ABCG2 inhibition as a therapeutic approach for overcoming multidrug resistance in cancer

Journal of Biosciences

Volumn 41, Issue 2, 2016, Pages 313-324

  Hasanabady, Maryam Hosseini ^a   Kalalinia, Fatemeh ^b  

^a ISLAMIC AZAD UNIVERSITY   (Iran)

^b MASHHAD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

ABCG2; ABCG2 inhibitors; BCRP; multidrug resistance (MDR); tyrosine kinases

Indexed keywords

ABC TRANSPORTER; ABCG2 INHIBITOR; ANTHRACYCLINE; ANTIMETABOLITE; ANTINEOPLASTIC AGENT; AROMATIC HYDROCARBON RECEPTOR; BREAST CANCER RESISTANCE PROTEIN; CAMPTOTHECIN DERIVATIVE; DASATINIB; DNA TOPOISOMERASE INHIBITOR; ELACRIDAR; ESTROGEN RECEPTOR ALPHA; FUMITREMORGIN C; HYPOXIA INDUCIBLE FACTOR 1; IMATINIB; LAPATINIB; MOTESANIB; NILOTINIB; ORTATAXEL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PONATINIB; PROGESTERONE RECEPTOR; PROTEIN TYROSINE KINASE INHIBITOR; SUNITINIB; TELATINIB; UNCLASSIFIED DRUG; ABCG2 PROTEIN, HUMAN; TUMOR PROTEIN;

CANCER; DRUG RESISTANCE; INHIBITOR; MEDICINE;

ADENOCARCINOMA; AHR GENE; ARTICLE; BREAST CANCER; CANCER CELL; CANCER CELL LINE; CANCER RESISTANCE; CERVICAL ADENOCARCINOMA; CHRONIC MYELOID LEUKEMIA; DRUG ADSORPTION; DRUG DISTRIBUTION; DRUG EXCRETION; DRUG MECHANISM; DRUG METABOLISM; EPIGENETIC MODIFICATION; GASTROINTESTINAL STROMAL TUMOR; GENE; GENETIC POLYMORPHISM; GENETIC REGULATION; HEMATOLOGIC MALIGNANCY; HUMAN; KIDNEY CARCINOMA; LUNG CARCINOMA; MULTIDRUG RESISTANCE; MULTIPLE CANCER; NEOPLASM; NONHUMAN; PHILADELPHIA CHROMOSOME POSITIVE CHRONIC MYELOGENOUS LEUKEMIA; POST TRANSCRIPTIONAL REGULATION; PPARG GENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; SOLID TUMOR; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; ANTAGONISTS AND INHIBITORS; BLOOD BRAIN BARRIER; DRUG RESISTANCE; GENETIC EPIGENESIS; GENETICS; METABOLISM; NEOPLASMS; PROTEIN SYNTHESIS; TRANSPORT AT THE CELLULAR LEVEL;

ANTINEOPLASTIC AGENTS; ATP BINDING CASSETTE TRANSPORTER, SUB-FAMILY G, MEMBER 2; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; EPIGENESIS, GENETIC; HUMANS; NEOPLASM PROTEINS; NEOPLASMS; PROTEIN BIOSYNTHESIS;

EID: 84962687847     PISSN: 02505991     EISSN: 09737138     Source Type: Journal    
DOI: 10.1007/s12038-016-9601-5     Document Type: Article

References (104)

1. Agundez JA 2008 Polymorphisms of human N-acetyltransferases and cancer risk. Curr. Drug Metab. 9 520–531
2. Ahmed-Belkacem A, Pozza A, Munoz-Martinez F, Bates SE, Castanys S, Gamarro F, Di Pietro A and Perez-Victoria JM 2005 Flavonoid structure-activity studies identify 6-prenylchrysin and tectochrysin as potent and specific inhibitors of breast cancer resistance protein ABCG2. Cancer Res. 65 4852–4860
3. Allen JD, van Loevezijn A, Lakhai JM, van der Valk M, van Tellingen O, Reid G, Schellens JH, Koomen GJ, et al. 2002 Potent and specific inhibition of the breast cancer resistance protein multidrug transporter in vitro and in mouse intestine by a novel analogue of fumitremorgin C. Mol. Cancer Ther. 1 417–425
4. Allikmets R, Schriml LM, Hutchinson A, Romano-Spica V and Dean M 1998 A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Res. 58 5337–5339
5. An Y and Ongkeko WM 2009 ABCG2: the key to chemoresistance in cancer stem cells? Expert Opin. Drug Metab. Toxicol. 5 1529–1542
6. Angelini S, Soverini S, Ravegnini G, Barnett M, Turrini E, Thornquist M, Pane F, Hughes TP, et al. 2013 Association between imatinib transporters and metabolizing enzymes genotype and response in newly diagnosed chronic myeloid leukemia patients receiving imatinib therapy. Haematologica 98 193–200
7. Aronica E, Gorter JA, Redeker S, van Vliet EA, Ramkema M, Scheffer GL, Scheper RJ, van der Valk P, et al. 2005 Localization of breast cancer resistance protein (BCRP) in microvessel endothelium of human control and epileptic brain. Epilepsia 46 849–857
8. Bernstein BE, Meissner A and Lander ES 2007 The mammalian epigenome. Cell 128 669–681
9. Bram EE, Stark M, Raz S and Assaraf YG 2009 Chemotherapeutic drug-induced ABCG2 promoter demethylation as a novel mechanism of acquired multidrug resistance. Neoplasia 11 1359–1370
10. Bunting KD 2002 ABC transporters as phenotypic markers and functional regulators of stem cells. Stem Cells 20 11–20
11. Chen H, Rossier C, Lalioti MD, Lynn A, Chakravarti A, Perrin G and Antonarakis SE 1996 Cloning of the cDNA for a human homologue of the Drosophila white gene and mapping to chromosome 21q22.3. Am. J. Hum. Genet. 59 66–75
12. Chua C, Zaiden N, Chong KH, See SJ, Wong MC, Ang BT and Tang C 2008 Characterization of a side population of astrocytoma cells in response to temozolomide. J. Neurosurg. 109 856–866
13. Cooray HC, Blackmore CG, Maskell L and Barrand MA 2002 Localisation of breast cancer resistance protein in microvessel endothelium of human brain. Neuroreport 13 2059–2063
14. Cusatis G and Sparreboom A 2008 Pharmacogenomic importance of ABCG2. Pharmacogenomics 9 1005–1009
15. Dai CL, Liang YJ, Wang YS, Tiwari AK, Yan YY, Wang F, Chen ZS, Tong XZ, et al. 2009 Sensitization of ABCG2-overexpressing cells to conventional chemotherapeutic agent by sunitinib was associated with inhibiting the function of ABCG2. Cancer Lett. 279 74–83
16. Dai CL, Tiwari AK, Wu CP, Su XD, Wang SR, Liu DG, Ashby CR, Jr., Huang Y, et al. 2008 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. 68 7905–7914
17. de Vries NA, Zhao J, Kroon E, Buckle T, Beijnen JH and van Tellingen O 2007 P-glycoprotein and breast cancer resistance protein: two dominant transporters working together in limiting the brain penetration of topotecan. Clin. Cancer Res. 13 6440–6449
18. Dietrich CG, Geier A and Oude Elferink RP 2003 ABC of oral bioavailability: transporters as gatekeepers in the gut. Gut 52 1788–1795
19. Doyle L and Ross DD 2003 Multidrug resistance mediated by the breast cancer resistance protein BCRP (ABCG2). Oncogene 22 7340–7358
20. Doyle LA, Yang W, Abruzzo LV, Krogmann T, Gao Y, Rishi AK and Ross DD 1998 A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc. Natl. Acad. Sci. USA 95 15665–15670
21. Durmus S, Sparidans RW, Wagenaar E, Beijnen JH and Schinkel AH 2012 Oral availability and brain penetration of the B-RAFV600E inhibitor vemurafenib can be enhanced by the P-GLYCOprotein (ABCB1) and breast cancer resistance protein (ABCG2) inhibitor elacridar. Mol. Pharm. 9 3236–3245
22. Elahian F, Kalalinia F and Behravan J 2009 Dexamethasone downregulates BCRP mRNA and protein expression in breast cancer cell lines. Oncol. Res. 18 9–15
23. Elahian F, Kalalinia F and Behravan J 2010 Evaluation of indomethacin and dexamethasone effects on BCRP-mediated drug resistance in MCF-7 parental and resistant cell lines. Drug Chem. Toxicol. 33 113–119
24. Gandhi YA and Morris ME 2009 Structure-activity relationships and quantitative structure-activity relationships for breast cancer resistance protein (ABCG2). AAPS J. 11 541–552
25. Gardner ER et al. 2006 Association of enzyme and transporter genotypes with the pharmacokinetics of imatinib. Clin. Pharmacol. Ther. 80 192–201
26. Giannoudis A, Davies A, Lucas CM, Harris RJ, Pirmohamed M and Clark RE 2008 Effective dasatinib uptake may occur without human organic cation transporter 1 (hOCT1): implications for the treatment of imatinib-resistant chronic myeloid leukemia. Blood 112 3348–3354
27. Gillet JP and Gottesman MM 2010 Mechanisms of multidrug resistance in cancer. Methods Mol. Biol. 596 47–76
28. Glavinas H, Krajcsi P, Cserepes J and Sarkadi B 2004 The role of ABC transporters in drug resistance, metabolism and toxicity. Curr. Drug Deliv. 1 27–42
29. Hirota S, Isozaki K, Moriyama Y, Hashimoto K, Nishida T, Ishiguro S, Kawano K, Hanada M, et al. 1998 Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 279 577–580
30. Houghton PJ, Germain GS, Harwood FC, Schuetz JD, Stewart CF, Buchdunger E and Traxler P 2004 Imatinib mesylate is a potent inhibitor of the ABCG2 (BCRP) transporter and reverses resistance to topotecan and SN-38 in vitro. Cancer Res. 64 2333–2337
31. Jiang Y, He Y, Li H, Li HN, Zhang L, Hu W, Sun YM, Chen FL, et al. 2012 Expressions of putative cancer stem cell markers ABCB1, ABCG2, and CD133 are correlated with the degree of differentiation of gastric cancer. Gastric Cancer 15 440–450
32. Jonker JW, Smit JW, Brinkhuis RF, Maliepaard M, Beijnen JH, Schellens JH and Schinkel AH 2000 Role of breast cancer resistance protein in the bioavailability and fetal penetration of topotecan. J. Natl. Cancer Inst. 92 1651–1656
33. Kalalinia F, Elahian F and Behravan J 2011 Potential role of cyclooxygenase-2 on the regulation of the drug efflux transporter ABCG2 in breast cancer cell lines. J. Cancer Res. Clin. Oncol. 137 321–330
34. Kalalinia F, Elahian F, Mosaffa F and Behravan J 2014 Celecoxib Up Regulates the Expression of Drug Efflux Transporter ABCG2 in Breast Cancer Cell Lines. Iran J. Pharm. Res. 13 1393–1401
35. Kalalinia F, Elahian F, Hassani M, Kasaeeian J and Behravan J 2012 Phorbol ester TPA modulates chemoresistance in the drug sensitive breast cancer cell line MCF-7 by inducing expression of drug efflux transporter ABCG2. Asian Pac. J. Cancer Prev. 13 2979–2984
36. Kim DH, Xu W, Kamel-Reid S, Liu X, Jung CW, Kim S and Lipton JH 2010 Clinical relevance of vascular endothelial growth factor (VEGFA) and VEGF receptor (VEGFR2) gene polymorphism on the treatment outcome following imatinib therapy. Ann. Oncol. 21 1179–1188
37. Knutsen T, Rao VK, Ried T, Mickley L, Schneider E, Miyake K, Ghadimi BM, Padilla-Nash H, et al. 2000 Amplification of 4q21-q22 and the MXR gene in independently derived mitoxantrone-resistant cell lines. Genes Chromosomes Cancer 27 110–116
38. Kruijtzer CM, Beijnen JH, Rosing H, ten Bokkel Huinink WW, Schot M, Jewell RC, Paul EM and Schellens JH 2002 Increased oral bioavailability of topotecan in combination with the breast cancer resistance protein and P-glycoprotein inhibitor GF120918. J. Clin. Oncol. 20 2943–2950
39. Lemos C, Kathmann I, Giovannetti E, Dekker H, Scheffer GL, Calhau C, Jansen G and Peters GJ 2008 Folate deprivation induces BCRP (ABCG2) expression and mitoxantrone resistance in Caco-2 cells. Int. J. Cancer 123 1712–1720
40. Lheureux S, Krieger S, Weber B, Pautier P, Fabbro M, Selle F, Bourgeois H, Petit T, et al. 2012 Expected benefits of topotecan combined with lapatinib in recurrent ovarian cancer according to biological profile: a phase 2 trial. Int. J. Gynecol. Cancer 22 1483–1488
41. Li X, Pan YZ, Seigel GM, Hu ZH, Huang M and Yu AM 2011 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. 81 783–792
42. Litman T et al. 2002 Use of peptide antibodies to probe for the mitoxantrone resistance-associated protein MXR/BCRP/ABCP/ABCG2. Biochim. Biophys. Acta 1565 6–16
43. Liu Y, Yang Y, Qi J, Peng H and Zhang JT 2008 Effect of cysteine mutagenesis on the function and disulfide bond formation of human ABCG2. J. Pharmacol. Exp. Ther. 326 33–40
44. Mahon FX et al. 2010 Discontinuation of imatinib in patients with chronic myeloid leukaemia who have maintained complete molecular remission for at least 2 years: the prospective, multicentre Stop Imatinib (STIM) trial. Lancet Oncol. 11 1029–1035
45. Maliepaard M, van Gastelen MA, de Jong LA, Pluim D, van Waardenburg RC, Ruevekamp-Helmers MC, Floot BG and Schellens JH 1999 Overexpression of the BCRP/MXR/ABCP gene in a topotecan-selected ovarian tumor cell line. Cancer Res. 59 4559–4563
46. Maliepaard M, Scheffer GL, Faneyte IF, van Gastelen MA, Pijnenborg AC, Schinkel AH, van De Vijver MJ, Scheper RJ, et al. 2001 Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues. Cancer Res. 61 3458–3464
47. Mao Q and Unadkat JD 2005 Role of the breast cancer resistance protein (ABCG2) in drug transport. AAPS J. 7 E118–E133
48. Martin V, Sanchez-Sanchez AM, Herrera F, Gomez-Manzano C, Fueyo J, Alvarez-Vega MA, Antolin I and Rodriguez C 2013 Melatonin-induced methylation of the ABCG2/BCRP promoter as a novel mechanism to overcome multidrug resistance in brain tumour stem cells. Br. J. Cancer 108 2005–2012
49. Mickley L, Jain P, Miyake K, Schriml LM, Rao K, Fojo T, Bates S and Dean M 2001 An ATP-binding cassette gene (ABCG3) closely related to the multidrug transporter ABCG2 (MXR/ABCP) has an unusual ATP-binding domain. Mamm. Genome. 12 86–88
50. Miyake K, Mickley L, Litman T, Zhan Z, Robey R, Cristensen B, Brangi M, Greenberger L, et al. 1999 Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes. Cancer Res. 59 8–13
51. Mo W and Zhang JT 2012 Human ABCG2: structure, function, and its role in multidrug resistance. Int. J. Biochem. Mol. Biol. 3 1–27
52. Moitra K 2015 Overcoming multidrug resistance in cancer stem cells. Biomed. Res. Int. 2015 635745
53. Molina JR, Kaufmann SH, Reid JM, Rubin SD, Galvez-Peralta M, Friedman R, Flatten KS, Koch KM, et al. 2008 Evaluation of lapatinib and topotecan combination therapy: tissue culture, murine xenograft, and phase I clinical trial data. Clin. Cancer Res. 14 7900–7908
54. Morfouace M, Cheepala S, Jackson S, Fukuda Y, Patel YT, Fatima S, Kawauchi D, Shelat AA, et al. 2015 ABCG2 transporter expression impacts group 3 medulloblastoma response to chemotherapy. Cancer Res. 75 3879–3889
55. Mosaffa F, Kalalinia F, Parhiz BH and Behravan J 2011 Tumor necrosis factor alpha induces stronger cytotoxicity in ABCG2-overexpressing resistant breast cancer cells compared with their drug-sensitive parental line. DNA Cell Biol. 30 413–418
56. Mosaffa F, Kalalinia F, Lage H, Afshari JT and Behravan J 2012 Pro-inflammatory cytokines interleukin-1 beta, interleukin 6, and tumor necrosis factor-alpha alter the expression and function of ABCG2 in cervix and gastric cancer cells. Mol. Cell. Biochem. 363 385–393
57. Munoz M, Henderson M, Haber M and Norris M 2007 Role of the MRP1/ABCC1 multidrug transporter protein in cancer. IUBMB Life 59 752–757
58. Nakagawa H, Tamura A, Wakabayashi K, Hoshijima K, Komada M, Yoshida T, Kometani S, Matsubara T, et al. 2008 Ubiquitin-mediated proteasomal degradation of non-synonymous SNP variants of human ABC transporter ABCG2. Biochem. J. 411 623–631
59. Natarajan K, Xie Y, Baer MR and Ross DD 2012 Role of breast cancer resistance protein (BCRP/ABCG2) in cancer drug resistance. Biochem. Pharmacol. 83 1084–1103
60. Niu Q, Wang W, Li Y, Ruden DM, Wang F, Li Y, Wang F, Song J, et al. 2012 Low molecular weight heparin ablates lung cancer cisplatin-resistance by inducing proteasome-mediated ABCG2 protein degradation. PLoS One 7 e41035
61. Ozvegy-Laczka C, Cserepes J, Elkind NB and Sarkadi B 2005 Tyrosine kinase inhibitor resistance in cancer: role of ABC multidrug transporters. Drug Resist. Updat. 8 15–26
62. Ozvegy C, Litman T, Szakacs G, Nagy Z, Bates S, Varadi A and Sarkadi B 2001 Functional characterization of the human multidrug transporter, ABCG2, expressed in insect cells. Biochem. Biophys. Res. Commun. 285 111–117
63. Pan YZ, Morris ME and Yu AM 2009 MicroRNA-328 negatively regulates the expression of breast cancer resistance protein (BCRP/ABCG2) in human cancer cells. Mol. Pharmacol. 75 1374–1379
64. Petain A, Kattygnarath D, Azard J, Chatelut E, Delbaldo C, Geoerger B, Barrois M, Seronie-Vivien S, et al. 2008 Population pharmacokinetics and pharmacogenetics of imatinib in children and adults. Clin. Cancer Res. 14 7102–7109
65. Plasschaert SL, van der Kolk DM, de Bont ES, Kamps WA, Morisaki K, Bates SE, Scheffer GL, Scheper RJ, et al. 2003 The role of breast cancer resistance protein in acute lymphoblastic leukemia. Clin. Cancer Res. 9 5171–5177
66. Polgar O, Robey RW and Bates SE 2008 ABCG2: structure, function and role in drug response. Expert Opin. Drug Metab. Toxicol. 4 1–15
67. Rabindran SK, Ross DD, Doyle LA, Yang W and Greenberger LM 2000 Fumitremorgin C reverses multidrug resistance in cells transfected with the breast cancer resistance protein. Cancer Res. 60 47–50
68. Ricci JW, Lovato D and Larson RS 2015 ABCG2 inhibitors: will they find clinical relevance? J. Dev. Drugs 4 138
69. Robey RW, Steadman K, Polgar O and Bates SE 2005 ABCG2-mediated transport of photosensitizers: potential impact on photodynamic therapy. Cancer Biol. Ther. 4 187–194
70. Robey RW, Steadman K, Polgar O, Morisaki K, Blayney M, Mistry P and Bates SE 2004 Pheophorbide a is a specific probe for ABCG2 function and inhibition. Cancer Res. 64 1242–1246
71. Robey RW, Medina-Perez WY, Nishiyama K, Lahusen T, Miyake K, Litman T, Senderowicz AM, Ross DD, et al. 2001 Overexpression of the ATP-binding cassette half-transporter, ABCG2 (Mxr/BCrp/ABCP1), in flavopiridol-resistant human breast cancer cells. Clin. Cancer Res. 7 145–152
72. Ross DD, Karp JE, Chen TT and Doyle LA 2000 Expression of breast cancer resistance protein in blast cells from patients with acute leukemia. Blood 96 365–368
73. Ross DD, Yang W, Abruzzo LV, Dalton WS, Schneider E, Lage H, Dietel M, Greenberger L, et al. 1999 Atypical multidrug resistance: breast cancer resistance protein messenger RNA expression in mitoxantrone-selected cell lines. J. Natl. Cancer Inst. 91 429–433
74. Sargent JM, Williamson CJ, Maliepaard M, Elgie AW, Scheper RJ and Taylor CG 2001 Breast cancer resistance protein expression and resistance to daunorubicin in blast cells from patients with acute myeloid leukaemia. Br. J. Haematol. 115 257–262
75. Sauerbrey A, Sell W, Steinbach D, Voigt A and Zintl F 2002 Expression of the BCRP gene (ABCG2/MXR/ABCP) in childhood acute lymphoblastic leukaemia. Br. J. Haematol. 118 147–150
76. Scotto KW 2003 Transcriptional regulation of ABC drug transporters. Oncogene 22 7496–7511
77. Sen R, Natarajan K, Bhullar J, Shukla S, Fang HB, Cai L, Chen ZS, Ambudkar SV, et al. 2012 The novel BCR-ABL and FLT3 inhibitor ponatinib is a potent inhibitor of the MDR-associated ATP-binding cassette transporter ABCG2. Mol. Cancer Ther. 11 2033–2044
78. Seong SJ, Lim M, Sohn SK, Moon JH, Oh SJ, Kim BS, Ryoo HM, Chung JS, et al. 2013 Influence of enzyme and transporter polymorphisms on trough imatinib concentration and clinical response in chronic myeloid leukemia patients. Ann. Oncol. 24 756–760
79. Shukla S, Robey RW, Bates SE and Ambudkar SV 2009 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. 37 359–365
80. Singh RR, Kunkalla K, Qu C, Schlette E, Neelapu SS, Samaniego F and Vega F 2011 ABCG2 is a direct transcriptional target of hedgehog signaling and involved in stroma-induced drug tolerance in diffuse large B-cell lymphoma. Oncogene 30 4874–4886
81. Sodani K, Patel A, Anreddy N, Singh S, Yang DH, Kathawala RJ, Kumar P, Talele TT, et al. 2014 Telatinib reverses chemotherapeutic multidrug resistance mediated by ABCG2 efflux transporter in vitro and in vivo. Biochem. Pharmacol. 89 52–61
82. Sparreboom A, Zamboni WC 2006 Topoisomerase I-targeting drugs (Lippincott Williams & Wilkins)
83. Staud F and Pavek P 2005 Breast cancer resistance protein (BCRP/ABCG2). Int. J. Biochem. Cell Biol. 37 720–725
84. Stewart CF, Tagen M, Schwartzberg LS, Blakely LJ, Tauer KW and Smiley LM 2014 Phase I dosage finding and pharmacokinetic study of intravenous topotecan and oral erlotinib in adults with refractory solid tumors. Cancer Chemother. Pharmacol. 73 561–568
85. Suvannasankha A, Minderman H, O'Loughlin KL, Nakanishi T, Greco WR, Ross DD and Baer MR 2004a Breast cancer resistance protein (BCRP/MXR/ABCG2) in acute myeloid leukemia: discordance between expression and function. Leukemia 18 1252–1257
86. Suvannasankha A, Minderman H, O'Loughlin KL, Nakanishi T, Ford LA, Greco WR, Wetzler M, Ross DD, et al. 2004b Breast cancer resistance protein (BCRP/MXR/ABCG2) in adult acute lymphoblastic leukaemia: frequent expression and possible correlation with shorter disease-free survival. Br. J. Haematol. 127 392–398
87. Takahashi N, Miura M, Scott SA, Kagaya H, Kameoka Y, Tagawa H, Saitoh H, Fujishima N, et al. 2010 Influence of CYP3A5 and drug transporter polymorphisms on imatinib trough concentration and clinical response among patients with chronic phase chronic myeloid leukemia. J. Hum. Genet. 55 731–737
88. Takano M, Yumoto R and Murakami T 2006 Expression and function of efflux drug transporters in the intestine. Pharmacol. Ther. 109 137–161
89. Tiwari AK, Sodani K, Dai CL, Ashby CR Jr and Chen ZS 2011 Revisiting the ABCs of multidrug resistance in cancer chemotherapy. Curr. Pharm. Biotechnol. 12 570–594
90. Tiwari AK, Sodani K, Wang SR, Kuang YH, Ashby CR Jr, Chen X and Chen ZS 2009 Nilotinib (AMN107, Tasigna) reverses multidrug resistance by inhibiting the activity of the ABCB1/Pgp and ABCG2/BCRP/MXR transporters. Biochem. Pharmacol. 78 153–161
91. Turner JG, Gump JL, Zhang C, Cook JM, Marchion D, Hazlehurst L, Munster P, Schell MJ, et al. 2006 ABCG2 expression, function, and promoter methylation in human multiple myeloma. Blood 108 3881–3889
92. van der Geer P, Hunter T and Lindberg RA 1994 Receptor protein-tyrosine kinases and their signal transduction pathways. Annu. Rev. Cell Biol. 10 251–337
93. Wang H, Lee EW, Cai X, Ni Z, Zhou L and Mao Q 2008a Membrane topology of the human breast cancer resistance protein (BCRP/ABCG2) determined by epitope insertion and immunofluorescence. Biochemistry 47 13778–13787
94. Wang L, Giannoudis A, Lane S, Williamson P, Pirmohamed M and Clark RE 2008b Expression of the uptake drug transporter hOCT1 is an important clinical determinant of the response to imatinib in chronic myeloid leukemia. Clin. Pharmacol. Ther. 83 258–264
95. Weroha SJ, Oberg AL, Ziegler KL, Dakhilm SR, Rowland KM, Hartmann LC, Moore DF Jr, Keeney GL, et al. 2011 Phase II trial of lapatinib and topotecan (LapTop) in patients with platinum-refractory/resistant ovarian and primary peritoneal carcinoma. Gynecol. Oncol. 122 116–120
96. Xiong H, Callaghan D, Jones A, Bai J, Rasquinha I, SmithC, Pei K, Walker D, et al. 2009 ABCG2 is upregulated in Alzheimer's brain with cerebral amyloid angiopathy and may act as a gatekeeper at the blood–brain barrier for Abeta(1-40) peptides. J. Neurosci. 29 5463–5475
97. Yang CH, Schneider E, Kuo ML, Volk EL, Rocchi E and Chen YC 2000 BCRP/MXR/ABCP expression in topotecan-resistant human breast carcinoma cells. Biochem. Pharmacol. 60 831–837
98. Yang WJ, Song MJ, Park EY, Lee JJ, Park JH, Park K, Park JH and Kim HP 2013 Transcription factors Sp1 and Sp3 regulate expression of human ABCG2 gene and chemoresistance phenotype. Mol. Cells 36 368–375
99. Yoh K, Ishii G, Yokose T, Minegishi Y, Tsuta K, Goto K, Nishiwaki Y, Kodama T, et al. 2004 Breast cancer resistance protein impacts clinical outcome in platinum-based chemotherapy for advanced non-small cell lung cancer. Clin. Cancer Res. 10 1691–1697
100. Zhang W, Mojsilovic-Petrovic J, Andrade MF, Zhang H, Ball M and Stanimirovic DB 2003 The expression and functional characterization of ABCG2 in brain endothelial cells and vessels. FASEB J. 17 2085–2087
101. Zhao L, Ren Y, Tang H, Wang W, He Q, Sun J, Zhou X, and Wang A 2015 Deregulation of the miR-222-ABCG2 regulatory module in tongue squamous cell carcinoma contributes to chemoresistance and enhanced migratory/invasive potential. Oncotarget 6 44538–44550
102. Zhao L, Pan Y, Gang Y, Wang H, Jin H, Tie J, Xia L, Zhang Y, et al. 2009 Identification of GAS1 as an epirubicin resistance-related gene in human gastric cancer cells with a partially randomized small interfering RNA library. J. Biol. Chem. 284 26273–26285
103. Zhou S, Schuetz JD, Bunting KD, ColapietroAM, Sampath J, Morris JJ, Lagutina I, Grosveld GC, 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
104. Zhuang Y, Fraga CH, Hubbard KE, Hagedorn N, Panetta JC, Waters CM and Stewart CF 2006 Topotecan central nervous system penetration is altered by a tyrosine kinase inhibitor. Cancer Res. 66 11305–11313