance. Cancer Res 2004; 64: 1403-10.
85. Owen M. Woodward, Anna Kottgen A, Kottgen M. ABCG transporters and disease FEBS J 2011; 278: 3215-25.
86. Allikmets R, Schriml LM, Hutchinson A. Romano-Spica V, Dean M. A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Res 1998; 58: 5337-9.
87. Mao Q, Unadkat JD. Role of the breast cancer resistance protein (ABCG2) in drug transport. AAPS J 2005; 7: 118-33.
88. Kerr ID, Haider AJ, Gelissen IC. The ABCG family of membraneassociated transporters: you don’t have to be big to be mighty. Br J Pharmacology 2011; 164: 1767-79.
89. Engel T, Lorkowski S, Lueken A, et al. The human ABCG4 gene is regulated by oxysterols and retinoids in monocyte-derived macrophages. Biochem Biophys Res Commun 2001; 288: 483-8.
90. Kusuhara H, Sugiyama Y. ATP-binding cassette, subfamily G (ABCG family). Pflugers Arch 2007; 453 (5): 735-44.
91. Tarr PT, Tarling EJ, Bojanic DD, Edwards PA, Baldan A. Emerging new paradigms for ABCG transporters. Biochim Biophys Acta 2009; 1791: 584-93.
92. Kobayashi DI, Ieiri I, Hirota T, et al. Functional assessment of ABCG2 (BCRP) gene polymorphisms to protein expression in human placenta. Drug Metab Dispos 2005; 33 (1): 94-101.
93. Gutmann H, Hruz P, Zimmermann C, Beglinger C, Drewe J. Distribution of breast cancer resistance protein (BCRP/ABCG2) mRNA expression along the human GI tract. Biochem Pharmacol 2005; 70: 695-9.
94. Robillard KR, Hoque T, Bendayan R. Expression of ATP-binding cassette membrane transporters in rodent and human sertoli cells: relevance to the permeability of antiretroviral therapy at the bloodtestis barrier. J Pharmacol Exp Ther 2012; 340: 96-108.
95. Fetsch PA, Abati A, Litman T, et al. Localization of the ABCG2 mitoxantrone resistance-associated protein in normal tissues. Cancer Lett 2006; 235: 84-92.
96. Huls M, Brown CD, Windass AS, et al. The breast cancer resistance protein transporter ABCG2 is expressed in the human kidney Proxima tubule apical membrane. Kidney Int 2008; 73: 220-5.
97. Merino G, Jonker JW, Wagenaar E, van Herwaarden AE, Schinkel AH. The breast cancer resistance protein (BCRP/ABCG2) affects pharmacokinetics, hepatobiliary excretion, and milk secretion of the antibiotic nitrofurantoin. Mol Pharmacol 2005; 67: 1758-64.
98. Tarr P, Edwards PA. ABCG1 and ABCG4 are co-expressed in neurons and astrocytes of the CNS and regulate cholesterol homeostasis trough SREBP-2. J Lipid Res 2008; 49: 169-82.
99. Wang N, Yvan-Charvet L, Lutjohann D, et al. ATP-binding cassette transporters G1 and G4 mediate cholesterol and desmosterol efflux to HDL and regulate sterol accumulation in the brain. FASEB J 2008; 22: 1073-82.
100. Zhou SF, Wang LL, Di YM, et al. Substrates and inhibitors of human multidrug resistance associated proteins and the implications in drug development. Curr Med Chem 2008; 15: 1981-2039.
101. Zhai X, Wang H, Zhu X, et al. Gene polymorphisms of ABC transporters are associated with clinical outcomes in children with acute lymphoblastic leukemia. Arch Med Sci 2012; 8; 8 (4): 659-71.
102. Zhang W, Yu BN, He YJ, et al. Role of BCRP 421C>A polymorphism on rosuvastatin pharmacokinetics in healthy Chinese males. Clin Chim Acta 2006; 373: 99-103.
103. Keskitalo JE, Pasanen MK, Neuvonen PJ, Niemi M. Different effects of the ABCG2 c.421C>A SNP on the pharmacokinetics of fluvastatin, pravastatin and simvastatin. Pharmacogenomics 2009; 10: 1617-24.
104. Tomlinson B, Hu M, Lee VW, et al. ABCG2 polymorphism is associated with the low-density lipoprotein cholesterol response to rosuvastatin. Clin Pharmacol Ther 2010; 87: 558-62.
105. Meissner K, Heydrich B, Jedlitschky G, Meyer zu Schwabedissen H. The ATP-binding cassette transporter ABCG2 (BCRP), a marker for side population stem cells, is expressed in human heart. J Histochem Cytochem 2006; 54 (2): 215-21.
106. Lazarowski A, Czornyj L, Lubienieki F, Girardi E, Vazquez S, D’Giano C. ABC transporters during epilepsy and mechanisms underlying multidrug resistance in refractory epilepsy. Epilepsia 2007; 48 (Suppl 5): 140-9.
107. Abuznait AH, Kaddoumi A. Role of ABC transporters in the pathogenesis of Alzheimer’s disease. ACS Chem Neurosci 2012; 3 (11): 820-31.
108. Granzotto M, Drigo I, Candussio L, et al. Rifampicin and verapamil induce the expression of P-glycoprotein in vivo in Ehrlich ascites tumor cells. Cancer Lett 2004; 8; 205 (1): 107-15.
109. Westphal KI, Weinbrenner A, Zschiesche M, et al. Induction of Pglycoprotein by rifampin increases intestinal secretion of talinolol in human beings: a new type of drug/drug interaction. Clin Pharmacol Ther 2000; 68 (4): 345-55.
110. Miller DS, Bauer B, Hartz AM. Modulation of P-glycoprotein at the blood-brain barrier: opportunities to improve central nervous system pharmacotherapy. Pharmacol Rev 2008; 60 (2): 196-209.
111. Shen S, Zhang W. ABC transporters and drug efflux at the bloodbrain barrier. Rev Neurosci 2010; 21 (1): 9-53.
112. Liang XJ, Chen CH, Zhao Y, Wang PC. Circumventing tumor resistance to chemotherapy by nanotechnology. Methods Mol Biol 2010; 596: 467-88.
113. Steinbach D, Gillet JP, Sauerbrey A, Gruhn B, et al. ABCA3 as a possible cause of drug resistance in childhood acute myeloid leukemia. Clin Cancer Res 2006; 12 (14): 4357-63.
114. Baecklund F, Foo JN, Bracci P, Darabi H. A comprehensive evaluation of the role of genetic variation in follicular lymphoma survival. BMC Med Genet 2014; 8, 15: 113.
115. Chauhan PS, Bhushan B, Singh LC, et al. Expression of genes related to multiple drug resistance and apoptosis in acute leukemia: Response to induction chemotherapy. Exp Mol Pathol 2012; 92: 44-9.
116. Au A, Baba AA, Azlan H, Norsa’adah B, Ankathil R. Clinical impact of ABCC1 and ABCC2 genotypes and haplotypes in mediating imatinib resistance among chronic myeloid leukaemia patients. J Clin Pharm Ther 2014; 39 (6): 685-90.
117. Hu S, Niu H, Inaba H, et al. Activity of the multikinase inhibitor sorafenib in combination with cytarabine in acute myeloid leukemia. J Natl Cancer Inst 2011; 103: 893-905.
118. Hauswald S, Duque-Afonso J, Wagner MM, et al. Histone deacetylase inhibitors induce a very broad, pleiotropic anticancer drug resistance phenotype in acute myeloid leukemia cells by modulation of multiple ABC transporter genes. Clin Cancer Res 2009; 15 (11): 3705-15.
119. Tiribelli M, Fabbro D, Franzoni A, Fanin R, Damante G, Damiani D. Q141K polymorphism of ABCG2 protein is associated with poor prognosis in adult acute myeloid leukemia treated with idarubicin-based chemotherapy. Haematologica 2013; 98: e28-9.
120. Natarajan K, Xie Y, Baer MR, Ross DD. Role of breast cancer resistance protein (BCRP/ABCG2) in cancer drug resistance. Biochem Pharmacol 2012; 83: 1084-103.
121. Plasschaert SL, van der Kolk DM, de Bont ES, et al. The role of breast cancer resistance protein in acute lymphoblastic leukemia. Clin. Cancer Res 2003; 9: 5171-7.
122. Nakanishi T, Ross DD. Breast cancer resistance protein (BCRP/ ABCG2): its role in multidrug resistance and regulation of its gene expression. Chin J Cancer 2012; 31 (2): 73-99.
123. Tang SC, Lagas JS, Lankheet NA, et al. Brain accumulation of sunitinib is restricted by P-Glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) and can be enhanced by oral elacridar and sunitinib coadministration. Int J Cancer 2012; 130: 223-33.
124. Sekine I, Shimizu Ch, Nishio K, Saijo N, Tamura T. A literature review of molecular markers predictive of clinical response to cytotoxic chemotherapy in patients with breast cancer. Int J Clin Oncol 2009; 14, 2: 112-9.
125. Yamada A, Ishikawa T, Ota I, et al. High expression of ATPbinding cassette transporter ABCC11 in breast tumors is associated with aggressive subtypes and low disease-free survival. Breast Cancer Res Treat 2013; 137: 773-82.
126. Litviakov NV, Garbukov EIu, Slonimskaia EM, Tsyganov MM. Correlation of metastasis-free survival in patients with breast cancer and changes in the direction of expression of multidrug resistance genes during neoadjuvant chemotherapy. Vopr Onkol 2013; 59 (3): 334-40.
127. Setia N, Abbas O, Sousa Y, Garb JL, Mahalingam M. Profiling of ABC transporters ABCB5, ABCF2 and nestin-positive stem cells in nevi, in situ and invasive melanoma. Modern Pathol 2012; 25: 1169-75.
128. Tsuda H, Ito K, Yaegashi N, et al. Relationship between ABCF2 expression and response to chemotherapy or prognosis in clear cell adenocarcinoma of the ovary. Int J Gynecol Cancer 2010; 20 (5): 794-7.
129. Wang Y, Yamada K, Tanaka Y, Ishikawa K, Inagaki N. Expression of ABCA2 protein in human vestibular schwannoma and peripheral nerve. J Neurol Sci 2005; 232: 59-63.
130. Bleau AM, Hambardzumyan D, Ozawa T, et al. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 2009; 4: 226-35.
131. Oberstadt M, Bien-Möller S, Weitmann K, et al. Epigenetic modulation of the drug resistance genes MGMT, ABCB1 and ABCG2 in glioblastoma multiforme. BMC Cancer 2013; 13: 617.
132. Hodges LM, Markova SM, Chinn LW. Very important pharmacogene summary: ABCB1 (MDR1, P-glycoprotein). Pharmacogenet Genom 2011; 21 (3): 152-61.
133. Nakano H, Nakamura Y, Soda H, et al. Methylation status of breast cancer resistance protein detected by methylation-specific polymerase chain reaction analysis is correlated inversely with its expression in drug-resistant lung cancer cells. Cancer 2008; 112 (5): 1122-30.
134. Jiang ZP, Xu P, Liu RR, et al. Correlation between MDR1 methylation status in the promoter region and MDR1 genetic polymorphism in 194 healthy Chinese Han subjects. Pharmacogenomics 2008; 9 (12): 1801-8.
135. Morisaki K, Robey RW, Ozvegy-Laczka C, et al. Single nucleotide polymorphisms modify the transporter activity of ABCG2. Cancer Chemother Pharmacol 2005; 56 (2): 161-72.
136. Berger W, Setinek U, Hollaus P, et al. 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 2005; 131: 355-63.
137. Amiri-Kordestani L. Targeting MDR in breast and lung cancer: discriminating its potential importance from the failure of drug resistance reversal studies. Drug Resist Updat 2012; 15 (1-2): 50-61.
138. Wangari-Talbot J, Hopper-Borge E. Drug Resistance Mechanisms in Non-Small Cell Lung Carcinoma. J Can Res Updates 2013; 2 (4): 265-82.
139. Boonstra R, Timmer-Bosscha H, Echten-Arends J, et al. Mitoxantrone resistance in a small cell lung cancer cell line is associated with ABCA2 upregulation. Br J Cancer 2004; 90: 2411-7.
140. Kunická T, Souček P. Importance of ABCC1 for cancer therapy and prognosis. Drug Metab 2014; 46 (3): 325-42.
141. Kunická T, Václavíková R, Hlaváč V, et al. Non-coding polymorphisms in nucleotide binding domain 1 in ABCC1 gene associate with transcript level and survival of patients with breast cancer. PLoS One 2014; 9 (7): 101740.
142. Yin JY, Huang Q, Yang Y, et al. Characterization and analyses of multidrug resistance-associated protein 1 (MRP1/ABCC1) polymorphisms in Chinese population. Pharmacogenet Genom 2009; 19 (3): 206-16.
143. Ota E, Abe Y, Oshika Y, et al. Expression of the multidrug resistance-associated protein (MRP) gene in nonsmall-cell lung cancer. Br J Cancer 1995; 72: 550-4.
144. Li J, Jaimes KF, Aller SG. Refined structures of mouse Pglycoprotein. Protein Sci 2014; 23: 34-46.
145. Li XQ, Li J, Shi SB, Chen P, Yu LC, Bao QL. Expression of MRP1, BCRP, LRP and ERCC1 as prognostic factors in non-small cell lung cancer patients receiving postoperative cisplatin-based chemotherapy. Int J Biol Markers 2009; 24 (4): 230-7.
146. Oguri T, Ozasa H, Uemura T, et al. MRP7/ABCC10 expression is a predictive biomarker for the resistance to paclitaxel in non-small cell lung cancer. Mol Cancer Ther 2008; 7 (5): 1150-5.
147. Assef Y, Rubio F, Coló G, del Mónaco S, Costas MA, Kotsias BA. Imatinib resistance in multidrug-resistant K562 human leukemic cells. Leuk Res 2009; 33 (5): 710-6.
148. Yamasaki MT, Makino T, Masuzawa Y, et al. Role of multidrug resistance protein 2 (MRP2) in chemoresistance and clinical outcome in oesophageal squamous cell carcinoma. Br J Cancer 2011; 104: 707-13.
149. Zhao Y, Lu H, Yan A, et al. ABCC3 as a marker for multidrug resistance in non-small cell lung cancer. Sci Rep 2013; 1, 3: 3120.
150. Hlavata I, Mohelnikova-Duchonova B, Vaclavikova R, et al. The role of ABC transporters in progression and clinical outcome of colorectal cancer. Mutagenesis 2012; 27 (2): 187-96.
151. Zelcer N, Saeki T, Reid G, Beijnen JH, Borst P. Characterization of drug transport by the human multidrug resistance protein 3 (ABCC3). J Biol Chem 2001; 276: 46400-7.
152. Rijavec M, Silar M, Triller N, et al. Expressions of topoisomerase II alpha and BCRP in metastatic cells are associated with overall survival in small cell lung cancer patients. Pathol Oncol Res 2011; 17: 691-6.
153. Tsunoda SI, Okumura T, Ito T, et al. ABCG2 expression is an independent unfavorable prognostic factor in esophageal squamous cell carcinoma. Oncology 2006; 71 (3-4): 251-8.
154. Trumpi K, Emmink BL, Prins M, et al. ABC-transporter expression does not correlate with response to irinotecan in patients with metastatic colorectal cancer. J Cancer 2015; 6 (11): 1079-86.
155. Larbcharoensub N, Leopairat J, Sirachainan E, et al. Association between multidrug resistance-associated protein 1 and poor prognosis in patients with nasopharyngeal carcinoma treated with radiotherapy and concurrent chemotherapy. Hum Pathol 2008; 39 (6): 837-45.
156. Surowiak P, Pawełczyk K, Maciejczyk A, et al. Positive correlation between cyclooxygenase 2 and the expression of ABC transporters in non-small cell lung cancer. Anticancer Res 2008; 28 (5): 2967-74.
157. Shukla S, Chen ZS, Ambudkar SV. Tyrosine kinase inhibitors as modulators of ABC transporter-mediated drug resistance. Drug Resist Updat 2012; 15 (1-2): 70-80.
158. Huang WC, Chen YJ, Li LY, et al. Nuclear translocation of epidermal growth factor receptor by Akt-dependent phosphorylation enhances breast cancer-resistant protein expression in gefitinibresistant cells. J Biol Chem 2011; 286: 20558-68.
159. Shi Z, Tiwari AK, Shukla S, et al. Inhibiting the function of ABCBI and ABCG2 by the EGFR tyrosine kinase inhibitor AG1478. Biochem Pharmacol 2009; 77: 781-93.
160. Zhang Z, Li X, Wang X, et al. The expression of ABCG4, VATPase and clinic significance of their correlation with NSCLC. Zhongguo Fei Ai Za Zhi 2008; 11 (5): 691-5.
161. Li L, Xiao-Dong L. Alterations in function and expression of ABC transporters at blood-brain barrier under diabetes and the clinical significances. Front Pharmacol 2014; 5: 273.
162. Grzywacz MJ, Yang JM, Hait WN. Effect of the multidrug resistance protein on the transport of the antiandrogen flutamide. Cancer Res 2003; 63: 2492-8.
163. Mruk DD, Su L, Cheng CY. Emerging role for drug transporters at the blood-testis barier. Trends Pharmacol Sci 2011; 32 (2): 99-106.
164. Cho S, Lu M, He X, et al. Notch1 regulates the expression of the multidrug resistance gene ABCC1/MRP1 in cultured cancer cells. Proc Natl Acad Sci USA 2011; 20; 108 (51): 20778-83.
165. Li K, Liu C, Zhou B, et al. Role of EZH2 in the growth of prostate cancer stem cells isolated from LNCaP cells. Int J Mol Sci 2013; 14 (6): 11981-3.
166. Liu CH, Li Z, Bi L, et al. NOTCH1 signaling promotes chemoresistance via regulating ABCC1 expression in prostate cancer stem cells. Mol Cell Biochem 2014; 393 (1-2): 265-70.
167. Montani M, Herrmanns T, Müntener M, Wild P, Sulser T, Kristiansen G. Multidrug resistance protein 4 (MRP4) expression in prostate cancer is associated with androgen signaling and decreases with tumor progression. Virchows Arch 2013; 462 (4): 437-43.
168. Cai C, Omwancha J, Hsieh CL, Shemshedini L. Androgen induces expression of the multidrug resistance protein gene MRP4 in prostate cancer cells. Prostat Cancer Prostat Dis 2007; 10: 39-45.
169. Karatas OF, Guzel E, Duz MB, Ittmann M, Ozen M. The role of ATP-binding cassette transporter genes in the progression of prostate cancer. Prostate 2016; 76 (5): 434-44.
170. Fletcher JI, Haber M, Henderson MJ, Norris MD. ABC transporters in cancer: more than just drug efflux pumps. Nat Rev Cancer 2010; 10 (2): 147-56.
171. Demidenko R, Razanauskas D, Daniunaite K, Lazutka JR, Jankevicius F, Jarmalaite S. Frequent down-regulation of ABC transporter genes in prostate cancer. BMC Cancer 2015; 15: 683.
172. LI G, Xiaoping Ch, Wang Q, Xu Z, Wanguang Z, YE Lu. The roles of four multi-drug resistance proteins in hepatocellular carcinoma multidrug resistance. J Huazhong Univ Sci Technol 2007; 27 (2): 173-5.
173. Korita PV, Wakai T, Shirai Y, et al. Multidrug resistanceassociated protein 2 determines the efficacy of cisplatin in patients with hepatocellular carcinoma. Oncol Rep 2010; 23 (4): 965-72.
174. Vander Borght S, Komuta M, Libbrecht L, et al. Expression of multidrug resistance-associated protein1in hepatocellular carcinoma is associated with a more aggressive tumour phenotype and may reflect a progenitor cell origin. Liver Int 2008; 1478-3223.
175. Duan Z, Brakora KA, Seiden MV. Inhibition of ABCB1 (MDR1) and ABCB4 (MDR3) expression by small interfering RNA and reversal of paclitaxel resistance in human ovarian cancer cells. Mol Cancer Ther 2004; 3 (7): 833-8.
176. Liedert B, Materna V, Schadendorf D, et al. Overexpression of cMOAT (MRP2/ABCC2) is associated with decreased formation of platinum-DNA adducts and decreased G2-arrest in melanoma cells resistant to cisplatin. J Invest Dermatol 2003; pp. 121: 172-6.
177. Materna V, Liedert B, Thomale J, Lage H. Protection of platinum-DNA adduct formation and reversal of cisplatin resistance by anti-MRP2 hammerhead ribozymes in human cancer cells. Int J Cancer 2005; 115: 393-402.
178. Materna V, Stege A, Surowiak P, Priebsch A, Lage H. RNA interference-triggered reversal of ABCC2-dependent cisplatin resistance in human cancer cells. Biochem Biophys Res Commun 2006; 348: 153-7.
179. Ozben T. Mechanism and strategies to overcome multiple dru resistance in cancer, FEBS Lett 2006; 580: 2903-009.
180. Itamoch H, Kigawa J, Sugiyama T, Kikuchi Y, Suzuki M, Terakawa N. Low proliferation activity may be associated with chemoresistance in clear cell carcinoma of the ovary. Obstet Gynecol 2002; 100: 281-7.
181. Ohishi Y, Oda Y, Uchiumi T, et al. ATP-binding cassette superfamily transporter gene expression in human primary ovarian carcinoma. Clin Cancer Res 2002; 8: 3767-75.
182. Takayanagi S, Kataoka T, Ohara O, Oishi M, Kuo MT, Ishikawa T. Human ATP-binding cassette transporter ABCC10: Expression profile and p53-dependent upregulation. J Exp Ther Oncol 2004; 4: 239-46.
183. Mohelnikova-Duchonova B, Brynychova V, Oliverius M, et al. Differences in transcript levels of ABC transporters between pancreatic adenocarcinoma and nonneoplastic tissues. Pancreas 2013; 42: 707-16.
184. Hagmann W, Jesnowski R, Faissner R, Guo C, Löhr JM. ATPbinding cassette C transporters in human pancreatic carcinoma cell lines. Upregulation in 5-fluorouracil-resistant cells. Pancreatology 2009; 9 (1-2): 136-44.
185. Yoshida M, Suzuki T, Komiya T, et al. Induction of MRP5 and SMRP mRNA by adriamycin exposure and its overexpression in human lung cancer cells resistant to adriamycin. Int J Cancer 2001; 94: 432-7.
186. König J, Hartel M, Nies AT, et al. Expression and localization of human multidrug resistance protein (ABCC) family members in pancreatic carcinoma. Int J Cancer 2005; 20; 115 (3): 359-67.
187. Longo-Sorbello GS, Bertino JR. Current understanding of methotrexate pharmacology and efficacy in acute leukemias. Use of newer antifolates in clinical trials. Haematologica 2001; 86: 121-7.
188. Choi CH. ABC transporters as multidrug resistance mechanizm and the development of chemosensitizers for their reversal. Cancer Cell Int 2005; 5: 30-43.
189. Bartosiewicz D, Anna K. Inhibitors of ABC transporters and biophysical methods to study their activity. Verglag der Zeitchrift fur Naturforschyng 2009; 64: 454-8.
190. Schmidt WF, Huber KR, Ettinger RS, Neuberg RW. Antiproliferative effect of verapamil alone on brain tumor cells in vitro. Cancer Res 1988; 148 (13): 3617-21.
191. Glavinas H, Krajcsi P, Cserepes J, Sarkali B. The role of ABC transporters in drug resistance, metabolism and toxicity. Curr Drug Deliv 2004, 1: 27-42.
192. Thomas H, Coley HM. Overcoming multidrug resistance in cancer: an update on the clinical strategy of inhibiting P-glycoprotein. Cancer Control 2003; 10: 159-65.
193. de Bruin M, Miyake K, Litman T, Robey R, Bates SE. Reversal of resistance by GF120918 in cell lines expressing the ABC halftransporter, MXR. Cancer Lett 1999; 146 (2): 117-26.
194. Minderman H, Brooks TA, O’Loughlim KL, Ojima I, Bernacki RJ, Bear MR. Broad-spectrum modulation of ATP-binding cassette transport proteins by the taxane derivatives ortataxel (IDN-519, BAY 59-8862) and tRA96023. Cancer Chemother Pharmacol 2004; 53: 363-9.
195. Qadir M, O’Loughlin KL, Fricke SM, et al. Cyclosporin A is a broad-spectrum multidrug resistance modulator. Clin Cancer Res 2005; 11: 2320-6.
196. Robey Rw, Steadman K, Polar O, et al. Pheophorbide a is a specific probe for ABCG2 fubction and inhibition. Cancer Res 2004; 64: 1242-6.
197. Shepard RL, Cao J, Starling JJ, Dantzig AH. Modulation of Pglycoprotein but not MRP1-or BCRP-mediated drug resistance by LY335979. Int J Cancer 2003; 103: 121-5.
198. Cheung L, Yu DM, Neiron Z, Failes TW, Arndt GM, Fletcher JI. Identification of new MRP4 inhibitors from a library of FDA approved drugs using a high-throughput bioluminescence screen. Biochem Pharmacol 2015; 93 (3): 380-8.
199. Enokizono J, Kusuhara H, Ose A, Schinkel AH, Sugiyama Y. Quantitative investigation of the role of breast cancer resistance protein (BCRP/ABCG2) in limiting brain and testis penetration of xenobiotic compounds. Drug Metab Dispos 2008; 36 (6): 995-1002.
200. Knauer MJ, Urquhart BL, Meyer zu Schwabedissen HE, et al. Human skeletal muscle drug transporters determine local exposure and toxicity of statins. Circ Res 2010; 106 (Suppl. 2): 297-306.
201. Yu M, Ocana A, Tannock IF. Reversal of ATP-binding cassette drug transporter activity to modulate chemoresistance: why has it failed to provide clinical benefit? Cancer Metastasis Rev 2013; 32: 211-27.
202. Patel J, Mitra AK. Strategies to overcome simultaneous Pglycoprotein mediated efflux and CYP3A4 mediated metabolism of drugs. Pharmacogenomics 2001; 2 (4): 401-15.
203. Ueda K. ABC proteins protect the human body and maintain optimal health. Biosci Biotechnol Biochem 2011; 75: 401-9.
204. Shukla S, Ohnuma S, Ambudkar SV. Improving cancer chemotherapy with modulators of ABC drug transporters. Curr Drug Targets 2011; 12 (5): 621-30.
205. Yague E, Higgins CF, Raguz S. Complete reversal of multidrug resistance by stable expression of small interfering RNAs targeting MDR1. Gene Ther 2004; 11: 1170-4.
206. Susa M, Iyer AK, Ryu K, Choy E. Inhibition of ABCB1 (MDR1) expression by an siRNA nanoparticulate delivery system to overcome drug resistance in osteosarcoma. PLoS One 2010; 5 (5): 10764.
207. Morrison R, Schleicher SM, Sun Y, et al. Targeting the mechanisms of resistance to chemotherapy and radiotherapy with the cancer stem cell hypothesis. J Oncol 2011; 2011: 941876.
208. Henderson MJ, Haber M, Porro A, et al. ABCC multidrug transporters in childhood neuro-blastoma: Clinical and biological effects independent of cyto-toxic drug efflux. J Natl Cancer Inst 2011; 103 (16): 1236-51.