ABC transporter inhibitors in reversing multidrug resistance to chemotherapy

Current Drug Targets

Volumn 16, Issue 12, 2015, Pages 1356-1371

  Cui, Haigang ^a   Zhang, Anna J ^a   Chen, Mingwei ^b   Liu, Johnson J ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

^b XI'AN JIAOTONG UNIVERSITY   (China)

Author keywords

ABC transporter inhibitor; Cancer stem cell; Chemotherapy; MicroRNA; Multidrug resistance; Tyrosine kinase inhibitor

Indexed keywords

1 TERT BUTYL 3 [6 (3,5 DIMETHOXYPHENYL) 2 (4 DIETHYLAMINOBUTYLAMINO)PYRIDO[2,3 D]PYRIMIDIN 7 YL]UREA; 4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; ABC TRANSPORTER; AFATINIB; BCR ABL PROTEIN; BREAST CANCER RESISTANCE PROTEIN; CEDIRANIB; DORAMAPIMOD; DOXORUBICIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB; GW 2974; GW 583340; IMATINIB; LAPATINIB; MASITINIB; MULTIDRUG RESISTANCE PROTEIN 1; NILOTINIB; NINTEDANIB; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PONATINIB; PROTEIN TYROSINE KINASE INHIBITOR; SARACATINIB; SUNITINIB; TANDUTINIB; TELATINIB; UNCLASSIFIED DRUG; UNINDEXED DRUG; VANDETANIB; VARLITINIB; VASCULOTROPIN; ANTINEOPLASTIC AGENT; BIOLOGICAL PRODUCT; MICRORNA; PROTEIN TYROSINE KINASE;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CHEMOTHERAPY; CARCINOMA; CELL ADHESION; CELL DIFFERENTIATION; CELL GROWTH; CELL MOTILITY; COLON CANCER; CYTOTOXICITY; DOWN REGULATION; FIBROSING ALVEOLITIS; GENE MUTATION; HUMAN; LEUKEMIA; LIVER CELL CARCINOMA; LUNG CANCER; LUNG CARCINOMA; MULTIDRUG RESISTANCE; MYELOID LEUKEMIA; NEOPLASM; NON SMALL CELL LUNG CANCER; NONHUMAN; OSTEOSARCOMA; PHASE 2 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SMALL CELL LUNG CANCER; TUMOR GROWTH; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CANCER STEM CELL; DRUG EFFECTS; DRUG RESISTANCE; NEOPLASMS;

ANIMALS; ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL PRODUCTS; DRUG RESISTANCE, NEOPLASM; HUMANS; MICRORNAS; NEOPLASMS; NEOPLASTIC STEM CELLS; PROTEIN-TYROSINE KINASES;

EID: 84946745812     PISSN: 13894501     EISSN: 18735592     Source Type: Journal    
DOI: 10.2174/1389450116666150330113506     Document Type: Article

References (134)

1. [1] Kaminski WE, Piehler A, Wenzel JJ. ABC A-subfamily transporters: structure, function and disease. Biochim Biophys Acta 2006; 1762: 510-24.
2. [2] Klaassen CD, Aleksunes LM. Xenobiotic, bile acid, and cholesterol transporters: function and regulation. Pharmacol Rev 2010; 62: 1-96.
3. [3] Endres CJ, Hsiao P, Chung FS, et al. The role of transporters in drug interactions. Eur J Pharm Sci 2006; 27: 501-17.
4. [4] Schinkel AH, Jonker JW. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv Drug Deliv Rev 2003; 55: 3-29.
5. [5] Kerb R. Implications of genetic polymorphisms in drug transporters for pharmacotherapy. Cancer Lett 2006; 234: 4-33.
6. [6] Glavinas H, Krajcsi P, Cserepes J, et al. The role of ABC transporters in drug resistance, metabolism and toxicity. Curr Drug Deliv 2004; 1: 27-42.
7. [7] Choi YH, Yu AM. ABC transporters in multidrug resistance and pharmacokinetics, and strategies for drug development. Curr Pharm Des 2014; 20: 793-807.
8. [8] Liu JJ, Lu J, McKeage MJ. Membrane transporters as determinants of the pharmacology of platinum anticancer drugs. Curr Cancer Drug Target 2012; 12: 962-86.
9. [9] Wu CP, Calcagno AM, Ambudkar SV. Reversal of ABC drug transporter-mediated multidrug resistance in cancer cells: evaluation of current strategies. Curr Mol Pharmacol 2008; 1: 93-105.
10. [10] Borowski E, Bontemps-Gracz M, Oiwkowska A. Strategies for overcoming ABC-transporters-mediated multidrug resistance (MDR) of tumor cells. Acta Biochim Pol 2005; 52: 609-27.
11. [11] Shukla S, Ohnuma S, Ambudkar SV. Improving cancer chemotherapy with modulators of ABC drug transporters. Curr Drug Targets 2011; 12: 621-30.
12. [12] Falasca M, Linton KJ. Investigational ABC transporter inhibitors. Expert Opin Investig Drugs 2012; 21: 657-66.
13. [13] Ferry DR, Traunecker H, Kerr DJ. Clinical trials of P-glycoprotein reversal in solid tumours. Eur J Cancer 1996; 32: 1070-81.
14. [14] Wandel C, Kim RB, Kajiji S, et al. P-glycoprotein and cytochrome P-450 3A inhibition: dissociation of inhibitory potencies. Cancer Res 1999; 59: 3944-8.
15. [15] Friedenberg WR, Rue M, Blood EA, et al. Phase III study of PSC- 833 (valspodar) in combination with vincristine, doxorubicin, and dexamethasone (valspodar/VAD) versus VAD alone in patients with recurring or refractory multiple myeloma (E1A95): a trial of the Eastern Cooperative Oncology Group. Cancer 2006; 106: 830-8.
16. [16] Baer MR, George SL, Dodge RK, et al. Phase 3 study of the multidrug resistance modulator PSC-833 in previously untreated patients 60 years of age and older with acute myeloid leukemia: Cancer and Leukemia Group B Study 9720. Blood 2002; 100: 1224-32.
17. [17] Seiden MV, Swenerton KD, Matulonis U, et al. A phase II study of the MDR inhibitor biricodar (INCEL, VX-710) and paclitaxel in women with advanced ovarian cancer refractory to paclitaxel therapy. Gynecol Oncol 2002; 86: 302-10.
18. [18] Gandhi L, Harding MW, Neubauer M, et al. A phase II study of the safety and efficacy of the multidrug resistance inhibitor VX-710 combined with doxorubicin and vincristine in patients with recurrent small cell lung cancer. Cancer 2007; 109: 924-32.
19. [19] Pajeva IK, Wiese M. Structure-activity relationships of tariquidar analogs as multidrug resistance modulators. AAPS J 2009; 11: 435- 44.
20. [20] Pusztai L, Wagner P, Ibrahim N, et al. Phase II study of tariquidar, a selective P-glycoprotein inhibitor, in patients with chemotherapyresistant, advanced breast carcinoma. Cancer 2005; 104: 682-91.
21. [21] Ruff P, Vorobiof DA, Jordaan JP, et al. A randomized, placebocontrolled, double-blind phase 2 study of docetaxel compared to docetaxel plus zosuquidar (LY335979) in women with metastatic or locally recurrent breast cancer who have received one prior chemotherapy regimen. Cancer Chemother Pharmacol 2009; 64: 763-8.
22. [22] Cripe LD, Uno H, Paietta EM, et al. Zosuquidar, a novel modulator of P-glycoprotein, does not improve the outcome of older patients with newly diagnosed acute myeloid leukemia: a randomized, placebo- controlled trial of the Eastern Cooperative Oncology Group 3999. Blood 2010; 116: 4077-85.
23. [23] Shukla S, Chen Z, Ambudkar SV. Tyrosine kinase inhibitors as modulators of ABC transporter-mediated drug resistance. Drug Resist Updat 2012; 15: 70-80.
24. [24] Hanks SK, Quinn AM, Hunter T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 1988; 241: 42-52.
25. [25] Hubbard SR, Till JH. Protein tyrosine kinase structure and function. Annu Rev Biochem 2000; 69: 373-98.
26. [26] Negi A, Ramarao P, Kumar R. Recent advancements in small molecule inhibitors of insulin-like growth factor-1 receptor (IGF- 1R) tyrosine kinase as anticancer agents. Mini Rev Med Chem 2013; 13: 653-81.
27. [27] Anreddy N, Gupta P, Kathawala RJ, et al. Tyrosine kinase inhibitors as reversal agents for ABC transporter mediated drug resistance. Molecules 2014; 19: 13848-77.
28. [28] He D, Zhao XQ, Chen XG, et al. BIRB796, the inhibitor of p38 mitogen-activated protein kinase, enhances the efficacy of chemotherapeutic agents in ABCB1 overexpression cells. PLoS One 2013; 8: e54181.
29. [29] He M, Wei MJ. Reversing multidrug resistance by tyrosine kinase inhibitors. Chin J Cancer 2012; 31: 126-33.
30. [30] Shukla S, Robey RW, Bates SE, et al. Sunitinib (Sutent, SU11248), a small-molecule receptor tyrosine kinase inhibitor, blocks function of the ATP-binding cassette (ABC) transporters P-glycoprotein (ABCB1) and ABCG2. Drug Metab Dispos 2009; 37: 359-65.
31. [31] Dai CL, Tiwari AK, Wu CP, et al. Lapatinib (Tykerb, GW572016) reverses multidrug resistance in cancer cells by inhibiting the activity of ATP-binding cassette subfamily B member 1 and G member 2. Cancer Res 2008; 68: 7905-14.
32. [32] Shi Z, Peng X, Kim I. Erlotinib (Tarceva, OSI-774) antagonizes ATP-binding cassette subfamily B member 1 and ATP-binding cassette subfamily G member 2-mediated drug resistance. Cancer Res 2007; 67: 11012-20.
33. [33] Mukai M, Che X, Furukawa T. Reversal of the resistance to STI571 in human chronic myelogenous leukemia K562 cells. Cancer Sci 2003; 94: 557-63.
34. [34] Liu KJ, He JH, Su XD, et al. Saracatinib (AZD0530) is a potent modulator of ABCB1-mediated multidrug resistance in vitro and in vivo. Int J Cancer 2013; 132: 224-35.
35. [35] Sen R, Natarajan K, Bhullar J, et al. The novel BCR-ABL and FLT3 inhibitor ponatinib is a potent inhibitor of the MDRassociated ATP-binding cassette transporter ABCG2. Mol Cancer Ther 2012; 11: 2033-44.
36. [36] Chen BA, Shan XY, Chen J, et al. Effects of imatinib and 5- bromotetrandrine on the reversal of multidrug resistance of the K562/A02 cell line. Chin J Cancer 2010; 29: 591-5.
37. [37] Houghton PJ, Germain GS, Harwood FC, et al. Imatinib mesylate is a potent inhibitor of the ABCG2 (BCRP) transporter and reverses resistance to topotecan and SN-38 in vitro. Cancer Res 2004; 64: 2333-7.
38. [38] Tiwari AK, Sodani K, Dai CL, et al. Nilotinib potentiates anticancer drug sensitivity in murine ABCB1-, ABCG2-, and ABCC10- multidrug resistance xenograft models. Cancer Lett 2013; 328: 307-17.
39. [39] Dohse M, Scharenberg C, Shukla S, et al. Comparison of ATPbinding cassette transporter interactions with the tyrosine kinase inhibitors imatinib, nilotinib, and dasatinib. Drug Metab Dispos 2010; 38: 1371-80.
40. [40] Nakamura Y, Oka M, Soda H, et al. Gefitinib ("Iressa", ZD1839), an epidermal growth factor receptor tyrosine kinase inhibitor, reverses breast cancer resistance protein/ABCG2-mediated drug resistance. Cancer Res 2005; 65: 1541-6.
41. [41] Shi Z, Parmar S, Peng XX, et al. The epidermal growth factor tyrosine kinase inhibitor AG1478 and erlotinib reverse ABCG2- mediated drug resistance. Oncol Rep 2009; 21: 483-9.
42. [42] Patel A, Tiwari AK, Chufan EE, et al. PD173074, a selective FGFR inhibitor, reverses ABCB1-mediated drug resistance in cancer cells. Cancer Chemother Pharmacol 2013; 72: 189-99.
43. [43] Xiang QF, Wang F, Su XD, et al. Effect of BIBF 1120 on reversal of ABCB1-mediated multidrug resistance. Cell Oncol 2011; 34: 33-44.
44. [44] Leggas M, Panetta JC, Zhuang Y, et al. Gefitinib modulates the function of multiple ATP-binding cassette transporters in vivo. Cancer Res 2006; 66: 4802-7.
45. [45] Shi Z, Tiwari AK, Shukla S, et al. Inhibiting the function of ABCB1 and ABCG2 by the EGFR tyrosine kinase inhibitor AG1478. Biochem Pharmacol 2009; 77: 781-93.
46. [46] Sodani K, Tiwari AK, Singh S, et al. GW583340 and GW2974, human EGFR and HER-2 inhibitors, reverse ABCG2- and ABCB1- mediated drug resistance. Biochem Pharmacol 2012; 83: 1613-22.
47. [47] Wang DS, Patel A, Sim HM, et al. ARRY-334543 reverses multidrug resistance by antagonizing the activity of ATP-binding cassette subfamily G member 2. J Cell Biochem 2014; 115: 1381- 91.
48. [48] Tao LY, Liang YJ, Wang F, et al. Cediranib (recentin, AZD2171) reverses ABCB1- and ABCC1-mediated multidrug resistance by inhibition of their transport function. Cancer Chemother Pharmacol 2009; 64: 961-9.
49. [49] Zheng LS, Wang F, Li YH, et al. Vandetanib (Zactima, ZD6474) antagonizes ABCC1- and ABCG2-mediated multidrug resistance by inhibition of their transport function. PloS One 2009; 4: e5172.
50. [50] Tong XZ, Wang F, Liang S, et al. Apatinib (YN968D1) enhances the efficacy of conventional chemotherapeutical drugs in side population cells and ABCB1-overexpressing leukemia cells. Biochem Pharmacol 2012; 83: 586-97.
51. [51] Sodani K, Patel A, Anreddy N, et al. Telatinib reverses chemotherapeutic multidrug resistance mediated by ABCG2 efflux transporter in vitro and in vivo. Biochem Pharmacol 2014; 89: 52- 61.
52. [52] Zhao XQ, Dai CL, Ohnuma S, et al. Tandutinib (MLN518/CT53518) targeted to stem-like cells by inhibiting the function of ATP-binding cassette subfamily G member 2. Eur J Pharm Sci 2013; 49: 441-50.
53. [53] Kathawala RJ, Chen JJ, Zhang YK, et al. Masitinib antagonizes ATP-binding cassette subfamily G member 2-mediated multidrug resistance. Int J Oncol 2014; 44: 1634-42.
54. [54] Kathawala RJ, Sodani K, Chen K, et al. Masitinib antagonizes ATP-binding cassette subfamily C member 10-mediated paclitaxel resistance: a preclinical study. Mol Cancer Ther 2014; 13: 714-23.
55. [55] Tiwari AK, Sodani K, Chen Z. Current advances in modulation of ABC transporter-mediated multidrug resistance in cancer. Int J Toxicol Pharmacol Res 2009; 1: 1-6.
56. [56] Marquez B, Van Bambeke F. ABC multidrug transporters: target for modulation of drug pharmacokinetics and drug-drug interactions. Curr Drug Targets 2011; 12: 600-20.
57. [57] Toth K, Vaughan MM, Schwartz G, et al. Expression of the MRP and MDR1 multidrug resistance gene products in 160 untreated human carcinomas studied by immunohistochemical methods in formalin-paraffin sections Int J Surg Pathol 1998; 6: 145-154.
58. [58] Wong K, Ma J, Rothnie A, et al. Towards understanding promiscuity in multidrug efflux pumps. Trends Biochem Sci 2014; 39: 8-16.
59. [59] Wang S, Ryder H, Pretswell I, et al. Studies on quinazolinones as dual inhibitors of Pgp and MRP1 in multidrug resistance. Bioorg Med Chem Lett 2002; 12: 571-4.
60. [60] Hyafil F, Vergely C, Du Vignaud P, et al. In vitro and in vivo reversal of multidrug resistance by GF120918, an acridonecarboxamide derivative. Cancer Res 1993; 53: 4595-602.
61. [61] Iwamoto FM, Lamborn KR, Robins HI, et al. Phase II trial of pazopanib (GW786034), an oral multi-targeted angiogenesis inhibitor, for adults with recurrent glioblastoma (North American Brain Tumor Consortium Study 06-02). Neuro Oncol 2010; 12: 855-61.
62. [62] Minocha M, Khurana V, Qin B, et al. Enhanced brain accumulation of pazopanib by modulating P-gp and Bcrp1 mediated efflux with canertinib or erlotinib. Int J Pharm 2012; 436: 127-34.
63. [63] Kaur R, Kapoor K, Kaur H. Plants as a source of anticancer agents. J Nat Prod Plant Resour 2011; 1: 119-24.
64. [64] Wu CP, Ohnuma S, Ambudkar SV. Discovering natural product modulators to overcome multidrug resistance in cancer chemotherapy. Curr Pharm Biotechnol 2011; 12: 609-20.
65. [65] Wesolowska O, Wisniewski J, Duarte N, et al. Inhibition of MRP1 transport activity by phenolic and terpenic compounds isolated from Euphorbia species. Anticancer Res 2007; 27: 4127-33.
66. [66] Wortelboer HM, Usta M, van Zanden JJ, et al. Inhibition of multidrug resistance proteins MRP1 and MRP2 by a series of alpha, beta-unsaturated carbonyl compounds. Biochem Pharmacol 2005; 69: 1879-90.
67. [67] Wang TH, Wan JY, Gong X, et al. Tetrandrine enhances cytotoxicity of cisplatin in human drug-resistant esophageal squamous carcinoma cells by inhibition of multidrug resistance-associated protein 1. Oncol Rep 2012; 28: 1681-6.
68. [68] Chen XS, Bao MH, Mei XD. Reversing multidrug resistance of epidermoid carcinoma drug-resistant cell line KB-MRP1 by tetrandrine. Ai Zheng 2007; 26: 846-50.
69. [69] Wang XB, Wang SS, Zhang QF, et al. Inhibition of tetramethylpyrazine on P-gp, MRP2, MRP3 and MRP5 in multidrug resistant human hepatocellular carcinoma cells. Oncol Rep 2010; 23: 211-5.
70. [70] Zhang Y, Liu X, Zuo T, et al. Tetramethylpyrazine reverses multidrug resistance in breast cancer cells through regulating the expression and function of P-glycoprotein. Med Oncol 2012; 29: 534-8.
71. [71] Pitchakarn P, Ohnuma S, Pintha K, et al. Kuguacin J isolated from Momordica charantia leaves inhibits P-glycoprotein (ABCB1)- mediated multidrug resistance. J Nutr Biochem 2012; 23: 76-84.
72. [72] El-Readi MZ, Eid S, Ashour ML, et al. Modulation of multidrug resistance in cancer cells by chelidonine and Chelidonium majus alkaloids. Phytomedicine 2013; 20: 282-94.
73. [73] Guo HQ, Zhang GN, Wang YJ, et al. beta-Elemene, a compound derived from Rhizoma zedoariae, reverses multidrug resistance mediated by the ABCB1 transporter. Oncol Rep 2014; 31: 858-66.
74. [74] Aoki S, Chen ZS, Higasiyama K, et al. Reversing effect of agosterol A, a spongean sterol acetate, on multidrug resistance in human carcinoma cells. Jpn J Cancer Res 2001; 92: 886-95.
75. [75] Al-Katib AM, Smith MR, Kamanda WS, et al. Bryostatin 1 downregulates mdr1 and potentiates vincristine cytotoxicity in diffuse large cell lymphoma xenografts. Clin Cancer Res 1998; 4: 1305-14.
76. [76] Shi Z, Jain S, Kim IW, et al. Sipholenol A, a marine-derived sipholane triterpene, potently reverses P-glycoprotein (ABCB1)- mediated multidrug resistance in cancer cells. Cancer Sci 2007; 98: 1373-80.
77. [77] Huang XC, Sun YL, Salim AA, et al. Parguerenes: Marine red alga bromoditerpenes as inhibitors of P-glycoprotein (ABCB1) in multidrug resistant human cancer cells. Biochem Pharmacol 2013; 85: 1257-68.
78. [78] Huang XC, Xiao X, Zhang YK, et al. Lamellarin O, a pyrrole alkaloid from an Australian marine sponge, Ianthella sp., reverses BCRP mediated drug resistance in cancer cells. Mar Drugs 2014; 12: 3818-37.
79. [79] Raju R, Piggott AM, Huang XC, et al. Nocardioazines: a novel bridged diketopiperazine scaffold from a marine-derived bacterium inhibits P-glycoprotein. Org Lett 2011; 13: 2770-3.
80. [80] Srinivasan S, Selvan ST, Archunan G, et al. MicroRNAs - the next generation therapeutic targets in human diseases. Theranostics 2013; 3: 930-42.
81. [81] Haenisch S, Werk AN, Cascorbi I. MicroRNAs and their relevance to ABC transporters. Br J Clin Pharmacol 2014; 77: 587-96.
82. [82] Feng DD, Zhang H, Zhang P, et al. Down-regulated miR-331-5p and miR-27a are associated with chemotherapy resistance and relapse in leukaemia. J Cell Mol Med 2011; 15: 2164-75.
83. [83] Zhu X, Li Y, Shen H, et al. miR-137 restoration sensitizes multidrug-resistant MCF-7/ADM cells to anticancer agents by targeting YB-1. Acta Biochim Biophys Sin (Shanghai) 2013; 45: 80- 6.
84. [84] Bao L, Hazari S, Mehra S, et al. Increased expression of Pglycoprotein and doxorubicin chemoresistance of metastatic breast cancer is regulated by miR-298. Am J Pathol 2012; 180: 2490-503.
85. [85] Kovalchuk O, Filkowski J, Meservy J, et al. Involvement of microRNA- 451 in resistance of the MCF-7 breast cancer cells to chemotherapeutic drug doxorubicin. Mol Cancer Ther 2008; 7: 2152-9.
86. [86] Shang Y, Zhang Z, Liu Z, et al. miR-508-5p regulates multidrug resistance of gastric cancer by targeting ABCB1 and ZNRD1. Oncogene 2013; 33(25): 3267-76.
87. [87] Yang T, Zheng ZM, Li XN, et al. MiR-223 modulates multidrug resistance via downregulation of ABCB1 in hepatocellular carcinoma cells. Exp Biol Med 2013; 238: 1024-32.
88. [88] Sui H, Cai GX, Pan SF, et al. miR-200c attenuates P-gp mediated MDR and metastasis by targeting JNK2/c-Jun signaling pathway in colorectal cancer. Mol Cancer Ther 2014; 13: 3137-51.
89. [89] Jiao X, Zhao L, Ma M, et al. MiR-181a enhances drug sensitivity in mitoxantone-resistant breast cancer cells by targeting breast cancer resistance protein (BCRP/ABCG2). Breast Cancer Res Treat 2013; 139: 717-30.
90. [90] Ma MT, He M, Wang Y, et al. MiR-487a resensitizes mitoxantrone (MX)-resistant breast cancer cells (MCF-7/MX) to MX by targeting breast cancer resistance protein (BCRP/ABCG2). Cancer Lett 2013; 339: 107-15.
91. [91] Li X, Pan YZ, Seigel GM, et al. Breast cancer resistance protein BCRP/ABCG2 regulatory microRNAs (hsa-miR-328, -519c and - 520h) and their differential expression in stem-like ABCG2+ cancer cells. Biochem Pharmacol 2011; 81: 783-92.
92. [92] Pan YZ, Morris ME, Yu AM. MicroRNA-328 negatively regulates the expression of breast cancer resistance protein (BCRP/ABCG2) in human cancer cells. Mol Pharmacol 2009; 75: 1374-9.
93. [93] Shen WW, Zeng Z, Zhu WX, et al. MiR-142-3p functions as a tumor suppressor by targeting CD133, ABCG2, and Lgr5 in colon cancer cells. J Mol Med (Berl) 2013; 91: 989-1000.
94. [94] Liang Z, Wu H, Xia J, et al. Involvement of miR-326 in chemotherapy resistance of breast cancer through modulating expression of multidrug resistance-associated protein 1. Biochem Pharmacol 2010; 79: 817-24.
95. [95] Xu K, Liang X, Shen K, et al. miR-297 modulates multidrug resistance in human colorectal carcinoma by down-regulating MRP-2. Biochem J 2012; 446: 291-300.
96. [96] Haenisch S, Cascorbi I. miRNAs as mediators of drug resistance. Epigenomics 2012; 4: 369-81.
97. [97] Akhtar K, Bussen W, Scott SP. Cancer stem cells - from initiation to elimination, how far have we reached? (Review). Int J Oncol 2009; 34: 1491-503.
98. [98] Bao B, Ahmad A, Azmi AS, et al. Overview of cancer stem cells (CSCs) and mechanisms of their regulation: implications for cancer therapy. Curr Protoc Pharmacol 2013; Chapter 14: Unit 14.25.
99. [99] Liao WT, Ye YP, Deng YJ, et al. Metastatic cancer stem cells: from the concept to therapeutics. Am J Stem Cells 2014; 3: 46-62.
100. [100] Dean M, Fojo T, Bates SE. Tumour stem cells and drug resistance. Nat Rev Cancer 2005; 5: 275-84.
101. [101] Dean M. ABC transporters, drug resistance, and cancer stem cells. J Mammary Gland Biol Neoplasia 2009; 14: 3-9.
102. [102] Zinzi L, Contino M, Cantore M, et al. ABC transporters in CSCs membranes as a novel target for treating tumor relapse. Front Pharmacol 2014; 5: 163.
103. [103] Golebiewska A, Brons NH, Bjerkvig R, et al. Critical appraisal of the side population assay in stem cell and cancer stem cell research. Cell Stem Cell 2011; 8: 136-47.
104. [104] Hirschmann-Jax C, Foster AE, Wulf GG, et al. A distinct ‘‘side population’’ of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA 2004; 101: 14228-33.
105. [105] Wouters J, Stas M, Gremeaux L, et al. The human melanoma side population displays molecular and functional characteristics of enriched chemoresistance and tumorigenesis. PLoS One 2013; 8: e76550.
106. [106] Van den Broeck A, Vankelecom H, Van Delm W, et al. Human pancreatic cancer contains a side population expressing cancer stem cell-associated and prognostic genes. PLoS One 2013; 8: e73968.
107. [107] Xiong B, Ma L, Hu X, et al. Characterization of side population cells isolated from the colon cancer cell line SW480. Int J Oncol 2014; 45: 1175-83.
108. [108] Eyre R, Harvey I, Stemke-Hale K, et al. Reversing paclitaxel resistance in ovarian cancer cells via inhibition of the ABCB1 expressing side population. Tumour Biol 2014; 35: 9879-92.
109. [109] Xu ZY, Wang K, Li XQ, et al. The ABCG2 transporter is a key molecular determinant of the efficacy of sonodynamic therapy with Photofrin in glioma stem-like cells. Ultrasonics 2013; 53: 232-8.
110. [110] Loebinger MR, Giangreco A, Groot KR, et al. Squamous cell cancers contain a side population of stem-like cells that are made chemosensitive by ABC transporter blockade. Br J Cancer 2008; 98: 380-7.
111. [111] Yang C, Xiong F, Wang J, et al. Anti-ABCG2 monoclonal antibody in combination with paclitaxel nanoparticles against cancer stem-like cell activity in multiple myeloma. Nanomedicine 2014; 9: 45-60.
112. [112] Martin V, Sanchez-Sanchez AM, Herrera F, et al. Melatonininduced methylation of the ABCG2/BCRP promoter as a novel mechanism to overcome multidrug resistance in brain tumour stem cells. Br J Cancer 2013; 108: 2005-12.
113. [113] Hou H, Sun H, Lu P, et al. Tunicamycin potentiates cisplatin anticancer efficacy through the DPAGT1/Akt/ABCG2 pathway in mouse Xenograft models of human hepatocellular carcinoma. Mol Cancer Ther 2013; 12: 2874-84.
114. [114] Shishido Y, Ueno S, Yamazaki R, et al. ABCG2 inhibitor YHO- 13351 sensitizes cancer stem/initiating-like side population cells to irinotecan. Anticancer Res 2013; 33: 1379-86.
115. [115] Tiwari AK, Sodani K, Wang SR, et al. Nilotinib (AMN107, Tasigna) reverses multidrug resistance by inhibiting the activity of the ABCB1/Pgp and ABCG2/BCRP/MXR transporters. Biochem Pharmacol 2009; 78: 153-61.
116. [116] Wang F, Wang XK, Shi CJ, et al. Nilotinib enhances the efficacy of conventional chemotherapeutic drugs in CD34(+)CD38(-) stem cells and ABC transporter overexpressing leukemia cells. Molecules 2014; 19: 3356-75.
117. [117] Wang XK, He JH, Xu JH, et al. Afatinib enhances the efficacy of conventional chemotherapeutic agents by eradicating cancer stemlike cells. Cancer Res 2014; 74: 4431-45.
118. [118] Gupta PB, Onder TT, Jiang G, et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009; 138: 645-59.
119. [119] Riccioni R, Dupuis ML, Bernabei M, et al. The cancer stem cell selective inhibitor salinomycin is a p-glycoprotein inhibitor. Blood Cells Mol Dis 2010; 45: 86-92.
120. [120] Fuchs D, Daniel V, Sadeghi M, et al. Salinomycin overcomes ABC transporter-mediated multidrug and apoptosis resistance in human leukemia stem cell-like KG-1a cells. Biochem Biophys Res Commun 2010; 394: 1098-104.
121. [121] Cheng C, Liu ZG, Zhang H, et al. Enhancing chemosensitivity in ABCB1- and ABCG2-overexpressing cells and cancer stem-like cells by an Aurora kinase inhibitor CCT129202. Mol Pharm 2012; 9: 1971-82.
122. [122] Wei L, Chen P, Chen Y, et al. Pien Tze Huang suppresses the stem-like side population in colorectal cancer cells. Mol Med Rep 2014; 9: 261-6.
123. [123] Xu Y, Zhi F, Xu G, et al. Overcoming multidrug-resistance in vitro and in vivo using the novel P-glycoprotein inhibitor 1416. Biosci Rep 2012; 32: 559-66.
124. [124] Zhang Y, Shi Y, Li X, et al. Proteasome inhibitor MG132 reverses multidrug resistance of gastric cancer through enhancing apoptosis and inhibiting P-gp. Cancer Biol Ther 2008; 7: 540-6.
125. [125] Onda K, Suzuki R, Tanaka S, et al. Decitabine, a DNA methyltransferase inhibitor, reduces P-glycoprotein mRNA and protein expressions and increases drug sensitivity in drug-resistant MOLT4 and Jurkat cell lines. Anticancer Res 2012; 32: 4439-44.
126. [126] Ding PR, Tiwari AK, Ohnuma S, et al. The phosphodiesterase-5 inhibitor vardenafil is a potent inhibitor of ABCB1/P-glycoprotein transporter. PloS One 2011; 6: e19329.
127. [127] Chu C, Abbara C, Tandia M, et al. Cetuximab increases concentrations of irinotecan and of its active metabolite SN-38 in plasma and tumour of human colorectal carcinoma-bearing mice. Fundam Clin Pharmacol 2014; 28: 652-60.
128. [128] Duan Z, Li X, Huang H, et al. Synthesis and evaluation of (2-(4-methoxyphenyl)-4-quinolinyl)(2-piperidinyl)methanol (NSC23925) isomers to reverse multidrug resistance in cancer. J Med Chem 2012; 55: 3113-21.
129. [129] Yamazaki R, Nishiyama Y, Furuta T, et al. Novel acrylonitrile derivatives, YHO-13177 and YHO-13351, reverse BCRP/ABCG2- mediated drug resistance in vitro and in vivo. Mol Cancer Ther 2011; 10: 1252-63.
130. [130] Peng H, Dong ZZ, Qi J, et al. A novel two mode-acting inhibitor of ABCG2-mediated multidrug transport and resistance in cancer chemotherapy. PloS One 2009; 4: e5676.
131. [131] Fletcher JI, Haber M, Henderson MJ, et al. ABC transporters in cancer: more than just drug efflux pumps. Nat Rev Cancer 2010; 10: 147-56.
132. [132] Quazi F, Molday RS. Lipid transport by mammalian ABC proteins. Essays Biochem 2011; 50: 265-90.
133. [133] Lopes EC, Garcia M, Benavides F, et al. Multidrug resistance modulators PSC 833 and CsA show differential capacity to induce apoptosis in lymphoid leukemia cell lines independently of their MDR phenotype. Leuk Res 2003; 27: 413-23.
134. [134] Shukla S, Skoumbourdis AP, Walsh MJ, et al. Synthesis and characterization of a BODIPY conjugate of the BCR-ABL kinase inhibitor Tasigna (nilotinib): evidence for transport of Tasigna and its fluorescent derivative by ABC drug transporters. Mol Pharm 2011; 8: 1292-302.