Human multidrug resistance associated protein 4 confers resistance to camptothecins

Pharmaceutical Research

Volumn 22, Issue 11, 2005, Pages 1837-1853

  Tian, Quan ^a   Zhang, Jing ^a   Tan, Theresa May Chin ^b   Chan, Eli ^a   Duan, Wei ^b   Sui, Yung Chan ^a   Boelsterli, Urs Alex ^a,b   Ho, Paul Chi Lui ^a   Yang, Hongyuan ^b   Bian, Jin Song ^b   Huang, Min ^c   Zhu, Yi Zhun ^b   Xiong, Weiping ^d   Li, Xiaotian ^e   Zhou, Shufeng ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c SUN YAT SEN UNIVERSITY   (China)

^d GUANGDONG PROVINCIAL PEOPLE'S HOSPITAL   (China)

^e FUDAN UNIVERSITY   (China)

Author keywords

Camptothecin; Cyclophosphamide; Drug transporter; Multidrug resistance

Indexed keywords

10 HYDROXYCAMPTOTHECIN; 3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; 7 ETHYL 10 HYDROXYCAMPTOTHECIN; ADEFOVIR DIPIVOXIL; BUTHIONINE SULFOXIMINE; CAMPTOTHECIN DERIVATIVE; CARBOPLATIN; CARBOXYLIC ACID DERIVATIVE; CELECOXIB; CYCLOPHOSPHAMIDE; CYCLOSPORIN; DICLOFENAC; ETOPOSIDE; FLUOROURACIL; GLUTAMATE CYSTEINE LIGASE; GLYCOPROTEIN P; IRINOTECAN; LACTONE DERIVATIVE; METHOTREXATE; MULTIDRUG RESISTANCE PROTEIN 4; NORCANTHARIDIN; PACLITAXEL; RUBITECAN; VERLUKAST; VINBLASTINE; VINCRISTINE;

ARTICLE; CELL STRAIN HEPG2; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG EFFECT; GENETIC TRANSFECTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADENINE; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CAMPTOTHECIN; CELL LINE; DRUG RESISTANCE, NEOPLASM; GLUTATHIONE; HUMANS; METHOTREXATE; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PACLITAXEL; PHOSPHONIC ACIDS;

EID: 27144541444     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-005-7595-z     Document Type: Article

References (86)

1. J. Wang 1996 DNA topoisomerases Annu. Rev. Biochem. 65 635 692
2. K. R. Hande 2003 Topoisomerase II inhibitors Cancer Chemother. Biol. Response Modif. 21 103 125
3. J. F. Pizzolato L. B. Saltz 2003 The camptothecins Lancet 361 2235 2242
4. M. R. Redinbo L. Stewart P. Kuhn J. J. Champoux W. G. Hol 1998 Crystal structures of human topoisomerase I in covalent andnoncovalent complexes with DNA Science 279 1504 1513
5. L. Stewart M. R. Redinbo X. Qiu W. G. Hol J. J. Champoux 1998 A model for the mechanism of human topoisomerase I Science 279 1534 1541
6. L. L. Jung W. C. Zamboni 2001 Cellular, pharmacokinetic, and pharmacodynamic aspects of response to camptothecins: can we improve it Drug Resist. Updat. 4 273 288
7. F. Goldwasser T. Shimizu J. Jackman Y. Hoki P. M. O'Connor K. W. Kohn Y. Pommier 1996 Correlations between S and G2 arrest and the cytotoxicity of camptothecin in human colon carcinoma cells Cancer Res.. 56 4430 4437
8. M. Wall M. C. Wani C. E. Cook K. H. Palmer A. T. Mcphail G. A. Sim 1966 Plant antitumor agents: 1, the isolation and structure of camptothecin, a novel alkaloidal leukemia and tumor inhibitor from Camptotheca acuminata J. Am. Chem. Soc. 88 3888 3890
9. J. Fassberg V. J. Stella 1992 A kinetic and mechanistic study of the hydrolysis of camptothecin and some analogues J. Pharm. Sci. 81 676 684
10. B. A. Chabner 1992 Camptothecins J. Clin. Oncol. 10 3 4
11. W. J. Slichenmyer E. K. Rowinsky R. C. Donehower S. H. Kaufmann 1993 The current status of camptothecin analogues as antitumor agents J. Natl. Cancer Inst. 85 271 291
12. R. P. Hertzberg R. W. Busby M. J. Caranfa K. G. Holden R. K. Johnson S. M. Hecht W. D. Kingsbury 1990 Irreversible trapping of the DNA-topoisomerase I covalent complex. Affinity labelling of the camptothesin binding site J. Biol. Chem. 265 19287 19295
13. M. L. Rothenberg J. R. Eckardt J. G. Kuhn H. A. Burris III J. Nelson S. G. Hilsenbeck G. I. Rodriguez A. M. Thurman L. S. Smith S. G. Eckhardt G. R. Weiss G. L. Elfring D. A. Rinaldi L. J. Schaaf D. D. Von Hoff 1996 Phase II trial of irinotecan in patients with progressive or rapidly recurrent colorectal cancer J. Clin. Oncol. 14 1128 1135
14. W. ten Bokkel Huinink M. Gore J. Carmichael A. Gordon J. Malfetano I. Hudson C. Broom C. Scarabelli N. Davidson M. Spanczynski G. Bolis H. Malmstrom R. Coleman C. Fields J. F. Heron 1997 Topotecan versus paclitaxel for the treatment of recurrent epithelial ovarian cancer J. Clin. Oncol. 15 2183 2193
15. M. Ciotti N. Basu M. Brangi I. S. Owens 1999 Glucuronidation of 7-ethyl-10-hydroxycamptothecin (SN-38) by the human UDP-glucuronosyltransferases encoded at the UGT1 locus Biochem. Biophys. Res. Commun. 260 199 202
16. Y. Kawato M. Aonuma Y. Hirota H. Kuga K. Sato 1991 Intracellular roles of SN-38, a metabolite of the camptothecin derivative CPT-11, in the antitumor effect of CPT-11 Cancer Res. 51 4187 4191
17. R. H. J. Mathijssen R. J. van Alphen J. Verweij W. J. Loos K. Nooter G. Stoter A. Sparreboom 2001 Clinical pharmacokinetics and metabolism of irinotecan (CPT-11) Clin. Cancer Res. 7 2182 2194
18. J. A. Ellerhorst A. Y. Bedikian T. M. Smith N. E. Papadopoulos C. Plager O. Eton 2002 Phase II trial of 9-nitrocamptothecin (RFS 2000) for patients with metastatic cutaneous or uveal melanoma Anticancer Drugs 13 169 172
19. H. A. Burris III S. Rivkin R. Reynolds J. Harris A. Wax H. Gerstein K. L. Mettinger A. Staddon 2005 Phase II trial of oral rubitecan in previously treated pancreatic cancer patients Oncologist 10 183 190
20. Z. A. Rasheed E. H. Rubin 2003 Mechanisms of resistance to topoisomerase I-targeting drugs Oncogene 22 7296 7304
21. E. Gupta R. Mick J. Ramirez X. Wang T. M. Lestingi E. E. Vokes M. J. Ratain 1997 Pharmacokinetic and pharmacodynamic evaluation of the topoisomerase inhibitor irinotecan in cancer patients J. Clin. Oncol. 15 1502 1510
22. S. Kudoh Y. Fujiwara Y. Takada H. Yamamoto A. Kinoshita Y. Ariyoshi K. Furuse M. Fukuoka 1998 Phase II study of irinotecan combined with cisplatin in patients with previously untreated small-cell lung cancer. West Japan Lung Cancer Group J. Clin. Oncol. 16 1068 1074
23. F. R. Luo P. V. Paranjpe A. Guo E. Rubin P. Sinko 2002 Intestinal transport of irinotecan in Caco-2 cells and MDCK II cells overexpressing efflux transporters Pgp, cMOAT, and MRP1 Drug Metab. Dispos. 30 763 770
24. X. Y. Chu Y. Kato Y. Sugiyama 1997 Multiplicity of biliary excretion mechanisms for irinotecan, CPT-11, and its metabolites in rats Cancer Res. 57 1934 1938
25. X. Y. Chu Y. Kato K. Ueda H. Susuki K. Niinuma C. A. Tyson V. Weizer J. E. Dabbs R. Froehlich C. E. Green Y. Sugiyama 1998 Biliary excretion mechanism of CPT-11 and its metabolites in humans: involvement of primary active transporters Cancer Res. 58 5137 5143
26. E. Gupta A. R. Safa X. Wang M. J. Ratain 1996 Pharmacokinetic modulation of irinotecan and metabolites by cyclosporin A Cancer Res. 56 1309 1314
27. X. Y. Chu Y. Kato Y. Sugiyama 1999 Possible involvement of P-glycoprotein in biliary excretion of CPT-11 in rats Drug Metab. Dispos. 27 440 441
28. M. D. Norris J. Smith K. Tanabe P. Tobin C. Flemming G. L. Scheffer P. Wielinga S. L. Cohn W. B. London G. M. Marshall J. D. Allen M. Haber 2005 Expression of multidrug transporter MRP4/ABCC4 is a marker of poor prognosis in neuroblastoma and confers resistance to irinotecan in vitro Mol. Cancer Ther. 4 547 553
29. C. J. Yang J. K. Horton K. H. Cowan E. Schneider 1995 Cross-resistance to camptothecin analogues in a mitoxantrone-resistant human breast carcinoma cell line is not due to DNA topoisomerase I alterations Cancer Res. 55 4004 4009
30. R. Rajendra M. K. Gounder A. Saleem J. H. Schellens D. D. Ross S. E. Bates P. Sinko E. H. Rubin 2003 Differential effects of the breast cancer resistance protein on the cellular accumulation and cytotoxicity of 9-aminocamptothecin and 9-nitrocamptothecin Cancer Res. 63 3228 3233
31. T. Nozawa H. Minami S. Sugiura A. Tsuji I. Tamai 2005 Role of organic anion transporter OATP1B1 (OATP-C) in hepatic uptake of irinotecan and its active metabolite, 7-ethyl-10-hydroxycamptothecin: in vitro evidence and effect of single nucleotide polymorphisms Drug Metab. Dispos. 33 434 439
32. P. Borst R. O. Elferink 2002 Mammalian ABC transporters in health and disease Annu. Rev. Biochem. 71 537 592
33. Q. Tian J. Zhang E. Chan W. Duan S. F. Zhou 2005 Multidrug resistance proteins (MRPs) and implication in drug development Drug Dev. Res. 51 1 18
34. M. Kool M. van der Linden M. de Haas G. L. Scheffer J. M. de Vree A. J. Smith G. Jansen G. J. Peters N. Ponne R. J. Scheper R. P. Elferink F. Baas P. Borst 1999 MRP3, an organic anion transporter able to transport anti-cancer drugs Proc. Natl. Acad. Sci. USA 96 6914 6919
35. H. Zeng L. J. Bain M. G. Belinsky G. D. Kruh 1999 Expression of multidrug resistance protein-3 (multispecific organic anion transporter-D) in human embryonic kidney 293 cells confers resistance to anticancer agents Cancer Res. 59 5964 5967
36. J. D. Allen A. H. Schinkel 2002 Multidrug resistance and pharmacological protection mediated by the breast cancer resistance protein (BCRP/ABCG2) Mol. Cancer Ther. 1 427 434
37. P. K. Smitherman J. ldridge E. L. Volk E. Schneider A. J. Townsend C. S. Morrow 2001 Resistance to mitoxantrone in multidrug-resistant MCF7 breast cancer cells: evaluation of mitoxantrone transport and the role of multidrug resistance protein family proteins Cancer Res. 61 5461 5467
38. L. Lai T. M. Tan 2002 Role of glutathione in the multidrug resistance protein 4 (MRP4/ABCC4)-mediated efflux of cAMP and resistance to purine analogues Biochem. J. 361 497 503
39. M. Leggas M. Adachi G. L. Scheffer D. Sun P. Wielinga G. Du K. E. Mercer Y. Zhuang J. C. Panetta B. Johnston R. J. Scheper C. F. Stewart J. D. Schuetz 2004 Mrp4 confers resistance to topotecan and protects the brain from chemotherapy Mol. Cell. Biol. 24 7612 7621
40. G. Lee M. Piquette-Miller 2001 Influence of IL-6 on MDR and MRP-mediated multidrug resistance in human hepatoma cells Can. J. Physiol. Pharmacol. 79 876 884
41. G. Lee M. Piquette-Miller 2003 Cytokines alter the expression and activity of the multidrug resistance transporters in human hepatoma cell lines; analysis using RT-PCR and cDNA microarrays J. Pharm. Sci. 92 2152 2163
42. T. R. Jones R. Zamboni M. Belley E. Champion L. Charette A. W. Ford-Hutchinson R. Frenette J. Y. Gauthier S. Leger P. Masson C. S. McFarlane H. Piechuta J. Rokach H. Williams R. N. Young N. de Haven S. S. Pong 1989 Pharmacology of L-660,711 (MK-571): a novel potent and selective leukotriene D4 receptor antagonist Can. J. Physiol. Pharmacol. 67 17 28
43. J. Bai L. Lai H. C. Yeo B. C. Goh T. M. Tan 2004 Multidrug resistance protein 4 (MRP4/ABCC4) mediates efflux of bimane-glutathione Int. J. Biochem. Cell Biol. 36 247 257
44. J. Carmichael W. G. DeGraff A. F. Gazdar J. D. Minna J. B. Mitchell 1987 Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing Cancer Res. 47 936 942
45. S. Zhou X. Feng P. Kestell J. W. Paxton B. C. Baguley E. Chan 2005 Transport of the investigational anti-cancer drug 5, 6-dimethylxanthenone-4- acetic acid and its acyl glucuronide by human intestinal Caco-2 cells Eur J. Pharm. Sci. 24 513 524
46. M. T. Huizing H. Rosing F. Koopman A. C. Keung H. M. Pinedo J. H. Beijnen 1995 High-performance liquid chromatographic procedures for the quantitative determination of paclitaxel (Taxol) in human urine J. Chromatogr. B Biomed. Appl. 664 373 382
47. K. Lee A. J. Klein-Szanto G. D. Kruh 2000 Analysis of the MRP4 drug resistance profile in transfected NIH3T3 cells J. Natl. Cancer Inst. 92 1934 1940
48. S. Dallas L. Schlichter R. Bendayan 2004 MRP4- and MRP5-mediated efflux of 9-(2-phosphonylmethoxyethyl)adenine (PMEA) by microglia J. Pharmacol. Exp. Ther. 309 1221 1229
49. R. Evers M. de Haas R. Sparidans J. Beijnen P. R. Wielinga J. Lankelma P. Borst 2000 Vinblastine and sulfinpyrazone export by the multidrug resistance protein MRP2 is associated with glutathione export Br. J. Cancer 83 375 383
50. C. C. Paulusma M. A. van Geer R. Evers M. Heijn R. Ottenhoff P. Borst R. P. Oude Elferink 1999 Canalicular multispecific organic anion transporter/multidrug resistance protein 2 mediates low-affinity transport of reduced glutathione Biochem. J. 338 Pt2 393 401
51. L. S. Gan M. A. Moseley B. Khosla P. F. Augustijns T. P. Bradshaw R. W. Hendren D. R. Thakker 1996 CYP3A-like cytochrome P450-mediated metabolism and polarized efflux of cyclosporin A in Caco-2 cells Drug Metab. Dispos. 24 344 349
52. P. F. Augustijns T. P. Bradshaw L. S. Gan R. W. Hendren D. R. Thakker 1993 Evidence for a polarized efflux system in Caco-2 cells capable of modulating cyclosporin A transport Biochem. Biophys. Res. Commun. 197 360 365
53. U. K. Walle T. Walle 1998 Taxol transport by human intestinal epithelial Caco-2 cells Drug Metab. Dispos. 26 343 346
54. A. Sparreboom J. van Asperen U. Mayer A. H. Schinkel J. W. Smit D. K. Meijer P. Borst W. J. Nooijen J. H. Beijnen O. van Tellingen 1997 Limited oral bioavailability and active epithelial excretion of paclitaxel (Taxol) caused by P-glycoprotein in the intestine Proc. Natl. Acad. Sci. USA 94 2031 2035
55. S. Hatse E. De Clercq J. Balzarini 1998 Enhanced 9-(2- phosphonylmethoxyethyl)adenine secretion by a specific, indomethacin-sensitive efflux pump in a mutant 9-(2-phosphonylmethoxyethyl)adenine-resistant human erythroleukemia K562 cell line Mol. Pharmacol. 54 907 917
56. R. V. Srinivas B. L. Robbins M. C. Connelly Y. F. Gong N. Bischofberger A. Fridland 1993 Metabolism and in vitro antiretroviral activities of bis(pivaloyloxymethyl) prodrugs of acyclic nucleoside phosphonates Antimicrob. Agents Chemother. 37 2247 2250
57. B. L. Robbins M. C. Connelly D. R. Marshall R. V. Srinivas A. Fridland 1995 A human T lymphoid cell variant resistant to the acyclic nucleoside phosphonate 9-(2-phosphonylmethoxyethyl)adenine shows a unique combination of a phosphorylation defect and increased efflux of the agent Mol. Pharmacol. 47 391 397
58. J. Wijnholds C. A. Mol L. van Deemter M. de Haas G. L. Scheffer F. Baas J. H. Beijnen R. J. Scheper S. Hatse E. De Clercq J. Balzarini P. Borst 2000 Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleotide analogs Proc. Natl. Acad. Sci. USA 97 7476 7481
59. G. Reid P. Wielinga N. Zelcer M. De Haas L. Van Deemter J. Wijnholds J. Balzarini P. Borst 2003 Characterization of the transport of nucleoside analog drugs by the human multidrug resistance proteins MRP4 and MRP5 Mol. Pharmacol. 63 1094 1103
60. M. A. McAleer M. A. Breen N. L. White N. Matthews 1999 pABC11 (also known as MOAT-C and MRP5), a member of the ABC family of proteins, has anion transporter activity but does not confer multidrug resistance when overexpressed in human embryonic kidney 293 cells J. Biol. Chem. 274 23541 23548
61. Z. S. Chen K. Lee S. Walther R. B. Raftogianis M. Kuwano H. Zeng G. D. Kruh 2002 Analysis of methotrexate and folate transport by multidrug resistance protein 4 (ABCC4): MRP4 is a component of the methotrexate efflux system Cancer Res. 62 3144 3150
62. J. H. Hooijberg H. J. Broxterman M. Kool Y. G. Assaraf G. J. Peters P. Noordhuis R. J. Scheper P. Borst H. M. Pinedo G. Jansen 1999 Antifolate resistance mediated by the multidrug resistance proteins MRP1 and MRP2 Cancer Res. 59 2532 2535
63. I. Chourpa J. M. Millot G. D. Sockalingum J. F. Riou M. Manfait 1998 Kinetics of lactone hydrolysis in antitumor drugs of camptothecin series as studied by fluorescence spectroscopy Biochim. Biophys. Acta 1379 353 366
64. L. P. Rivory E. Chatelut P. Canal A. Mathieu-Boue J. Robert 1994 Kinetics of the in vivo interconversion of the carboxylate and lactone forms of irinotecan (CPT-11) and of its metabolite SN-38 in patients Cancer Res. 54 6330 6333
65. Y. Sasaki H. Hakusui S. Mizuno M. Morita T. Miya K. Eguchi T. Shinkai T. Tamura Y. Ohe N. Saijo 1995 A pharmacokinetic and pharmacodynamic analysis of CPT-11 and its metabolite SN-38 Jpn. J. Cancer Res. 86 101 110
66. K. Kobayashi B. Bouscarel Y. Matsuzaki S. Ceryak S. Kudoh H. Fromm 1999 pH-dependent uptake of irinotecan and its active metabolite, SN-38, by intestinal cells Int. J. Cancer 83 491 496
67. K. Kobayashi B. Bouscarel Y. Matsuzaki S. Ceryak H. Fromm 1998 Uptake mechanism of irinotecan (CPT-11) and its metabolite (SN-38) by hamster intestinal cells Gastroenterology 114 G2578
68. X. Y. Chu H. Suzuki K. Ueda Y. Kato S. Akiyama Y. Sugiyama 1999 Active efflux of CPT-11 and its metabolites in human KB-derived cell lines J. Pharmacol. Exp. Ther. 288 735 741
69. X. Y. Chu Y. Kato K. Niinuma K. I. Sudo H. Hakusui Y. Sugiyama 1997 Multispecific organic anion transporter is responsible for the biliary excretion of the camptothecin derivative irinotecan and its metabolites in rats J. Pharmacol. Exp. Ther. 281 304 314
70. R. Xie R. H. Mathijssen A. Sparreboom J. Verweij M. O. Karlsson 2002 Clinical pharmacokinetics of irinotecan and its metabolites: a population analysis J. Clin. Oncol. 20 3293 3301
71. T. G. Burke Z. Mi 1994 The structural basis of camptothecin interactions with human serum albumin: impact on drug stability J. Med. Chem. 37 40 46
72. N. Kaneda Y. Hosokawa T. Yokokura S. Awazu 1997 Plasma pharmacokinetics of 7-ethyl-10-hydroxycamptothecin (SN-38) after intravenous administration of SN-38 and irinotecan (CPT-11) to rats Biol. Pharm. Bull. 20 992 996
73. M. C. Haaz L. P. Rivory C. Riche J. Robert 1997 The transformation of irinotecan (CPT-11) to its active metabolite SN-38 by human liver microsomes. Differential hydrolysis for the lactone and carboxylate forms Naunyn-Schmiedeberg's Arch. Pharmacol. 356 257 262
74. M. N. Tallman J. K. Ritter P. C. Smith 2005 Differential rates of glucuronidation for 7-ethyl-10-hydroxy-camptothecin (SN-38) lactone and carboxylate in human and rat microsomes and recombinant UGT isoforms Drug Metab. Dispos. 33 977 983
75. P. R. Wielinga I. van der Heijden G. Reid J. H. Beijnen J. Wijnholds P. Borst 2003 Characterization of the MRP4- and MRP5-mediated transport of cyclic nucleotides from intact cells J. Biol. Chem. 278 17664 17671
76. P. Borst R. Evers M. Kool J. Wijnholds 2000 A family of drug transporters: the multidrug resistance-associated proteins J. Natl. Cancer Inst. 92 1295 1302
77. F. Goldwasser I. Bae M. Valenti K. Torres Y. Pommier 1995 Topoisomerase I-related parameters and camptothecin activity in the colon carcinoma cell lines from the National Cancer Institute anticancer screen Cancer Res. 55 2116 2121
78. E. Gupta F. Luo A. Lallo S. Ramanathan V. Vyas E. Rubin P. Sinko 2000 The intestinal absorption of camptothecin, a highly lipophilic drug, across Caco-2 cells is mediated by active transporter(s) Anticancer Res. 20 1013 1016
79. J. Ma M. Maliepaard K. Nooter W. J. Loos H. J. Kolker J. Verweij G. Stoter J. H. Schellens 1998 Reduced cellular accumulation of topotecan: a novel mechanism of resistance in a human ovarian cancer cell line Br. J. Cancer 77 1645 1652
80. A. C. Croce G. Bottiroli R. Supino E. Favini V. Zuco F. Zunino 2004 Subcellular localization of the camptothecin analogues, topotecan and gimatecan Biochem. Pharmacol. 67 1035 1045
81. J. van Ark-Otte M. A. Kedde J. van der Vijgh A. M. Dingemans W. J. Jansen H. M. Pinedo E. Boven G. Giaccone 1998 Determinants of CPT-11 and SN-38 activities in human lung cancer cells Br. J. Cancer 77 2171 2176
82. J. Cummings G. Boyd B. T. Ethell J. S. Macpherson B. Burchell J. F. Smyth D. I. Jodrell 2002 Enhanced clearance of topoisomerase I inhibitors from human colon cancer cells by glucuronidation Biochem. Pharmacol. 63 607 613
83. O. C. Trifan W. F. Durham V. S. Salazar J. Horton B. D. Levine B. S. Zweifel T. W. Davis J. L. Masferrer 2002 Cyclooxygenase-2 inhibition with celecoxib enhances antitumor efficacy and reduces diarrhea side effect of CPT-11 Cancer Res. 62 5778 5784
84. M. Kool M. de Haas G. L. Scheffer R. J. Scheper M. J. van Eijk J. A. Juijn F. Baas P. Borst 1997 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. 57 3537 3547
85. S. Jorajuria N. Dereuddre-Bosquet F. Becher S. Martin F. Porcheray A. Garrigues A. Mabondzo H. Benech J. Grassi S. Orlowski D. Dormont P. Clayette 2004 ATP binding cassette multidrug transporters limit the anti-HIV activity of zidovudine and indinavir in infected human macrophages Antiviral Ther. 9 519 528
86. R. G. Manzano K. A. Wright P. R. Twentyman 1996 Modulation by acrolein and chloroacetaldehyde of multidrug resistance mediated by the multidrug resistance-associated protein (MRP) Clin. Cancer Res. 2 1321 1326