Interactions of cyclin-dependent kinase inhibitors AT-7519, flavopiridol and SNS-032 with ABCB1, ABCG2 and ABCC1 transporters and their potential to overcome multidrug resistance in vitro

Cancer Chemotherapy and Pharmacology

Volumn 76, Issue 1, 2015, Pages 105-116

  Cihalova, Daniela ^a   Staud, Frantisek ^a   Ceckova, Martina ^a  

^a Charles University in Prague Faculty of Pharmacy   (Czech Republic)

Author keywords

ABC transporter; AT 7519; Cyclin dependent kinase inhibitor; Flavopiridol; Multidrug resistance; SNS 032

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; AT 7519; BREAST CANCER RESISTANCE PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR; DAUNORUBICIN; FLAVOPIRIDOL; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 1; N [5 (5 TERT BUTYL 2 OXAZOLYLMETHYLTHIO) 2 THIAZOLYL]ISONIPECOTAMIDE; TOPOTECAN; UNCLASSIFIED DRUG; 4-(2,6-DICHLOROBENZOYLAMINO)-1H-PYRAZOLE-3-CARBOXYLIC ACID PIPERIDIN-4-YLAMIDE; FLAVONOID; N-(5-(((5-(1,1-DIMETHYLETHYL)-2-OXAZOLYL)METHYL)THIO)-2-THIAZOLYL)-4-PIPERIDINECARBOXAMIDE; OXAZOLE DERIVATIVE; PIPERIDINE DERIVATIVE; PROTEIN KINASE INHIBITOR; PYRAZOLE DERIVATIVE; THIAZOLE DERIVATIVE;

ACCUMULATION ASSAY; ANIMAL CELL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; ATPASE ACTIVITY ASSAY; CANCER CELL; CANCER CELL LINE; CANCER RESISTANCE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG INHIBITION; DRUG POTENCY; DRUG PROTEIN BINDING; HEPG2 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; MEMBRANE VESICLE; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SF9 CELL LINE; XTT ASSAY; ANIMAL; DOG; DRUG EFFECTS; DRUG INTERACTION; MDCK CELL LINE; METABOLISM;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CELL PROLIFERATION; DOGS; DRUG INTERACTIONS; DRUG RESISTANCE, MULTIPLE; FLAVONOIDS; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; OXAZOLES; PIPERIDINES; PROTEIN KINASE INHIBITORS; PYRAZOLES; THIAZOLES;

EID: 84934444471     PISSN: 03445704     EISSN: 14320843     Source Type: Journal    
DOI: 10.1007/s00280-015-2772-1     Document Type: Article

References (48)

1. Choi YH, Yu AM (2014) ABC transporters in multidrug resistance and pharmacokinetics, and strategies for drug development. Curr Pharm Des 20:793-807
2. Wu CP, Hsieh CH, Wu YS (2011) The emergence of drug transporter-mediated multidrug resistance to cancer chemotherapy. Mol Pharm 8:1996-2011
3. Shukla S, Wu CP, Ambudkar SV (2008) Development of inhibitors of ATP-binding cassette drug transporters: present status and challenges. Expert Opin Drug Metab Toxicol 4:205-223
4. Shukla S, Ohnuma S, Ambudkar SV (2010) Improving cancer chemotherapy with modulators of ABC drug transporters. Curr Drug Targets 12:621-630
5. Yang AK, Zhou ZW, Wei MQ, Liu JP, Zhou SF (2010) Modulators of multidrug resistance associated proteins in the management of anticancer and antimicrobial drug resistance and the treatment of inflammatory diseases. Curr Top Med Chem 10:1732-1756
6. Coley HM (2010) Overcoming multidrug resistance in cancer: clinical studies of p-glycoprotein inhibitors. Methods Mol Biol 596:341-358
7. Robey RW, Ierano C, Zhan Z, Bates SE (2011) The challenge of exploiting ABCG2 in the clinic. Curr Pharm Biotechnol 12:595-608
8. Kathawala RJ, Gupta P, Ashby CR Jr, Chen ZS (2015) The modulation of ABC transporter-mediated multidrug resistance in cancer: a review of the past decade. Drug Resist Updat 18:1-17
9. Eadie LN, Hughes TP, White DL (2014) Interaction of the efflux transporters ABCB1 and ABCG2 with imatinib, nilotinib, and dasatinib. Clin Pharmacol Ther 95:294-306
10. Anreddy N, Gupta P, Kathawala RJ, Patel A, Wurpel JN, Chen ZS (2014) Tyrosine kinase inhibitors as reversal agents for ABC transporter mediated drug resistance. Molecules 19:13848-13877
11. Lolli G, Johnson LN (2005) CAK-cyclin-dependent activating kinase: a key kinase in cell cycle control and a target for drugs? Cell Cycle 4:572-577
12. Morgan DO (1995) Principles of CDK regulation. Nature 374:131-134
13. Pavletich NP (1999) Mechanisms of cyclin-dependent kinase regulation: structures of Cdks, their cyclin activators, and Cip and INK4 inhibitors. J Mol Biol 287:821-828
14. Malumbres M, Barbacid M (2009) Cell cycle, CDKs and cancer: a changing paradigm. Nat Rev Cancer 9:153-166
15. Canavese M, Santo L, Raje N (2012) Cyclin dependent kinases in cancer: potential for therapeutic intervention. Cancer Biol Ther 13:451-457
16. Cicenas J, Valius M (2011) The CDK inhibitors in cancer research and therapy. J Cancer Res Clin Oncol 137:1409-1418
17. Gallorini M, Cataldi A, di Giacomo V (2012) Cyclin-dependent kinase modulators and cancer therapy. BioDrugs 26:377-391
18. Lin TS, Ruppert AS, Johnson AJ, Fischer B, Heerema NA, Andritsos LA, Blum KA, Flynn JM, Jones JA, Hu W, Moran ME, Mitchell SM, Smith LL, Wagner AJ, Raymond CA, Schaaf LJ, Phelps MA, Villalona-Calero MA, Grever MR, Byrd JC (2009) Phase II study of flavopiridol in relapsed chronic lymphocytic leukemia demonstrating high response rates in genetically high-risk disease. J Clin Oncol 27:6012-6018
19. Bible KC, Peethambaram PP, Oberg AL, Maples W, Groteluschen DL, Boente M, Burton JK, Gomez Dahl LC, Tibodeau JD, Isham CR, Maguire JL, Shridhar V, Kukla AK, Voll KJ, Mauer MJ, Colevas AD, Wright J, Doyle LA, Erlichman C (2012) A phase 2 trial of flavopiridol (Alvocidib) and cisplatin in platin-resistant ovarian and primary peritoneal carcinoma: MC0261. Gynecol Oncol 127:55-62
20. Heath EI, Bible K, Martell RE, Adelman DC, Lorusso PM (2008) A phase 1 study of SNS-032 (formerly BMS-387032), a potent inhibitor of cyclin-dependent kinases 2, 7 and 9 administered as a single oral dose and weekly infusion in patients with metastatic refractory solid tumors. Invest New Drugs 26:59-65
21. Tong WG, Chen R, Plunkett W, Siegel D, Sinha R, Harvey RD, Badros AZ, Popplewell L, Coutre S, Fox JA, Mahadocon K, Chen T, Kegley P, Hoch U, Wierda WG (2010) Phase I and pharmacologic study of SNS-032, a potent and selective Cdk2, 7, and 9 inhibitor, in patients with advanced chronic lymphocytic leukemia and multiple myeloma. J Clin Oncol 28:3015-3022
22. Cihalova D, Hofman J, Ceckova M, Staud F (2013) Purvalanol A, olomoucine II and roscovitine inhibit ABCB1 transporter and synergistically potentiate cytotoxic effects of daunorubicin in vitro. PLoS ONE 8:e83467
23. Cui Y, Konig J, Buchholz JK, Spring H, Leier I, Keppler D (1999) Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells. Mol Pharmacol 55:929-937
24. Sarkadi B, Price EM, Boucher RC, Germann UA, Scarborough GA (1992) Expression of the human multidrug resistance cDNA in insect cells generates a high activity drug-stimulated membrane ATPase. J Biol Chem 267:4854-4858
25. Chou TC (2006) Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 58:621-681
26. Gottesman MM, Fojo T, Bates SE (2002) Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2:48-58
27. Xia CQ, Smith PG (2012) Drug efflux transporters and multidrug resistance in acute leukemia: therapeutic impact and novel approaches to mediation. Mol Pharmacol 82:1008-1021
28. Scripture CD, Figg WD (2006) Drug interactions in cancer therapy. Nat Rev Cancer 6:546-558
29. Hofman J, Ahmadimoghaddam D, Hahnova L, Pavek P, Ceckova M, Staud F (2012) Olomoucine II and purvalanol A inhibit ABCG2 transporter in vitro and in situ and synergistically potentiate cytostatic effect of mitoxantrone. Pharmacol Res 65:312-319
30. Hofman J, Kucera R, Cihalova D, Klimes J, Ceckova M, Staud F (2013) Olomoucine II, but not purvalanol A, is transported by breast cancer resistance protein (ABCG2) and P-glycoprotein (ABCB1). PLoS ONE 8:e75520
31. Zhou L, Schmidt K, Nelson FR, Zelesky V, Troutman MD, Feng B (2009) The effect of breast cancer resistance protein and P-glycoprotein on the brain penetration of flavopiridol, imatinib mesylate (Gleevec), prazosin, and 2-methoxy-3-(4-(2-(5-methyl-2-phenyloxazol-4-yl)ethoxy)phenyl)propanoic acid (PF-407288) in mice. Drug Metab Dispos 37:946-955
32. Xia B, Liu X, Zhou Q, Feng Q, Li Y, Liu W, Liu Z (2013) Disposition of orally administered a promising chemotherapeutic agent flavopiridol in the intestine. Drug Dev Ind Pharm 39:845-853
33. Robey RW, Medina-Perez WY, Nishiyama K, Lahusen T, Miyake K, Litman T, Senderowicz AM, Ross DD, Bates SE (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
34. Nakanishi T, Karp JE, Tan M, Doyle LA, Peters T, Yang W, Wei D, Ross DD (2003) Quantitative analysis of breast cancer resistance protein and cellular resistance to flavopiridol in acute leukemia patients. Clin Cancer Res 9:3320-3328
35. Hooijberg JH, Broxterman HJ, Scheffer GL, Vrasdonk C, Heijn M, de Jong MC, Scheper RJ, Lankelma J, Pinedo HM (1999) Potent interaction of flavopiridol with MRP1. Br J Cancer 81:269-276
36. Kamath AV, Chong S, Chang M, Marathe PH (2005) P-glycoprotein plays a role in the oral absorption of BMS-387032, a potent cyclin-dependent kinase 2 inhibitor, in rats. Cancer Chemother Pharmacol 55:110-116
37. Loschmann N, Michaelis M, Rothweiler F, Zehner R, Cinatl J, Voges Y, Sharifi M, Riecken K, Meyer J, von Deimling A, Fichtner I, Ghafourian T, Westermann F, Cinatl J Jr (2013) Testing of SNS-032 in a panel of human neuroblastoma cell lines with acquired resistance to a broad range of drugs. Transl Oncol 6:685-696
38. Szakacs G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM (2006) Targeting multidrug resistance in cancer. Nat Rev Drug Discov 5:219-234
39. Glavinas H, Mehn D, Jani M, Oosterhuis B, Heredi-Szabo K, Krajcsi P (2008) Utilization of membrane vesicle preparations to study drug-ABC transporter interactions. Expert Opin Drug Metab Toxicol 4:721-732
40. Baumann KH, Kim H, Rinke J, Plaum T, Wagner U, Reinartz S (2013) Effects of alvocidib and carboplatin on ovarian cancer cells in vitro. Exp Oncol 35:168-173
41. Nagaria TS, Williams JL, Leduc C, Squire JA, Greer PA, Sangrar W (2013) Flavopiridol synergizes with sorafenib to induce cytotoxicity and potentiate antitumorigenic activity in EGFR/HER-2 and mutant RAS/RAF breast cancer model systems. Neoplasia 15:939-951
42. Walsby E, Lazenby M, Pepper C, Burnett AK (2011) The cyclin-dependent kinase inhibitor SNS-032 has single agent activity in AML cells and is highly synergistic with cytarabine. Leukemia 25:411-419
43. Karp JE, Garrett-Mayer E, Estey EH, Rudek MA, Smith BD, Greer JM, Drye DM, Mackey K, Dorcy KS, Gore SD, Levis MJ, McDevitt MA, Carraway HE, Pratz KW, Gladstone DE, Showel MM, Othus M, Doyle LA, Wright JJ, Pagel JM (2012) Randomized phase II study of two schedules of flavopiridol given as timed sequential therapy with cytosine arabinoside and mitoxantrone for adults with newly diagnosed, poor-risk acute myelogenous leukemia. Haematologica 97:1736-1742
44. Carrick S, Parker S, Wilcken N, Ghersi D, Marzo M, Simes J (2005) Single agent versus combination chemotherapy for metastatic breast cancer. Cochrane Database Syst Rev CD003372
45. Saxena M, Stephens MA, Pathak H, Rangarajan A (2011) Transcription factors that mediate epithelial-mesenchymal transition lead to multidrug resistance by upregulating ABC transporters. Cell Death Dis 2:e179
46. Hilgendorf C, Ahlin G, Seithel A, Artursson P, Ungell AL, Karlsson J (2007) Expression of thirty-six drug transporter genes in human intestine, liver, kidney, and organotypic cell lines. Drug Metab Dispos 35:1333-1340
47. Rathos MJ, Joshi K, Khanwalkar H, Manohar SM, Joshi KS (2012) Molecular evidence for increased antitumor activity of gemcitabine in combination with a cyclin-dependent kinase inhibitor, P276-00 in pancreatic cancers. J Transl Med 10:161
48. Rosato RR, Almenara JA, Maggio SC, Atadja P, Craig R, Vrana J, Dent P, Grant S (2005) Potentiation of the lethality of the histone deacetylase inhibitor LAQ824 by the cyclin-dependent kinase inhibitor roscovitine in human leukemia cells. Mol Cancer Ther 4:1772-1785