Combined use of anticancer drugs and an inhibitor of multiple drug resistance-associated protein-1 increases sensitivity and decreases survival of glioblastoma multiforme cells in vitro

Neurochemical Research

Volumn 36, Issue 8, 2011, Pages 1397-1406

  Peigñan, Lilia ^a   Garrido, Wallys ^a   Segura, Rodrigo ^b   Melo, Rómulo ^b   Rojas, David ^b   Cárcamo, Juan Guillermo ^a   San Martín, Rody ^a   Quezada, Claudia ^a  

^a UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

^b Neurocritical Care Service   (Chile)

Author keywords

Glioblastoma multiforme; Mrp1; Multiple drugs resistance

Indexed keywords

ANTINEOPLASTIC AGENT; BREAST CANCER RESISTANCE PROTEIN; CARRIER PROTEIN; ETOPOSIDE; GLYCOPROTEIN P; MULTIDRUG RESISTANCE PROTEIN 1; PROBENECID; TEMOZOLOMIDE; VERLUKAST; VINCRISTINE;

ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL SURVIVAL; CELL VIABILITY; CHEMOSENSITIZATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EXPOSURE; DRUG SENSITIVITY; DRUG USE; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR BIOPSY;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; ATP-BINDING CASSETTE TRANSPORTERS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; CHILD; DRUG THERAPY, COMBINATION; ETOPOSIDE; GLIOBLASTOMA; HUMANS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NEOPLASM PROTEINS; P-GLYCOPROTEIN; RNA, SMALL INTERFERING; VINCRISTINE;

EID: 79961206982     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-011-0464-8     Document Type: Article

References (62)

1. FJ Sharom 2008 ABC multidrug transporters: structure, function and role in chemoresistance Pharmacogenomics 9 105 127 18154452 10.2217/14622416.9.1.105 1:CAS:528:DC%2BD1cXhtFOjsg%3D%3D (Pubitemid 351560534)
2. T Ozben 2006 Mechanisms and strategies to overcome multiple drug resistance in cancer FEBS Lett 580 2903 2909 16497299 10.1016/j.febslet.2006.02. 020 1:CAS:528:DC%2BD28XltVKnt7c%3D (Pubitemid 43729172)
3. H Thomas HM Coley 2003 Overcoming multidrug resistance in cancer: an update on the clinical strategy of inhibiting p-glycoprotein Cancer Control 10 159 165 12712010 (Pubitemid 36437822)
4. MM Gottesman T Fojo SE Bates 2002 Multidrug resistance in cancer: role of ATP-dependent transporters Nat Rev Cancer 2 48 58 11902585 10.1038/nrc706 1:CAS:528:DC%2BD38XhvF2jtL8%3D (Pubitemid 37328807)
5. S Awasthi S Singhal J Singhal, et al. 2007 Role of RLIP76 in lung cancer doxorubicin resistance: III. Anti-RLIP76 antibodies trigger apoptosis in lung cancer cells and synergistically increase doxorubicin cytotoxicity Int J Oncol 22 721 732
6. E Steiner K Holzmann L Elbling, et al. 2006 Cellular functions of vaults and their involvement in multidrug resistance Curr Drug Targets 7 923 16918321 10.2174/138945006778019345 1:CAS:528:DC%2BD28XnslClsrc%3D
7. A Paredes JL Blanco M Echenique-Elizondo 2006 Expression of multidrug resistance (MDR) associated proteins in solid tumors Cir Esp 79 202 214 16753100 10.1016/S0009-739X(06)70855-7
8. CH Choi 2005 ABC transporters as multidrug resistance mechanisms and the development of chemosensitizers for their reversal Cancer Cell Int 5 30 16202168 10.1186/1475-2867-5-30 (Pubitemid 41554983)
9. J Ahmedin R Siegel J Xu, et al. 2010 Cancer statistics, 2010 CA Cancer J Clin 65 277 300
10. SM Chang NA Butowski PK Sneed, et al. 2006 Standard treatment and experimental targeted drug therapy for recurrent glioblastoma multiforme Neurosurg Focus 20 E4 16709035
11. R Stupp MJ van den Bent ME Hegi 2005 Optimal role of temozolomide in the treatment of malignant gliomas Curr Neurol Neurosci Rep 5 198 206 15865885 10.1007/s11910-005-0047-7 1:CAS:528:DC%2BD28Xks1Krtw%3D%3D (Pubitemid 40873035)
12. W Loscher H Potschka 2005 Drug resistance in brain diseases and the role of drug efflux transporters Nat Rev Neurosci 6 591 602 16025095 10.1038/nrn1728 (Pubitemid 41059334)
13. H Yuan X Li J Wu, et al. 2008 Strategies to overcome or circumvent P-glycoprotein mediated multidrug resistance Curr Med Chem 15 470 476 18289002 10.2174/092986708785747634 1:CAS:528:DC%2BD1cXnsVyisLY%3D (Pubitemid 351472413)
14. M Hennessy JP Spiers 2007 A primer on the mechanics of P-glycoprotein the multidrug transporter Pharmacol Res 55 1 15 17095241 10.1016/j.phrs.2006.10.007 1:CAS:528:DC%2BD2sXntlequg%3D%3D (Pubitemid 46108588)
15. T Mizutani A Hattori 2005 New horizon of MDR1 (P-glycoprotein) study Drug Metab Rev 37 489 510 16257832 10.1080/03602530500205358 1:CAS:528: DC%2BD2MXhtFyqu7fI (Pubitemid 41434160)
16. KL Mealey 2004 Therapeutic implications of the MDR-1 gene J Vet Pharmacol Ther 27 257 264 15500562 10.1111/j.1365-2885.2004.00607.x 1:CAS:528: DC%2BD2cXhtVKntrfI (Pubitemid 39482230)
17. M Liscovitch Y Lavie 2002 Cancer multidrug resistance: a review of recent drug discovery research IDrugs 5 349 355 15565517 1:CAS:528: DC%2BD38XlvVSitbs%3D (Pubitemid 38133051)
18. B Benyahia S Huguet X Declèves, et al. 2004 Multidrug resistance-associated protein MRP1 expression in human gliomas: chemosensitization to vincristine and etoposide by indomethacin in human glioma cell lines overexpressing MRP1 J Neuro-oncol 66 65 70 10.1023/B:NEON.0000013484. 73208.a4 1:STN:280:DC%2BD2c7isVGmuw%3D%3D (Pubitemid 38258360)
19. C Calatozzolo M Gelati E Ciusani, et al. 2005 Expression of drug resistance proteins Pgp, MRP1, MRP3, MRP5 and GST-pi in human glioma J Neuro-oncol 74 113 121 10.1007/s11060-004-6152-7 1:CAS:528:DC%2BD2MXht12hurvF (Pubitemid 41478906)
20. X Decléves A Amiel JY Delattre, et al. 2006 Role of ABC transporters in the chemoresistance of human gliomas Curr Cancer Drug Targets 6 433 445 16918310 10.2174/156800906777723930 (Pubitemid 44033391)
21. Y Matsumoto K Miyake K Kunishio, et al. 2004 Reduction of expression of the multidrug resistance protein (MRP)1 in glioma cells by antisense phosphorothioate oligonucleotides J Med Invest 51 194 201 15460906 10.2152/jmi.51.194 (Pubitemid 39610914)
22. X Decléves A Fajac J Lehmann-Che, et al. 2002 Molecular and functional MDR1-Pgp and MRPs expression in human glioblastoma multiforme cell lines Int J Cancer 98 173 180 11857404 10.1002/ijc.10135 (Pubitemid 34150798)
23. W Zhang J Mojsilovic-Petrovic MF Andrade, et al. 2003 The expression and functional characterization of ABCG2 in brain endothelial cells and vessels FASEB J 17 2085 2087 12958161
24. CA Quezada WX Garrido MA González-Oyarzún, et al. 2008 Effect of tacrolimus on activity and expression of P-glycoprotein and ATP-binding cassette transporter A5 (ABCA5) proteins in hematoencephalic barrier cells Biol Pharm Bull 31 1911 1916 18827354 10.1248/bpb.31.1911 1:CAS:528:DC%2BD1cXhsVOjtbbP
25. J Echevarria-Lima F Kyle-Cezar DFP Leite, et al. 2005 Expression and activity of multidrug resistance protein 1 in a murine thymoma cell line Immunology 114 468 475 15804283 10.1111/j.1365-2567.2005.02116.x 1:CAS:528:DC%2BD2MXjtFeqtLk%3D (Pubitemid 40478141)
26. CL Hammond R Marchan SM Krance, et al. 2007 Glutathione export during apoptosis requires functional multidrug resistance-associated proteins J Biol Chem 282 14337 14347 17374608 10.1074/jbc.M611019200 1:CAS:528: DC%2BD2sXkvVynsLY%3D (Pubitemid 47100459)
27. AL Dogan O Legrand AM Faussat, et al. 2004 Evaluation and comparison of MRP1 activity with three fluorescent dyes and three modulators in leukemic cell lines Leuk Res 28 619 622 15120939 10.1016/j.leukres.2003.10.015 1:CAS:528:DC%2BD2cXjs1equr0%3D (Pubitemid 38543199)
28. V Gekeler W Ise KH Sanders, et al. 1995 The leukotriene LTD4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance Biochem Biophys Res Commun 208 345 352 7887949 10.1006/bbrc.1995.1344 1:CAS:528:DyaK2MXktFGrsL4%3D
29. T Abe T Mori Y Wakabayashi M Nakagawa, et al. 1998 Expression of multidrug resistance protein gene in patients with glioma after chemotherapy J Neuro-oncol 40 11 18 10.1023/A:1005954406809 1:STN:280:DyaK1M%2FovFGktQ%3D%3D (Pubitemid 28548367)
30. M Bredel J Zentner 2002 Brain-tumour drug resistance: the bare essentials Lancet Oncol 3 397 406 12142169 10.1016/S1470-2045(02)00786-6 1:CAS:528:DC%2BD38Xls1Wisr8%3D (Pubitemid 36958270)
31. M Patel C McCully K Godwin, et al. 2003 Plasma and cerebrospinal fluid pharmacokinetics of intravenous temozolomide in non-human primates J Neuro-oncol 61 203 207 10.1023/A:1022592913323 (Pubitemid 36342297)
32. S Ostermann C Csajka T Buclin, et al. 2004 Plasma and cerebrospinal fluid population pharmacokinetics of temozolomide in malignant glioma patients Clin Cancer Res 10 3728 3736 15173079 10.1158/1078-0432.CCR-03-0807 1:CAS:528:DC%2BD2cXksVKntrw%3D (Pubitemid 38697606)
33. JE Chang HI Robins MP Mehta 2007 Therapeutic advances in the treatment of brain metastases Clin Adv Hematol Oncol 5 54 64 17339829 (Pubitemid 46336328)
34. 6- methylguanine methyltransferase (MGMT) promoter methylation with clinical outcomes in glioblastoma and clinical strategies to modulate MGMT activity J Clin Oncol 26 4189 4199 18757334 10.1200/JCO.2007.11.5964 1:CAS:528: DC%2BD1cXhtFKisb7M
35. G Liu Y Akasaki HT Khong, et al. 2005 Cytotoxic T cell targeting of TRP-2 sensitizes human malignant glioma to chemotherapy Oncogene 24 5226 5234 15897911 10.1038/sj.onc.1208519 1:CAS:528:DC%2BD2MXmvFemsb4%3D (Pubitemid 41192439)
36. ET Valera HR Machado CA Scrideli, et al. 2007 Drug-resistance in central nervous system tumors: from the traditional cell-resistance model to the genetically driven approaches on therapy Curr Pharm Biotechnol 8 105 113 17430159 10.2174/138920107780487500 1:CAS:528:DC%2BD2sXls1ygtLc%3D (Pubitemid 46711702)
37. S Spiegl-Kreinecker J Buchroithner L Elbling, et al. 2002 Expression and functional activity of the ABC-transporter proteins P-glycoprotein and multidrug-resistance protein 1 in human brain tumor cells and astrocytes J Neuro-oncol 57 27 36 10.1023/A:1015735815111 (Pubitemid 34692611)
38. L Chen P Feng S Li, et al. 2009 Effect of hypoxia-inducible factor-1alpha silencing on the sensitivity of human brain glioma cells to doxorubicin and etoposide Neurochem Res 34 984 990 18937067 10.1007/s11064-008-9864-9 1:CAS:528:DC%2BD1cXht1Kms7%2FJ
39. E Ota Y Abe Y Oshika Y Ozeki, et al. 1995 Expression of the multidrug resistance-associated protein (MRP) gene in non-small-cell lung cancer Br J Cancer 72 550 554 7669560 10.1038/bjc.1995.372 1:CAS:528:DyaK2MXotV2kt78%3D
40. W Berger U Setinek P Hollaus, et al. 2005 Multidrug resistance markers P-glycoprotein, multidrug resistance protein 1, and lung resistance protein in non-small cell lung cancer: prognostic implications J Cancer Res Clin Oncol 131 355 363 15856298 10.1007/s00432-004-0653-9 1:CAS:528:DC%2BD2MXjs1OlsLk%3D (Pubitemid 40674620)
41. TC Hsia CC Lin JJ Wang, et al. 2002 Relationship between chemotherapy response of small cell lung cancer and P-glycoprotein or multidrug resistance-related protein expression Lung 180 173 179 12177731 10.1007/s004080000091 1:CAS:528:DC%2BD38XmsFejt7c%3D (Pubitemid 36002494)
42. TH Kuo FY Liu CY Chuang, et al. 2003 To predict response chemotherapy using technetium-99 m tetrofosmin chest images in patients with untreated small cell lung cancer and compare with p-glycoprotein, multidrug resistance related protein-1, and lung resistance-related protein expression Nucl Med Biol 30 627 632 12900288 10.1016/S0969-8051(03)00058-1 1:CAS:528:DC%2BD3sXlvFynsbY%3D (Pubitemid 37289324)
43. J Kartenbeck U Leuschner R Mayer, et al. 1996 Absence of the canalicular isoform of the MRP gene-encoded conjugate export pump from the hepatocytes in Dubin-Johnson syndrome Hepatology 23 1061 1066 8621134 1:STN:280: DyaK283gs1GgsQ%3D%3D
44. K Nooter GB de la Riviere J Klijn, et al. 1997 Multidrug resistance protein in recurrent breast cancer Lancet 349 1885 1886 9217765 10.1016/S0140-6736(05)63876-7 1:STN:280:DyaK2szmtVyjsA%3D%3D (Pubitemid 27270127)
45. M Rudas M Filipits S Taucher, et al. 2003 Expression of MRP1, LRP and Pgp in breast carcinoma patients treated with preoperative chemotherapy Breast Cancer Res Treat 81 149 157 14572157 10.1023/A:1025751631115 1:CAS:528:DC%2BD3sXntlGqt74%3D (Pubitemid 37211132)
46. GF Sullivan PS Amenta JD Villanueva, et al. 1998 The expression of drug resistance gene products during the progression of human prostate cancer Clin Cancer Res 4 1393 1403 9626455 1:CAS:528:DyaK1cXktVWhsLg%3D (Pubitemid 28265221)
47. J Zalcberg XF Hu A Slater, et al. 2000 MRP1 not MDR1 gene expression is the predominant mechanism of acquired multidrug resistance in two prostate carcinoma cell lines Prostate Cancer Prostatic Dis 3 66 75 12497102 10.1038/sj.pcan.4500394 1:CAS:528:DC%2BD3cXmsF2ntbY%3D (Pubitemid 30663591)
48. M Haber J Smith SB Bordow, et al. 2006 Association of high-level MRP1 expression with poor clinical outcome in a large prospective study of primary neuroblastoma J Clin Oncol 24 1546 1553 16575006 10.1200/JCO.2005.01.6196 1:CAS:528:DC%2BD28XjvFyktrc%3D (Pubitemid 46638777)
49. WK Yung RE Albright J Olson, et al. 2000 A phase II study of temozolomide vs. procarbazine in patients with glioblastoma multiforme at first relapse Br J Cancer 83 588 593 10944597 10.1054/bjoc.2000.1316 1:CAS:528: DC%2BD3cXmvVCgsrs%3D (Pubitemid 30636298)
50. M Brada K Hoang-Xuan R Rampling, et al. 2001 Multicenter phase II trial of temozolomide in patients with glioblastoma multiforme at first relapse Ann Oncol 12 259 266 11300335 10.1023/A:1008382516636 1:STN:280: DC%2BD3M3gvFamtg%3D%3D (Pubitemid 32223879)
51. M Brada S Stenning R Gabe, et al. 2010 Temozolomide versus procarbazine, lomustine, and vincristine in recurrent high-grade glioma J Clin Oncol 28 4601 4608 20855843 10.1200/JCO.2009.27.1932 1:CAS:528:DC%2BC3cXhsFaitLzP
52. S Pédeboscq B L'Azou D Liguoro, et al. 2007 Interindividual differences in anticancer drug cytotoxicity in primary human glioblastoma cells Exp Toxicol Pathol 58 247 253 17123803 10.1016/j.etp.2006.08.003 (Pubitemid 44855540)
53. I Akan S Akan H Akca, et al. 2005 Multidrug resistance-associated protein 1 (MRP1) mediated vincristine resistance: effects of N-acetylcysteine and Buthionine sulfoximine Cancer Cell Int 5 22 16042792 10.1186/1475-2867-5-22 (Pubitemid 41460744)
54. DW Loe RG Deeley SP Cole 1998 Characterization of vincristine transport by the M(r) 190, 000 multidrug resistance protein (MRP): evidence for cotransport with reduced glutathione Cancer Res 58 5130 5136 9823323 1:CAS:528:DyaK1cXnsFSmtL8%3D (Pubitemid 28521173)
55. J Styczynski D Olszewska-Slonina B Kolodziej, et al. 2006 Activity of bortezomib in glioblastoma Anticancer Res 26 4499 4503 17201170 1:CAS:528:DC%2BD2sXpslGjug%3D%3D (Pubitemid 46031523)
56. CT Kuan K Wakiya JE Herndon II, et al. 2010 MRP3: a molecular target for human glioblastoma multiforme immunotherapy BMC Cancer 10 468 482 20809959 10.1186/1471-2407-10-468
57. A Bodo E Bakos F Szeri, et al. 2003 Differential modulation of the human liver conjugate transporters MRP2 and MRP3 by bile acids and organic anions J Biol Chem 278 23529 23537 12704183 10.1074/jbc.M303515200 1:CAS:528: DC%2BD3sXkslygtr4%3D (Pubitemid 36830172)
58. SW Lee WJ Kim JA Park, et al. 2006 Blood-brain barrier interfaces and brain tumors Arch Pharm Res 29 265 275 16681030 10.1007/BF02968569 1:CAS:528:DC%2BD28XltF2gtrs%3D (Pubitemid 43685278)
59. BT Hawkins TP Davis 2005 The blood-brain barrier/neurovascular unit in health and disease Pharmacol Rev 57 173 185 15914466 10.1124/pr.57.2.4 1:CAS:528:DC%2BD2MXlsFejtL0%3D (Pubitemid 41043883)
60. F Wang F Zhou GD Kruh, et al. 2010 Influence of blood-brain barrier efflux pumps on the distribution of vincristine in brain and brain tumors Neuro Oncol 12 1043 1049 20501632 10.1093/neuonc/noq056 1:CAS:528:DC%2BC3cXht1WhsL%2FO
61. RW Robey S Shukla EM Finley, et al. 2008 Inhibition of P-glycoprotein (ABCB1)- and multidrug resistance-associated protein 1 (ABCC1)-mediated transport by the orally administered inhibitor, CBT-1(R) Biochem Pharmacol 75 1302 1312 18234154 10.1016/j.bcp.2007.12.001 1:CAS:528:DC%2BD1cXislamtLs%3D
62. RA Peck J Hewett MW Harding, et al. 2001 Phase I and pharmacokinetic study of the novel MDR1 and MRP1 inhibitor biricodar administered alone and in combination with doxorubicin J Clin Oncol 19 3130 3141 11408511 1:CAS:528:DC%2BD3MXltFektLY%3D (Pubitemid 32565452)