Molecular pathways: Regulation and therapeutic implications of multidrug resistance

Clinical Cancer Research

Volumn 18, Issue 7, 2012, Pages 1863-1869

  Chen, Kevin G ^a,b   Sikic, Branimir I ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOSPORIN; DAUNORUBICIN; DOXORUBICIN; ETOPOSIDE; GLYCOPROTEIN P; HISTONE H3; MUTANT PROTEIN; TUMOR SUPPRESSOR PROTEIN; VALSPODAR; ZOSUQUIDAR;

ACB1 GENE; ACUTE GRANULOCYTIC LEUKEMIA; CANCER RESISTANCE; CHROMATIN STRUCTURE; DEACETYLATION; DEMETHYLATION; DNA MODIFICATION; DRUG FATALITY; DRUG MEGADOSE; EPIGENETICS; GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE INTERACTION; GENE MUTATION; GENE REARRANGEMENT; GENOME; GENOMIC INSTABILITY; HUMAN; MOLECULARLY TARGETED THERAPY; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ACETYLATION; DNA METHYLATION; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; MODELS, GENETIC; NEOPLASMS; P-GLYCOPROTEIN;

EID: 84859376472     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-1590     Document Type: Review

References (68)

1. 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. (Pubitemid 43185280)
2. Mahadevan D, List AF. Targeting the multidrug resistance-1 transporter in AML: molecular regulation and therapeutic strategies. Blood 2004;104:1940-51. (Pubitemid 39297842)
3. Sikic BI. Modulation of multidrug resistance: a paradigm for translational clinical research. Oncology (Williston Park) 1999;13[5A]:183-7 [Williston Park].
4. Clarke R, Leonessa F, Trock B. Multidrug resistance/P-glycoprotein and breast cancer: review and meta-analysis. Semin Oncol 2005;32[Suppl 7]:S9-15.
5. Scotto KW. Transcriptional regulation of ABC drug transporters. Oncogene 2003;22:7496-511. (Pubitemid 37487172)
6. Sikic BI, Fisher GA, Lum BL, Halsey J, Beketic-Oreskovic L, Chen G. Modulation and prevention of multidrug resistance by inhibitors of P-glycoprotein. Cancer Chemother Pharmacol 1997;40[Suppl]:S13-9.
7. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2002;2:48-58. (Pubitemid 37328807)
8. Allen JD, Brinkhuis RF, van Deemter L, Wijnholds J, Schinkel AH. Extensive contribution of the multidrug transporters P-glycoprotein and Mrp1 to basal drug resistance. Cancer Res 2000;60:5761-6.
9. Smit JW, Schinkel AH, Müller M, Weert B, Meijer DK. Contribution of the murine mdr1a P-glycoprotein to hepatobiliary and intestinal elimination of cationic drugs as measured in mice with an mdr1a gene disruption. Hepatology 1998;27:1056-63. (Pubitemid 28160492)
10. Chen G, Jaffrézou JP, Fleming WH, Durán GE, Sikic BI. Prevalence of multidrug resistance related to activation of the mdr1 gene in human sarcoma mutants derived by single-step doxorubicin selection. Cancer Res 1994;54:4980-7. (Pubitemid 24289431)
11. Dumontet C, Duran GE, Steger KA, Beketic-Oreskovic L, Sikic BI. Resistance mechanisms in human sarcoma mutants derived by single-step exposure to paclitaxel (Taxol). Cancer Res 1996;56:1091-7. (Pubitemid 26065405)
12. Chen GK, Durán GE, Mangili A, Beketic-Oreskovic L, Sikic BI. MDR 1 activation is the predominant resistance mechanism selected by vinblastine in MES-SA cells. Br J Cancer 2000;83:892-8.
13. Chen KG, Wang YC, Schaner ME, Francisco B, Durán GE, Juric D, et al. Genetic and epigenetic modeling of the origins of multidrug-resistant cells in a human sarcoma cell line. Cancer Res 2005;65:9388-97. (Pubitemid 41508007)
14. Jaffrézou JP, Chen G, Durán GE, Kühl JS, Sikic BI. Mutation rates and mechanisms of resistance to etoposide determined from fluctuation analysis. J Natl Cancer Inst 1994;86:1152-8. (Pubitemid 24249301)
15. Huff LM, Lee JS, Robey RW, Fojo T. Characterization of gene rearrangements leading to activation of MDR-1. J Biol Chem 2006;281:36501-9. (Pubitemid 46042117)
16. Mickley LA, Lee JS, Weng Z, Zhan Z, Alvarez M, Wilson W, et al. Genetic polymorphism in MDR-1: a tool for examining allelic expression in normal cells, unselected and drug-selected cell lines, and human tumors. Blood 1998;91:1749-56. (Pubitemid 28110341)
17. Chin KV, Ueda K, Pastan I, Gottesman MM. Modulation of activity of the promoter of the human MDR1 gene by Ras and p53. Science 1992;255:459-62.
18. Cornwell MM, Smith DE. A signal transduction pathway for activation of the mdr1 promoter involves the proto-oncogene c-raf kinase. J Biol Chem 1993;268:15347-50. (Pubitemid 23222019)
19. Yang JM, Vassil AD, Hait WN. Activation of phospholipase C induces the expression of the multidrug resistance (MDR1) gene through the Raf-MAPK pathway. Mol Pharmacol 2001;60:674-80. (Pubitemid 32900248)
20. Thottassery JV, Zambetti GP, Arimori K, Schuetz EG, Schuetz JD. p53-dependent regulation of MDR1 gene expression causes selective resistance to chemotherapeutic agents. Proc Natl Acad Sci U S A 1997;94:11037-42. (Pubitemid 27430856)
21. Sampath J, Sun D, Kidd VJ, Grenet J, Gandhi A, Shapiro LH, et al. Mutant p53 cooperates with ETS and selectively up-regulates human MDR1 not MRP1. J Biol Chem 2001;276:39359-67.
22. Johnson RA, Ince TA, Scotto KW. Transcriptional repression by p53 through direct binding to a novel DNA element. J Biol Chem 2001;276:27716-20.
23. Michaelis M, Rothweiler F, Klassert D, von Deimling A, Weber K, Fehse B, et al. Reversal of P-glycoprotein-mediated multidrug resistance by the murine double minute 2 antagonist nutlin-3. Cancer Res 2009;69:416-21.
24. Desiderato L, Davey MW, Piper AA. Demethylation of the human MDR1 5′ region accompanies activation of P-glycoprotein expression in a HL60 multidrug resistant subline. Somat Cell Mol Genet 1997;23:391-400. (Pubitemid 127726627)
25. Kantharidis P, El-Osta A, deSilva M, Wall DM, Hu XF, Slater A, et al. Altered methylation of the human MDR1 promoter is associated with acquired multidrug resistance. Clin Cancer Res 1997;3:2025-32. (Pubitemid 27505129)
26. Nakayama M, Wada M, Harada T, Nagayama J, Kusaba H, Ohshima K, et al. Hypomethylation status of CpG sites at the promoter region and overexpression of the human MDR1 gene in acute myeloid leukemias. Blood 1998;92:4296-307. (Pubitemid 28544347)
27. Garcia-Manero G, Bueso-Ramos C, Daniel J, Williamson J, Kantarjian HM, Issa JP. DNA methylation patterns at relapse in adult acute lymphocytic leukemia. Clin Cancer Res 2002;8:1897-903. (Pubitemid 34633752)
28. Tada Y, Wada M, Kuroiwa K, Kinugawa N, Harada T, Nagayama J, et al. MDR1 gene overexpression and altered degree of methylation at the promoter region in bladder cancer during chemotherapeutic treatment. Clin Cancer Res 2000;6:4618-27. (Pubitemid 32110396)
29. Jin S, Scotto KW. Transcriptional regulation of the MDR1 gene by histone acetyltransferase and deacetylase is mediated by NF-Y. Mol Cell Biol 1998;18:4377-84. (Pubitemid 28287960)
30. Baker EK, Johnstone RW, Zalcberg JR, El-Osta A. Epigenetic changes to the MDR1 locus in response to chemotherapeutic drugs. Oncogene 2005;24:8061-75. (Pubitemid 41746749)
31. To KK, Polgar O, Huff LM, Morisaki K, Bates SE. Histone modifications at the ABCG2 promoter following treatment with histone deacetylase inhibitor mirror those in multidrug-resistant cells. Mol Cancer Res 2008;6:151-64. (Pubitemid 351378175)
32. Chen GK, Sale S, Tan T, Ermoian RP, Sikic BI. CCAAT/enhancer-binding protein beta (nuclear factor for interleukin 6) transactivates the human MDR1 gene by interaction with an inverted CCAAT box in human cancer cells. Mol Pharmacol 2004;65:906-16. (Pubitemid 38420496)
33. Combates NJ, Rzepka RW, Chen YN, Cohen D. NF-IL6, a member of the C/EBP family of transcription factors, binds and trans-activates the human MDR1 gene promoter. J Biol Chem 1994;269:29715-9. (Pubitemid 24365130)
34. Kowenz-Leutz E, Leutz A. A C/EBP beta isoform recruits the SWI/SNF complex to activate myeloid genes. Mol Cell 1999;4:735-43.
35. Harikrishnan KN, Chow MZ, Baker EK, Pal S, Bassal S, Brasacchio D, et al. Brahma links the SWI/SNF chromatin-remodeling complex with MeCP2-dependent transcriptional silencing. Nat Genet 2005;37:254-64. (Pubitemid 41716252)
36. Conze D, Weiss L, Regen PS, Bhushan A, Weaver D, Johnson P, et al. Autocrine production of interleukin 6 causes multidrug resistance in breast cancer cells. Cancer Res 2001;61:8851-8. (Pubitemid 34013900)
37. David GL, Yegnasubramanian S, Kumar A, Marchi VL, De Marzo AM, Lin X, et al. MDR1 promoter hypermethylation in MCF-7 human breast cancer cells: changes in chromatin structure induced by treatment with 5-Aza-cytidine. Cancer Biol Ther 2004;3:540-8. (Pubitemid 41351125)
38. El-Osta A, Kantharidis P, Zalcberg JR, Wolffe AP. Precipitous release of methyl-CpG binding protein 2 and histone deacetylase 1 from the methylated human multidrug resistance gene (MDR1) on activation. Mol Cell Biol 2002;22:1844-57. (Pubitemid 34175000)
39. Hassan AH, Prochasson P, Neely KE, Galasinski SC, Chandy M, Carrozza MJ, et al. Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell 2002;111:369-79. (Pubitemid 35345152)
40. Oda Y, Sakamoto A, Shinohara N, Ohga T, Uchiumi T, Kohno K, et al. Nuclear expression of YB-1 protein correlates with P-glycoprotein expression in human osteosarcoma. Clin Cancer Res 1998;4:2273-7. (Pubitemid 28415677)
41. Bargou RC, Jürchott K, Wagener C, Bergmann S, Metzner S, Bommert K, et al. Nuclear localization and increased levels of transcription factor YB-1 in primary human breast cancers are associated with intrinsic MDR1 gene expression. Nat Med 1997;3:447-50. (Pubitemid 27145688)
42. Yahanda AM, Alder KM, Fisher GA, Brophy NA, Halsey J, Hardy RI, et al. Phase I trial of etoposide with cyclosporine as a modulator of multidrug resistance. J Clin Oncol 1992;10:1624-34. (Pubitemid 23057993)
43. Lum BL, Kaubisch S, Yahanda AM, Adler KM, Jew L, Ehsan MN, et al. Alteration of etoposide pharmacokinetics and pharmacodynamics by cyclosporine in a phase I trial to modulate multidrug resistance. J Clin Oncol 1992;10:1635-42. (Pubitemid 23057994)
44. Bartlett NL, Lum BL, Fisher GA, Brophy NA, Ehsan MN, Halsey J, et al. Phase I trial of doxorubicin with cyclosporine as a modulator of multidrug resistance. J Clin Oncol 1994;12:835-42. (Pubitemid 24110926)
45. Advani R, Fisher GA, Lum BL, Hausdorff J, Halsey J, Litchman M, et al. A phase I trial of doxorubicin, paclitaxel, and valspodar (PSC 833), a modulator of multidrug resistance. Clin Cancer Res 2001;7:1221-9. (Pubitemid 32708673)
46. Advani R, Lum BL, Fisher GA, Halsey J, Chin DL, Jacobs CD, et al. A phase I trial of liposomal doxorubicin, paclitaxel and valspodar (PSC-833), an inhibitor of multidrug resistance. Ann Oncol 2005;16:1968-73. (Pubitemid 41724288)
47. Baer MR, George SL, Dodge RK, O'Loughlin KL, Minderman H, Caligiuri MA, 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. (Pubitemid 34864276)
48. List AF, Kopecky KJ, Willman CL, Head DR, Persons DL, Slovak ML, et al. Benefit of cyclosporine modulation of drug resistance in patients with poor-risk acute myeloid leukemia: a Southwest Oncology Group study. Blood 2001;98:3212-20.
49. Liu Yin JA, Wheatley K, Rees JK, Burnett AKUK MRC Adult Leukemia Working Party. Comparison of 'sequential' versus 'standard' chemotherapy as re-induction treatment, with or without cyclosporine, in refractory/relapsed acute myeloid leukaemia (AML): results of the UK Medical Research Council AML-R trial. Br J Haematol 2001;113:713-26. (Pubitemid 32524396)
50. Cripe LD, Uno H, Paietta EM, Litzow MR, Ketterling RP, Bennett JM, 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.
51. Lancet JE, Baer MR, Duran GE, List AF, Fielding R, Marcelletti JF, et al. A phase I trial of continuous infusion of the multidrug resistance inhibitor zosuquidar with daunorubicin and cytarabine in acute myeloid leukemia. Leuk Res 2009;33:1055-61.
52. Marcelletti JF, Multani PS, Lancet JE, Baer MR, Sikic BI. Leukemic blast and natural killer cell P-glycoprotein function and inhibition in a clinical trial of zosuquidar infusion in acute myeloid leukemia. Leuk Res 2009;33:769-74.
53. Qadir M, O'Loughlin KL, Fricke SM, Williamson NA, Greco WR, Minderman H, et al. Cyclosporin Ais a broad-spectrum multidrug resistance modulator. Clin Cancer Res 2005;11:2320-6. (Pubitemid 40490193)
54. van Der Kolk DM, Vellenga E, van Der Veen AY, Noordhoek L, Timmer-Bosscha H, Ossenkoppele GJ, et al. Deletion of the multidrug resistance protein MRP1 gene in acute myeloid leukemia: the impact on MRP activity. Blood 2000;95:3514-9. (Pubitemid 30428485)
55. van der Kolk DM, de Vries EG, Noordhoek L, van den Berg E, van der Pol MA, Müller M, et al. Activity and expression of the multidrug resistance proteins P-glycoprotein, MRP1, MRP2, MRP3 and MRP5 in de novo and relapsed acute myeloid leukemia. Leukemia 2001;15:1544-53. (Pubitemid 32994673)
56. van den Heuvel-Eibrink MM, Wiemer EA, Prins A, Meijerink JP, Vossebeld PJ, van der Holt B, et al. Increased expression of the breast cancer resistance protein (BCRP) in relapsed or refractory acute myeloid leukemia (AML). Leukemia 2002;16:833-9. (Pubitemid 34537555)
57. van der Kolk DM, Vellenga E, Scheffer GL, Müller M, Bates SE, Scheper RJ, et al. Expression and activity of breast cancer resistance protein (BCRP) in de novo and relapsed acute myeloid leukemia. Blood 2002;99:3763-70. (Pubitemid 34534549)
58. Raaijmakers MH, de Grouw EP, van der Reijden BA, de Witte TJ, Jansen JH, Raymakers RA. ABCB1 modulation does not circumvent drug extrusion from primitive leukemic progenitor cells and may preferentially target residual normal cells in acute myelogenous leukemia. Clin Cancer Res 2006;12:3452-8.
59. Sikic BI. Multidrug resistance and stem cells in acutemyeloid leukemia. Clin Cancer Res 2006;12:3231-2.
60. Calcagno AM, Fostel JM, To KK, Salcido CD, Martin SE, Chewning KJ, et al. Single-step doxorubicin-selected cancer cells overexpress the ABCG2 drug transporter through epigenetic changes. Br J Cancer 2008;98:1515-24. (Pubitemid 351652329)
61. Robey RW, Zhan Z, Piekarz RL, Kayastha GL, Fojo T, Bates SE. Increased MDR1 expression in normal and malignant peripheral blood mononuclear cells obtained from patients receiving depsipeptide (FR901228, FK228, NSC630176). Clin Cancer Res 2006;12:1547-55.
62. Tabe Y, Konopleva M, Contractor R, Munsell M, Schober WD, Jin L, et al. Up-regulation of MDR1 and induction of doxorubicin resistance by histone deacetylase inhibitor depsipeptide (FK228) and ATRA in acute promyelocytic leukemia cells. Blood 2006;107:1546-54. (Pubitemid 43242393)
63. Matsubara H, Watanabe M, Imai T, Yui Y, Mizushima Y, Hiraumi Y, et al. Involvement of extracellular signal-regulated kinase activation in human osteosarcoma cell resistance to the histone deacetylase inhibitor FK228 [(1S,4S,7Z,10S,16E,21R)-7-ethylidene-4,21-bis(propan-2-yl)-2-oxa-12,13-dithia-5, 8,20,23-tetraazabicyclo[8.7.6]tricos-16-ene-3,6,9,19,22-pentone]. J Pharmacol Exp Ther 2009;328:839-48.
64. Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V, et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007;445:656-60. (Pubitemid 46232886)
65. Ventura A, Kirsch DG, McLaughlin ME, Tuveson DA, Grimm J, Lintault L, et al. Restoration of p53 function leads to tumour regression in vivo. Nature 2007;445:661-5. (Pubitemid 46232887)
66. Tang Y, Zhao W, Chen Y, Zhao Y, Gu W. Acetylation is indispensable for p53 activation. Cell 2008;133:612-26. (Pubitemid 351636297)
67. Gryshchenko I, Hofbauer S, Stoecher M, Daniel PT, Steurer M, Gaiger A, et al. MDM2 SNP309 is associated with poor outcome in B-cell chronic lymphocytic leukemia. J Clin Oncol 2008;26:2252-7.
68. Heist RS, Zhou W, Chirieac LR, Cogan-Drew T, Liu G, Su L, et al.MDM2 polymorphism, survival, and histology in early-stage non-small-cell lung cancer. J Clin Oncol 2007;25:2243-7. (Pubitemid 46954650)