3β-Acetyl tormentic acid reverts MRP1/ABCC1 mediated cancer resistance through modulation of intracellular levels of GSH and inhibition of GST activity

European Journal of Pharmacology

Volumn 741, Issue , 2014, Pages 140-149

  Rocha, Gleice Da Graça ^a   Oliveira, Rodrigo Rodrigues ^a   Kaplan, Maria Auxiliadora Coelho ^a   Gattass, Cerli Rocha ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

3 acetyl tormentic acid; Cancer; MRP1 ABCC1 inhibitor; Multidrug resistance reversal; Triterpenes

Indexed keywords

ANTINEOPLASTIC AGENT; ENZYME INHIBITOR; GLUTATHIONE; GLUTATHIONE TRANSFERASE; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE-ASSOCIATED PROTEIN 1; TORMENTIC ACID; TRITERPENE;

ANTAGONISTS AND INHIBITORS; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; DRUG RESISTANCE; HUMAN; INTRACELLULAR FLUID; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; ENZYME INHIBITORS; GLUTATHIONE; GLUTATHIONE TRANSFERASE; HUMANS; INTRACELLULAR FLUID; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; TRITERPENES;

EID: 84906959625     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2014.07.054     Document Type: Article

References (47)

1. T. Asano, A. Tsutsuda-Asano, and Y. Fukunaga Indomethacin overcomes doxorubicin resistance by decreasing intracellular content of glutathione and its conjugates with decreasing expression of gamma-glutamylcysteine synthetase via promoter activity in doxorubicin-resistant leukemia cells Cancer Chemother. Pharmacol. 64 2009 715 721
2. B. Benyahia, S. Huguet, X. Declèves, K. Mokhtari, E. Crinière, J.F. Bernaudin, J.M. Scherrmann, and J.Y. Delattre Multidrug resistance-associated protein MRP1 expression in human gliomas, chemosensitization to vincristine and etoposide by indomethacin in human glioma cell lines overexpressing MRP1 J. Neurooncol. 66 2004 65 70
3. W. Berger, L. Elbling, E. Hauptmann, and M. Micksche Expression of the multidrug resistance-associated protein (MRP) and chemoresistance of human non-small-cell lung cancer cells Int. J. Cancer 73 1997 84 93
4. P.G. Board, and D. Menon Glutathione transferases, regulators of cellular metabolism and physiology Biochim. Biophys. Acta 1830 2013 3267 3288
5. P. Borst, R. Evers, M. Kool, and J. Wijnholds A family of drug transporters: the multidrug resistance-associated proteins J. Nat. Cancer Inst. 92 2000 1295 1302
6. F. Braga, D. Ayres-Saraiva, C.R. Gattass, and M.A. Capella Oleanolic acid inhibits the activity of the multidrug resistance protein ABCC1 (MRP1) but not of the ABCB1 (P-glycoprotein), possible use in cancer chemotherapy Cancer Lett. 248 2007 147 152
7. H.M. Brechbuhl, R. Kachadourian, E. Min, D. Chan, and B.J. Day Chrysin enhances doxorubicin-induced cytotoxicity in human lung epithelial cancer cell lines, the role of glutathione Toxicol. Appl. Pharmacol. 258 2012 1 9
8. Z.J. Chen, H.B. Le, Y.K. Zhang, L.Y. Qian, K.R. Sekhar, and W.D. Li Lung resistance protein and multidrug resistance protein in non-small cell lung cancer and their clinical significance J. Int. Med. Res. 39 2011 1693 1700
9. Z.S. Chen, and A.K. Tiwari Multidrug resistance proteins (MRPs/ABCCs) in cancer chemotherapy and genetic diseases FEBS J. 278 2011 3226 3245
10. S.P. Cole, K.E. Sparks, K. Fraser, D.W. Loe, C.E. Grant, G.M. Wilson, and R.G. Deeley Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells Cancer Res. 54 1994 5902 5910
11. S.P. Cole, and R.G. Deeley Transport of glutathione and glutathione conjugates by MRP1 Trends Pharmacol. Sci. 27 2006 438 446
12. O.M. Colvin, H.S. Friedman, M.P. Gamcsik, C. Fenselau, and J. Hilton Role of glutathione in cellular resistance to alkylating agents Adv. Enzyme Regul. 33 1993 19 26
13. D.J. de Groot, M. van der Deen, T.K. Le, A. Regeling, S. de Jong, and E.G. de Vries Indomethacin induces apoptosis via a MRP1-dependent mechanism in doxorubicin-resistant small-cell lung cancer cells overexpressing MRP1 Br. J. Cancer 97 2007 1077 1083
14. X. Declèves, A. Amiel, J.Y. Delattre, and J.M. Scherrmann Role of ABC transporters in the chemoresistance of human gliomas Curr. Cancer Drug Targets 6 2006 433 445
15. R.G. Deeley, C. Westlake, and S.P. Cole Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins Physiol. Rev. 86 2006 849 899
16. S. Gallego, A. Llort, A. Parareda, and J.S. De Toledo Expression of multidrug resistance-1 and multidrug resistance associated protein genes in pediatric rhabdomyosarcoma Oncol. Rep. 11 2004 179 183
17. W. Garrido, M. Muñoz, R. San Martín, and C. Quezada FK506 confers chemosensitivity to anticancer drugs in glioblastoma multiforme cells by decreasing the expression of the multiple resistance-associated protein-1 Biochem. Biophys. Res. Commun. 411 2011 62 68
18. G. Jedlitschky, I. Leier, U. Buchholz, K. Barnouin, G. Kurz, and D. Keppler Transport of glutathione, glucuronate, and sulfate conjugates by the MRP gene-encoded conjugate export pump Cancer Res. 56 1996 988 994
19. E. Laborde Glutathione transferases as mediators of signaling pathways involved in cell proliferation and cell death Cell Death Differ. 17 2010 1373 1380
20. S.L. Lai, J. Hwang, R.P. Perng, and J. Whang-Peng Modulation of cisplatin resistance in acquired-resistant nonsmall cell lung cancer cells Oncol. Res. 7 1995 31 38
21. C.H. Lee Reversing agents for ATP-binding cassette drug transporters Methods Mol. Biol. 596 2010 325 340
22. E.M. Leslie, R.G. Deeley, and S.P. Cole Bioflavonoid stimulation of glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1) Drug Metab. Dispos. 31 2003 11 15
23. S. Li, Y. Lei, Y. Jia, N. Li, M. Wink, and Y. Ma Piperine, a piperidine alkaloid from Piper nigrum re-sensitizes P-gp, MRP1 and BCRP dependent multidrug resistant cancer cells Phytomedicine 19 2011 83 87
24. D.W. Loe, R.G. Deeley, and S.P. Cole Characterization of vincristine transport by the 190 kDa multidrug resistance protein, MRP, evidence for co-transport with reduced glutathione Cancer Res. 58 1998 5130 5136
25. Q. Mao, R.G. Deeley, and S.P. Cole Functional reconstitution of substrate transport by purified multidrug resistance protein MRP1 (ABCC1) in phospholipid vesicles J. Biol. Chem. 275 2000 34166 34172
26. M. Marra, A. Lombardi, E. Agostinelli, G. Giuberti, S. Zappavigna, G. Tempera, G. Vitale, M. Bifulco, A. Abbruzzese, and M. Caraglia Bovine serum amine oxidase and spm potentiate docetaxel and interferon-α effects in inducing apoptosis on human cancer cells through the generation of oxidative stress Biochim. Biophys. Acta 1783 2008 2269 2278
27. R.R. Oliveira, G.G. Leitão, M.C.C. Moraes, D. Lopes, J.P.P. Carauta, and M.A.C. Kaplan Gradient elution for triterpene separation from Cecropia lyratiloba Miquel by HSCCC J. Liq. Chromatogr. Relat. Technol. 28 2005 1985 1992
28. W. Priebe, M. Krawczyk, M.T. Kuo, Y. Yamane, N. Savaraj, and T. Ishikawa Doxorubicin- and daunorubicin-glutathione conjugates, but not unconjugated drugs, competitively inhibit leukotriene C4 transport mediated by MRP/GS-X Pump1 Biochem. Biophys. Res. Commun. 247 1998 859 863
29. Gda G. Rocha, M. Simões, K.A. Lúcio, R.R. Oliveira, M.A.C. Kaplan, and C.R. Gattass Natural triterpenoids from Cecropia lyratiloba are cytotoxic to both sensitive and multidrug resistant leukemia cell lines Bioorg. Med. Chem. 15 2007 7355 7360
30. Gda G. Rocha, M. Simões, R.R. Oliveira, M.A. Kaplan, and C.R. Gattass 3β-acetyl tormentic acid induces apoptosis of resistant leukemia cells independently of P-gp/ABCB1 activity or expression Invest. New Drugs 30 2012 105 113
31. Gda G. Rocha, M. Simões, R.R. Oliveira, M.A. Kaplan, and C.R. Gattass Effects of 3β-acethyl tormentic acid (3ATA) on ABCC proteins activity Int. J. Mol. Sci. 13 2012 6757 6771
32. A. Rothnie, G. Conseil, A.Y. Lau, R.G. Deeley, and S.P. Cole Mechanistic differences between GSH transport by multidrug resistance protein 1 (MRP1/ABCC1) and GSH modulation of MRP1-mediated transport Mol. Pharmacol. 74 2008 1630 1640
33. A. Sau, F. Pellizzari Tregno, F. Valentino, G. Federici, and A.M. Caccuri Glutathione transferases and development of new principles to overcome drug resistance Arch. Biochem. Biophys. 500 2010 116 122
34. S. Shukla, S. Ohnuma, and S.V. Ambudkar Improving cancer chemotherapy with modulators of ABC drug transporters Curr. Drug Targets 12 2011 621 630
35. B. Stordal, and M. Davey Understanding cisplatin resistance using cellular models IUBMB Life 59 2007 696 699
36. T. Sugiyama, and Y. Sadzuka Theanine and glutamate transporter inhibitors enhance the antitumor efficacy of chemotherapeutic agents Biochim. Biophys. Acta 1653 2003 47 59
37. H. Takemura, Y. Urasaki, A. Yoshida, T. Fukushima, and T. Ueda Simultaneous treatment with 1-beta-d-arabinofuranosylcytosine and daunorubicin induces cross-resistance to both drugs due to a combination-specific mechanism in HL60 cells Cancer Res. 61 2001 172 177
38. A.K. Tiwari, K. Sodani, C.L. Dai, C.R. Ashby Jr., and Z.S. Chen Revisiting the ABCs of multidrug resistance in cancer chemotherapy Curr. Pharm. Biotechnol. 12 2011 570 594
39. D. Trachootham, J. Alexandre, and P. Huang Targeting cancer cells by ROS-mediated mechanisms, a radical therapeutic approach? Nat. Rev. Drug Discov. 8 2009 579 591
40. J.P. van Brussel, M.A. Oomen, P.J. Vossebeld, E.A. Wiemer, P. Sonneveld, and G.H. Mickisch Identification of multidrug resistance-associated protein 1 and glutathione as multidrug resistance mechanisms in human prostate cancer cells: chemosensitization with leukotriene D4 antagonists and buthionine sulfoximine BJU Int. 93 2004 1333 1338
41. W.T. van der Graaf, E.G. de Vries, H. Timmer-Bosscha, G.J. Meersma, G. Mesander, E. Vellenga, and N.H. Mulder Effects of amiodarone, cyclosporin A, and PSC 833 on the cytotoxicity of mitoxantrone, doxorubicin, and vincristine in non-Pglycoprotein human small cell lung cancer cell lines Cancer Res. 54 1994 5368 5373
42. J.J. van Zanden, A. de Mul, H.M. Wortelboer, M. Usta, P.J. van Bladeren, I.M. Rietjens, and N.H. Cnubben Reversal of in vitro cellular MRP1 and MRP2 mediated vincristine resistance by the flavonoid myricetin Biochem. Pharmacol. 69 2005 1657 1665
43. C.P. Wu, C.H. Hsieh, and Y.S. Wu The emergence of drug transporter-mediated multidrug resistance to cancer chemotherapy Mol. Pharm. 8 2011 1996 2011
44. H.W. Xu, L. Xu, J.H. Hao, C.Y. Qin, and H. Liu Expression of P-glycoprotein and multidrug resistance-associated protein is associated with multidrug resistance in gastric cancer J. Int. Med. Res. 38 2010 34 42
45. B.R. You, and W.H. Park Gallic acid-induced lung cancer cell death is related to glutathione depletion as well as reactive oxygen species increase Toxicol. In Vitro 24 2010 1356 1362
46. G.J. Zaman, N.H. Cnubben, P.J. van Bladeren, R. Evers, and P. Borst Transport of the glutathione conjugate of ethacrynic acid by the human multidrug resistance protein MRP FEBS Lett. 391 1996 126 130
47. J.G. Zijlstra, E.G. de Vries, and N.H. Mulder Multifactorial drug resistance in an adriamycin-resistant human small cell lung carcinoma cell line Cancer Res. 47 1987 1780 1784